Biology and Biotechnology of Environmental Stress Tolerance in Plants: Volume 1: Secondary Metabolites in Environmental Stress 9781774912812, 9781774912829, 9781774912836, 9781774912843, 9781003346173

Citation preview

Biology and Biotechnology of Environmental Stress Tolerance in Plants Volume 1: Secondary Metabolites in Environmental Stress Tolerance

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Set of 3 Volumes ISBN: 978-1-77491-281-2 (hbk) ISBN: 978-1-77491-282-9 (pbk) Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1: Secondary Metabolites in Environmental Stress Tolerance ISBN: 978-1-77491-283-6 (hbk) ISBN: 978-1-77491-284-3 (pbk) ISBN: 978-1-00334-617-3 (ebk) Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 2: Trace Elements in Environmental Stress Tolerance ISBN: 978-1-77491-285-0 (hbk) ISBN: 978-1-77491-286-7 (pbk) ISBN: 978-1-00334-620-3 (ebk) Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 3: Sustainable Approaches in Enhancing Environmental Stress Tolerance ISBN: 978-1-77491-287-4 (hbk) ISBN: 978-1-77491-288-1 (pbk) ISBN: 978-1-00334-640-1 (ebk)

Biology and Biotechnology of Environmental Stress Tolerance in Plants Volume 1: Secondary Metabolites in Environmental Stress Tolerance Edited by

Aryadeep Roychoudhury, PhD

CRC Press 6000 Broken Sound Parkway NW, Suite 300, Boca Raton, FL 33487-2742 USA 4 Park Square, Milton Park, Abingdon, Oxon, OX14 4RN UK © 2024 by Apple Academic Press, Inc. Apple Academic Press exclusively co-publishes with CRC Press, an imprint of Taylor & Francis Group, LLC Reasonable efforts have been made to publish reliable data and information, but the authors, editors, and publisher cannot assume responsibility for the validity of all materials or the consequences of their use. The authors, editors, and publishers have attempted to trace the copyright holders of all material reproduced in this publication and apologize to copyright holders if permission to publish in this form has not been obtained. If any copyright material has not been acknowledged, please write and let us know so we may rectify in any future reprint. Except as permitted under U.S. Copyright Law, no part of this book may be reprinted, reproduced, transmitted, or utilized in any form by any electronic, mechanical, or other means, now known or hereafter invented, including photocopying, microfilming, and recording, or in any information storage or retrieval system, without written permission from the publishers. For permission to photocopy or use material electronically from this work, access www.copyright.com or contact the Copyright Clearance Center, Inc. (CCC), 222 Rosewood Drive, Danvers, MA 01923, 978-750-8400. For works that are not available on CCC please contact [email protected] Trademark notice: Product or corporate names may be trademarks or registered trademarks and are used only for identification and explanation without intent to infringe. Library and Archives Canada Cataloguing in Publication Title: Biology and biotechnology of environmental stress tolerance in plants / edited by Aryadeep Roychoudhury, PhD. Names: Roychoudhury, Aryadeep, editor. Description: First edition. | Includes bibliographical references and indexes. | Content: Volume 1: Secondary Metabolites in Environmental Stress Tolerance. Identifiers: Canadiana (print) 20230155588 | Canadiana (ebook) 20230155626 | ISBN 9781774912812 (set ; hardcover) | ISBN 9781774912829 (set ; softcover) | ISBN 9781774912836 (v. 1 ; hardcover) | ISBN 9781774912843 (v. 1 ; softcover) | ISBN 9781003346173 (v. 1 ; ebook) Subjects: LCSH: Plant metabolites—Biotechnology. | LCSH: Plants—Effect of stress on. | LCSH: Plants—Adaptation. Classification: LCC QK881 .B56 2023 | DDC 572/.42—dc23 Library of Congress Cataloging-in-Publication Data

CIP data on file with US Library of C ​ ​ongress

ISBN: 978-1-77491-283-6 (hbk) ISBN: 978-1-77491-284-3 (pbk) ISBN: 978-1-00334-617-3 (ebk)

About the Editor Aryadeep Roychoudhury, PhD Assistant Professor, Department of Biotechnology, St. Xavier’s College (Autonomous), Kolkata, India Aryadeep Roychoudhury, PhD, is an Assistant Professor in the Department of Biotechnology at St. Xavier’s College (Autonomous), Kolkata, West Bengal, India. He has over 22 years of research experience in the field of abiotic stress responses in plants with perspectives of physiology, molecular biology, and cell signaling under diverse stress conditions. Dr. Roychoudhury is currently handling several government-funded projects on abiotic stress responses in rice and supervising five PhD students as Principal Investigator. To date, he has published over 200 articles in peer-reviewed journals and chapters in books of international and national repute. He has edited many books from reputed publishers and has also guest edited several special journal issues. He is a regular reviewer of articles in high-impact international journals, a life member of several scientific associations and societies, and the recipient of the Young Scientist Award 2019, conferred by the International Foundation for Environment and Ecology, at the University of Allahabad, Prayagraj, Uttar Pradesh, India. His name is included in the Stanford University’s List of World’s Top 2% Scientists. Dr. Roychoudhury received his BSc (Hons.) in Botany from Presidency College, Kolkata, and his MSc in Biophysics and Molecular Biology from the University of Calcutta, West Bengal, India. He did his PhD at the Bose Institute, Kolkata, under Jadavpur University, Kolkata, India.

Contents Contributors..............................................................................................................ix Abbreviations..........................................................................................................xiii Preface.................................................................................................................... xxi PART I: Pathways for Secondary Metabolite Production...................................1 1.

Plant Secondary Metabolites and Environmental Stress: An Overview.....................................................................................................3



Umair Riaz, Ayesha Hassan, Madiha Fatima, Humera Aziz, Madiha Rasool, and Ghulam Murtaza

2.

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway in Environmental Stress Response......................................27



Anamika Paul, Krishnendu Acharya, and Nilanjan Chakraborty

3.

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway and Regulation of Environmental Stress Tolerance...................................................................67



Lekshmy Sathee, M. K. Malini, Pramod Kumar, and Sudhir Kumar

PART II: Individual Secondary Metabolites in Tolerance...............................101 4.

Role of Diverse Classes of Terpenoids in Tolerance Against Different Environmental Stresses...............................................................103



Nehan Shamim, Anamika Paul, Maryam Haghighi, and Nilanjan Chakraborty

5.

Terpenoids in Plant Tolerance Against Different Environmental Stress...................................................................................137



Anwesha Chatterjee and Harshata Pal

6.

Role of Anthocyanin in Plants to Survive Against Environmental Stresses...............................................................................163



Suprava Nath, Subhashisa Praharaj, Sagar Maitra, Akbar Hossain, Tanmoy Shankar, Biswajit Pramanick, Mahua Banerjee, Bishal Mukherjee, Dinkar Jagannath Gaikwad, Masina Sairam, and Rajesh Shriram Kalasare

Contents

viii

7.

Role of Carotenoids in Tolerance Against Different Environmental Stress...................................................................................179



Bhupinder Dhir

8.

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance.................................................................191



Shreya Nath, Anish Nag, Swarnali Dey, Rita Kundu, and Subhabrata Paul

9.

Role of Phenolic Acids and Flavonoids in the Mitigation of Environmental Stress in Plants...................................................................227



Ankur Singh and Aryadeep Roychoudhury

PART III: Application and Analysis of Secondary Metabolites......................249 10. Seedling and Seed Priming in Regulating Secondary Metabolite Level for Stress Tolerance........................................................251

Robab Salami, Masoumeh Kordi, Nasser Delangiz, Behnam Asgari Lajayer, and Tess Astatkie

11. Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism for Stress Tolerance.............................................263

Subir Ghosh, Kuntal Bera, Puspendu Dutta, and Sanjoy Sadhukhan

12. Tools and Approaches for Assessing Stress-Responsive Secondary Metabolites to Design Climate-Smart Crops..........................305

Debapriya Rajlakshmi Das, Monolina Sarkar, and Anindita Paul

Index......................................................................................................................371

Contributors Krishnendu Acharya

Molecular and Applied Mycology and Plant Pathology Laboratory, Department of Botany, University of Calcutta, Kolkata – 700019, West Bengal, India

Tess Astatkie

Faculty of Agriculture, Dalhousie University, Truro, NS B2N 5E3, Canada, E-mail: [email protected]

Humera Aziz

Department of Environmental Science, Government College University, Faisalabad, Pakistan

Mahua Banerjee

Palli Siksha Bhavana, Visva-Bharati, Sriniketan – 731204, West Bengal, India

Kuntal Bera

Plant Molecular Biology Laboratory, Department of Botany, Raiganj University, Raiganj – 733134, Uttar Dinajpur, West Bengal, India; Department of Seed Science and Technology, Uttar Banga Krishi Viswavidyalaya, Pundibari – 736165, Cooch Behar, West Bengal, India, E-mail: [email protected], ORCID: https://orcid.org/0000-0002-6879-6418

Nilanjan Chakraborty

Scottish Church College, Department of Botany, Kolkata – 700006, West Bengal, India, E-mail: [email protected]

Anwesha Chatterjee

Amity Institute of Biotechnology, Amity University, Major Arterial Road (South-East), Action Area II, Newtown, Kolkata – 700135, West Bengal, India

Debapriya Rajlakshmi Das

Department of Botany, Taki Government College, Taki – 743429, West Bengal, India

Nasser Delangiz

Department of Plant Biotechnology and Breeding, Faculty of Agriculture, University of Tabriz, Tabriz, Iran

Swarnali Dey

Department of Botany, University of Calcutta, 35 Ballygunge Circular Road, Kolkata – 700019, West Bengal, India

Bhupinder Dhir

School of Sciences, Indira Gandhi National Open University, New Delhi, India

Puspendu Dutta

Department of Seed Science and Technology, Uttar Banga Krishi Viswavidyalaya, Pundibari – 736165, Cooch Behar, West Bengal, India, E-mail: [email protected], ORCID: https://orcid.org/0000-0001-6659-8402

Madiha Fatima

Department of Zoology, The Women’s University Multan, Multan, Pakistan

Dinkar Jagannath Gaikwad

Centurion University of Technology and Management, Odisha – 761211, India

x

Contributors

Subir Ghosh

Plant Molecular Biology Laboratory, Department of Botany, Raiganj University, Raiganj – 733134, Uttar Dinajpur, West Bengal, India, E-mail: [email protected], ORCID: https://orcid. org/0000-0003-3684-7265

Maryam Haghighi

Department of Horticulture, College of Agriculture, Isfahan University of Technology, Iran

Ayesha Hassan

Department of Environmental Science, University of Okara, Okara, Pakistan

Akbar Hossain

Bangladesh Wheat and Maize Research Institute, Dinajpur – 5200, Bangladesh

Rajesh Shriram Kalasare

Centurion University of Technology and Management, Odisha – 761211, India

Masoumeh Kordi

Department of Plant Sciences and Biotechnology, Faculty of Life Sciences and Biotechnology, Shahid Beheshti University, Tehran, Iran

Pramod Kumar

Division of Plant Physiology, ICAR–Indian Agricultural Research Institute, New Delhi, India

Sudhir Kumar

Division of Plant Physiology, ICAR–Indian Agricultural Research Institute, New Delhi, India

Rita Kundu

Department of Botany, University of Calcutta, 35 Ballygunge Circular Road, Kolkata – 700019, West Bengal, India

Behnam Asgari Lajayer

Health and Environment Research Center, Tabriz University of Medical Science, Tabriz, Iran, E-mail: [email protected]

Sagar Maitra

Centurion University of Technology and Management, Odisha – 761211, India, E-mail: [email protected]

M. K. Malini

Division of Plant Physiology, ICAR–Indian Agricultural Research Institute, New Delhi, India

Bishal Mukherjee

Bidhan Chandra Krishi Viswavidyalaya, Mohanpur – 741252, West Bengal, India

Ghulam Murtaza

Institute of Soil and Environmental Sciences, University of Agriculture, Faisalabad, Pakistan

Anish Nag

Department of Life Sciences, CHRIST (Deemed to be University), Bangalore – 560029, Karnataka, India

Shreya Nath

School of Biotechnology, Presidency University (2nd Campus), Kolkata – 700156, West Bengal, India

Suprava Nath

University of Agricultural Sciences, Bangalore – 560065, Karnataka, India

Harshata Pal

Amity Institute of Biotechnology, Amity University, Major Arterial Road (South-East), Action Area II, Newtown, Kolkata – 700135, West Bengal, India, Email: [email protected]

Contributors

xi

Anamika Paul

Scottish Church College, Department of Botany, Kolkata – 700006, West Bengal, India

Anindita Paul

Molecular Biophysics Unit, Indian Institute of Science, Bangalore – 560012, Karnataka, India, E-mail: [email protected]

Subhabrata Paul

School of Biotechnology, Presidency University (2nd Campus), Kolkata – 700156, West Bengal, India

Subhashisa Praharaj

Centurion University of Technology and Management, Odisha – 761211, India

Biswajit Pramanick

Dr. Rajendra Prasad Central Agricultural University, Pusa, Samastipur, Bihar – 848125, India

Madiha Rasool

Department of Zoology, The Women University Multan, Multan, Pakistan

Umair Riaz

Soil and Water Testing Laboratory for Research, Bahawalpur – 63100, Pakistan, Phone: +92-3006208789, E-mail: [email protected]

Aryadeep Roychoudhury

Post-Graduate Department of Biotechnology, St. Xavier’s College (Autonomous), 30, Mother Teresa Sarani, Kolkata – 700016, West Bengal, India, E-mail: [email protected]

Sanjoy Sadhukhan

Plant Molecular Biology Laboratory, Department of Botany, Raiganj University, Raiganj – 733134, Uttar Dinajpur, West Bengal, India, E-mail: [email protected], ORCID: https://orcid.org/0000-0002-2619-8700

Masina Sairam

Centurion University of Technology and Management, Odisha – 761211, India

Robab Salami

Department of Plant Sciences and Biotechnology, Faculty of Life Sciences and Biotechnology, Shahid Beheshti University, Tehran, Iran

Monolina Sarkar

Department of Botany, Sammilani Mahavidyalaya, Eastern Metropolitan Bypass, Kolkata – 700094, West Bengal, India

Lekshmy Sathee

Division of Plant Physiology, ICAR–Indian Agricultural Research Institute, New Delhi, India, E-mail: [email protected]

Nehan Shamim

Scottish Church College, Department of Botany, Kolkata – 700006, West Bengal, India

Tanmoy Shankar

Centurion University of Technology and Management, Odisha – 761211, India

Ankur Singh

Post-Graduate Department of Biotechnology, St. Xavier’s College (Autonomous), 30, Mother Teresa Sarani, Kolkata – 700016, West Bengal, India

Abbreviations 4CL 4-coumarate: CoA ligase AAO ABA-aldehyde oxidase ABA abscisic acid ABA-GE ABA-glucosyl ester ABAld abscisic aldehyde ABC ATP-binding cassette ABFs ABRE-binding factors ABRE ABA-responsive elements ACCT acetoacetyl CoA acetyltransferase AGO-CLIP argonaute cross-linking and immunoprecipitation alfAFP alfalfa anti-fungal peptide AM arbuscular mycorrhizal ANS anthocyanidin synthase AP2/ERF apetala2/ethylene-responsive factors APCI atmospheric pressure chemical ionization API atmospheric pressure ionization APPI atmospheric pressure photoionization APX ascorbate peroxidase ASE allele-specific expression ASM acibenzolar-S-methyl AS-SDR ABA-specific short-chain dehydrogenase/reductase BCAT4 branched-chain amino acid aminotransferase 4 BGLUs β-glucosidase enzymes BVOC biogenic volatile organic compound C4H cinnamate 4-hydroxylase Ca calcium CAD cinnamyl alcohol dehydrogenase cADPR cyclic ADP ribose cap analysis of gene expression CAGE CaMV cauliflower mosaic virus CAT catalase CBF C-repeat binding factor CBL calcineurin B-like protein CBSC carbon-based secondary compounds

xiv

Abbreviations

CCoAOMT caffeoyl CoA 3-O-methyltransferase Cd cadmium cDNA complementary DNA CDPKs calcium-dependent protein kinases 4-cytidine 5´-diphospho-2-C-methyl-D-erythriol CDP-ME CE capillary electrophoresis CE coupling element CE-MS capillary electrophoresis-mass spectrometry CHI chalcone isomerase CHS chalcone synthase CID collision-induced dissociation CIPKs CBL interacting protein kinases CoA coenzyme A COGs cluster of orthologous groups COSY coumarin synthase COU coumarin Cptio 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline Cr chromium CRE cis-regulatory element Cs cesium CsTPS cannabis terpene synthase genes CTAB cetyltrimethylammonium bromide Cu copper DAG diacylglycerol kinase DAHPS 3-deoxy-D-arabino-heptulosonate-7-phosphate-synthase DART direct analysis in real time DE differentially expressed DEGs differentially expressed genes DEPC diethyl pyrocarbonate DESI desorption electrospray ionization DFR dihydroflavonol 4-reductase DHBA dihydroxybenzoic acid DHD 3-dehydroquinate dehydratase DHQ synthase 3-dehydroquinate synthase DHS 3-dehydroshikimate DI direct infusion DIMS direct infusion-MS DMADP dimethylallyl diphosphate DMAPP dimethylallyl pyrophosphate DMNT 4,8-dimethyl-1,3,7-nonatriene

Abbreviations

xv

DPA dihydrophaseic acid dehydration-responsive element binding DREB DREB2A dehydration-responsive element-binding protein 2a DXP 1-deoxy-D-xylulose 5-phosphate 1-deoxy-D-xylulose-5-phosphate synthase DXS E4P erythrose-4-phosphate EASI easy ambient sonic spray ionization ECD electron-capture dissociation ECOSY exclusive correlation spectroscopy EDTA ethylenediaminetetraacetic acid EI electron ionization EPSP 5-enolpyruvylshikimate-3-phosphate eQTL expression quantitative trait locus ERCC external RNA controls consortium ESI electrospray ionization EST expressed sequence tag ETC electron transport chain ETD electron-transfer dissociation F3’5’H flavonoid 3’5’-hydroxylase F3H flavanone-3-hydroxylase F6’H1 feruloyl-CoA 6’-hydroxylase-1 FAB fast atom bombardment FaNES1 Fragaria ananassa nerolidol synthase 1 FD field desorption Fe-S iron-sulfur FFPE formalin-fixed paraffin-embedded FFPP farnesol farnesyl pyrophosphate FGT flavonoid glycosyltransferases FI flow-injection FIMS flow injection-MS FIT fer-like iron deficiency induced transcription factor FLS flavonol synthase FPKM fragments per kilobase million FPP farnesyl pyrophosphate FT-ICR-MS Fourier transform ion cyclotron resonance mass spectrometry FT-IR Fourier transform infrared spectroscopy G6PDH glucose-6-phosphate dehydrogenase GA gibberellic acid GABA γ-aminobutyric acid

xvi

GC GC-FID GC-MS GDSL GEO GGGP GGPP GHGs Gly I GM GMD GML GMUCT GPP GPX GR GWAS H2O2 HAB1 HBA HCA HCD HDR HILIC HMG-CoA HPAEC HPLC HPTLC HR-MAS HSP HSQC HT ICE IDI IFR IFS IP IPK IPP

Abbreviations

gas chromatography GC-flame ionization detection gas chromatography-mass spectrometry GDSL esterase/lipase gene expression omnibus geranylgeranyl diphosphate geranylgeranyl pyrophosphate greenhouse gases glyoxalase I genetically modified Golm metabolome database global metabolome labeling genome-wide mapping of uncapped and cleaved transcripts geranyl pyrophosphate glutathione peroxidase glutathione reductase genome-wide association studies hydrogen peroxide hypersensitive to ABA1 hydroxybenzoic acids hydroxycinnamic acids high-energy collision dissociation 4-hydroxy-3-methyl but-2-enyl diphosphate reductase hydrophilic interaction liquid chromatography 3-hydroxyl-3-methyl glutaryl CoA high-performance anion-exchange liquid chromatography high-performance LC high-performance thin-layer chromatography high-resolution magic angle spinning heat-shock protein heteronuclear single-quantum correlation spectroscopy high temperature inducer of CBF expression isopentyl diphosphate isomerase isoflavone reductase isoflavone synthase inositol phosphate isopentenyl phosphate kinase isopentenyl diphosphate

Abbreviations

xvii

ISPS isoprene synthase ion trap IT IUPAC International Union of Pure and Applied Chemistry JA jasmonic acid K potassium LAESI laser ablation ESI LC liquid chromatography LC-MS liquid chromatography-mass spectrometry LEA late embryogenesis abundant LHC light-harvesting complexes LiCl lithium chloride LMD laser microdissection lncRNAs long non-coding RNAs LOX lipoxygenase L-Phe L-phenylalanine LSIMS liquid secondary ion mass spectrometry L-Trp L-tryptophan L-Tyr L-tyrosine LYC-ε lycopene ε cyclase MAE microwave-assisted extraction MALDI matrix-assisted laser desorption ionization MAMI1 methylthioalkylmalate synthase 1 MAPK mitogen-activated protein kinase MCT 2-C-methyl-D-erythritol-4-phosphate-cytidyltransferase MDA malondialdehyde MEcDP methylerythritol 2,4-cyclodiphosphate MeJA methyl jasmonate MEP methylerythritol phosphate MERFISH multiplexed error-robust fluorescence in situ hybridization MFC minimum fungicidal concentration Mg magnesium miRNA microRNA MK mevalonate kinase MS mass spectrometry MSI mass spectrometry imaging MSI metabolomic standard initiative MSTFA N-methyl-trimethylsilyl trifluoroacetamide MTPSLs microbial terpene synthase-like genes MVA mevalonic acid

xviii

Abbreviations

MVD diphosphomevalonate decarboxylase MVP mevalonate-5-phosphate MYB2 MYB domain protein 2 NaCl sodium chloride NADPH oxidase NADPHox NCED 9-cis-epoxycarotenoid dioxygenase NCEI 9-cis-epoxycarotenoid forming isomerase ncRNAs non-coding RNAs NGS next-generation sequencing Ni nickel NMR nuclear magnetic resonance NO nitric oxide NOESY nuclear Overhauser effect spectroscopy NOx nitrogen oxides NPQ non-photochemical quenching NR nitrate reductase OSHA Occupational Safety and Health Administration P phosphorus PA phaseic acid PA phosphatidic acid PAL phenylalanine ammonia-lyase PARE parallel analysis of RNA ends Pb lead PCD programmed cell death PD plasma desorption PEG polyethene glycol PEP phosphoenolpyruvate PEPC phosphoenolpyruvate carboxylase PESI probe ESI PFD photon flux density PGC porous graphitic carbon PGPRs plant growth promoting rhizobacteria PKS polyketide synthase PKSB polyketide synthase B PlantTFDB plant transcription factor database PLC phospholipase C PMN plant metabolic network POD peroxidase Pp Phakopsora pachyrhizi

Abbreviations

xix

PP2Cs 2C protein phosphatases polyphenol oxidase PPO PRO-seq precision nuclear run-on sequencing PS-II photo system-II PTIO 2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide PUFA polyunsaturated fatty acid PVP polyvinylpyrrolidone QIT quadrupole ion trap qPCR quantitative polymerase chain reaction QqQ quadrupole RAB18 responsive to ABA 18 RACE 5’-rapid amplification of cDNA ends Rboh respiratory burst oxidase RD29B responsive to desiccation 29B RIN RNA integrity number RNAP RNA polymerase active RNA-Seq RNA sequencing RNSs reactive nitrogen species ROESY rotating-frame nuclear overhauser effect spectroscopy ROS reactive oxygen species RP reversed-phase RPKM reads per kilobase million RWC relative water content S8H scopoletin 8-hydroxylase SA salicylic acid SAGE serial analysis of gene expression SBR soybean rust SCOPE-seq2 single-cell optical phenotyping and expression SDE simultaneous distillation–extraction SDH shikimate-5-dehydrogenase SDS sodium dodecyl sulfate SFE supercritical fluid extraction SKDH shikimate dehydrogenase SLAC1 s-type anion channel SLs strigolactones SmCin1 synthase one gene smFISH single molecule FISH SMRT single molecule real time SMs secondary metabolites

xx

Abbreviations

SNP sodium nitroprusside sucrose non-fermenting protein-1 related kinases 2 SnRK2s SOD superoxide dismutase SOLiD sequencing by oligonucleotide ligation and detection salt overly sensitive SOS SPME solid-phase microextraction SPME–GC–MS solid-phase microextraction–gas chromatography-mass spectrometry SPOTs sequential probing of targets SSNMR solid-state NMR T65 Taichung 65 TAL tyrosine ammonia lyase TFs transcription factors THF tetrahydrofuran TL tracer labeling TMS trimethylsilyl TMV tobacco mosaic virus TOCSY total correlation spectroscopy TOF time-of-flight ToRSV tomato ringspot virus TPS terpene synthase TSGS terpene synthase genes TSP thermospray TSP23 terpene synthase 23 TSSs transcription start sites UAE ultrasound-assisted extraction UFGT UDP flavonoid glycosyltransferase UGT UDP-glycosyltransferases UHPLC ultra-high-performance LC UMI unique molecular identifiers UPLC ultra-performance LC UTR untranslated regions UV ultraviolet VOC volute organic compound VT volatile terpenes WUE water use efficiency ZEP zeaxanthin epoxidase Zn zinc

Preface One of the major causes responsible for restricted plant growth and agricultural production in recent times is the increasing occurrence of different forms of abiotic stresses such as drought, high salt, cold, heat, UV radiation, heavy metals, etc., which are gradually becoming more alarming due to the threat of global climate changes. It is estimated that agricultural production should be enhanced by 100–110% by 2050 in order to meet the per capita caloric demands and provide food security to the ever-increasing human population. Therefore, it becomes imperative to study the underlying mechanism of stress tolerance to form a proper understanding of the cross-talks of diverse metabolites and the biosynthesis pathways for metabolite production to maintain osmotic balance under diverse environmental stresses. Plant secondary metabolites do not play any fundamental role in controlling growth and development and regulation of life processes, but they do enhance plant adaptation and defense against abiotic and biotic stress. Such metabolites mostly use primary metabolites like carbohydrates, lipids, and proteins as precursor molecules for their synthesis. With stress exposure, increased production of the secondary metabolite is caused because growth is often inhibited more than photosynthesis, so the fixed carbon is chiefly allocated to secondary metabolites. Plant exposure to stressed conditions often results in an exchange between carbon to biomass production for the biosynthesis of defensive secondary compounds. A prominent response to ensure stress tolerance is the enhanced production of a repertoire of secondary metabolites like terpenoids, carotenoids, anthocyanins, flavonoids, tannins, and alkaloids and the up-regulation of genes and enzymes controlling their biosynthetic pathways. Several antioxidant and anti-radical functions have been ascribed to such secondary metabolites that assist plants to cope with oxidative stress conditions. Even secondary metabolites, applied exogenously, participate in stress tolerance in plants by regulating different signaling pathways. Enhanced polyphenol content in plant tissues during salinity has been reported due to stimulated polyphenol synthesis. Anthocyanin accumulation has been reported during drought stress and cold acclimation. During cold stress, phenolic production and their subsequent incorporation and deposition as suberin or lignin within the cell wall has been observed. UV-B stress has been found to stimulate the anthocyanin and

xxii Preface

flavonoid synthesis and phenylalanine ammonia-lyase (PAL) activity. The production and concentration of secondary metabolites are determined by proper equilibrium between biosynthesis, storage, and degradation. Perturbation in secondary metabolite biosynthesis is triggered as a result of alteration in any of the stress factors. Secondary metabolites are also involved in extensive crosstalk and signaling processes between different pathways that include the participation of diverse molecules like polyamines, jasmonic, and salicylic acid, abscisic acid (ABA), calcium (Ca), and nitric oxides. Although secondary metabolites can be detected throughout the plant body, their actual site of synthesis is more often restricted to a particular organ, following which they undergo symplastic or apoplastic transport through vascular tissues to the different regions and ultimately to the storage sites like root, shoot, leaf, flower, callus or somatic embryos and sometimes special structures like periderm, glandular trichomes, and phellem. Secondary metabolites like glucosinolates, tannins, and alkaloids that are hydrophilic are accumulated in idioblasts or vacuoles, while terpenoids which are lipophilic are stored in thylakoid membranes, resin ducts, or cuticles. Metabolomics and transcriptomics technologies, along with bioinformatics pipelines, augmented the analysis of increased genome sequences and secondary metabolites they produce, together with a proper understanding of stress-associated genes and pathways involved in secondary metabolite production. However, there are quite a number of analytical limitations, like reliable quantification, tissue-specific variation in secondary metabolites, and variation in the quantity of a secondary metabolite, depending on the duration and intensity of stress. There exists a lot of challenges in ascertaining the stress physiology and production of secondary metabolite to a specific stress factor because of the existence of interconnected effects of complex stress factors in secondary metabolite-mediated plant defense. The higher production of the major secondary metabolites is part of a chemical defense response system that enhances tolerance capability against diverse environmental stress. Therefore, a comprehensive understanding of the mechanisms mediating biosynthesis, accumulation, and degradation of such metabolites would ensure the formulation of novel strategies to improve their production and manipulate them for enhancing abiotic stress tolerance in plants. Volume 1 of this three-volume book set, entitled ‘Secondary Metabolites in Environmental Stress Tolerance,’ exclusively focuses on the diverse secondary metabolites commonly upregulated in plants during different environmental stress and their implications in enhancing the tolerance mechanism.

PART I Pathways for Secondary Metabolite Production

CHAPTER 1

Plant Secondary Metabolites and Environmental Stress: An Overview

UMAIR RIAZ,1* AYESHA HASSAN,2 MADIHA FATIMA,3 HUMERA AZIZ,4 MADIHA RASOOL,3 and GHULAM MURTAZA5

Soil and Water Testing Laboratory for Research, Bahawalpur – 63100, Pakistan 1

Department of Environmental Science, University of Okara, Okara, Pakistan

2

3

Department of Zoology, The Women University Multan, Multan, Pakistan

Department of Environmental Science, Government College University, Faisalabad, Pakistan

4

Institute of Soil and Environmental Sciences, University of Agriculture, Faisalabad, Pakistan

5

*

Corresponding author. E-mail: [email protected]

ABSTRACT Plant secondary metabolites have been increasing over the last 50 years. These molecules are known to play a major role in the adaptation of plants to stressful environments. These are not only a useful array of natural products but also an important part of the plant defense system against pathogenic attacks and environmental stresses. The classes of secondary plant metabolites include phenolics, alkaloids, saponins, terpenes, lipids, and carbohydrates. Plants may face continuous exposure to environmental factors due to their sessile nature, and they need to maintain an efficient mechanism that Biology and Biotechnology of Environmental Stress Tolerance in Plants: Secondary Metabolites in Environmental Stress Tolerance, Volume 1. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

4

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

can work under unfavorable circumstances to withstand normal life. It is also reported that the forecast and occurrence of stresses significantly contribute to and disturbs the development and yield of plants and a 70% reduction in crop productivity. Plants that produce more polyphenols in response to abiotic stresses tend to be more adaptable to constraining environmental conditions. Many abiotic elements such as weather patterns, nanoparticles, and pesticides not only initiate but enhance the endogenous phenolic biosynthesis within various plant species and assist in resisting against phytotoxic impacts of the above-mentioned abiotic stress conditions. 1.1 INTRODUCTION Plants are exposed to a swerve of various abiotic and biotic stresses all over their lives, which may lead to negatively affect not only their growth and development but also impact on their productivity (Dresselhaus & Huckelhoven, 2018). Insect pests, fungi, and weeds are examples of biological factors, while abiotic stresses comprise of salinity, water shortages (drought), heavy metal accumulation, insecticides, pesticides, UV radiation, and temperature fluctuations. Anthropogenic activities triggered the level and severity of biotic and abiotic stresses in present times (Mittler & Blumwald, 2010). The main concern at present is to reduce crop productivity losses by developing multiple approaches to enhance crop performance. The application of plants’ bio-stimulants, as well as the stimulation of secondary metabolism in plants, are the two main tactics in this regard (Shahzad et al., 2017). Phenolic compounds are responsible for influencing a number of factors in plants, such as plant growth and development, seed and biomass germination, and efficient metabolism (Nazr et al., 2011). Secondary metabolism is mainly regarded as the biogenetic producer of numerous useful metabolites that can be used in the agricultural, pharmaceutical, chemical, food, and cosmetic manufacturing sectors. Secondary metabolism is not actually essential for the subsistence of individual cells, but it benefits the complete plant structure. Plants biosynthesize three types of secondary metabolites: (i) phenolic substances; (ii) terpenoids, isoprenoids, and alkaloid compounds; and (iii) glucosinolate metabolites, i.e., nitrogen (N) or sulfur (S)-containing compounds (Aharoni & Galili, 2011). The shikimic pathway is responsible for biosynthesizing phenolic compounds, which are readily available in plants. In plants, the shikimic pathway is found in the chloroplast. They are aromatic substances and play critical roles as antioxidants, pigments, communicating agents, the structural element lignan, signaling mediators, defense mechanisms, and electron transportation (Macherous et al., 1999).

Plant Secondary Metabolites and Environmental Stress: An Overview

5

1.2 TOXIC EFFECTS OF ENVIRONMENTAL STRESSES ON PLANTS Environmental stresses have increased rapidly in plants in the past few decades. Climate change and global warming are major environmental issues faced by plants. Increased concentrations of greenhouse gases (GHGs), including CO2, methane, ozone, and oxides of nitrogen, are the prime reasons for global warming, and estimations showed that the concentration of GHGs will remain in an increasing trend from 3–5°C on an average annually in coming 50–100 years (Le Quere et al., 2009). Environmental (including abiotic and biotic) factors like droughts, ozone, salt levels, and heavy metal concentrations clearly stimulate phenylpropanoid metabolism. Plants have various mechanisms and pathways to deal with abiotic/environmental stresses (Godoy et al., 2021). 1.2.1 THE PHENYLPROPANOID AND SHIKIMIC ACID PATHWAY All attributes of plant and their response toward biotic and abiotic stimulations are strongly affected by phenylpropanoids. They act as plant stressresponse indicators to alterations in light and/or mineral treatment, and phenylpropanoids are also vital for the battle of plants against pests. The phenylpropanoid pathway is a significant source of secondary metabolites in plants, required for lignin biosynthesis and a preliminary point for the supply of many other compounds like flavonoids, coumarins, and lignans. The phenylpropanoids are characterized as a broad class of substances, sourced from the carbon skeleton of phenylalanine that perform significant roles in plants like defense, structural strength, and ability to survive. In addition to the well-known antioxidant mechanism of specialized enzymatic and non-enzymatic antioxidants, recent studies underlined the prime functions of phenylpropanoid mechanism along with its metabolites, especially flavonoids are considered as the nominal antioxidants (Mishra et al., 2014). Phenylpropanoids belong to the largest class of phenols and are recognized as secondary metabolites in plants ranging from simple rings of aromatic compounds to complicated substances, i.e., lignins. As these compounds are derived from phenylalanine, they are also known as phenylpropanoids. The phenylpropanoid pathway is among the key pathways in plants. This pathway can account for more than 20% of total metabolism in a cell and the enzyme chorismate mutase is a significant signaling point (Zhang et al., 2015). The pathway is of particular importance primarily because of its ability to form various lignins, lignans, flavonoids, and anthocyanins. The major end product is the enzyme PAL, which is responsible to convert phenylalanine

6

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

into trans-cinnamic acid by a non-oxidative deamination. The most important is the one that leads to flavonoids, in which the enzyme (coumaryl-CoA) is combined with three C2 molecules through malonyl-CoA. The chalcone synthase (CHS) enzyme catalyzes this reaction (CHS). The CHS enzyme is thoroughly investigated, and a range of genetic material from a variety of plant species have been colonized and genetically modified (GM). This enzyme results in a unique ring-like closed assembly within the coumaryl-CoA’s condensation product and the three malonyl-CoA units (Zhang et al., 2015). Enzymatic responses that convert phenylalanine to hydroxycinnamic acid have been known since 450 million years ago, correlating with plant colonialization of the terrestrial ecosystem (Biala & Jasinski, 2018). The metabolism of phenylpropanoid remains at the acid level and is targeted to the biosynthesis of flavonoids, implying that initial steps on the evolution process involves in the lignification were existing in bryophytic ancestors (Weng & Chapple, 2010). Polymers based on phenylpropanoids, such as suberin, lignins, or condensed tannins, significantly contribute towards the stabilization and reproducibility of gymnosperms and angiosperms from climatic and environmental impacts, like drought or illnesses. Depending on the few substrates of the shikimate pathway, phenylpropanoid metabolism produces a vast array of secondary metabolites (Vogt, 2010). The shikimate pathway (Shikimic Acid pathway) among plant species is the initial stage in the biosynthesis of phenylpropanoids. For more than a decade, scientists have been studying its intracellular, plastidial destination, and intricate regulation. The two enzymes of prime importance are Shikimate dehydrogenase (SKDH) as well as glucose-6-phosphate dehydrogenase (G6PDH) which catalyzes the biotic response essential for the generation of vital originators for phenylpropanoid mechanism (Kovácik et al., 2009). Shikimic acid is produced through the hydrogenation reaction catalyzed by the enzyme known as Shikimate dehydrogenase. Shikimic acid pathway produces aromatic amino acids from precursors resultant from the pentose phosphate mechanism and glycolysis, with phenylalanine act as a regular intermediate (Bartwal et al., 2013). 1.3 INVOLVEMENT OF MEVALONATE AND METHYLERYTHRITOL PHOSPHATE (MEP) MECHANISM IN ENVIRONMENTAL STRESS RESPONSE The mevalonate pathway (MVA) and the mevalonate-independent methylerythritol phosphate (MEP) mechanisms are both known to yield isopentenyl diphosphate (IPP) in plant cells, which is then used by various enzymes to

Plant Secondary Metabolites and Environmental Stress: An Overview

7

produce over 50,000 varying isoprenoid structures (Skorupinska-Tudek et al., 2008). C5 molecules through the MEP pathway are incorporated not only in the production of isoprene, chlorophyll, mono- and di-terpenes, and carotenoid, but also the gibberellin, strigolactone, and abscisic acid (ABA) metabolites (Perreca et al., 2020). Eubacteria were the first organism that were studied to describe the MEP pathway while the enzymes catalyzing the MEP mechanism have been primarily recognized within Escherichia coli. Since Arabidopsis thaliana contains genotypes for all of the bacterial genes of the MEP pathway, a similar group of enzymes is supposed to be responsible for the MEP pathway in plants. The MEP pathway in plastids may also be responsible for the production of IPP and DMAPP for ent-kaurene biosynthesis (Kasahara et al., 2002). Under suitable water levels and controlled environment, the metabolites and the end-products of MEP mechanism isoprene integrate prescribed 13CO2 towards higher rates (75–85%), signifying a direct correlation to photosynthesis (SkorupinskaTudek et al., 2008). The levels of Phytol and α-tocopherol in Brachypodium distachyon were also found to be higher at the initial phases of water shortage as compared to well-watered vegetative stage, however, decreased during the longer water stress situations (Ahkami et al., 2019). The use of specifically labeled [13C] glucose is most commonly used to estimate the mutual contribution of pathways which leads towards the generation of an investigated isoprenoid substance. The origins of the isoprenoid byproducts can be determined using a specified pattern for the pathway of 13C labeling in the isoprenoid byproducts (Disch et al., 1998; Kobayashi et al., 2007). 1.3.1 ROLE OF DIVERSE CLASSES OF TERPENOIDS IN TOLERANCE AGAINST DIFFERENT ENVIRONMENTAL STRESS Among all the classes of secondary metabolites, terpenoids exist in wide variety. These substances are produced by combining the 5-carbon precursor unit isopentenyl pyrophosphate (IPP) and relevant active isomer known as dimethylallyl pyrophosphate (DMAPH). Terpenes are simplified hydrocarbons derived from DMAPP and ID variations, whereas terpenoids (also called isoprenoids) are the terpene molecule with an oxygen atom and supplementary formational alterations (Boncan et al., 2020). Plant volatiles are known as the least molecular weight (300 Da) substances which play a key function in plant–environment relations and to a lesser degree, abiotic stress reactions (Dudareva et al., 2006). Major groups of plants secondary

8

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

metabolites include terpenes (55%), alkaloids (27%), and phenolics (18%). Terpenes belong to the largest class (Honey et al., 1988). Volatile terpenes (VTs) are terpenoids that are released to interact with the physical environment and consist of hemi-, mono-, homo-, sesqui-, and also few di-terpenoids. The storage and volatility of terpenoids is highly affected from the biochemical characteristics (e.g., vapor pressure and water solubility), whereas their emission ratios and trends are influenced by a variety of abiotic and biotic parameters such as temperature, humidity, seasonal variations, solar activity, and ability to interact with other plants and organisms (Yazaki et al., 2017). Terpenoids are stored in plant tissues with distinguished assemblies like secretory chambers, resin tunnels, latex waterways, and follicular trichomes (Holopainen et al., 2013). Plant perspective and response towards environmental stresses is a complicated phenomenon that incorporates many genes, nucleic acids, receptors, enzymes, and metabolites in a well-controlled system (Zhu, 2016). The SnRK2 subfamily, a crucial aspect of the salt overly sensitive (SOS) mechanism, takes part in the terpene-phytohormone ABA signaling mechanism, which activates transcription factors (TFs) as well as the mitogen-activated protein kinase (MAPK) cluster (Hamann, 2012). Terpenoids are recognized in mediating the interaction between plants and insects, for instance, pollinators, predators, parasites, and herbivores. In general, plant-herbivore interactions give advantage to plants while harming the insects (Boncan et al., 2020). Plants’ resistance to abiotic stress is directly controlled through the interaction of terpenoids with oxidants, both intracellularly and at the leaf-environment level, membrane stabilization, and indirect alterations in ROS modulation (Sewelam et al., 2016). Terpene compounds help pollinators find their suitable host by acting as a signal. When talking about noctuid moths Hadena bicruris, lilac aldehydes, regarded as the primary constituent for the aroma of Silene latifolia, attract these insects (Dötterl et al., 2006). 1.3.2 ROLE OF PHENOLICS AND TANNINS IN TOLERANCE AGAINST DIFFERENT ENVIRONMENTAL STRESSES Phenolic accumulation is critical for mitigating the negative impacts of water shortage conditions in plants (Naikoo et al., 2019). Several phenolic acids, such as caffeic acid, caftaric acid, cinnamylmalic acid, gallic acid, ferulic, and vanillic acid, get accumulated in plants during saline environmental conditions (Ben-Abdallah et al., 2019). Polyphenols are unique due to the presence of numerous phenolic structures. The quantity and properties

Plant Secondary Metabolites and Environmental Stress: An Overview

9

of the phenol molecules fortifies distinctive physio-chemical and biological characteristics of individual compounds (Sharma et al., 2019). Polyphenols are formed in plants under most suitable as well as (to a greater extent) unfavorable environmental situations and perform key performance in the progression, including transduction of signals, cellular distribution, hormone settings, photosynthesis activity monitoring, seed germination, and reproduction ratio. Species of plants that grow in extreme weather conditions can biosynthesize more phenolic compounds than plants that grow in normal climates (Selmar, 2008). Phenolics reduce thickness and enhance the porosity of the outer membrane of seeds that not only aids in water absorption but also increases seed germination. Plants growing under pesticide stress activate phenolic biosynthetic pathways as well. This causes an increase in the absorption of phenols in plants, which helps in providing resistance to pesticides toxicity (Mahdavi et al., 2015). This enthused biosynthesis of phenolic compounds is the result of key instigation of biosynthetic enzymes and enhanced cellular response of significant genetic material of phenylpropanoid division, containing PAL and CHS (Sharma et al., 2016). Excessive concentration of anthocyanin in plant leaves enhanced due to the insecticide application that assist in retrieval photosynthetic productivity of plants (Sharma et al., 2016). Likewise, under extreme temperature conditions (heat situation and chilled environment), plants produce more phenolic substances like anthocyanin, flavonoids, flavonols, and phenolic acids, which play an essential role in plant protection (Sharma et al., 2019). Some phenolics, such as salicylic acid, stimulate phenol formation and biosynthesis in plants facing higher temperature stresses. It can cause an increase in the deposition of phenols, which aids in the ROS detoxification and provides heat resistance to plants (Cingroz & Gurel, 2016). 1.3.3 ROLE OF FLAVONOIDS IN TOLERANCE AGAINST DIFFERENT ENVIRONMENTAL STRESS The frequently studied class of polyphenols and flavonoids, which have over 6,000 diverse assemblies (Panche et al., 2016). The flavonoids are classified into six main subclasses: flavones, flavonols, flavanones, flavanols, anthocyanidins, and isoflavones (Ross & Kasum, 2002). There are no unified and consistent pathways for the production, aggregation, or exudation of flavonoids that have been proposed as of yet, however, there are two elements

10

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

of total flavonoids and individual substances that can be mentioned. The first content is dependent solely on the plant species and its reactions to environmental stresses. This can be perfectly described as “plant health” while the second is concerned with alterations linked to human consumption. This second dimension can also be illustrated as “human health” (Cetinkaya et al., 2017). The flavonoid accumulation in plants is a dependent stress factor including the occurrence and timing and duration of stress. An exchange of carbon and biomass output or the initiation of protective secondary metabolites occurs, implying that secondary metabolites are actively engaged in plant protective mechanism in reaction to environmental stressors. For instance, the production of phenyl amide and aggregation of anthocyanin as well as polyamine is observed as a result of environmental stresses (Bryant et al., 1983; Akula & Ravishankar, 2011). Flavonoids can exert immediate scavenging of oxygen radicals. They can quickly release hydrogen ions while scavenging reactive oxygen molecules. Thus, while flavonoids deactivate reactive oxygen species (ROS), flavonoids revert to the phenoxyl radical. The phenoxyl radical in flavonoids can interact with available ions to form less-reactive Quinone composition (Pietta, 2000). 1.3.4 ROLE OF ANTHOCYANINS IN TOLERANCE AGAINST DIFFERENT ENVIRONMENTAL STRESS Anthocyanin belongs to a class of secondary metabolites known as flavonoids. Anthocyanin exists in a variety of colors, i.e., orange, purple, blue, and red in seeds, flowers, fruits, and vegetative tissues. Being water-soluble pigments, they are localized in the cell vacuoles. In nature, more than 600 anthocyanins have been identified; however, six anthocyanins are the most common, which include pelargonidin, delphinidin, peonidin, petunidin, and malvidin, and cyaniding. Anthocyanin plays a crucial protective role against numerous biological and physical stresses (Liu et al., 2018). Anthocyanins are usually found in epidermal and/or mesophyll cells of leaves as vacuolar solutions, or sometimes may be found as red pigments bound to the cell wall of epidermal cells in certain bryophytes. However, regardless of their cellular placement, foliar biosynthesis of anthocyanin is up-regulated most of the time in response to stressors like robust light, UV-B emissions, temperatures beyond tolerance range, water scantiness, high ozone, insufficiencies of utilizable N and P, infectious disease arising due to pathogenic bacteria

Plant Secondary Metabolites and Environmental Stress: An Overview

11

and fungi, feeding by herbivores, herbicides, and environmental pollutants. Therefore, anthocyanins are considered a symptom of stress as well as it is a key player in mechanism for mitigation against adverse effects of it due to their association with a variety of environmental stressors (Hooijmaijers & Gould, 2007; Gould et al., 2008). 1.3.4.1 ROLE OF ANTHOCYANIN IN DEFENSE AGAINST ULTRAVIOLET RADIATIONS Besides their role in protecting plants from high irradiance, anthocyanin has also been linked to protect plants from UV radiations. UV radiations are classified as, Ultraviolet-A (320 to 390 nm), Ultraviolet-B (280 to 320 nm) and Ultraviolet-C (less than 280 nm). Most of the UV (B and C) radiations are absorbed by stratospheric ozone (O3). However, UV-A radiations are not filtered by O3. UV rays with high energy level have a negative impact on DNA (Hoque & Remus, 1999). Plants have developed diverse mechanisms to protect themselves and reduce the UV penetration in tissues. The biosynthesis of anthocyanin and other flavonoids is activated by UV exposure in plants. Recent studies have shown that the presence of anthocyanin for longer term have detrimental effects rather than beneficial. In an experiment on purple-leafed rice, it was observed that anthocyanin absorbs UV-A radiation, which activates photolyase, an enzyme involved in DNA repair. Such hampering of DNA repair may offset short-term gain by UV absorption (Hada et al., 2003). 1.3.4.2 ROLE OF ANTHOCYANIN IN PHOTOPROTECTION If the influx of incident light exceeds than the plant’s capacity to consume or drive away that energy an imbalanced situation is triggered. This spare excitation energy present in the photosynthetic apparatus causes a strain on chloroplast performance and adversely affects the productiveness of photosystem II which eventually result in carbon fixation reduction. In order to avoid lethal effects of excessive irradiance plants have developed a variety of morphological and physiological mechanisms, i.e., spatial orientation of leaf, intra-cellular position of chloroplast, ROS scavenging systems, squandering absorbed solar energy in the form of heat, activation of recycling of electron in photo respiratory pathways. Anthocyanins have a significant role in modifying the quantity and quality of incident light on chloroplasts. The

12

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

anthocyanins present in vegetative tissues are the red anthocyanins which show high absorbance at 550 nm and wavelength less than 400 nm however absorbance is lower for 450 nm light, while little light is absorbed at 650 nm or above (Gould et al., 2008). 1.3.4.3 ROLE OF ANTHOCYANIN AGAINST FUNGAL GROWTH Studies have shown that anthocyanin has a crucial role in protecting fruits against fruit-rot-fungi. Certain in-vitro studies have shown that plants with high concentration of anthocyanin were less prone to fruit-rot-fungi. The antifungal activity of anthocyanin may be the reason for its occurrence in vegetative tissues and roots of plants (Schaefer et al., 2008). 1.3.4.4 ROLE OF ANTHOCYANIN IN METAL CHELATING Anthocyanin has metal chelating capacity for various metals commonly found in plants. Metal chelating property of anthocyanin is due to 3’,4’-O-dihydroxyl group in the B ring of the flavonoid skeleton. Thus, metal chelating property of anthocyanin lessen the accumulation of ionized species in cell and mitigate the deleterious effect of toxic metal ions (Landi et al., 2015). 1.3.5 ROLE OF CAROTENOIDS IN TOLERANCE AGAINST DIFFERENT ENVIRONMENTAL STRESS Carotenoids (Cars) belong to a group of isoprenoids known as tetraterpenes, occurs in fruits, roots, and chloroplast in a variety of colors including orange, red, and yellow. Due to the possession of conjugated double bond in structure, Carotenoids have the ability to absorb light ranging from 350–500 nm. More than 600 Carotenoids have been identified in plants, animals, fungi, bacteria, and humans (Strzałka et al., 2003). Biochemical formulation of Carotenoids depends on the multifarious factors including plant habitat, its pattern of development and genealogy. Several studies report that if plant shows carotenoid deficiency it may suffer photodamage. Carotenoids play crucial roles against environmental stresses by: (i) dispersing excess energy influx; (ii) photoprotective and photo-oxidative role; and (iii) maintenance of molecular dynamics of membrane. That’s why expression of genes involved in cellular carotenoid biosynthesis is up-regulated if plant is facing any exogenous stresses (Esteban et al., 2015).

Plant Secondary Metabolites and Environmental Stress: An Overview

13

1.3.5.1 PHOTO-PROTECTIVE AND PHOTO-OXIDATIVE ROLE Carotenoids play a crucial in protecting photosynthetic apparatus against photo-oxidative stress in multiple ways. When the antenna system become overexcited in the presence of excessive light, carotenoids of reaction centers (b-carotenes) and light-harvesting complex (lutein and neoxanthin) have a crucial role in shielding photosynthetic apparatus against photo-oxidative stress in two ways: (i) β-carotenes directly quench triplet state of chlorophyll molecules and singlet oxygen; and (ii) xanthophyll lowers the formation of triplet chlorophyll by quenching excited singlet chlorophyll (Pandhair & Sekhon, 2006). 3 Chl* + 1 β-Car 1

Chl + 3 β-Car*

3 β-Car*

1 β-Car + Heat

During photosynthesis production of ROS in chloroplast is inevitable. This phenomenon is especially common under environmental stress conditions when photosynthetic processes are inhibited and result in unrestrained light absorption. Reduced O2 is liberated due to the transfer of electron from enzymes of ETC to molecular oxygen O2. The resultant ROS act as a strong electrophile agent and react with biological molecules, i.e., lipids, proteins, and DNA. Moreover, this singlet oxygen may cause cell death in leaves or may trigger a cascade of reactions that induce programmed cell death (PCD). Carotenoids also have a pivotal role in scavenging ROS (ROO*) by electron transfer, transfer of hydrogen atom or addition of hydrogen (Strzałka et al., 2003; Ramel, 2012). The interaction between carotenoids and singlet oxygen mostly relies on the process of physical quenching rather than chemical method. Physical process direct contact-based energy transfer. The carotenoid molecule fetches the excited electrons of nascent oxygen and convert it to molecular oxygen and itself transformed to a triplet excited state. The carotenoids will lose this acquired energy by dissipating it into surroundings and regain ground state. It is evident that the carotenoids remain chemically unaltered after each cycle, therefore, can be utilized multiple times in this energy-quenching mechanism. Carotenes and xanthophylls are the most efficient quenchers of singlet oxygen among all the carotenoids. The number of conjugated double covalent bonds present in carotenoid molecules directly correlates with the ability of carotenoids for physical quenching, which determines their lowest triplet energy level. Lycopene, an open-ring carotenoid, being the most

14

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

efficient. Lycopene possesses a singlet oxygen quenching capacity that is as two folds than β-carotene (vit-A relation) and decuple higher compared to α-tocopherol (vit-E) (Stahl & Sies, 2003). 1.3.5.2 CAROTENOIDS AND MEMBRANES Carotenoid pigments are constituents of lipid bilayer of plasma membranes of most cell types. Carotenoids possess somewhat bacillary structure often carrying a polar group at the end. Normally the molecular structure of a carotenoid makes it hydrophobic like membrane core‚ therefore carotenoids are the localized or oriented within the membrane. Hence carotenoids have an effect on the structure and dynamics of lipid membranes. Carotenoids have a potent role in maintenance of physical state of membrane, which is controlled by hydrophobic interactions between rod like ends of carotenoids and membrane (Gruszecki, 1999). Efficiency of photosynthesis depends on the mobility of charged particles across the thylakoid membrane. The physical state of the grana membrane is important for the diffusion of molecular oxygen across the membrane as well as for rummaging ROS by lipid-soluble antioxidants, such as plastoquinone, and A-tocopherol. The effectiveness of these molecular scavengers depends mainly on intensity collision between biomolecules, which is directly correlated to the membrane fluidity. Carotene in the DPPC membrane poses a fluidizing effect. The more carotene in the membrane more is fluidity and more effective is the process (Strzałka et al., 2003). 1.3.6 ROLE OF DIVERSE ALKALOIDS IN TOLERANCE AGAINST DIFFERENT ENVIRONMENTAL STRESS Alkaloids are low-weight nitrogenous compounds. They are composed of N-containing heterocyclic rings and are usually alkalescent in nature. Alkaloids are accredited for copious medicative properties they possess. These secondary plant metabolites are categorized into 20 different classes on the basis of parent molecule, e.g., tryptophan acts as a precursor for all indole alkaloids (Yang & Stöckigt, 2010). An important function played by alkaloids in plants includes augmenting reproductive capabilities in either of two ways, by improving resistances against environmental stresses or by altering the rate of pollination and seed/ fruit dispersal by animals. Alkaloids cause toxicity or bitter taste, which repel feeding herbivore or their antioxidant system may serve in damage repair (Vilariño & Ravetta, 2008; Matsuura & Fett-Neto, 2013).

Plant Secondary Metabolites and Environmental Stress: An Overview

15

1.3.6.1 TOXIC ALKALOIDS It is a common notion that alkaloid has a toxic effect against predators and pathogens. Moreover, singlet oxygen is found to be inhibited by various structural alkaloids especially, indole alkaloids. These alkaloids have a rigid, cage-like structure with a nitrogen atom in it, such as strychnine and brucine are more effective. These alkaloids also work via physical quenching mechanism, like carotenoids remain chemically unaffected during the process of quenching (Ali, 2000). Therefore, one alkaloid is sufficient for inactivation of many molecules of singlet oxygen. There are some alkaloids, like putrescine, which can be produced from polyamines. Polyamines play versatile physiological activities during the process of growth and development of plant as well as possess a potent role as scavengers of ROS and inhibit lipid peroxidation (Ali, 2000; Selmar, 2008). 1.3.6.2 ROLE OF ALKALOIDS AGAINST HERBIVORES/INSECTS Alkaloids adversely affect metabolic activities of herbivore/predators, such as enzyme’s function, DNA synthesis, and repair. Moreover, they pose strong effect on their physiological system, e.g., nervous system. Solanaceae, Papaveraceae, Apocynaceae, and Ranunculaceae are the alkaloid rich families in plants. For example, Colchicum autumnale has the ability to synthesize Colchicine. It binds with tubulin and inhibit polymerization of microtubules leading to failure of spindle apparatus organization which stops the mitosis. Colchicine proves toxic (EC50) at a concentration of 0.03%, to Apis mellifera, honeybee, if included in food. Imino sugars, also known as sugar mimicking alkaloid, work as inhibitors of glycosidases and other enzymes involved in sugar metabolism. In insects, alkaloids cause inhibition of enzymes sucrase and trehalase, present in the digestive tract and body tissues, respectively, rendering them unable to assimilate sucrose and trehalose, which results in retarded growth and toxicity. The trihydroxyindolizidine alkaloid, present in legumes is an inhibitor of αmannosidase. Caffeine, a naturally occurring compound can act as a pesticide. It hinders the activity of phosphodiesterase and causes paralysis in the insect by due to increased intracellular c-AMP level. Likewise, Sanguinarine, interfere nerve impulse transmission in variety of ways, i.e., by choline acetyltransferase inhibition, which is necessary for synthesis of acetylcholine a neurotransmitter, obstructing replication of DNA and altering activity of neuroreceptors. Alkaloids are capable of antagonizing the action of neurotransmitter by occupying binding sites on

16

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

neuroreceptors or can block/displace the cytoplasmic neurotransmitters (Mithöfer & Boland, 2012). 1.4 INVOLVEMENT OF CHALCONE AND CHALCONE SYNTHASE (CHS) IN ENVIRONMENTAL STRESS TOLERANCE Secondary metabolites are produced as byproducts of normal metabolic activities by plants; they are not necessary for growth but prove protective against toxins and insects. Chalcones are among some of these metabolites; they exhibit significant antioxidant, anti-inflammatory, and antiproliferative properties, as well as act as precursors for flavonoids and iso-flavonoids. Moreover, they guard plants against harmful UV light, pathogenic organisms and pests (Jiwrajka et al., 2016). Chalcones find application in food production and agriculture system because they provide natural immunity to plants because they have the ability to neutralize the deleterious effects produced by phytotoxicity, biological agents including a variety of microorganisms like bacteria, viruses, fungi, and helminths and insect pests. They regulate the growth of plants without any environmental hazard (Rossi, 2016). 1.4.1 ANTIVIRAL ACTIVITY OF CHALCONES Chalcones show significant antiviral activity, for example, against tomato ringspot virus (ToRSV). In a study conducted on Chenopodium quinoa, 2-hydroxychalcone was found weak inhibitor of ToRSV infection. In another study, more than 50% antiviral activity was reported by 21 different chalcones. During this study, it was found that antiviral activity of chalcones can be altered, it is upregulated by hydroxylation of the ring A at carbon 2’,3’,4’ and ring B at carbon 4’, on the other hand it is inhibited by if carbon 5’ undergoes hydroxylation and is reduced if B ring experiences methoxylation (Rozmer & Perjési, 2016; Malhotra et al., 1996). 1.4.2 ANTIFUNGAL ACTIVITY Chalcones are lethal to a wide variety of plant pathogens that are responsible economic losses of arable land worldwide. Chalcone exhibit more potent antifungal properties as compared to commercial fungicides against U. scitaminea, C. falcatum, C. paradoxa, P. atropurpurea, F. moniliforme, and C. pallescens. For example, DMC chalcone and stercurensin obtained from the tissues of plant of Myrica serrata, were found to cease the progression of

Plant Secondary Metabolites and Environmental Stress: An Overview

17

fungus C. cucumerinum, a pathogen of cucumber. Additionally, natural chalcones isolated from Zuccagnia punctata (Fabaceae) shows adverse effect on growth of the disease-causing fungal strains including P. longicolla, A. alternate, F. graminearum, F. equiseti, F. verticillioides, C. truncatum and S. bataticola (Rozmer & Perjési, 2016; Díaz-Tielas et al., 2014). 1.4.3 NEMATICIDES, INSECT DETERRENTS, AND ANTIFEEDANTS Chalcones are extremely noxious against nematodes parasites affecting plants, e.g., trans-chalcone was found to kill (nematicide) or stop the growth (nematostatic) of potato cyst nematodes. Some synthetic chalcones, for example, chalcone (2E)-1-(4’-nitrophenyl)-3(2,4,5-trimethoxyphenyl) prop2-en-1-one can halt progression of a coffee crop pathogen Meloidogyne exigua. The mechanism underlying this inhibition involves inactivation of caffeic acid 3-O-methyltransferase (Nunes et al., 2013). The majority of agricultural losses are caused by pest belonging to insects. The redox activity of ring A & B accounts for enhanced antibacterial effectiveness of chalcones against pathogenic strains. Plutella xylostella (diamondback moth) is amongst the most catastrophic pests of cabbage family (Cruciferae). Some chalcones are found to be effective against this moth (Kumar et al., 2012). Lonchocarpin, derricin, derricidin, and isocordoin, chalcones isolated from Lonchocarpus neuroscapha, exhibit inhibitory effect against larvae of Spodoptera species. Furthermore, Chalcone derivatives act as antifeedant agents against larvae of Achaea janata, which feeds on Brassica and Ficus (Thirunarayanan & Vanangamudi, 2014). Chalcones are phytotoxic compounds affecting a variety of weed plants Slight differences of chalcones structure may exhibit different biological activity attributed to the variations in number and position of free hydroxyl groups in this molecule with different phytotoxic effects, i.e., kukulcanin B (2’,4’,4-trihydroxy-3’-methoxychalcone) and heliannone A (2’,4-dihydroxy-3’,4’-dimethoxychalcone) showed inhibited shoot growth and inhibited germination of L. esculentum respectively (Díaz-Tielas et al., 2014). Chalcones can act as selective bioherbicides in a variety of agricultural systems. We need to select a compound which exhibits high herbicidal activity against weeds at the lower concentration being non-toxic to the crops. For example, trans-chalcone (1,3-diphenyl-2-propen-1-one) is effective against a variety of weeds but did not harm the related crop species. Trans-chalcone could be used for weed control in the following agricultural

18

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

systems: Oryza sativa-Echinochloa crus-Galli, Zea mays-Amaranthus retroflexus, and Triticum aestivum-Plantago lanceolata (Díaz-Tielas et al., 2014; Yun et al., 2009). Studies have shown that chalcone has an inhibitory effect on two major enzymes of lignin biosynthesis, namely phenylalanine ammonia ligase and the 4-coumarate: CoA ligase (4CL). Lignin synthesis is important phenomenon in plant development, any impairment in these enzymes will result in lower lignin synthesis, or may completely block the process, consequently, lead to the inhibited plant growth. Moreover, a correlation between the inhibited root growth and declined activity of root peroxidases was demonstrated which have a role in lignin biosynthesis and ROS production, both compounds are key regulators for cellular growth and differentiation (DíazTielas et al., 2014; Chen et al., 2011). 1.4.4 CHALCONE SYNTHASE (CHS) Chalcone synthase (CHS) is a vital enzyme in the biosynthesis of flavonoid/ isoflavonoid pathway. In addition to plant developmental process, CHS gene expression is prompted in plants under biotic and abiotic stresses such as UV light, bacterial, and fungal infection (Dao et al., 2011). 1.4.5 PHYTOALEXINS These are antimicrobial metabolites produced in response to microbial stress. Phytoalexins are produced from various classes of metabolites, i.e., flavonoids, stilbenoids, sesquiterpenoids, steroids, and alkaloids. Additionally, CHS helps the plant to produce more flavonoids, isoflavonoid-type phytoalexins and other relevant metabolites to protect plants against stress. Phytoalexin accumulation has been seen in many plant species, in response to pathogen attack, and their importance as antimicrobial phytoalexins is well known. Studies has shown phytoalexin flavonoid in legumes, cereals, sorghum, rice, Cephalocereus senilis, Beta vulgaris, and some isoflavonoids in Lupin luteus after infection with Fusarium oxysporum (Dao et al., 2011). 1.4.6 PHYTOANTICIPINS Phytoanticipins are low molecular weight antimicrobial compounds; however, there is no clear demarcation between phytoalexins and phytoanticipins compounds. Phytoanticipins are classed into several chemical groups, such as flavonoids, terpenoids, steroids, glucosinolates, and alkaloids. In

Plant Secondary Metabolites and Environmental Stress: An Overview

19

plants, they enhance colors and attract insects, thereby increasing pollination and seed dispersal, protect against the harmful effects of light, furthermore phytoanticipins show antiviral and antimicrobial activities (Dao et al., 2011). CHS expression causes accumulation of flavonoid which results in inhibition of polar auxin transport, thereby causing a local buildup of auxin, which induces nodule growth and development. Inhibition of auxin transport also increases the resistance against Fusarium oxysporum (Dao et al., 2011). 1.4.7 LIGHT PROTECTION Expression of CHS genes is synchronized by light via a photoreceptormediated mechanism. Receptors of UV A or B light when activated by light, upregulate the expression of CHS gene. Activation of CHS enzyme leads to accumulation of visibly detectable levels of anthocyanin pigments. In response to light intensity, anthocyanins play a role as sunscreen. Phenolic compounds like flavonoids strongly absorb UV light and thus are able to protect plants from DNA damage caused by UV (Dao et al., 2011). 1.5 GENETIC ENGINEERING OF SECONDARY METABOLITES FOR ENHANCED STRESS TOLERANCE Being sessile plants are unable to escape environmental stresses that may adversely affect their growth and yield. Therefore, they have adopted physiological and biochemical mechanisms to overcome the damaging effects of these stresses. One of these defense mechanisms is the production of secondary metabolites. Secondary metabolites protect plants against both biotic (predators/herbivores) and abiotic (drought, salinity, and temperature) stress (Ahanger et al., 2020). Mostly biosynthetic pathways yielding secondary metabolites are multistage processes assisted by enzymes and complex regulatory mechanisms at transcriptional and/or posttranscriptional level. Therefore, industrial production of secondary compounds is an enormously intricate procedure (Sheludko, 2010). Biotechnology offers great potential of improving crop traits, quality, and their protection. Specific desired traits can be integrated successfully in any plant through genetic engineering. Genetic engineering involves transferring a gene of interest from any source (plants, animals, microorganisms or even artificially synthesized genes) across taxonomic boundaries, in host plant genome in the form of recombinant DNA molecule generated by ligating desired gene

20

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

with a suitable vector, to impart a new economically valuable traits to that plant. Transgenic technology is regarded as the fastest growing technology in agriculture (Parmar et al., 2017). It may involve induced mutagenesis and recombination brought about by protoplast fusion and other approaches like improving precursor concentration or synthesis of rate-limiting enzymes of SM biosynthesis pathway, controlling regulatory genes, transforming the transcription and translation machinery and knocking out genes for competing pathways (Baltz, 2016). The major advantages of transgenic technology are that the genes controlling desirable traits can be sourced from any background —plants or microorganisms, etc., and can be incorporated into the target plant being transformed with ease. Plant biotechnology is an area of focus, since the commercialization of ‘Flavr-Savr’ first ever GM crop, tomato with improved shelf-life. Plants with insect-pest resistance and herbicide tolerance has successfully commercialized while ongoing research focuses on virus resistance and male sterility, etc. Papaya crops has been GM against papaya ring spot virus. With advancement in rDNA technology, various genes have been incorporated genes for biotic and abiotic stress tolerance/resistance (Parmar et al., 2017). KEYWORDS • • • • • • • •

abiotic stress catalyzes this reaction climate change environmental changes greenhouse gases nanotechnology phenolics phenylalanine ammonia-lyase

REFERENCES Ahanger, M. A., Bhat, J. A., Siddiqui, M. H., Rinklebe, J., & Ahmad, P., (2020). Integration of silicon and secondary metabolites in plants: A significant association in stress tolerance. Journal of Experimental Botany, 71(21), 6758–6774.

Plant Secondary Metabolites and Environmental Stress: An Overview

21

Aharoni, A., & Galili, G., (2011). Metabolic engineering of the plant primary-secondary metabolism interface. Current Opinion in Biotechnology, 22, 239–244. Ahkami, A. H., Wang, W., Wietsma, T. W., Winkler, T., Lange, I., & Jansson, C., (2019). Metabolic shifts associated with drought-induced senescence. Brachypodium. Plant Science, 289, 110278. Akula, R., & Ravishankar, G. A., (2011). Influence of abiotic stress signals on secondary metabolites in plants. Plant Signaling & Behavior, 6(11), 1720–1731. Ali, R. M., (2000). Role of putrescine in salt tolerance of Atropa belladonna plant. Plant Science, 152(2), 173–179. Baltz, R. H., (2016). Genetic manipulation of secondary metabolite biosynthesis for improved production in Streptomyces and other actinomycetes. Journal of Industrial Microbiology and Biotechnology, 43(2, 3), 343–370. Bartwal, A., Mall, R., Lohani, P., Guru, S. K., & Arora, S., (2013). Role of secondary metabolites and brassinosteroids in plant defense against environmental stresses. Journal of Plant Growth Regulation, 32(1), 216–232. Ben-Abdallah, S., Zorrig, W., Amyot, L., Renaud, J., Hannoufa, A., Lachâal, M., & KarrayBouraoui, N., (2019). Potential production of polyphenols, carotenoids and glycoalkaloids in Solanum villosum mill. under salt stress. Biologia., 74, 309–324. Biala, W., & Jasinski, M., (2018). The phenylpropanoid case – It is transport that matters. Frontiers in Plant Science, 1(9), 1610. Boncan, D. A. T., Tsang, S. S. K., Li, C., Lee, I. H. T., Lam, H., Chan, T., & Hui, J. H. L., (2020). Terpenes and terpenoids in plants: Interactions with environment and insects. International Journal of Molecular Sciences, 21, 7382. Bryant, J. P., Chapin, F. S. I., & Klein, D. R., (1983). Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos, 40, 357–368. Cetinkaya, H., Kulak, M., Karaman, M., Karaman, H. S., & Kocer, F., (2017). Flavonoid accumulation behavior in response to the abiotic stress: Can a uniform mechanism be illustrated for all plants? In: Goncalo, C. J., (eds.), Flavonoids - From Biosynthesis to Human Health. CHEN, W. J., YUN, M. S., Deng, F., & Yogo, Y., (2011). Chalcone suppresses lignin biosynthesis in illuminated soybean cells. Weed Biology and Management, 11(1), 49–56. Cingoz, G. S., & Gurel, E., (2016). Effects of salicylic acid on thermotolerance and cardenolide accumulation under high temperature stress in Digitalis trojana ivanina. Plant Physiology and Biochemistry, 105, 145–149. Dao, T. T. H., Linthorst, H. J. M., & Verpoorte, R., (2011). Chalcone synthase and its functions in plant resistance. Phytochemistry Reviews, 10(3), 397–412. Del, P. V. M., & Ravetta, D. A., (2008). Tolerance to herbivory in lupin genotypes with different alkaloid concentration: Interspecific differences between Lupinus albus L. and L. angustifolius L. Environmental and Experimental Botany, 63(1–3), 130–136. Díaz-Tielas, C., Graña, E., Reigosa, M. J., & Sánchez-Moreiras, A. M., (2016). Biological activities and novel applications of chalcones. Planta Daninha, 34(3), 607–616. Díaz-Tielas, C., Sotelo, T., Graña, E., Reigosa, M. J., & Sánchez-Moreiras, A. M., (2014). Phytotoxic potential of trans-chalcone on crop plants and model species. Journal of Plant Growth Regulation, 33(2), 181–194. Disch, A., Hemmerlin, A., Bach, T. J., & Rohmer, M., (1998). Mevalonate-derived isopentenyl diphosphate is the biosynthetic precursor of ubiquinone prenyl side chain in tobacco BY-2 cells. Journal of Biochemistry, 331(2), 615–621.

22

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Dötterl, S., Jurgens, A., Seifert, K., Laube, T., Weissbecker, B., & Schutz, S., (2006). Nursery pollination by a moth in Silene latifolia: The role of odors in eliciting antennal and behavioral responses. New Phytology, 169, 707–718. Dresselhaus, T., & Huckelhoven, R., (2018). Biotic and abiotic stress response in crop plants. Agronomy, 8(267), 1–6. Dudareva, N., Negre, F., Nagegowda, D. A., Orlova, I., & Negre-Zakharov, F., (2006). Plant volatiles: Recent advances and future perspectives. Critical Reviews in Plant Science, 25, 417–440. Esteban, R., Moran, J. F., Becerril, J. M., & García-Plazaola, J. I., (2015). Versatility of carotenoids: An integrated view on diversity, evolution, functional roles and environmental interactions. Environmental and Experimental Botany, 119, 63–75. Gershenzon, J., & Dudareva, N., (2007). The function of terpene natural products in the natural world. Nature Chemical Biology, 3, 408–414. Godoy, F., Olivos-Hernandez, K., Stange, C., & Handford, M., (2021). Abiotic stress in crop species: Improving tolerance by applying plant metabolites. Plants, 10(2), 186. Gould, K., Davies, K. M., & Winefield, C., (2008). Anthocyanins: Biosynthesis, Functions, and Applications. Springer Science & Business Media. Gruszecki, W. I., (1999). Carotenoids in membranes. In: The Photochemistry of Carotenoids (pp. 363–379). Springer, Dordrecht. Hada, H., Hidema, J., Maekawa, M., & Kumagai, T., (2003). Higher amounts of anthocyanins and UV‐absorbing compounds effectively lowered CPD photorepair in purple rice (Oryza sativa L.). Plant, Cell & Environment, 26(10), 1691–1701. Hamann, T., (2012). Plant cell wall integrity maintenance as an essential component of biotic stress response mechanisms. Frontiers in Plant Science, 3, 77. Holopainen, J. K., Himanen, S. J., Yuan, J. S., Chen, F., & Stewart, C. N., (2013). Ecological Functions of Terpenoids in Changing Climates (pp. 2913–2940). Natural Products, Springer Science and Business Media LLC: Berlin/Heidelberg, Germany. Honey, J. D., Gosz, J. R., & Cates, R. G., (1988). The role of carbon-based plant secondary metabolites in decomposition in terrestrial ecosystem. The American Naturalist, 132(6), 869–883. Hooijmaijers, C. A. M., & Gould, K. S., (2007). Photo-protective pigments in red and green gametophytes of two New Zealand liverworts. New Zealand Journal of Botany, 45(3), 451–461. Hoque, E., & Remus, G., (1999). Natural UV‐screening mechanisms of Norway spruce (Picea abies [L.] Karst.) needles. Photochemistry and Photobiology, 69(2), 177–192. Jiwrajka, M., Phillips, A., Butler, M., Rossi, M., & Pocock, J. M., (2016). The plant-derived chalcone 2, 2′, 5′-trihydroxychalcone provides neuroprotection against toll-like receptor 4 triggered inflammation in microglia. Oxidative Medicine and Cellular Longevity, 2016. Kasahara, H., Hanada, A., Kuzuyama, T., Takagi, M., Kamiya, Y., & Yamaguchi, S., (2002). Contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthesis of gibberellins in Arabidopsis. The Journal of Biological Chemistry, 277(47), 45188–45194. Kaur, G., Kumar, S., Nayyar, H., & Upadhyaya, H. D., (2008). Cold stress injury during the pod-filling phase in chickpea (Cicer arietinum L.): Effects on quantitative and qualitative components of seeds. Journal of Agronomy and Crop Science, 194(6), 457–464. Keiffer, M., Neve, J., & Kepinski, S., (2010). Defining auxin response context in plants development. Current Opinion in Plant Biology, 13(1), 12–20.

Plant Secondary Metabolites and Environmental Stress: An Overview

23

Kobayashi, K., Suzuki, M., Tang, J., Nagata, N., Ohyama, K., Seki, H., Kiuchi, R., et al., (2007). Lovastatin insensitive 1-a novel pentatricopeptide repeat protein, is a potential regulatory factor of isoprenoid biosynthesis in Arabidopsis. Plant and Cell Physiology, 48(2), 322–331. Kovácik, J., Klejdus, B., Hedbavny, J., Štork, F., & Backor, M., (2009). Comparison of cadmium and copper effect on phenolic metabolism, mineral nutrients and stress-related parameters in Matricaria chamomilla plants. Plant and Soil, 320(1), 231–242. Kumar, R., Sharma, P., Shard, A., Tewary, D. K., Nadda, G., & Sinha, A. K., (2012). Chalcones as promising pesticidal agents against diamondback moth (Plutella xylostella): Microwaveassisted synthesis and structure-activity relationship. Medicinal Chemistry Research, 21(6), 922–931. Landi, M., Tattini, M., & Gould, K. S., (2015). Multiple functional roles of anthocyanins in plant-environment interactions. Environmental and Experimental Botany, 119, 4–17. Le Quere, C., Raupach, M. R., Canadell, J. G., Marland, G., & Bopp, L., (2009). Trends in the sources and sinks of carbon dioxide. Nature Geoscience, 2, 831–836. Liu, Y., Tikunov, Y., Schouten, R. E., Marcelis, L. F., Visser, R. G., & Bovy, A., (2018). Anthocyanin biosynthesis and degradation mechanisms in solanaceous vegetables: A review. Frontiers in Chemistry, 6, 52. Macherous, P., Schmid, J., Amrhein, N., & Schaller, A., (1999). A unique reaction in a common pathway: Mechanism and function of chorismate synthase in the shikimate pathway. Planta, 207, 325–334. Mahdavi, V., Farimani, M. M., Fathi, F., & Ghassempour, A., (2015). A targeted metabolomics approach toward understanding metabolic variations in rice under pesticide stress. Analytical Biochemistry, 478, 65–72. Malhotra, B., Onyilagha, J. C., Bohm, B. A., Towers, G. H. N., James, D., Harborne, J. B., & French, C. J., (1996). Inhibition of tomato ringspot virus by flavonoids. Phytochemistry, 43(6), 1271–1276. Matsuura, H. N., & Fett-Neto, A. G., (2015). Plant alkaloids: Main features, toxicity, and mechanisms of action. Plant Toxins, 2(7), 1–15. McELROY, J. S., & Kopsell, D. A., (2009). Physiological role of carotenoids and other antioxidants in plants and application to turfgrass stress management. New Zealand Journal of Crop and Horticultural Science, 37(4), 327–333. Mishra, B., Sangwan, R. S., Mishra, S., Jadaun, J. S., Sabir, F., & Sangwan, N. S., (2014). Effect of cadmium stress on inductive enzymatic and nonenzymatic responses of ROS and sugar metabolism in multiple shoot cultures of ashwagandha (Withania somnifera Dunal). Protoplasma, 251, 1031–1045. Mithöfer, A., & Boland, W., (2012). Plant defense against herbivores: Chemical aspects. Annual Review of Plant Biology, 63, 431–450. Mittler, R., & Blumwald, E., (2010). Genetic engineering for modern agriculture. Annual Review of Plant Biology, 61, 443–462. Naikoo, M. I., Dar, M. I., Raghib, F., Jaleel, H., Ahmad, B., Raina, A., Khan, F. A., & Naushin, F., (2019). Role and regulation of plants phenolics in abiotic stress tolerance: An overview. In: Plant Signaling Molecules (pp. 157–168). Elsevier: Amsterdam, The Netherlands. Nazar, R., Iqbal, N., Syeed, S., & Khan, N. A., (2011). Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. Journal of Plant Physiology, 168, 807–815.

24

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Nunes, A. S., Campos, V. P., Mascarello, A., Stumpf, T. R., Chiaradia-Delatorre, L. D., Machado, A. R. T., Júnior, H. M. S., et al., (2013). Activity of chalcones derived from 2, 4, 5-trimethoxybenzaldehyde against Meloidogyne exigua and in silico interaction of one chalcone with a putative caffeic acid 3-O-methyltransferase from Meloidogyne incognita. Experimental Parasitology, 135(4), 661–668. Panche, A. N., Diwan, A. D., & Chandra, S. R., (2016). Flavonoids: An overview. Journal of Nutritional Science, 5, e47. Pandhair, V., & Sekhon, B. S., (2006). Reactive oxygen species and antioxidants in plants: An overview. Journal of Plant Biochemistry and Biotechnology, 15(2), 71–78. Parmar, N., Singh, K. H., Sharma, D., Singh, L., Kumar, P., Nanjundan, J., Khan, Y. J., et al., (2017). Genetic engineering strategies for biotic and abiotic stress tolerance and quality enhancement in horticultural crops: A comprehensive review. 3 Biotech, 7(4), 1–35. Perreca, E., Rohwer, J., Gonzalez-Cabanelas, D., Loreto, F., Schmidt, A., Gershenzon, J., & Wright, L. P., (2020). Effect of drought on the methylerythritol 4-phosphate (MEP) pathway in the isoprene emitting conifer Picea glauca. Frontiers in Plant Science, 11, 548296. Pietta, P. G., (2000). Flavonoids as antioxidants. Journal of Natural Products, 63(7), 1035–1042. Ramel, F., Birtic, S., Ginies, C., Soubigou-Taconnat, L., Triantaphylidès, C., & Havaux, M., (2012). Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proceedings of the National Academy of Sciences, 109(14), 5535–5540. Ross, J. A., & Kasum, C. M., (2002). Dietary flavonoids: Bioavailability, metabolic effects and safety. Annual Review of Nutrition, 22, 19–34. Rossi, M., (2016). The Plant-Derived Chalcone 2, 2′, 5′-Trihydroxychalcone Provides Neuroprotection Against Toll-Like Receptor 4 Trig. Rozmer, Z., & Perjési, P., (2016). Naturally occurring chalcones and their biological activities. Phytochemistry Reviews, 15(1), 87–120. Samec, D., Karalija, E., Sola, I., Vujcic, B. V., & Salopek-Sondi, B., (2021). The role of polyphenols in abiotic stresses response: The influence of molecular structure. Plants, 10(1), 118. Schaefer, H. M., Rentzsch, M., & Breuer, M., (2008). Anthocyanins reduce fungal growth in fruits. Natural Product Communications, 3(8), 1934578X0800300808. Selmar, D., (2008). Potential of salt and drought stress to increase pharmaceutical significant secondary compounds in plants. Agricultural Research in Volkenrode, 58(1, 2)139. Sewelam, N., Kazan, K., & Schenk, P. M., (2016). Global plant stress signaling: Reactive oxygen species at the crossroad. Frontiers in Plant Science, 7, 187. Shahzad, B., Tanveer, M., Zhao, C., & Rehman, A., (2017). Role of 24-epibrassinolide (EBL) in mediating heavy metal and pesticide-induced oxidative stress in plants: A review. Ecotoxicology and Environmental Safety, 147, 935–944. Sharma, A., Kumar, V., Singh, R., Thukral, A. K., & Bhardwaj, R., (2016). Effect of seed pre-soaking with 24-epibrassinolide on growth and photosynthetic parameters of Brassica juncea L. in imidacloprid soil. Ecotoxicology & Environmental Safety, 133, 195–201. Sharma, A., Shahzad, B., Rehman, A., Bhardwaj, R., Landi, M., & Zheng, B., (2019). Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules, 24(2452), 1–22. Sharma, A., Thakur, S., Kumar, V., Kanwar, M. K., Kesavan, A. K., Thukral, A. K., Bhardwaj, R., et al., (2016). Pre-sowing seed treatment with 24-epibrassinolide ameliorates pesticide

Plant Secondary Metabolites and Environmental Stress: An Overview

25

stress in Brassica juncea L. through the modulation of stress markers. Frontiers in Plant Science, 7, 1569. Sharma, A., Yuan, H., Kumar, V., Ramakrishnan, M., Kohli, S. K., Kaur, R., Thukral, A. K., et al., (2019). Castasterone attenuates insecticide induced phytotoxicity in mustard. Ecotoxicology & Environmental Safety, 179, 50–61. Sheludko, Y. V., (2010). Recent advances in plant biotechnology and genetic engineering for production of secondary metabolites. Cytology and Genetics, 44(1), 52–60. Skorupinska-Tudek, K., Poznanski, J., Wojcik, J., Bienkowski, T., Szostkiewicz, I., ZekmanFemiak, M., Bajda, A., et al., (2008). Contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthesis of dolichols in plants. The Journal of Biological Chemistry, 283(30), 21024–21035. Stahl, W., & Sies, H., (2003). Antioxidant activity of carotenoids. Molecular Aspects of Medicine, 24(6), 345–351. Strzałka, K., Kostecka-Gugała, A., & Latowski, D., (2003). Carotenoids and environmental stress in plants: Significance of carotenoid-mediated modulation of membrane physical properties. Russian Journal of Plant Physiology, 50(2), 168–173. Thirunarayanan, G., & Vanangamudi, G., (2014). Synthesis, spectral studies, antimicrobial and insect antifeedant activities of some substituted styryl 4′-fluorophenyl ketones. Arabian Journal of Chemistry, 7(6), 1055–1064. Tobe, K., Zhang, L., Qiu, G. Y., Shimizu, H., & Omasa, K., (2001). Characteristics of seed germination in five non-halophytic Chinese desert shrub species. Journal of Arid Environments, 47(2), 191–201. Vogt, T., (2010). Phenylpropanoid biosynthesis. Molecular Plant, 3, 2–20. Weng, J., & Chapple, C., (2010). The origin and synthesis of lignin biosynthesis. New Phytologist, 187, 273–285. Yang, L., & Stöckigt, J., (2010). Trends for diverse production strategies of plant medicinal alkaloids. Natural Product Reports, 27(10), 1469–1479. Yazaki, K., Arimura, G. I., & Ohnishi, T., (2017). ‘Hidden’ terpenoids in plants: Their biosynthesis, localization and ecological roles. Plant Cell Physiology, 58, 1615–1621. YUN, M. S., Chen, W., Deng, F., & Yogo, Y., (2009). Selective growth suppression of five annual plant species by chalcone and naringenin correlates with the total amount of 4‐ coumarate: Coenzyme A ligase. Weed Biology and Management, 9(1), 27–37. Zhang, Y., Butelli, E., Alseekh, S., & Tohge, T., (2015). Multi-level engineering facilitates the production of phenylpropanoid compounds in tomato. Nature Communications, 6, 8635. Zhu, J. K., (2016). Abiotic stress signaling and responses in plants. Cell, 167, 313–324.

CHAPTER 2

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway in Environmental Stress Response

ANAMIKA PAUL,1 KRISHNENDU ACHARYA,2 and NILANJAN CHAKRABORTY1*

Scottish Church College, Department of Botany, Kolkata – 700006, West Bengal, India

1

Molecular and Applied Mycology and Plant Pathology Laboratory, Department of Botany, University of Calcutta, Kolkata – 700019, West Bengal, India

2

*

Corresponding author. E-mail: [email protected]

ABSTRACT The shikimic acid and phenylpropanoid pathways are two interlinked pathways for a large number of secondary metabolites biosynthesis of plants. The shikimic acid pathway involves the condensation of erythrose-4-phosphate (E4P) and phosphoenolpyruvate (PEP), and it ends with the formation of three aromatic amino acids. Among them, L-phenylalanine serves as a precursor of the phenylpropanoid pathway. Through phenylpropanoid pathway, several phenolic compounds like phenolic acids, flavonoids, monolignols, lignins, coumarins, anthocyanins, and condensed tannins are derived either directly or from many branches of this pathway (like flavonoid biosynthesis pathway and monolignol pathway). The production of such secondary metabolite is not only included for a broad range of applications in humankind, but also these are some eminent plants derived unique compounds that have a role in Biology and Biotechnology of Environmental Stress Tolerance in Plants: Secondary Metabolites in Environmental Stress Tolerance, Volume 1. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

28

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

building defense responses in plants under the stresses. Hence, for resisting the environmental stresses like drought, temperature, UV-radiation, heavy metals, etc., plants exhibit responses via modification in the biosynthesis pathways by altering the gene expression or regulating enzymes activities, and alteration of their secondary metabolites production. Nowadays, abiotic stresses are in the pinpoint of focus by scientific communities and in this present chapter an updated information regarding potential roles of these two important pathways against challenging environmental circumstances has been focused. 2.1 INTRODUCTION Plant faces a number of stresses in their entire life. Plant stresses are categorized as abiotic and biotic stresses, where abiotic stresses are imposed by environmental factors that may be chemical or physical, and biotic stresses are created by biological organisms. Although, these are the main reasons for the reduction in annual productivity by the plants. On the other hand, stresses have a major role in triggering a wide variety of plant responses like exhibition of cellular metabolic dysfunctions, alteration in gene expression, prevents seed formation and flowering, induce senescence, etc. (Gull et al., 2019; Verma et al., 2013). About 100 years ago, it was reported that primary metabolites (carbohydrates, proteins, vitamins, amino acids, etc.) play an important role in cell growth and division, photosynthesis, respiration, as well as in reproduction (Bourgaud et al., 2001). Thereafter, Kossel (1891) was the first scientist who has first discloses that the roles of secondary metabolites (SMs) are opposed to the primary metabolites. Then the plant biology was introduced about the concept of secondary metabolites (Akhi et al., 2021; Kossel, 1891). Metabolites are so-called because they are the products of metabolism. The SMs are plant-produced an unlimited and diverse range of organic compounds, majority of them do not take part directly in plant growth and development, but they give support against stresses. SMs are limited in some taxonomic groups within plant kingdom (Jain et al., 2019). Among the three principal kinds of SMs of plants ((i) phenolic compounds; (ii) terpenoids/isoprenoids; and (iii) alkaloids and glucosinolates), phenolic compounds are synthesized through shikimic acid, phenylpropanoid pathway and many other branches of pathways in plants (Aharoni et al., 2011; Macheroux et al., 1999). Plant produced polyphenols are a specialized class of SMs that responses

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

29

throughout the life cycle of plant, including stresses. It was established by the researchers that phenylpropanoid biosynthetic pathway found to be activated to play an important role under many harmful environmental conditions like drought, salinity, heavy metal stresses, extreme temperatures, and ultraviolet radiations. To response in stress condition, plant as a sessile organism, make changes in genetic patterns of protein synthesis and metabolites biosynthesis that involved in the interaction between plant and environment. These alterations of pathway due to stresses may result in accumulation of a variety of phenolic compounds (Linić et al., 2019; Sharma et al., 2019a). This chapter deals with the response of shikimic acid/phenylpropanoid pathway against environmental stress factors. The pathways are controlled by the gene expressions and enzymatic reactions, which give to the result in the alteration of phenolic compounds production and accumulation. 2.2 SHIKIMIC ACID PATHWAY AND PHENYLPROPANOID PATHWAY: MULTI-STEP BIOSYNTHETIC PATHWAYS OF PHENOLIC COMPOUNDS IN PLANTS Shikimic acid pathway and phenylpropanoid pathway are two interlinked pathways for a large number of SMs biosynthesis of plants. These are interlinked because the end product of mostly occurring shikimic acid pathway is L-phenylalanine (L-Phe), which acts as precursor of phenylpropanoid pathway (Bond et al., 2016; Santos-Sánchez et al., 2018). Shikimic acid pathway and phenylpropanoid pathway are localized in the chloroplast (Macheroux et al., 1999) and plastid (Richards et al., 2006) of plants, respectively. These two interconnected pathways either directly or with the help of their side branches (like flavonoid biosynthesis pathway and monolignol pathway) may produce a lot of phenolic compounds in their different steps (Aharoni et al., 2011; Macheroux et al., 1999). Phenolic compounds of plants are the main components of plant SMs production through some extended pathways. Whereas phenolic compounds are mainly divided into phenolic acids and polyphenol (Harborne et al., 1999; Minatel et al., 2017). The prime phenolic compounds synthesized from L-Phe are phenolic acids, coumarins, cinnamic acids and esters, chalcones, flavonoids, isoflavonoids, neoflavonoids, monolignols, lignins, anthocyanins, and condensed tannins (Cheynier et al., 2013; Santos-Sánchez et al., 2018).

30

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

2.2.1 SHIKIMIC ACID PATHWAY Shikimic acid pathway is an important pathway which linked primary and SMs production by providing aromatic amino acids (Macheroux et al., 1999). This is so named because the shikimic acid was first isolated from the Japanese shikimi fruit (Illicium religiosum) in 1886 by Eykman (Eykman, 1886). Shikimic acid pathway shows seven steps of reactions to produce chorismate or chorismic acid as the end-product (Maeda & Dudareva, 2012). All the steps of the shikimic acid pathway are shown in Figure 2.1. In the first step of reaction, 3-deoxy-D-arabinoheptulosonate-7-phosphate (DAHP) has been produced by an aldol-type condensation of phosphoenolpyruvate (PEP) and E4P, and the reaction is catalyzed by 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase (DAHPS; EC 4.1.2.15, now EC 2.5.1.54). Where, the source of PEP is from the glycolytic pathway and E4P is a carbohydrate which came from the pentose phosphate cycle (Santos-Sánchez et al., 2018; Zhang et al., 2012). In the second step, 3-dehydroquinate synthase (DHQ synthase) (DHQS; EC 4.2.3.4) catalyzes the step to form a cyclohexane derivative 3-dehydroquinate (DHQ). Besides these two steps, the next remaining steps are required for the adhesion of two of the three double bonds and side chains to convert DHQ (a cyclohexane) into a benzene ring (the main feature of an aromatic compound). In the third step, the dehydration of dehydroquinate occurs in the presence of DHQ dehydratase (DHD) (EC 4.2.1.10) enzyme to produce 3-dehydroshikimate (DHS). The fourth reaction is a reversible reduction step, where DHS is reduced using NADPH into shikimate or shikimic acid, i.e., catalyzed by shikimate-5-dehydrogenase (SDH) (EC 1.1.1.25). DHD and SDH show their monofunctional nature in Escherichia coli but bifunctional nature in their fused form (DHD-SDH enzyme) was observed in plants. In the fifth step, shikimate-3-phosphate produced by using ATP as substrate for the phosphorylation of shikimate at its C3 hydroxyl group. This step is catalyzed by shikimate kinase (SK; EC 2.7.1.71). In the sixth step of reaction, 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS; EC 2.5.1.19) transfer the enolpyruvyl moiety of phosphoenolpyruvate into shikimate-3-phosphate to generate 5-enolpyruvylshikimate-3-phosphate (EPSP). Among these seven steps, chorismate synthase (CS; EC 4.2.3.5) is the final enzyme of the shikimic acid pathway that converts EPSP into chorismate or chorismic acid. In this step, chorismate is produced by establishing a second double bond in the ring, which cause due to the

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

31

elimination of C6-pro-R hydrogen from EPSP and 1,4-anti-elimination of the 3-phosphate (Jan et al., 2021; Maeda & Dudareva, 2012; Zhang et al., 2012). In the higher plants, chorismate is the precursor of three important aromatic amino acids (tryptophan, tyrosine, and phenylalanine) that are used for the generation of several SMs, tetrahydrofolate (vitamin B9) and phylloquinone (vitamin K1). Very few steps are there for generation of tryptophan, tyrosine, and phenylalanine from the chorismate and some of the important enzymes take parts in the reactions are chorismate mutase, anthranilate synthase, others are iso-chorismate synthase, and aminodeoxychorismate synthase (Tzin & Galili, 2010a).

FIGURE 2.1  Shikimic acid biosynthetic pathway in plants. Note: DAHPS: 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase; DHQS: 3-dehydroquinate synthase; DHD: 3-dehydroquinate dehydratase; SDH: Shikimate-5-dehydrogenase; SK: Shikimate kinase; EPSPS: 5-enolpyruvylshikimate-3-phosphate synthase; CS: Chorismate synthase.

32

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

2.2.2 PHENYLPROPANOID PATHWAY On the basis of the presence of end products of the shikimic acid pathway, the phenylpropanoid pathway can metabolites a vast range of SMs (Vogt, 2010). Microorganisms can only synthesize aromatic amino acids L-phenylalanine (L-Phe), L-tryptophan (L-Trp), and L-tyrosine (L-Tyr) as end products of shikimic acid pathway for protein biosynthesis. Whereas plants are used these amino acids as precursors for the production of several SMs that play crucial role in plant growth and immune response (Tzin & Galili, 2010b; Weaver & Herrmann, 1997). The products, produced by the phenylpropanoid pathway are involved in many stages of plant growth and giving structural supports, as well as in many other activities to help the plant to live on the land (Biala & Jasiński, 2018). These SMs are not only play a fundamental role in various abiotic stress response like heavy metal stress, drought, salinity (Sharma et al., 2019a), pesticide toxicity (Mahdavi et al., 2015), but also used as mediators for interaction of plant with other organisms (Jan et al., 2021). L-phenylalanine, the end product of the shikimic acid pathway, plays a key role as a precursor for phenylpropanoid biosynthesis pathway. The three main enzymes of general phenylpropanoid pathway are phenylalanine ammonia-lyase (PAL), cinnamate-4-hydroxylase (C4H) and 4-coumarate: CoA ligase (4CL) helps to catalyze the important first three steps of it that finally ends by giving 4-coumaroyl CoA (represented in (A) part of Figure 2.2). In the first step, phenylalanine ammonia-lyase (PAL) catalyzes the deamination reaction of L-phenylalanine to produce trans-cinnamic acid. In the second step, a hydroxylation reaction occurs, where trans-cinnamic acid converted to 4-coumarate by the activity of cinnamic acid 4-hydroxylase (C4H) enzyme. In the final step of this pathway, 4-coumarate-CoA ligase (4CL) catalyzes the conversion of 4-coumarate to 4-coumaroyl-CoA (Biala & Jasiński, 2018; Bond et al., 2016). 4-coumaroyl-CoA acts as a precursor for other branched pathways from phenylpropanoid pathway like flavonoid biosynthesis pathway (represented in (B) part of Figure 2.2) and monolignol specific pathway (represented by the combination of (C) and (D) part of Figure 2.2). These pathways include the production of several phenolic compounds like flavones, flavonols, flavonoids, anthocyanins, proanthocyanidins (condensed tannins), monolignols, lignin polymers, etc. (Nguyen et al., 2016; Tai et al., 2014; Zhu et al., 2015). Figure 2.2 represents the phenolic compounds production steps related to the phenylpropanoid pathway and its side branches.

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

33

FIGURE 2.2  Phenylpropanoid biosynthetic pathway along with flavonoid biosynthesis pathway and monolignol specific pathway in plants. Note: (A) Area represents general phenylpropanoid pathway; (B) represents flavonoid biosynthesis pathway; (C) and (D) areas represent monolignol specific pathway, where (D) area only shows polymerization of lignin. Note: PAL: Phenylalanine ammonia-lyase; C4H: Cinnamate-4-hydroxylase; 4CL: 4-coumarate: CoA ligase; CHS: Chalcone synthase; CHI: Chalcone isomerase; F3H: Flavanone3-hydroxylase; F3’H: Flavonoid 3’-hydroxylase; DFR: Dihydroflavonol 4-reductase; ANS: Anthocyanidin synthase; UFGT: UDP flavonoid glycosyltransferase; FNS: Flavone synthase; FLS: Flavonol synthase; LAR: Leucoanthocyanidin reductase; ANR: Anthocyanidin reductase; HCT: ρ-hydroxycinnamoyl-CoA: quinate/shikimate ρ-hydroxycinnamoyl transferase; CCR: Cinnamoyl-CoA reductase; C3H: p-coumarate 3-hydroxylase; CCoAOMT: CaffeoylCoA O-methyltransferase; F5H: Ferulate 5-hydroxylase; COMT: Caffeic acid O-methyltransferase; CAD: Cinnamyl alcohol dehydrogenase.

34

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

2.3 OVERVIEW OF PHENOLIC COMPOUNDS AND THEIR PHYSIOLOGICAL EFFECTS ON PLANTS Among the plant SMs, phenolic compounds are the largest studied group. It includes above 8,000 molecules. They commonly have one or more hydroxyl substituent’s depending on either they are simple phenolics (e.g., vanillin, caffeic acid, and gallic acid) or polyphenols (e.g., flavonoids, stilbenes, lignins, and polymers), respectively. Besides that, they are attached directly to one or more aromatic or benzene rings. Whereas their structures are varied extensively that can be said above all (González-Sarrías et al., 2020; Šamec et al., 2021). All the polyphenols are biosynthesized via shikimate/phenylpropanoid pathway. These processes produce several monomeric and/or polymeric polyphenols (Sharma et al., 2019a). Phenolic compounds are either found in free form or found as a conjugated form. They are found to be conjugated by β-glycosidic bonds to a hydroxyl group (O-glycosides) of one or more sugar residues (monosaccharides, disaccharides, or oligosaccharides) or aromatic ring (C-glycosides) containing a carbon atom (González-Sarrías et al., 2020; Šamec et al., 2021). According to their chemical structures, they are categorized into subgroups where they are soluble or bounded. Naturally they are synthesized in the endoplasmic reticulum and preserved then in vacuoles. Whereas transformation of soluble phenolic compounds to cell wall gives rise to bounded phenolic compounds (Gan et al., 2019; Jan et al., 2021). Structures and physiological properties of phenolic compounds are discussed in subsections. 2.3.1 PHENOLIC ACIDS Phenolic acids are distinguished by showing the attachment of a carboxyl group with a benzene ring. The free forms of phenolic acids are rarely found in nature. Mainly they are found to be linked by acetal, ether, or ester bonds to the other polyphenols like flavonoids, plant cell structural components like cellulose, lignin, proteins, or other organic molecules like quinic, tartaric, or maleic acids, and glucose (Andreasen et al., 2000; Lam et al., 2001). Phenolic compounds can be classified into two classes, such as derivatives of cinnamic acid (known as hydroxycinnamic acids (HCA) with C6–C3) and derivatives of benzoic acid (known as hydroxybenzoic acids (HBA) with C6–C1), depending on their structure (Goleniowski et al., 2013). HBA include gallic acid, vanillic acid, p-hydroxybenzoic acid, protocatechuic acid and variations of dihydroxybenzoic acid (DHBA) like 2,3-DHBA, 2,5-DHBA, 3,4-DHBA, and 3,5-DHBA; and HCA includes cinnamic acid, caffeic acid, ferulic acid, 4-coumaric acid, sinapic acid (Goleniowski et al.,

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

35

2013; Šamec et al., 2021). The variations in HBAs structures and variations in the acids derived from 4-coumaric acid are mainly due to the hydroxylations and methylations of the aromatic ring. Whereas a second hydroxyl group is added into p-coumaric acid catalyzed by monophenol mono-oxygenases (Šamec et al., 2021; Strack, 1997). Some of the simple HBAs are produced via the shikimic acid pathway as intermediate molecules, like gallic acid produced from dehydroshikimic acid. Though, the enzyme involve for this catalysis is still unclear. In case of HCAs, ferulic acid produced from the caffeic acid by methylation, which acts as precursor for lignin biosynthesis with 4-coumaric acid (Goleniowski et al., 2013; Šamec et al., 2021). 2.3.2 FLAVONOIDS Flavonoid is a varied group of phenolic compounds with low molecular weight. These are omnipresent in the plant kingdom, and these are very common in the human diet in the form of phytonutrients. Till date, about 8,000 molecules of flavonoids have been reported. Flavonoids show specified chemical structures, where they contain 15-carbon in their skeleton with a heterocyclic ring and phenyl ring. A wide variety of functions have been shown by flavonoids. In the case of plant system, flavonoids used in plant defense and pigmentation systems. In industrial level, these are used in cosmetic products, pharmaceutical, medicine manufacturing industry. In the case of human health, these have been used in health-promoting activities by altering cellular enzymes activities. Besides that, flavonoids have anticarcinogenic, anti-inflammatory, antioxidative, and antimutagenic properties (Jan et al., 2021; Walker et al., 2000). Besides the free form of flavonoids, many derivatives are synthesized via the processes of methylation, glycosidation, acetylation, prenylation, and polymerization. These processes can affect their bioactivity. O-methylation and C-methylation are two common forms of methylation patterns of flavonoids. The free forms of flavonoid glycosides are more common, though the methylated forms of flavonoids are rare. Methylation of flavonoids may increase the entry of flavonoids into cells and prevents degradation of cells (Wen et al., 2017). Commonly flavonoids are classified into six sub-classes, such as isoflavonoids (e.g., genistin, genistein, daidzein, daidzin, glycitein), flavonols (quercetin, kaempferol, myricetin, rutin, morin), flavanones (apigenin, tangeretin, baicalein, rhoifolin), flavanones (hesperidin, naringin, naringenin, eriodictyol, hesperidin), chalcones (phloretin, arbutin, chalconaringenin, phloridzin), and anthocyanins (cyaniding, malvidin, delphinidin, peonidin) (Jan et al., 2021).

36

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

2.3.3 LIGNIN After cellulose and hemicellulose, lignin is complex phenolic biopolymer on the earth, and it serves about 30% of organic carbon to the nature. Among the cell wall components, lignin is one of the complex racemic heteropolymers with high molecular weight. Three 4-hydroxycinnamoyl alcohol monomers (known as monolignols) primarily produce lignin by oxidative combinatorial coupling. It is an important SM which helps in plant growth, tissues, and organs development, providing resistance, abiotic, and biotic stress tolerance, etc. Lignification gives mechanical strength and vascular integrity to the plant (Cesarino et al., 2012; Jan et al., 2021). 2.3.4 TANNINS Tannins are known as astringent, the third crucial set of bitter phenolic compounds. They can bind with proteins and a variety of organic compounds, including alkaloids and amino acids. It has the ability to precipitate proteins, gelatin, glycoside, heavy metals, and alkaloids. Depending on the chemical structures, tannin can be classified into hydrolysable tannin and condensed tannin. Tannins have varied molecular weights, ranging from 500 to above 3,000. These are composed of a varied group of oligomers and polymers of plants (Minocha et al., 2015). In tannins, protocatechuic acid and chlorogenic acid play important roles in many environmental stresses like heavy metal stress, salinity stress, etc. (Al-Ghamdi & Elansary, 2018; Kısa et al., 2016; Lee et al., 2014). 2.3.5 COUMARIN Coumarins, commonly represented as benzo-α-pyrone (2H-1-benzopyran2-one), is simple phenolic compounds. They are organic heterocycles, and its systematic nomenclature was placed by International Union of Pure and Applied Chemistry (IUPAC). Coumarins are produced from the fusion of α-pyrone ring and a benzene ring. Coumarins were reported before 200-year ego, from the plant Coumarouna odorata (Dipteryx odorata) and then identified in about 150 species from 30 families (Jan et al., 2021; Venugopala et al., 2013). Coumarins are classified on the basis of their complexity and chemical diversity, such as simple coumarins, biscoumarins, furanocoumarins, isocoumarins, pyranocoumarins (both angular and linear), and other coumarins like phenylcoumarins (Zhu & Jiang, 2018).

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

37

2.4 EFFECTS OF ENVIRONMENTAL STRESSES ON PLANTS Plant faces a broad range of environmental variation throughout their life on land. Therefore, they require changes both in their external and internal processes for survival (Fahad et al., 2017). Due to these reasons, plants are capable of sensing diverse environmental signals through its receptor and show the changes in their physiology, genetic expression, and metabolism by altering its genomics, transcriptomics, and proteomics levels (Liu et al., 2014; Zhu, 2016). Sometimes serious or chronic environmental changes lead to the physical harm also. It also reduces crop yields (Fahad et al., 2017). The environmental stress mediated basic signaling pathways can be explained by following steps: perception of signals, signals carried by some second messengers, signal transduction, regulation in transcription level (through transcription factors), stress-responsive gene expression, and it ends by turning on the physiological, and metabolic responses (Pérez-Clemente et al., 2013; Wang et al., 2016a, b; Yamaguchi-Shinozaki & Shinozaki, 2006). A schematic representation of this process is shown in Figure 2.3. Excessive production of reactive oxygen species (ROS) with rapid alteration in cellular redox homeostasis can cause damage in cell organelles and initiates ROS-induced signaling pathways (Noctor et al., 2018). Rather than that, abiotic stresses can misbalance the ROS generation by scavenging and accelerating ROS propagation. This may damage vital macromolecules (carbohydrates, lipids, nucleic acids, and proteins), so that cell moves toward death (Kristensen et al., 2004). The whole process starts with perceiving signal by receptor present in plant cell wall or membrane, or through the sensors. Then the extracellular signals are transferred to the intracellular ones by the second messengers like calcium ions (Ca2+), ROS, inositol phosphate (IP), cyclic nucleotides (cGMP and cAMP), and nitric oxide (NO). Thereafter, the second messenger initiates signal transduction that may be occurs via the phosphorylation and dephosphorylation of proteins. Protein kinase and phosphatases mediate the phosphorylation and dephosphorylation reactions, respectively. Some of the important signal transduction pathways include mitogen-activated protein kinases (MAPKs) pathway and calcium-dependent protein kinases (CDPKs) pathway (Bhargava & Sawant, 2013; Chaves et al., 2009; Singh et al., 2003; Wang et al., 2016a, b). After the phosphorylation cascade, protein kinase and/or phosphatases either activate or suppress transcription factors (TFs) that bind with the cis-regulatory element (CRE) of the promoter of stress-responsive genes and control their transcription (Danquah et al., 2014). Actually, the main functions of TFs are: (i) recognition and binding with short, specific sequences of DNA within regulatory regions; and (ii) binding with the protein that takes part in transcriptional regulation (Cheatle & Hinman, 2015).

38

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Besides transcription, post-transcriptional modification includes ubiquitination and sumoylation lead to the regulation of stress-responsive gene expression. Alteration in stress-responsive gene expression can modify physiological and metabolic responses (Dong et al., 2006; Miura et al., 2007; Wang et al., 2016a, b). However, to understand the stress-associated genes expressions and the pathways involved in secondary metabolites biosynthesis in medicinal plants, authors have taken the help of transcriptomic and metabolomic technologies (Rai et al., 2017; Sharma & Shrivastava, 2016). Moreover, irreversible carbonylation inside chains resulted by the oxidation of lysine, threonine, and arginine residues, oxidation of methionine and cysteine residues form methionine sulfoxide and cystine (disulfide bond formed), respectively that cause ROSinduced protein damage (Kristensen et al., 2004; Sharma et al., 2019a).

FIGURE 2.3  Schematic presentation of signaling pathways mediated by environmental stress factors. Note: JA: Jasmonic acid; SA: Salicylic acid; ABA: Abscisic acid; NO: Nitric oxide; ROS: Reactive oxygen species; IP: Inositol phosphate; cGMP: Cyclic guanosine monophosphate; cAMP: Cyclic adenosine monophosphate; MAPK: Mitogen-activated protein kinases; CDPK: Calcium-dependent protein kinases.

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

39

2.5 ROLE OF POLYPHENOLS IN PLANTS AGAINST ENVIRONMENTAL STRESSES Secondary metabolite biosynthesis and accumulation is strictly dependent on the condition where the plant is growing, and the influencers of biosynthetic pathways include elicitors or signaling molecules. As we know, plants are sessile in nature, so they are daily exposed to various environmental stresses like temperature, salinity, UV light, drought, alkalinity, etc., i.e., the abiotic stresses. These can cause consequential damage to the plants (Seigler, 2012). The external factors not only damage the plant growth and development, but also, they help the plants to elicit their photochemical profiles by inducing biosynthesis of SMs for the production of bioactive compounds. Though, SMs producing plants can synthesize SMs in regular basis due to the response of regular environmental stresses. Hence, SMs play an important role to help the plants in adaptation and to survive themselves against environmental stimulus and stresses throughout their life (Jan et al., 2021; Verma & Shukla, 2015). The abiotic stresses resulted in the increase of biosynthetic rates of polyphenols. The phenolics are the most ubiquitous groups of SMs that possess anti-aging, anti-inflammation, anticarcinogenic, antiapoptosis, and antioxidant properties (Clé et al., 2008). Although, all polyphenols are biosynthesized via shikimate/phenylpropanoid pathway. Though phenylpropanoid pathway with it side branches, produces a broad array of monomeric and polymeric polyphenols include flavonoids, isoflavonoids, lignin, furanocoumarins, coumarin, and tannins, etc. (Clé et al., 2008; Sharma et al., 2019a). Most importantly, plants growing in stress condition have the capability to biosynthesize more phenolic compounds. This biosynthesis process altered enzyme activities that regulate phenolic compounds production, where PAL and CHS (chalcone synthase) are known as key enzyme (Selmar, 2008; Sharma et al., 2019a). Besides the accumulation of phenolics to protect the plants from adverse environmental conditions, the suberin deposition and lignification into the cell wall give resistance against cold stress. The main side effects of freezing temperature are freezing-induced dehydration and mechanical stresses. Whereas this increases cell wall thickening, this helps the plants from cell collapse by providing freezing resistance (Griffith & Yaish, 2004). The synthesis and accumulation of phenolic compounds in association with different environmental stresses are discussed in subsections.

40

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

2.5.1 HEAVY METAL Heavy metals are one of the most common environmental stresses that influence agrotechnology, industry, as well as their high bioaccumulation show toxic effects. Heavy metal-induced alterations in enzyme activity for SM productions are reported in many cases (Chen et al., 2019a; Zafari et al., 2016). For example, metals like Cr, Cd, Pb, Al have been reported to play a vital role in the regulation of SM biosynthetic pathway in plants (Handa et al., 2019; Kohli et al., 2017; Mishra & Sangwan, 2019; Smirnov et al., 2015). Although, phenolic compounds production and accumulation increase due to the up-regulation of enzymes involved in phenylpropanoid biosynthetic pathways, such as phenylalanine ammonia-lyase (PAL), chalcone synthase (CHS), cinnamyl alcohol dehydrogenase (CAD), shikimate dehydrogenase (SKDH), and polyphenol oxidase (PPO) (Chen et al., 2019a; Zafari et al., 2016). Shikimate dehydrogenase (SKDH) and glucose-6-phosphate dehydrogenase (G6PDH) enzymes take part for the production of vital precursors of phenylpropanoid pathways, and CAD enzyme is required for production of precursors for lignin biosynthesis pathway. Hence, these enzymes along with PAL were involved in phenylpropanoid biosynthetic pathway. Furthermore, heavy metals stimulate these enzymes activities and simultaneously up-regulate SM production (Kováčik et al., 2009; Mishra & Sangwan, 2019). Flavonoids have the ability to alter metals chelation (e.g., Zn, Ni, Fe, Cu) that follow Fenton’s reaction to generate hydroxyl radical. This metal chelation gives an effective form of defense against high metals toxicity. The biosynthesis of the phenolic compound is intensified due to stress conditions which are used as precursors of lignin biosynthetic pathway (Akhi et al., 2021; Michalak, 2006). SKDH, PPO, CAD enzymes activity increases in Kandelia obovata when it exposed to Cd and Zn (Chen et al., 2019a). Whereas Prosopis farcta shows increase in caffeic acid, ferulic acid, cinnamic acid, daidzein, resveratrol, vitexin, kaempferol, myricetin, quercetin, luteolin, naringenin, and diosmin contents, as well as increased PAL activity resulted in the elevation of total phenol contents (Zafari et al., 2016). Altered production of phenolic compounds with enzyme activities under various heavy metal stresses are presented in Table 2.1.

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

41

TABLE 2.1  List of Alterations in Production of Some Phenolic Compounds under Various Heavy Metal Stresses Sl. Family No. 1. Brassicaceae

Plant Name Name of Heavy Metal Cu Brassica juncea (L.) Czern.

2.

Brassicaceae

3.

Brassicaceae

4.

Brassicaceae

5.

Poaceae

Brassica juncea (L.) Czern. Brassica juncea (L.) Czern. Brassica juncea (L.) Czern. Zea mays L.

6.

Fabaceae

7.

Rhizophoraceae Kandelia obovata Sheue, Liu, and Yong

8.

Solanaceae

9.

Polygonaceae

Cr

Cd

Pb

Cu, Pb, Cd

Pb Prosopis farcta (Banks and Sol.) J.F. Macbr.

Withania somnifera (L.) Dunal Fagopyrum esculentum Moench

Cd and Zn

Cd

Al

Note: PAL: Phenylalanine ammonia lyase.

Response of Phenolic Compounds Total phenol content, phenolic compounds including kaempferol, caffeic acid, coumaric acid, catechin, anthocyanins are increased. Total phenol content increases along with flavonoids and anthocyanins production. Enhance in phenol, polyphenol, flavonoids, and anthocyanins contents. Augment in total contents of phenols, anthocyanins, and flavonoids. Enhanced level of total phenols and some polyphenols (vanillic acid and chlorogenic acid). Increase in caffeic acid, ferulic acid, cinnamic acid, daidzein, resveratrol, vitexin, kaempferol, myricetin, quercetin, luteolin, naringenin, and diosmin contents. Increased PAL enzyme activity resulted in elevated total phenol contents. Increase in shikimate dehydrogenase, polyphenol oxidase, cinnamyl alcohol dehydrogenase enzymes activity. The content of flavonoids and phenolics were increased. Total phenol content, anthocyanin, and flavonoid content increases with PAL enzyme activity.

References Poonam et al. (2015)

Handa et al. (2019) Kaur et al. (2018) Kohli et al. (2017) Kısa et al. (2016) Zafari et al. (2016)

Chen et al. (2019a)

Mishra & Sangwan (2019) Smirnov et al. (2015)

42

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

2.5.2 DROUGHT Drought is one of the most important abiotic stresses that leads to the reduction in plant growth, as well as in plant development, that finally resulted in agricultural yield loss. Approximately 40% and 21% of yield loss observed for maize and wheat due to the water reduction, respectively (Daryanto et al., 2016). Whereas, in Africa, cowpea production reduced in between 34% and 68% because of the drought stress came on the time of plant development (Farooq et al., 2017). Moreover, several studies have been reported that increased phenolics content was observed in Arabidopsis thaliana for enhancing drought tolerance under water deficiency (Nakabayashi et al., 2014). Phenolic compounds are found to be accumulated under the drought stress because of the modification in phenylpropanoid biosynthetic pathway. The drought-related enzymes of the phenylpropanoid pathway are translated in high level due to the up-regulated of genes expressions. This results in the high production of phenolic compounds (Sharma et al., 2019a). Drought stress increases the biosynthesis and accumulation of phenolic acids and flavonoids (Rezayian et al., 2018; Gharibi et al., 2019; Sharma et al., 2019a). Drought stress generated harmful H2O2 molecules can be detoxified by the accumulation of flavonoids in cytoplasm. At the ending, flavonoids are reconverted into primary metabolites due to the oxidation of flavonoids which mediated by ascorbic acid (Hernandez et al., 2009; Sharma et al., 2019a). Moreover, chlorogenic acid, caffeic acid, 1,3-dicaffeoylquinic acid, rutin, luteolin, luteolin-7-O-glycoside, apigenin, and kaempferol productions were reported to increase when Achillea sp. plant was exposed to drought under 21 days (Gharibi et al., 2019). PAL enzyme activity was found to be increased in tobacco plant due to drought stress (Silva et al., 2018). Drought stress leads to the increase in total phenol, flavonoid, phenolic compounds were observed in many plants like Brassica napus, Thymus vulgaris, Ocimum sp., Triticum aestivum, etc. (Ma et al., 2014; Ghasemi et al., 2017; Khalil et al., 2018; Rezayian et al., 2018). Table 2.2 shows a list of plants with their response against drought stress. TABLE 2.2  List of Alterations in Production of Some Phenolic Compounds under Drought Stress Sl. Family No. 1. Brassicaceae 2.

Fabaceae

Plant Name

Response of Phenolic Compounds References

Brassica napus L. Lotus japonicus L.

Up-regulation in total phenols, flavonol, and flavonoid content. Augmentation in kaempferol and quercetin content.

Rezayian et al. (2018) GarciaCalderon et al. (2015)

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

43

TABLE 2.2  (Continued) Sl. Family No.

Plant Name

3.

Cucumis sativus L. Vitis vinifera L.

4.

5. 6.

7. 8.

9.

Cucurbitaceae

Response of Phenolic Compounds References

Increase in vanillic acid and 4-hydroxycinnamic acid. Vitaceae Enhance in polyphenol contents including ferulic acid, 4-coumaric acid, cis-resveratrol-3-O-glucoside, caffeic acid, catechin, caftaric acid, epicatechin, quercetin-3-O glucuronide, cyanidin-3-O-glucoside, epicatechin gallate, kaempferol-3-Oglucoside, quercetin-3-O-glucoside, trans-resveratrol-3-O-glucoside, and anthocyanin content. Brassicaceae Increased accumulation of flavoArabidopsis noids, isoflavonoids. thaliana L. Zygophyllaceae Larrea Cav. Enhance in polyphenol contents (proanthocyanidins, flavonoids, and flavonols). Lamiaceae Enhance in total flavonoids and Thymus vulpolyphenols contents. garis L. Asteraceae Chlorogenic acid, caffeic acid, Achillea L. 1,3-dicaffeoylquinic acid, rutin, luteolin, luteolin-7-O-glycoside, apigenin, and kaempferol productions were increased under 21 days when exposure to drought. Solanaceae Capsicum an- Increase in apigenin, chlorogenic acid, and luteolin. nuum L.

10. Solanaceae 11. Asteraceae 12. Lamiaceae 13. Asteraceae

14. Poaceae

Li et al. (2018) Castellarin et al. (2007); Griesser et al. (2015)

Nakabayashi et al. (2014) Varela et al. (2016) Khalil et al. (2018) Gharibi et al. (2019)

RodríguezCalzada et al. (2019) Enhance in PAL enzyme activity Silva et al. Nicotiana and lignin content. (2018) tabacum L. Galieni et al. Lactuca sativa Enhance in phenolic compounds content like rutin and caftaric acid. (2015) L. Enhance in total phenols content. Ghasemi et al. Ocimum L. (2017) Total phenol content increases Hodaei et al. Chrysanthemum morifo- along with up-regulation in antho- (2018) lium (Ramat.) cyanins, quercetin, chlorogenic acid, ferulic acid, luteolin, rutin, Hemsl. and apigenin production. Ma et al. Triticum aesti- Enhance in phenolics, anthocyanins, and flavonoids content. (2014) vum L.

Note: PAL: Phenylalanine ammonia-lyase.

44

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

2.5.3 SALINITY Salinity stress is known as the most hazardous and injurious abiotic stress that affect the plants growth, physiology, and productivity. It imposes negative effects on growth by inducing physiological and morphological changes, decreasing the water potential of the leaf, producing ROS, alteration in biochemical processes, osmotic stress, and ion toxicity increases (Khan et al., 2014). Salinity stress stimulate phenylpropanoid biosynthetic pathway, which induces the production of various phenolic compounds having strong antioxidative potential (Bistgani et al., 2019; Rossi et al., 2016). The polyphenols are accumulated in the mangrove plants grown in the moderate salinity (Parida et al., 2004; Rezazadeh et al., 2012). In the case of paper fruits, total phenolics contents increased with increasing salinity and the mature fruits became changed to red (Navarro et al., 2006; Rezazadeh et al., 2012). Many of the plant species are identified with their increasing phenolic compounds contents due to the effect of salinity stress. Cynara cardunculus showed enhance in phenolic compounds contents like luteolin-O-glucoside, gallocatechin, leucocyanidin, apigenin 6-c-glucoside 8-c-arabinoside, and quercitrin, whereas decrease in chrysin, apigenin, daidzein, genistein, and ferulic acid contents (Lucini et al., 2016; Sharma et al., 2019a). Enhance in total phenolics content, HCAs (caffeic acid, p-coumaric acid, m-coumaric acid, chlorogenic acid, ferulic acid, trans-cinnamic acid, sinapic acid), flavonoids (rutin, hyperoside, iso-quercetin) and HBA (vanillic acid, gallic acid, syringic acid, ellagic acid, p-hydroxybenzoic acid) were observed when Amaranthus tricolor was subjected to salinity stress (Sarker & Oba, 2018). Enhance in phenolics like robinin, chlorogenic acid, apigein, rutin, and caffeic acid were noted in case of Asparagus aethiopicus under salinity stress (Al-Ghamdi & Elansary, 2018). Alteration in production of some phenolic compounds under salinity stress is shown in Table 2.3. TABLE 2.3  Alterations in Production of Some Phenolic Compounds under Salinity Stress Sl. Family No. 1. Asparagaceae

2.

Lamiaceae

Plant Name

Response of Phenolic Compounds

Enhance in phenolics like robinin, Asparagus aethiopicus L. chlorogenic acid, apigein, rutin, and caffeic acid. Enhance in phenolic compounds contents Ocimum like caftaric acid, caffeic acids, quercetinbasilicum L. rutinoside, feruloyl tartaric acid, cinnamyl malic acid, and rosmarinic acid.

References Al-Ghamdi & Elansary (2018) Scagel et al. (2019)

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

45

TABLE 2.3  (Continued) Sl. Family No.

Plant Name

3.

Enhance in phenolic compounds contents Cynara cardunculus L. like luteolin-O-glucoside, gallocatechin, leucocyanidin, apigenin 6-c-glucoside 8-c-arabinoside, and quercitrin.

Asteraceae

Solanum lycopersicon L. 5. Ranunculaceae Nigella sativa L. 6. Fabaceae Glycine max (L.) Merr. 7. Poaceae Triticum aestivum L. 8. Solanaceae Solanum villosum Mill. 9. Asteraceae Carthamus tinctorius L. 10. Lamiaceae Mentha piperita L. 11. Lamiaceae Thymus L. 4.

Solanaceae

12. Amaranthaceae Amaranthus tricolor L.

13. Lamiaceae

14. Malvaceae

Salvia mirzayanii Rech. f. and Esfand Gossypium L.

Response of Phenolic Compounds

Decrease in chrysin, apigenin, daidzein, genistein, and ferulic acid contents. Enhance in content of total caffeoylquinic acid. Increase in biosynthesis of apigenin. Enhance in flavone synthase enzyme activity. Enhance in content of total phenols.

References Lucini et al. (2016)

Martinez et al. (2016) Mekawy et al. (2018) Yan et al. (2014)

Kaur & Zhawar (2015) Enhance in contents of total phenolics, Ben-Abdallah et quercetin-3-β-D-glucoside, and caffeic acid. al. (2019) Enhance in total flavonoid and phenol Wang et al. contents. (2016a, b) Total phenol content increases. Ma et al. (2019) Enhance in various phenolic compounds contents like caffeic acid, trans-2hydroxycinnamic acid, gallic acid, rutin, syringic acid, cinnamic acid, rosmarinic acid, quercitrin, vanillic acid, apigenin, luteolin, and naringenin. Enhance in total phenolics content, hydroxycinnamic acids (caffeic acid, p-coumaric acid, m-coumaric acid, chlorogenic acid, ferulic acid, transcinnamic acid. Sinapic acid), flavonoids (rutin, hyperoside, iso-quercetin) and hydroxybenzoic acids (vanillic acid, gallic acid, syringic acid, ellagic acid, p-hydroxybenzoic acid). Enhance in total phenol content and PAL enzyme activity.

Bistgani et al. (2019)

Enhance in tannin (tannic acid).

Wang et al. (2015)

Sarker & Oba (2018)

Valifard et al. (2014, 2015)

46

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

TABLE 2.3  (Continued) Sl. Family No.

Plant Name

Salvia macrosiphon Boiss. 16. Amaranthaceae Chenopodium quinoa C.L. Willdenow (Willd.) 17. Oleaceae Olea europaea L. 15. Lamiaceae

18. Hypericaceae

19. Poaceae

Hypericum pruinatum Boiss. and Balansa Hordeum vulgare L.

Response of Phenolic Compounds

References

Enhance in total phenol content and PAL enzyme activity.

Valifard et al. (2015)

Enhance in total flavonoid and polyphenol contents.

Aloisi et al. (2016)

Enhance in polyphenolic compound (oleuropein), total phenolics, quercetin, and kaempferol content. Increase in accumulation of hyperoside, chlorogenic acid, rutin, quercitrine, isoquercetine, and quercetine.

Petridis et al. (2012); Rossi et al. (2016) Caliskan et al. (2017)

Total phenol content increases.

Ma et al. (2019)

Note: PAL: Phenylalanine ammonia-lyase.

2.5.4 ULTRAVIOLET RADIATION Ultraviolet (UV) radiation (UV-B: 280–320 nm) is another harmful stress factor. It comes in concern because of the ozone layer depletion. This nature of UV radiation effects on the concentrations and compositions of SMs (Jan et al., 2021; Waterman, 1989). The plants are affected in their macromolecules when its exposure to ambient solar UV-B radiation by ROS generation (Akhi et al., 2021; Regvar et al., 2012). Actually, the exposure of UV-B radiation causes damage in protein structure, injurious mutation in DNA structure and harmful ROS generation (Daayf & Lattanzio, 2009; Naikoo et al., 2019). Simultaneously plants synthesized phenolic compounds act inside the epidermal cell layer and help the plants to defend themselves from radiationmediated damage by adjusting antioxidant systems at both the entire organism level and the cell (Akhi et al., 2021; Regvar et al., 2012). They help in the reduction of DNA damage by reducing the dimerization of thymine residues and by preventing photo-damage of vital enzymes like NAD/NADP (Daayf & Lattanzio, 2009; Naikoo et al., 2019). UV irradiation-mediated studies were done in buckwheat genotypes (Fagopyrum tataricum and F. esculentum), where F. esculentum showed a definite increase in quercetin concentration (Akhi et al., 2021; Regvar et al., 2012). Goyal et al. (2014) reported that UV

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

47

irradiation increases total phenol and flavonoid content in contrast with PAL and CHI enzyme activities. In lettuce, UV radiation up-regulate PAL gene expression, and PAL enzyme activity increases simultaneously that effects on increase of total phenolic and anthocyanin contents. In addition, enhance in contents of total flavonoids, phenolics, anthocyanins, and phenolic acids (vanillic acid, rosmarinic acid, chlorogenic acid, p-anisic acid, and methoxycinnamic acid) were noted (Lee et al., 2014; Sytar et al., 2018). Caryopteris mongolica showed an increase in anthocyanidins and flavonoids content along with CHI and PAL enzyme activity (Liu et al., 2012). An experiment with Triticum aestivum showed a significant increase in total phenolics, p-coumaric acid, ferulic acid, and vanillic acid contents after 3 days of UV light exposure to the plants. Whereas syringic acid, p-hydroxybenzoic acid, and sinapic acid contents were unchangeable (Chen et al., 2019b). Table 2.4 shows a list of plants with their response against UV radiation. TABLE 2.4  Alterations in Production of Some Phenolic Compounds under UV Radiation Sl. Family No. 1. Brassicaceae 2.

Crassulaceae

3.

Fabaceae

4.

Lamiaceae

5.

Solanaceae

6.

Asteraceae

Plant Name Response of Phenolic Compounds Augmentation in sinapic acid and Brassica oleracea L. gallic acid contents. Enhance in quercitrin and total Kalanchoe flavonoids contents. pinnata (Lam.) Pers. Vigna radi- Total phenol and flavonoid content increases in contrast with ate (L.) R. PAL and CHI enzymes activities. Wilczek Caryopteris Anthocyanidins and flavonoids content increases along with CHI mongolica and PAL enzyme activity. Bunge Enhance in total phenolic content. Solanum lycopersicum L. Enhance in contents of total flaLactuca vonoids, phenolics, anthocyanins, sativa L. and phenolic acids (vanillic acid, rosmarinic acid, chlorogenic acid, p-anisic acid, and methoxycinnamic acid). Increased PAL enzyme activity due to up-regulation of PAL gene expression effects on increase of total phenolic and anthocyanin contents.

References Moreira-Rodriguez et al. (2017) Nascimento et al. (2015) Goyal et al. (2014) Liu et al. (2012)

Mariz-Ponte et al. (2018) Lee et al. (2014); Sytar et al. (2018)

48

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

TABLE 2.4  (Continued) Sl. Family No.

Plant Name Response of Phenolic Compounds

References

7.

Apiaceae

8.

Ericaceae

Cuminum cyminum L. Arbutus unedo L.

Ghasemi et al. (2019) Nenadis et al. (2015)

9.

Grossulariaceae

10.

Vitaceae

11.

Poaceae

12.

Rosaceae

Enhance in phenolics and anthocyanins contents. Enhance in phenolic compounds content like avicularin, theogallin, and juglanin. Enhance in anthocyanins, flavoRibes ninols, hydroxybenzoic acids, and grum L. hydroxycinnamic contents. Vitis vinifera Enhance in phenolic compounds content like cyaniding, peonidin, L. petunidin, protocatechuic acid, myricetin, malvidin, kaempferol, quercetin, gallic acid, procyanidin, and vanillic acid. Enhance in total phenolics, Triticum aestivum L. p-coumaric acid, ferulic acid, and vanillic acid contents were observed after 3 days of exposure to UV light. No changes noted in syringic acid, p-hydroxybenzoic acid, and sinapic acid contents. Fragaria × Enhance in kaempferol, glucoside, and ellagic acid derivatives ananassa of cyaniding, pelargonidin, and Duchesne quercetin contents.

Huyskens-Keil et al. (2012) Berli et al. (2011)

Chen et al. (2019b)

Xu et al. (2017)

Note: PAL: Phenylalanine ammonia-lyase; CHI: Chalcone isomerase.

2.5.5 TEMPERATURE In the 20th century, global temperature increases rapidly and that stands by ~0.47°C. This causes global warming, and it will considerably affect the secondary metabolites production. Not even the high temperature (HT) is an abiotic stress, low temperature also creates cold stress. Plants use many strategies such as alteration in metabolism; increase the essential metabolites level for their survival from the stresses unfavorable conditions (Karwasara et al., 2013). Phenolic compounds are highly synthesized at low temperature, and in the plant cell wall, they are integrated as suberin or lignin. Whereas the plants grow under the cold stress show high level of chlorogenic acid synthesis for their adaptation in cold environments. It was reported in winter

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

49

rye (Secale cereale) that cold stress was increased the phenolic production either as lignin or suberin into the cell wall. This lignification or suberin deposition can protect the plant from freezing (Griffith & Yaish, 2004). Under the heat stress condition, Festuca trachyphylla showed augmentation in the phenolic compounds’ contents like caffeic acid, coumaric acid, benzoic acid, 4-hydroxybenzoic acid, gallic acid, cinnamic acid, ferulic acid, homovanillic acid, salicylic acid, and vanillic acid. These enhancement and accumulation of phenolic compounds helped the plant to survive against HT (Wang et al., 2019a). In Prunus persica, PAL, 4CL, C4H, and CHI enzymes activities were increased during cold stress, simultaneously an enhanced level of phenolic compounds contents like protocatechuic acid, chlorogenic acid, catechin, neocholorogenic acid, quercetin-3-glucoside, kaempferol-3-rutinoside, and quercetin-3-rutinoside were noted (Wang et al., 2019b). Table 2.5 shows a list of plants with their response against differential temperatures. TABLE 2.5  Alterations in Production of Some Phenolic Compounds under Differential Temperature Sl. Family No. 1. –

Plant Name

Environmental Response of Phenolic Factors Compounds All land plants Cold stress Enhance in lignins like pinoresinol.

2.

Poaceae

Festuca brachyphylla Schultes

3.

Solanaceae Nicotiana tabacum L.

Cold stress

4.

Rosaceae

Prunus persica (L.) Stokes

Cold stress

Heat stress

Enhance in the phenolic compounds’ contents like benzoic acid, 4-hydroxybenzoic acid, caffeic acid, gallic acid, cinnamic acid, coumaric acid, ferulic acid, homovanillic acid, salicylic acid, and vanillic acid. Various metabolites produced from phenylalanine metabolic pathway are altered their amount. PAL, 4CL, C4H, and CHI enzymes activities were increased and enhance in phenolic compounds contents like protocatechuic acid, cholorogenic acid, catechin, neocholorogenic acid, quercetin-3-glucoside, kaempferol-3-rutinoside, and quercetin-3-rutinoside.

References Griffith & Yaish (2004); Jan et al. (2021) Wang et al. (2019a)

Zhou et al. (2018)

Wang et al. (2019b)

50

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

TABLE 2.5  (Continued) Sl. Family No. 5.

6.

Plant Name

Environmental Response of Phenolic Factors Compounds

Heat stress Vigna angularis (Willd.) Ohwi and H. Ohsdhi Solanaceae Nicotiana Heat stress langsdorffii Weinm. Fabaceae

Lens culinaris Heat stress Medik.

7.

Fabaceae

8.

Solanaceae Solanum Heat stress lycopersicum L.

References

Escalation in the flavonoids and Zlotek et al. anthocyanins contents. (2015)

Escalation in total polyphenols contents, as well as increase in p-coumaric acid, neochlorogenic acid cryptochlorogenic acid, chlorogenic acid, and ferulic acid contents. Increase in total flavonoids and phenolics, as well as in gallic acid, chlorogenic acid, salicylic acid, naringenin, and ferulic acid contents. Enhance in content of total flavonol.

Ancillotti et al. (2015)

Swieca (2015)

Martinez et al. (2016)

Note: PAL: Phenylalanine ammonia lyase; 4CL: 4-coumarate: CoA ligase; C4H: Cinnamate 4-hydroxylase; CHI: Chalcone isomerase.

2.5.6 OTHER STRESS FACTORS Many other abiotic factors are also included for the enhancement of enzymes actions along with the production of SMs. Besides the factors mentioned before, there are many such stresses like oxidative stress, insecticide, and several nanoparticles mediated stresses are involved in the alteration of phenylpropanoid pathway, in conjugation with flavonoid biosynthetic pathway and monolignol specific pathway. These help the plants to protect against environmental stresses. Plants growing under pesticide stress surroundings showed a significant increase in phenolic biosynthetic pathways. These lead to the more synthesis and accumulation of phenolics to confer resistance of the plants against pesticide stress (Mahdavi et al., 2015; Sharma et al., 2016, 2019a). Up-regulation of PAL and CHS genes may involve in the activation of biosynthesis of enzymes which are required for phenolic biosynthesis (Sharma et al., 2019a, b). 24-epibrassinolide stimulates the biosynthesis of phenolics which are involved in the decrease of heat generated oxidative stress. This process is also involved in ROS scavenging (Gao et al., 2016). Altered production of phenolic compounds with enzyme activities under various stress factors are presented in Table 2.6.

Sl. Family No.

Plant Name

Name of Stress Response of Phenolic Compounds Factors

References

1.

Poaceae

Oryza sativa L.

Insecticide

2.

Brassicaceae

Brassica juncea (L.) Czern.

Insecticide

Mahdavi et al. (2015) Sharma et al. (2016, 2019a)

3.

Amaryllidaceae

Allium porrum L.

Oxidative stress

4.

Amaryllidaceae

Allium cepa L.

Oxidative stress

5.

Juglandaceae

Juglans regia L.

Oxidative stress

6.

Fabaceae

Oxidative stress

7. 8.

Malvaceae Fagaceae

Glycine max (L.) Merr. Gossypium L. Quercus robur L.

9.

Fabaceae

10. Pinaceae 11. Saxifragaceae

Lotus corniculatus Oxidative stress Enhance in tannin (like gallotannin). L. Oxidative stress Enhance in tannin (like gallotannin). Tsuga Carrière Saxifraga ligulata (Wall.) Engl. All plants All plants

Oxidative stress Enhance in bergenin which belongs to the class of isocoumarins. Oxidative stress Enhance in biflavonoids like amentoflavone. Oxidative stress Enhance in biflavonoids like amentoflavone.

Jain et al. (2015) Jain et al. (2015) Chi et al. (2011); Jan et al. (2021) Reiter et al. (2008) Wang et al. (2015) Gan et al. (2018); Jan et al. (2021) Gan et al. (2018); Jan et al. (2021) Gan et al. (2018); Jan et al. (2021) Pushpalatha et al. (2015) Yu et al. (2017) Yu et al. (2017)

51

12. Selaginellaceae 13. Euphorbiaceae

Oxidative stress Oxidative stress

Enhance in phenylalanine, ferulic acid, and 4-hydroxybenzoic acid contents. Enhance in total phenol polyphenol, and anthocyanin contents regulated by the enhanced PAL and CHS gene expression. Enhance in flavonoid contents like quercetin, kaempferol, and myrecetin. Enhance in flavonoid contents like quercetin, kaempferol, and myrecetin. Enhance in juglone which belongs to the class naphthoquinone. Enhance in flavonoid contents like genistein, daidzein, and glycitein. Enhance in tannin (tannic acid). Enhance in tannin (like gallotannin).

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

TABLE 2.6  List of Alterations in Production of Some Phenolic Compounds under Other Stress Factors

52

TABLE 2.6  (Continued) Plant Name

Name of Stress Response of Phenolic Compounds Factors

References

14. Cupressaceae 15. Anacardiaceae

All plants Anacardium occidentale L. Withania somnifera (L.) Dunal Solanum tuberosum L. Vitis vinifera L.

Oxidative stress Enhance in isoflavonoids like amentoflavone. Oxidative stress Enhance in biflavonoids like agathisflavone

Yu et al. (2017) Andrade et al. (2019) Singh et al. (2018)

16. Solanaceae 17. Solanaceae 18. Vitaceae

Copper nanoparticle Zinc nanoparticle Titanium nanoparticle

Enhance in total phenolics and flavonoids contents. Enhance in total phenolics and anthocyanins contents. Enhance in total phenolics, kaempferol derivative, and quercetin derivatives.

Note: PAL: Phenylalanine ammonia-lyase; CHS: Chalcone synthase.

Raigond et al. (2017) Korosi et al. (2019)

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Sl. Family No.

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

53

2.6 GENETIC ALTERATION LEADING TO SECONDARY METABOLITE PRODUCTION DURING ENVIRONMENTAL STRESS RESPONSE Besides the alteration in enzyme activity, the alteration in gene expression also reflects its action on SMs production. Biosynthetic pathways can regulate by the gene, where increased enzyme activity is in correspondence with the up-regulation of expressions of respective genes. Some of the important genes encoding biosynthetic enzymes are like PAL (phenylalanine ammonia lyase), C4H (cinnamate 4-hydroxylase), 4CL (4-coumarate: CoA ligase), CHS (chalcone synthase), CHI (chalcone isomerase), F3H (flavanone-3-hydroxylase), F3’H (flavonoid-3’-hydroxylase), F3’5’H (flavonoid 3’5’-hydroxylase), DFR (dihydroflavonol 4-reductase), FLS (flavonol synthase), IFS (isoflavone synthase), IFR (isoflavone reductase), and UFGT (UDP flavonoid glycosyltransferase) (Gharibi et al., 2019; Ma et al., 2014; Sharma et al., 2019a; Zhou et al., 2018). For example, Brassica juncea showed the up-regulation of PAL and CHS genes expressions when they were subjected to heavy metal stress created by Cd, Cr or Pb (Handa et al., 2019; Kaur et al., 2017; Kohli et al., 2017). Whereas Vitis vinifera showed enhanced transcription of PAL, DFR, F3H, C4H, CHS genes. The encoding enzymes of those are required for phenolic biosynthesis, but UFGT and ANR genes were down-regulated (Leng et al., 2015). Drought stress can stimulate the expression of key genes related to phenylpropanoid pathway that increases the production and accumulation of phenolic compounds. For example, in Scutellaria baicalensis, drought stress induces the expressions of several genes related to flavonoid biosynthesis pathway. As well as this stress induces PAL gene expression in lettuce plants (Jan et al., 2021; Yuan et al., 2012). UV exposure leads to the up-regulation of key genes like PAL; FLS; CHS (chalcone synthase); CHI (chalcone isomerase); F3H (flavanone 3-hydroxylase), DFR (dihydroflavonol-4-reductase); and FGT (flavonoid glycosyltransferases) (Goyal et al., 2014; Sharma et al., 2019a; Xu et al., 2017). Table 2.7 shows a list of plants with their response in genetic levels against various environmental stress factors.

54

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

TABLE 2.7  Alterations in Genes Expressions under Various Environmental Stress Factors Stress Factors Heavy metal (Cr) Heavy metal (Cd) Heavy metal (Pb) Heavy metal (Cu)

Drought

Drought

Drought

Drought

Drought Drought

Drought

Salinity Salinity Salinity

Family

Plant Name

Brassicaceae Brassica juncea (L.) Czern. Brassicaceae Brassica juncea (L.) Czern. Brassicaceae Brassica juncea (L.) Czern. Vitaceae Vitis vinifera L.

Alterations in Genomic Level

Up-regulation of PAL and CHS genes expression. Increases the expressions PAL and CHS gene. Up-regulation of PAL and CHS genes expression. PAL, DFR, F3H, C4H, CHS genes encoding enzymes required for phenolic biosynthesis show enhanced transcription and UFGT and ANR genes are downregulated. Brassicaceae Brassica napus Enhanced PAL expression leads to L. the augmentation in PAL enzyme activity. Fabaceae Lotus japonicus PAL, DFR, C4H, CHI, 4CL, IFS, L. CHS, and IFR genes showed improved in transcription level. Poaceae Triticum Up-regulation in CHS, F3H, CHI, aestivum L. FNS, DFR, ANS, and FLS genes expression. Asteraceae Achillea L. PAL, CHI, CHS, F3H, F3’5’H, F3’H, and FLS genes showed enhance rate of transcription. Vitaceae Vitis vinifera L. Enhance in UFGT, F3H, and CHS genes expression. Asteraceae Chrysanthemum Enhanced transcript levels of CHI, PAL, and F3H genes observed morifolium (Ramat.) Hemsl. particularly in Taraneh cultivar. Rosaceae Fragaria Up-regulation in ANS, PAL, C4H, ananassa DFR, 4CL, UFGT, and FLS genes Duchesne expression. Oleaceae Olea europaea Up-regulation in PAL, CHS, C4H, L. CHI, and 4CL expressions. Solanaceae Solanum Enhanced PAL and FLS genes villosum Mill. expression. Solanaceae Nicotiana Up-regulation of NtCHS1 tabacum L. expression increase flavonoid biosynthesis.

References Handa et al. (2019) Kaur et al. (2017) Kohli et al. (2017) Leng et al. (2015)

Rezayian et al. (2018) GarciaCalderon et al. (2015) Chen et al. (2019b) Gharibi et al. (2019) Castellarin et al. (2007) Hodaei et al. (2018) Perin et al. (2019) Rossi et al. (2016) Ben-Abdallah et al. (2019) Chen et al. (2019c)

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

55

TABLE 2.7  (Continued) Stress Factors

Family

Plant Name

Alterations in Genomic Level

References

Salinity

Rosaceae

Up-regulation in PAL, DFR, F3H, C4H, and FLS expressions.

Perin et al. (2019)

Salinity

Fabaceae

Salinity

Lamiaceae

Lamiaceae

Up-regulation in GmFNSII-1 and GmFNSII-2 genes expression. Enhanced PAL enzyme activity showed due to up-regulation of PAL gene expression. Enhanced PAL enzyme activity showed due to up-regulation of PAL gene expression.

Yan et al. (2014) Valifard et al. (2015)

Salinity

UV radiation

Apiaceae

Fragaria ananassa Duchesne Glycine max (L.) Merr. Salvia macrosiphon Boiss. Salvia mirzayanii Rech. f. and Esfand Cuminum cyminum L.

UV radiation

Asteraceae

Lactuca sativa L.

UV radiation

Poaceae

Triticum aestivum L.

UV radiation

Fragaria × ananassa Duchesne Brassicaceae Brassica juncea (L.) Czern. Solanaceae Nicotiana tabacum L.

Insecticide Cold stress

Rosaceae

Enhanced DAHP and PAL genes expression helps to increase phenolics and anthocyanins contents. PAL enzyme activity correspondence with up-regulation of PAL expression. PAL, 4CL, C4H, and COMT genes expressions were altered in transcript levels after 3 days of exposure to UV light. Increased in expression of genes related to flavonoid pathways like CHS, CHI, FLS, DFR, and FGT. Up-regulation in PAL and CHS genes expressions, PAL, HCT, and CAD genes expressions were up-regulated.

Valifard et al. (2015)

Ghasemi et al. (2019)

Lee et al. (2014) Chen et al. (2019b)

Xu et al. (2017) Sharma et al. (2019a) Zhou et al. (2018)

Note: PAL: Phenylalanine ammonia lyase; CHS: Chalcone synthase; DFR: Dihydroflavonol 4-reductase; F3H: Flavanone-3-hydroxylase; C4H: Cinnamate 4-hydroxylase; UFGT: UDP flavonoid glycosyltransferase; ANR: Anthocyanidin reductase; CHI: Chalcone isomerase; 4CL: 4-coumarate: CoA ligase; IFS: Isoflavone synthase; IFR: Isoflavone reductase; FNS: Flavone synthase; ANS: Anthocyanidin synthase; FLS: Flavonol synthase; F3’5’H: Flavonoid 3’,5’-hydroxylase; F3’H: Flavonoid 3’-hydroxylase; DAPH: Deoxyribonino heptulosinate 7-phosphate synthase; COMT: Caffeic acid O-methyltransferase; FGT: Flavonoid 3-O-glycosyltransferase; HCT: Hydroxycinnamoyl transferase; CAD: Alcohol dehydrogenase.

56

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

2.7 CONCLUSIONS Shikimic acid pathway and phenylpropanoid pathway are two important pathways for the production of phenolic group of SMs in plants. L-phenylalanine, end product of shikimic acid pathway can act as precursor for phenylpropanoid pathway that made inter-connection between these two pathways. Then phenylpropanoid pathway gives rise to a broad variety of phenolic compounds, including coumarin, anthocyanins, lignins, flavonoids, tannins, either directly or by the side branch pathways (like flavonoid biosynthesis pathway and monolignol pathway). On the other hand, the plant faces numerous environments-created stresses (environmental stress factors) throughout their life on earth. To protect against environmental stresses, plants alter the gene expressions as well as enzyme activities associated with shikimic acid and/or phenylpropanoid pathway. This alteration may help in the production and accumulation of phenolic compounds in the plants for making them resistant. KEYWORDS • • • • • •

enzymes gene expression phenolic compounds phenylalanine ammonia-lyase phenylpropanoid pathway shikimic acid

REFERENCES Aharoni, A., & Galili, G., (2011). Metabolic engineering of the plant primary secondary metabolism interface. Curr. Opin. Biotech., 22, 239–244. Akhi, M. Z., Haque, M. M., & Biswas, M. S., (2021). Role of secondary metabolites to attenuate stress damages in plants. In: Waisundara, V., (ed.), Antioxidants- Benefits, Sources, Mechanisms of Action. IntechOpen. Al-Ghamdi, A. A., & Elansary, H. O., (2018). Synergetic effects of 5-aminolevulinic acid and Ascophyllum nodosum seaweed extracts on Asparagus phenolics and stress-related genes under saline irrigation. Plant Physiol. Biochem., 129, 273–284.

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

57

Aloisi, I., Parrotta, L., Ruiz, K. B., Landi, C., Bini, L., Cai, G., Biondi, S., & Del, D. S., (2016). New insight into quinoa seed quality under salinity: Changes in proteomic and amino acid profiles, phenolic content, and antioxidant activity of protein extracts. Front. Plant Sci., 7, 656. Ancillotti, C., Bogani, P., Biricolti, S., Calistri, E., Checchini, L., Ciofi, L., Gonnelli, C., & Del, B. M., (2015). Changes in polyphenol and sugar concentrations in wild type and genetically modified Nicotiana langsdorffi Weinmann in response to water and heat stress. Plant Physiol. Biochem., 97, 52–61. Andrade, A. W. L., Figueiredo, D. D. R., Islam, M. T., Nunes, A. M. V., Da Conceição, M. K., Da Conceição, M. K., Uddin, S. J., et al., (2019). Toxicological evaluation of the biflavonoid, agathisflavone in albino Swiss mice. Biomed. Pharmacother., 110, 68–73. Andreasen, M. F., Christensen, L. P., Meyer, A. S., & Hansen, A., (2000). Content of phenolic acids and ferulic acid dehydrodimers in 17 rye (Secale cereale L.) varieties. J. Agric. Food Chem., 48, 2837–2842. Ben-Abdallah, S., Zorrig, W., Amyot, L., Renaud, J., Hannoufa, A., Lachâal, M., & KarrayBouraoui, N., (2019). Potential production of polyphenols, carotenoids and glycoalkaloids in Solanum villosum Mill. under salt stress. Biologia, 74, 309–324. Berli, F. J., Fanzone, M., Piccoli, P., & Bottini, R., (2011). Solar UV-B and ABA are involved in phenol metabolism of Vitis vinifera L. increasing biosynthesis of berry skin polyphenols. J. Agric. Food Chem., 59, 4874–4884. Bhargava, S., & Sawant, K., (2013). Drought stress adaptation: Metabolic adjustment and regulation of gene expression. Plant Breed., 132, 21–32. Biala, W., & Jasiński, M., (2018). The phenylpropanoid case – It is transport that matters. Front. Plant Sci., 9, 1610. Bistgani, Z. E., Hashemi, M., DaCosta, M., Craker, L., Maggi, F., & Morshedloo, M. R., (2019). Effect of salinity stress on the physiological characteristics, phenolic compounds and antioxidant activity of Thymus vulgaris L. and Thymus daenensis celak. Ind. Crops Prod., 135, 311–320. Bond, D. M., Albert, N. W., Lee, R. H., Gillard, G. B., Brown, C. M., Hellens, R. P., & Macknight, R. C., (2016). Infiltration‑RNAseq: Transcriptome profiling of Agrobacteriummediated infiltration of transcription factors to discover gene function and expression networks in plants. Plant Methods, 12, 41. Bourgaud, F., Gravot, A., Milesi, S., & Gontier, E., (2001). Production of plant secondary metabolites: A historical perspective. Plant Sci., 161, 839–851. Caliskan, O., Radusiene, J., Temizel, K. E., Staunis, Z., Cirak, C., Kurt, D., & Odabas, M. S., (2017). The effects of salt and drought stress on phenolic accumulation in greenhousegrown Hypericum pruinatum. Ital. J. Agron. 2017, 12. Castellarin, S. D., Pfeiffer, A., Sivilotti, P., Degan, M., Peterlunger, E., & Di Gaspero, G., (2007). Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant Cell Environ., 30, 1381–1399. Cesarino, I., Araújo, P., Domingues, Jr. A. P., & Mazzafera, P., (2012). An overview of lignin metabolism and its effect on biomass recalcitrance. Braz. J. Bot., 35, 303–311. Chaves, M. M., Flexas, J., & Pinheiro, C., (2009). Photosynthesis under drought and salt stress: Regulation mechanisms from whole plant to cell. Ann. Bot., 103, 551–560. Cheatle, J. A. M., & Hinman, V. F., (2015). Evolution of transcription factor function as a mechanism for changing metazoan developmental gene regulatory networks. Evodevo, 6, 3.

58

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Chen, S., Wang, Q., Lu, H., Li, J., Yang, D., Liu, J., & Yan, C., (2019a). Phenolic metabolism and related heavy metal tolerance mechanism in Kandelia obovata under Cd and Zn stress. Ecotoxicol. Environ. Saf., 169, 134–143. Chen, S., Wu, F., Li, Y., Qian, Y., Pan, X., Li, F., Wang, Y., et al., (2019c). NtMYB4 and NtCHS1are critical factors in the regulation of flavonoid biosynthesis and are involved in salinity responsiveness. Front. Plant Sci., 10, 178. Chen, Z., Ma, Y., Yang, R., Gu, Z., & Wang, P., (2019b). Effects of exogenous Ca2+ on phenolic accumulation and physiological changes in germinated wheat (Triticum aestivum L.) under UV-B radiation. Food Chem., 288, 368–376. Cheynier, V., Comte, G., Davies, K. M., Lattanzio, V., & Martens, S., (2013). Plant phenolics: Recent advances on their biosynthesis, genetics and ecophysiology. Plant Physiol. Biochem., 72, 1–20. Chi, W. C., Fu, S. F., Huang, T. L., Chen, Y. A., Chen, C. C., & Huang, H. J., (2011). Identification of transcriptome profiles and signaling pathways for the allelochemical juglone in rice roots. Plant Mol. Biol., 77, 591–607. Clé, C., Hill, L. M., Niggeweg, R., Martin, C. R., Guisez, Y., Prinsen, E., & Jansen, M. A., (2008). Modulation of chlorogenic acid biosynthesis in Solanum lycopersicum; consequences for phenolic accumulation and UV-tolerance. Phytochemistry, 69, 2149–2156. Daayf, F., & Lattanzio, V., (2009). Recent Advances in Polyphenol Research (Vol. 1). John Wiley & Sons: USA. Danquah, A., De Zelicourt, A., Colcombet, J., & Hirt, H., (2014). The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol. Adv., 32, 40–52. Daryanto, S., Wang, L., & Jacinthe, P. A., (2016). Global synthesis of drought effects on maize and wheat production. PLoS One, 11, e0156362. Dong, C. H., Agarwal, M., Zhang, Y., Xie, Q., & Zhu, J. K., (2006). The negative regulator of plant cold responses, HOS1, is a RINGE3 ligase that mediates the ubiquitination and degradation of ICE1. Proc. Natl. Acad. Sci. U.S.A., 103, 8281–8286. Eykman, J. F., (1886). Sur l’illicium religiosum. Compendium of Chemical Works of the Netherlands, 4, 32–54. Fahad, S., Bajwa, A. A., Nazir, U., Anjum, S. A., Farooq, A., Zohaib, A., Sadia, S., et al., (2017). Crop production under drought and heat stress: Plant responses and management options. Front. Plant Sci., 29, 8. Farooq, M., Gogoi, N., Barthakur, S., Baroowa, B., Bharadwaj, N., & Alghamdi, S. S., (2017). Drought stress in grain legumes during reproduction and grain filling. J. Agron. Crop Sci., 203, 81–102. Galieni, A., Di Mattia, C., De Gregorio, M., Speca, S., Mastrocola, D., Pisante, M., & Stagnari, F., (2015). Effects of nutrient deficiency and abiotic environmental stresses on yield, phenolic compounds and antiradical activity in lettuce (Lactuca sativa L.). Sci. Hortic., 187, 93–101. Gan, R. Y., Chan, C. L., Yang, Q. Q., Li, H. B., Zhang, D., Ge, Y. Y., Gunaratne, A., et al., (2019). Bioactive compounds and beneficial functions of sprouted grains. In: Feng, H., Nemzer, B., & DeVries, J. W., (eds.), Sprouted Grains: Nutritional Value, Production and Applications (pp. 191–246). AACC International Press: USA. Gan, R. Y., Kong, K. W., Li, H. B., Wu, K., Ge, Y. Y., Chan, C. L., Shi, X. M., & Corke, H., (2018). Separation, identification, and bioactivities of the main gallotannins of red sword bean (Canavalia gladiata) coats. Front. Chem., 6, 39.

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

59

Gao, H., Zhang, Z., Lv, X., Cheng, N., Peng, B., & Cao, W., (2016). Effect of 24-epibrassinolide on chilling injury of peach fruit in relation to phenolic and proline metabolisms. Post. Biol. Technol., 111, 390–397. Garcia-Calderon, M., Pons-Ferrer, T., Mrazova, A., Palˊove-Balang, P., Vilkova, M., PerezDelgado, C. M., Vega, J. M., et al., (2015). Modulation of phenolic metabolism under stress conditions in a Lotus japonicus mutant lacking plastidic glutamine synthetase. Front. Plant Sci., 6, 760. Gharibi, S., Sayed, T. B. E., Saeidi, G., Talebi, M., & Matkowski, A., (2019). The effect of drought stress on polyphenolic compounds and expression of flavonoid biosynthesisrelated genes in Achillea pachycephala rech. f. Phytochemistry, 162, 90–98. Ghasemi, P. A., Malekpoor, F., Salimi, A., & Golparvar, A., (2017). Exogenous application of chitosan on biochemical and physiological characteristics, phenolic content and antioxidant activity of two species of basil (Ocimum ciliatum and Ocimum basilicum) under reduced irrigation. Sci. Hortic., 217, 114–122. Ghasemi, S., Kumleh, H. H., & Kordrostami, M., (2019). Changes in the expression of some genes involved in the biosynthesis of secondary metabolites in Cuminum cyminum L. under UV stress. Protoplasma, 256, 279–290. Goleniowski, M. E., Bonfill, M., Cusido, R., & Palazon, J., (2013). Phenolic acids. In: Ramawat, K., Mérillon, J. M., (eds.), Natural Products (pp. 1951–1973). Springer Science and Business Media: Berlin/Heidelberg, Germany. González-Sarrías, A., Tomás-Barberán, F. A., & García-Villalba, R., (2020). Structural diversity of polyphenols and distribution in foods. In: Tomás-Barberán, F. A., GonzálezSarrías, A., & García-Villalba, R. R., (eds.), Dietary Polyphenols: Their Metabolism and Health Effects (pp. 1–29). Wiley: Chichester, UK. Goyal, A., Siddiqui, S., Upadhyay, N., & Soni, J., (2014). Effects of ultraviolet irradiation, pulsed electric field, hot water and ethanol vapors treatment on functional properties of mung bean sprouts. J. Food Sci. Technol., 51, 708–714. Griesser, M., Weingart, G., Schoedl-Hummel, K., Neumann, N., Becker, M., Varmuza, K., Liebner, F., et al., (2015). Severe drought stress is affecting selected primary metabolites, polyphenols, and volatile metabolites in grapevine leaves (Vitis vinifera cv. pinot noir). Plant Physiol. Biochem., 88, 17–26. Griffith, M., & Yaish, M. W., (2004). Antifreeze proteins in overwintering plants: A tale of two activities. Trends Plant Sci., 9, 399–405. Gull, A., Lone, A. A., & Wani, N. U. I., (2019). In: De Oliveira, A. B., (ed.), Abiotic and Biotic Stress in Plants. Intech Open. Handa, N., Kohli, S. K., Sharma, A., Thukral, A. K., Bhardwaj, R., Abd, A. E. F., Alqarawi, A. A., & Ahmad, P., (2019). Selenium modulates dynamics of antioxidative defense expression, photosynthetic attributes and secondary metabolites to mitigate chromium toxicity in Brassica juncea L. plants. Environ. Exp. Bot., 161, 180–192. Harborne, J. B., Baxter, H., & Moss, G. P., (1999). Phytochemical Dictionary: A Handbook of Bioactive Compounds from Plants (2nd edn., p. 976). London: Taylor & Francis. Hernandez, I., Alegre, L., Van, B. F., & Munne-Bosch, S., (2009). How relevant are flavonoids as antioxidants in plants? Trends Plant Sci., 14, 125–132. Hodaei, M., Rahimmalek, M., Arzani, A., & Talebi, M., (2018). The effect of water stress on phytochemical accumulation, bioactive compounds and expression of key genes involved in flavonoid biosynthesis in Chrysanthemum morifolium L. Ind. Crops Prod., 120, 295–304.

60

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Huyskens-Keil, S., Eichholz, I., Kroh, L., & Rohn, S., (2012). UV-B induced changes of phenol composition and antioxidant activity in black currant fruit (Ribes nigrum L.). J. App. Bot. Food Qual., 81, 140–144. IUPAC, (1979). Nomenclature of Organic Chemistry. Pergamon Press: Oxford, UK. Jain, A., Singh, A., Singh, S., & Singh, H. B., (2015). Phenols enhancement effect of microbial consortium in pea plants restrains Sclerotinia sclerotiorum. Biol. Control, 89, 23–32. Jain, C., Khatana, R., & Vijayvergia, R., (2019). Bioactivity of secondary metabolites of various plants: A review. Int. J. Pharm. Sci. Res., 10, 494–498. Jan, R., Asaf, S., Numan, M., Lubna, & Kim, K. M., (2021). Plant secondary metabolite biosynthesis and transcriptional regulation in response to biotic and abiotic stress conditions. Agronomy, 11, 968. Karwasara, V. S., & Dixit, V. K., (2013). Culture medium optimization for camptothecin production in cell suspension cultures of Nothapodytes nimmoniana (J. Grah.) Mabberley. Plant Biotechnol. Rep., 7, 357–369. Kaur, L., & Zhawar, V. K., (2015). Phenolic parameters under exogenous ABA, water stress, and salt stress in two wheat cultivars varying in drought tolerance. Ind. J. Plant Physiol., 20, 151–156. Kaur, P., Bali, S., Sharma, A., Vig, A. P., & Bhardwaj, R., (2017). Effect of earthworms on growth, photosynthetic efficiency and metal uptake in Brassica juncea L. plants grown in cadmium-polluted soils. Environ. Sci. Pollut. Res., 24, 13452–13465. Kaur, P., Bali, S., Sharma, A., Vig, A. P., & Bhardwaj, R., (2018). Role of earthworms in phytoremediation of cadmium (Cd) by modulating the antioxidative potential of Brassica juncea L. Appl. Soil Ecol., 124, 306–316. Khalil, N., Fekry, M., Bishr, M., El-Zalabani, S., & Salama, O., (2018). Foliar spraying of salicylic acid-induced accumulation of phenolics increased radical scavenging activity and modified the composition of the essential oil of water-stressed Thymus vulgaris L. Plant Physiol. Biochem., 123, 65–74. Khan, N. A., Khan, M. I. R., Asgher, M., Fatma, M., Masood, A., & Syeed, S., (2014). Salinity tolerance in plants: Revisiting the role of sulfur metabolites. J. Plant Biochem. Physiol., 2, 120. Kısa, D., Elmasta, S. M., Öztürk, L., & Kayır, Ö., (2016). Responses of the phenolic compounds of Zea mays under heavy metal stress. Appl. Biol. Chem., 59, 813–820. Kohli, S. K., Handa, N., Sharma, A., Kumar, V., Kaur, P., & Bhardwaj, R., (2017). Synergistic effect of 24-epibrassinolide and salicylic acid on photosynthetic efficiency and gene expression in Brassica juncea L. under Pb stress. Turk. J. Biol., 41, 943–953. Korosi, L., Bouderias, S., Csepregi, K., Bognar, B., Teszlak, P., Scarpellini, A., Castelli, A., Hideg, E., & Jakab, G., (2019). Nanostructured TiO2-induced photocatalytic stress enhances the antioxidant capacity and phenolic content in the leaves of Vitis vinifera in a genotypedependent manner. J. Photochem. Photobiol. B, 190, 137–145. Kossel, A., (1891). About Mucus and Mucus-Forming Substances (Vol. 17, pp. 1297–1299). Dtsch. Med. Wochenschr. Kováčik, J., Klejdus, B., Hedbavny, J., Štork, F., & Bačkor, M., (2009). Comparison of cadmium and copper effect on phenolic metabolism, mineral nutrients and stress-related parameters in Matricaria chamomilla plants. Plant Soil, 320, 231. Kristensen, B. K., Askerlund, P., Bykova, N. V., Egsgaard, H., & Moller, I. M., (2004). Identification of oxidised proteins in the matrix of rice leaf mitochondria

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

61

by immunoprecipitation and two-dimensional liquid chromatography-tandem mass spectrometry. Phytochemistry, 65, 1839–1851. Lam, T. B. T., Kadoya, K., & Liyama, K., (2001). Bonding of hydroxycinnamic acids to lignin: Ferulic and p-coumaric acids are predominantly linked at the benzyl position of lignin, not the beta-position, in grass cell walls. Phytochemistry, 57, 987–992. Lee, M. J., Son, J. E., & Oh, M. M., (2014). Growth and phenolic compounds of Lactuca sativa L. grown in a closed-type plant production system with UV-A, -B, or -C lamp. J. Sci. Food Agric., 94, 197–204. Leng, X., Jia, H., Sun, X., Shangguan, L., Mu, Q., Wang, B., & Fang, J., (2015). Comparative transcriptome analysis of grapevine in response to copper stress. Sci. Rep., 5, 17749. Li, M., Li, Y., Zhang, W., Li, S., Gao, Y., Ai, X., Zhang, D., Liu, B., & Li, Q., (2018). Metabolomics analysis reveals that elevated atmospheric CO2 alleviates drought stress in cucumber seedling leaves. Anal. Biochem., 559, 71–85. Linić, I., Šamec, D., Grúz, J., Vujčić, B. V., Strnad, M., & Salopek. S. B., (2019). Involvement of phenolic acids in short-term adaptation to salinity stress is species-specific among Brassicaceae. Plants, 8, 155. Liu, J. H., Peng, T., & Dai, W., (2014). Critical cis-acting elements and interacting transcription factors: Key players associated with abiotic stress responses in plants. Plant Mol. Biol. Report., 32, 303–317. Liu, M., Cao, B., Zhou, S., & Liu, Y., (2012). Responses of the flavonoid pathway to UV-B radiation stress and the correlation with the lipid antioxidant characteristics in the desert plant Caryopteris mongolica. Acta Ecol. Sin., 32, 150–155. Lucini, L., Borgognone, D., Rouphael, Y., Cardarelli, M., Bernardi, J., & Colla, G., (2016). Mild potassium chloride stress alters the mineral composition, hormone network, and phenolic profile in artichoke leaves. Front. Plant Sci., 7, 948. Ma, D., Sun, D., Wang, C., Li, Y., & Guo, T., (2014). Expression of flavonoid biosynthesis genes and accumulation of flavonoid in wheat leaves in response to drought stress. Plant Physiol. Biochem., 80, 60–66. Ma, Y., Wang, P., Gu, Z., Tao, Y., Shen, C., Zhou, Y., Han, Y., & Yang, R., (2019). Ca2+ involved in GABA signal transduction for phenolics accumulation in germinated hulless barley under NaCl stress. Food Chem. X, 2, 100023. Macheroux, P., Schmid, J., Amrhein, N., & Schaller, A., (1999). A unique reaction in a common pathway: Mechanism and function of chorismate synthase in the shikimate pathway. Planta, 207, 325–334. Maeda, H., & Dudareva, N., (2012). The shikimate pathway and aromatic amino acid biosynthesis in plants. Annu. Rev. Plant Biol., 63, 73–105. Mahdavi, V., Farimani, M. M., Fathi, F., & Ghassempour, A., (2015). A targeted metabolomics approach toward understanding metabolic variations in rice under pesticide stress. Anal. Biochem., 478, 65–72. Mariz-Ponte, N., Mendes, R. J., Sario, S., De Oliveira, J. F., Melo, P., & Santos, C., (2018). Tomato plants use non-enzymatic antioxidant pathways to cope with moderate UV-A/B irradiation: A contribution to the use of UV-A/B in horticulture. J. Plant Physiol., 221, 32–42. Martinez, V., Mestre, T. C., Rubio, F., Girones-Vilaplana, A., Moreno, D. A., Mittler, R., & Rivero, R. M., (2016). Accumulation of flavonols over hydroxycinnamic acids favors oxidative damage protection under abiotic stress. Front. Plant Sci., 7, 838.

62

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Mekawy, A. M. M., Abdelaziz, M. N., & Ueda, A., (2018). Apigenin pretreatment enhances growth and salinity tolerance of rice seedlings. Plant Physiol. Biochem., 130, 94–104. Michalak, A., (2006). Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol. J. Environ. Stud., 15, 523–530. Minatel, I. O., Borges, C. V., Ferreira, M. I., Gomez, H. A. G., Oliver, C. C. Y., & Lima, G. P. P., (2017). Phenolic compounds: Functional properties, impact of processing and bioavailability. In: Soto-Hernandez, M., Palma-Tenango, M., & Garcia-Mateos, M. D. R., (eds.), Phenolic Compounds - Biological Activity. IntechOpen. Minocha, S., Kumari, S., Tiwari, A., Gupta, A. K., Gandhi, S., & Sharma, A., (2015). An overview on tannins. IJPBA, 3, 9–11. Mishra, B., & Sangwan, N. S., (2019). Amelioration of cadmium stress in Withania somnifera by ROS management: Active participation of primary and secondary metabolism. Plant Growth Regul., 87, 403–412. Miura, K., Jin, J. B., Lee, J., Yoo, C. Y., Stirm, V., Miura, T., Ashworth, E. N., et al., (2007). SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell, 19, 1403–1414. Moreira-Rodriguez, M., Nair, V., Benavides, J., Cisneros-Zevallos, L., & Jacobo-Velazquez, D. A., (2017). UVA, UVB light, and methyl jasmonate, alone or combined, redirect the biosynthesis of glucosinolates, phenolics, carotenoids, and chlorophylls in broccoli sprouts. Int. J. Mol. Sci., 18, 2330. Naikoo, M. I., Dar, M. I., Raghib, F., Jaleel, H., Ahmad, B., Raina, A., Khan, F. A., & Naushin, F., (2019). Role and regulation of plants phenolics in abiotic stress tolerance: An overview. In: Khan, M. I. R., Reddy, P. S., Ferrante, A., & Khan, N. A., (ed.), Plant Signaling Molecules (pp. 157–168). Elsevier: Amsterdam, The Netherlands. Nakabayashi, R., Yonekura-Sakakibara, K., Urano, K., Suzuki, M., Yamada, Y., Nishizawa, T., Matsuda, F., et al., (2014). Enhancement of oxidative and drought tolerance in Arabidopsis by over accumulation of antioxidant flavonoids. Plant J., 77, 367–379. Nascimento, L., Leal-Costa, M. V., Menezes, E. A., Lopes, V. R., Muzitano, M. F., Costa, S. S., & Tavares, E. S., (2015). Ultraviolet-B radiation effects on phenolic profile and flavonoid content of Kalancho epinnata. J. Photochem. Photobiol. B, 148, 73–81. Navarro, J. M., Flores, P., Garrido, C., & Martinez, V., (2006). Changes in the contents of antioxidant compounds in pepper fruits at different ripening stages, as affected by salinity. Food Chem., 96, 66–73. Nenadis, N., Llorens, L., Koufogianni, A., Diaz, L., Font, J., Gonzalez, J. A., & Verdaguer, D., (2015). Interactive effects of UV radiation and reduced precipitation on the seasonal leaf phenolic content/composition and the antioxidant activity of naturally growing Arbutus unedo plants. J. Photochem. Photobiol. B, 153, 435–444. Nguyen, T. N., Son, S. H., Jordan, M. C., Levin, D. B., & Ayele, B. T., (2016). Lignin biosynthesis in wheat (Triticum aestivum L.): Its response to waterlogging and association with hormonal levels. BMC Plant Biol., 16, 28. Noctor, G., Reichheld, J. P., & Foyer, C. H., (2018). ROS-related redox regulation and signaling in plants. Semin. Cell Dev. Biol., 80, 3–12. Parida, A. K., Das, A. B., Sanada, Y., & Mohanty, P., (2004). Effects of salinity on biochemical components of the mangrove, Aegiceras corniculatum. Aqua. Bot., 80, 77–87. Pérez-Clemente, R. M., Vives, V., Zandalinas, S. I., López-Climent, M. F., Munoz, V., & Gomez-Cadenas, A., (2013). Biotechnological approaches to study plant responses to stress. Biomed Res. Int., 2013, 654120.

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

63

Perin, E. C., Da Silva, M. R., Borowski, J. M., Crizel, R. L., Schott, I. B., Carvalho, I. R., Rombaldi, C. V., & Galli, V., (2019). ABA-dependent salt and drought stress improve strawberry fruit quality. Food Chem., 271, 516–526. Petridis, A., Therios, I., Samouris, G., & Tananaki, C., (2012). Salinity-induced changes in phenolic compounds in leaves and roots of four olive cultivars (Olea europaea L.) and their relationship to antioxidant activity. Environ. Exp. Bot., 79, 37–43. Poonam, R. K., Bhardwaj, R., & Sirhindi, G., (2015). Castasterone regulated polyphenolic metabolism and photosynthetic system in Brassica juncea plants under copper stress. J. Pharmacogn. Phytochem., 4, 282–289. Pushpalatha, H. B., Pramod, K., Devanathan, R., & Sundaram, R., (2015). Use of bergenin as an analytical marker for standardization of the polyherbal formulation containing Saxifraga ligulata. Pharmacogn. Mag., 11, S60. Rai, M., Rai, A., Kawano, N., Yoshimatsu, K., Takahashi, H., Suzuki, H., Kawahara, N., et al., (2017). De novo RNA sequencing and expression analysis of Aconitum carmichaelii to analyze key genes involved in the biosynthesis of diterpene alkaloids. Molecules, 22, 2155. Raigond, P., Raigond, B., Kaundal, B., Singh, B., Joshi, A., & Dutt, S., (2017). Effect of zinc nanoparticles on antioxidative system of potato plants. J. Environ. Biol., 38, 435–439. Regvar, M., Bukovnik, U., Likar, M., & Kreft, I., (2012). UV-B radiation affects flavonoids and fungal colonization in Fagopyrum esculentum and F. tataricum. Open Life Sci., 7, 275–283. Reiter, R., Paredes, S., Korkmaz, A., Jou, M. J., & Tan, D. X., (2008). Melatonin combats molecular terrorism at the mitochondrial level. Interdiscip. Toxicol., 1, 137–149. Rezayian, M., Niknam, V., & Ebrahimzadeh, H., (2018). Differential responses of phenolic compounds of Brassica napus under drought stress. Iran. J. Plant Physiol., 8, 2417–2425. Rezazadeh, A., Ghasemnezhad, A., Barani, M., & Telmadarrehei, T., (2012). Effect of salinity on phenolic composition and antioxidant activity of artichoke (Cynara scolymus L.) leaves. Res. J. Med. Plants, 6, 245–252. Richards, T. A., Dacks, J. B., Campbell, S. A., Blanchard, J. L., Foster, P. G., McLeod, R., & Roberts, C. W., (2006). Evolutionary origins of the eukaryotic shikimic pathway: Gene fusions, horizontal gene transfer, and endosymbiotic replacements. Eukaryot. Cell, 5, 1517–1531. Rodríguez-Calzada, T., Qian, M., Strid, A., Neugart, S., Schreiner, M., Torres-Pacheco, I., & Guevara-González, R. G., (2019). Effect of UV-B radiation on morphology, phenolic compound production, gene expression, and subsequent drought stress responses in chili pepper (Capsicum annuum L.). Plant Physiol. Biochem., 134, 94–102. Rossi, L., Borghi, M., Francini, A., Lin, X., Xie, D. Y., & Sebastiani, L., (2016). Salt stress induces differential regulation of the phenylpropanoid pathway in Olea europaea cultivars frantoio (salt-tolerant) and leccino (salt-sensitive). J. Plant Physiol., 204, 8–15. Šamec, D., Karalija, E., Šola, I., Vujˇci´c Bok, V., & Salopek-Sondi, B., (2021). The role of polyphenols in abiotic stress response: The influence of molecular structure. Plants, 10, 118. Santos-Sánchez, N. F., Salas-Coronado, R., Hernández-Carlos, B., & Villanueva-Cañongo, C., (2019). Shikimic acid pathway in biosynthesis of phenolic compounds. In: SotoHernández, M., García-Mateos, R., & Palma-Tenango, M., (eds.), Plant Physiological Aspects of Phenolic Compounds. IntechOpen.

64

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Sarker, U., & Oba, S., (2018). Augmentation of leaf color parameters, pigments, vitamins, phenolic acids, flavonoids and antioxidant activity in selected Amaranthus tricolor under salinity stress. Sci. Rep., 8, 12349. Scagel, C. F., Lee, J., & Mitchell, J. N., (2019). Salinity from NaCl changes the nutrient and polyphenolic composition of basil leaves. Ind. Crops Prod., 127, 119–128. Seigler, D. S., (2012). Plant Secondary Metabolism. Springer Science & Business Media: Dordrecht, The Netherland. Selmar, D., (2008). Potential of salt and drought stress to increase pharmaceutical significant secondary compounds in plants. Landbauforsch. Volkenrode, 58, 139. Sharma, A., Kumar, V., Thukral, A. K., & Bhardwaj, R., (2016). Epibrassinolide-imidacloprid interaction enhances non-enzymatic antioxidants in Brassica juncea L. Ind. J. Plant Physiol., 21, 70–75. Sharma, A., Shahzad, B., Rehman, A., Bhardwaj, R., Landi, M., & Zheng, B., (2019a). Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules, 24, 2452. Sharma, A., Yuan, H., Kumar, V., Ramakrishnan, M., Kohli, S. K., Kaur, R., Thukral, A. K., Bhardwaj, R., & Zheng, B., (2019b). Castasterone attenuates insecticide induced phytotoxicity in mustard. Ecotoxicol. Environ. Saf., 179, 50–61. Sharma, S., & Shrivastava, N., (2016). Renaissance in phytomedicines: Promising implications of NGS technologies. Planta, 244, 19–38. Silva, F. L. B., Vieira, L. G. E., Ribas, A. F., Moro, A. L., Neris, D. M., & Pacheco, A. C., (2018). Proline accumulation induces the production of total phenolics in transgenic tobacco plants under water deficit without increasing the G6PDH activity. Theor. Exp. Plant Physiol., 30, 251–260. Singh, O. S., Pant, N. C., Laishram, M. L., Tewari, R. D., Joshi, K., & Pandey, C., (2018). Effect of CuO nanoparticles on polyphenols content and antioxidant activity in ashwagandha (Withania somnifera L. Dunal). J. Pharmacogn. Phytochem., 7, 3433–3439. Singh, R. P., Rizvi, S. M. H., & Jaiwal, P. K., (2003). Genetic engineering for enhancing abiotic stress tolerance. In: Jaiwal, P., & Singh, R., (eds.), Improvement Strategies of Leguminosae Biotechnology (pp. 223–243). Dordrecht: Springer. Smirnov, O. E., Kosyan, A. M., Kosyk, O. I., & Taran, N. Y., (2015). Response of phenolic metabolism induced by aluminium toxicity in Fagopyrum esculentum Moench. plants. Ukr. Biochem. J., 87, 129–135. Strack, D., (1997). Phenolic metabolism. In: Dey, P. M., & Harborne, J. B., (eds.), Plant Biochemistry (p. 387). Academic Press: London, UK. Swieca, M., (2015). Elicitation with abiotic stresses improves pro-health constituents, antioxidant potential and nutritional quality of lentil sprouts. Saudi J. Biol. Sci., 22, 409–416. Sytar, O., Zivcak, M., Bruckova, K., Brestic, M., Hemmerich, I., Rauh, C., & Simko, I., (2018). Shift in accumulation of flavonoids and phenolic acids in lettuce attributable to changes in ultraviolet radiation and temperature. Sci. Hortic., 239, 193–204. Tai, D., Tian, J., Zhang, J., Song, T., & Yao, Y., (2014). A Malus crabapple chalcone synthase gene, McCHS, regulates red petal color and flavonoid biosynthesis. PLoS One, 9, e110570. Tzin, V., & Galili, G., (2010a). The biosynthetic pathways for shikimate and aromatic amino acids in Arabidopsis thaliana. Arabidopsis Book, 8, e0132. Tzin, V., & Galili, G., (2010b). Amino acids biosynthesis pathways in plants. Mol. Plant., 3, 956–972.

Involvement of Phenylpropanoid Pathway and Shikimic Acid Pathway

65

Valifard, M., Mohsenzadeh, S., Kholdebarin, B., & Rowshan, V., (2014). Effects of salt stress on volatile compounds, total phenolic content and antioxidant activities of Salvia mirzayanii. S. Afr. J. Bot., 93, 92–97. Valifard, M., Mohsenzadeh, S., Niazi, A., & Moghadam, A., (2015). Phenylalanine ammonialyase isolation and functional analysis of phenylpropanoid pathway under salinity stress in ‘Salvia’ species. Aust. J. Crop Sci., 9, 656–665. Varela, M. C., Arslan, I., Reginato, M. A., Cenzano, A. M., & Luna, M. V., (2016). Phenolic compounds as indicators of drought resistance in shrubs from Patagonian shrub lands (Argentina). Plant Physiol. Biochem., 104, 81–91. Venugopala, K., Rashmi, V., & Odhav, B., (2013). Review on natural coumarin lead compounds for their pharmacological activity. Biomed. Res. Int., 2013, 963248. Verma, N., & Shukla, S., (2015). Impact of various factors responsible for fluctuation in plant secondary metabolites. J. Appl. Res. Med. Aromat. Plants, 2, 105–113. Verma, S., Nizam, S., & Verma, P. K., (2013). Biotic and abiotic stress signaling in plants. In: Sarwat, M., Ahmad, A., & Abdin, M. Z., (eds.), Stress Signaling in Plants: Genomics and Proteomics Perspective (Vol. 1, pp. 25–49). Springer Science: New York, USA. Vogt, T., (2010). Phenylpropanoid biosynthesis. Mol. Plant, 3, 2–20. Walker, E. H., Pacold, M. E., Perisic, O., Stephens, L., Hawkins, P. T., Wymann, M. P., & Williams, R. L., (2000). Structural determinants of phosphoinositide 3-kinase inhibition by wortmannin, LY294002, quercetin, myricetin, and staurosporine. Mol. Cell, 6, 909–919. Wang, F., Zhu, H., Chen, D., Li, Z., Peng, R., & Yao, Q., (2016b). A grape bHLH transcription factor gene, VvbHLH1, increases the accumulation of flavonoids and enhances salt and drought tolerance in transgenic Arabidopsis thaliana. Plant Cell Tiss. Org. Cult., 125, 387–398. Wang, H., Wang, H., Shao, H., & Tang, X., (2016a). Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front. Plant Sci., 7, 67. Wang, J., Yuan, B., & Huang, B., (2019a). Differential heat-induced changes in phenolic acids associated with genotypic variations in heat tolerance for hard fescue. Crop Sci., 59, 667–674. Wang, L., Shan, T., Xie, B., Ling, C., Shao, S., Jin, P., & Zheng, Y., (2019b). Glycine betaine reduces chilling injury in peach fruit by enhancing phenolic and sugar metabolisms. Food Chem., 272, 530–538. Wang, Q., Eneji, A. E., Kong, X., Wang, K., & Dong, H., (2015). Salt stress effects on secondary metabolites of cotton in relation to gene expression responsible for aphid development. PLoS One, 10, e0129541. Waterman, P. G., & Mole, S., (1989). Extrinsic factors influencing production of secondary metabolites in plants. Insect-Plant Interact., 1, 107–134. Weaver, L. M., & Herrmann, K. M., (1997). Dynamic of the shikimate pathway. Trends Plant Sci., 9, 346–351. Wen, L., Jiang, Y., Yang, J., Zhao, Y., Tian, M., & Yang, B., (2017). Structure, bioactivity, and synthesis of methylated flavonoids. Ann. N. Y. Acad. Sci., 1398, 120–129. Xu, Y., Charles, M. T., Luo, Z., Mimee, B., Veronneau, P. Y., Rolland, D., & Roussel, D., (2017). Preharvest ultraviolet C irradiation increased the level of polyphenol accumulation and flavonoid pathway gene expression in strawberry fruit. J. Agric. Food Chem., 65, 9970–9979.

66

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Yamaguchi-Shinozaki, K., & Shinozaki, K., (2006). Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol., 57, 781–803. Yan, J., Wang, B., Jiang, Y., Cheng, L., & Wu, T., (2014). GmFNSII-controlled soybean flavone metabolism responds to abiotic stresses and regulates plant salt tolerance. Plant Cell Physiol., 55, 74–86. Yu, S., Yan, H., Zhang, L., Shan, M., Chen, P., Ding, A., & Li, S. F. Y., (2017). A review on the phytochemistry, pharmacology, and pharmacokinetics of amentoflavone, a naturally occurring biflavonoid. Molecules, 22, 299. Yuan, Y., Liu, Y., Wu, C., Chen, S., Wang, Z., Yang, Z., Qin, S., & Huang, L., (2012). Water deficit affected flavonoid accumulation by regulating hormone metabolism in Scutellaria baicalensis Georgi roots. PLoS One, 7, e42946. Zafari, S., Sharifi, M., Ahmadian, C. N., & Mur, L. A., (2016). Modulation of Pb-induced stress in Prosopis shoots through an interconnected network of signaling molecules, phenolic compounds and amino acids. Plant Physiol. Biochem., 99, 11–20. Zhang, Z. Z., Li, X. X., Chu, Y. N., Zhang, M. X., Wen, Y. Q., Duan, C. Q., & Pan, Q. H., (2012). Three types of ultraviolet irradiation differentially promote expression of shikimate pathway genes and production of anthocyanins in grape berries. Plant Physiol. Biochem., 57, 74–83. Zhou, P., Li, Q., Liu, G., Xu, N., Yang, Y., Zeng, W., Chen, A., & Wang, S., (2018). Integrated analysis of transcriptomic and metabolomic data reveals critical metabolic pathways involved in polyphenol biosynthesis in Nicotiana tabacum under chilling stress. Funct. Plant Biol., 46, 30–43. Zhu, J. J., & Jiang, J. G., (2018). Pharmacological and nutritional effects of natural coumarins and their structure-activity relationships. Mol. Nutr. Food Res., 62. Zhu, J. K., (2016). Abiotic stress signaling and responses in plants. Cell, 167, 313–324. Zhu, Q., Sui, S., Lei, X., Yang, Z., Lu, K., Liu, G., Liu, Y. G., & Li, M., (2015). Ectopic expression of the coleus R2R3 MYB-type proanthocyanidin regulator gene SsMYB3 alters the flower color in transgenic tobacco. PLoS One, 10, e0139392. Zlotek, U., Szymanowska, U., Baraniak, B., & Karas, M., (2015). Antioxidant activity of polyphenols of adzuki bean (Vigna angularis) germinated in abiotic stress conditions. Acta Sci. Pol. Technol. Aliment., 14, 55–63.

CHAPTER 3

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway and Regulation of Environmental Stress Tolerance

LEKSHMY SATHEE*, M. K. MALINI, PRAMOD KUMAR, and SUDHIR KUMAR

Division of Plant Physiology, ICAR–Indian Agricultural Research Institute, New Delhi, India *

Corresponding author. E-mail: [email protected]

ABSTRACT Two spatially separated yet inter-connected pathways, mevalonic acid (MVA) and methylerythritol phosphate (MEP) pathways generate terpenoid precursors in plants. Terpenoid compounds play a significant role in plant metabolism and environmental stress defense. Terpenoids compounds include plant hormones, pigments, and commercially important products. This chapter elaborates on the information on terpenoid biosynthesis and the role of terpenoid compounds in stress protection. The possession of both MVA and MEP pathways provides higher plants an added advantage to overcome the constraints of the sedentary lifestyle. The spatial distribution of the MEP pathway in plastids and the MVA pathway in the cytoplasm helps optimize terpene biosynthesis based on Carbon and ATP flux. Utilizing the buffering capacity of two pathways, plants have diversified the terpenoid cafeteria to adapt to the complex soil and environmental conditions. The perusal of the information highlights the importance of terpenoid compounds Biology and Biotechnology of Environmental Stress Tolerance in Plants: Secondary Metabolites in Environmental Stress Tolerance, Volume 1. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

68

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

for adaptation to ecological vagaries, such as extremes of temperature, drought, flooding, nutrient stress, and ozone. 3.1 INTRODUCTION Terpenoids, also called isoprenoids, are one of the largest and most diverse natural secondary metabolites (Tholl, 2015; Tarkowská & Strnad, 2018). Isoprene is a volatile compound produced by the action of the enzyme isoprene synthase (ISPS). Many plant species emit isoprene, leading to the output of 600 Tg per year globally. Plants spend approximately 2% of fixed Carbon for isoprene emission (Lantz et al., 2019). Based on the number of 5 carbon units, terpenoids are classified into, i.e., Hemi- (C5), mono- (C10), sesqui- (C15), di- (C20), sester- (C25), tri- (C30) and tetra- (C40: carotenoids) terpenoids (Yazaki et al., 2017). Terpene synthase (TPS) produces the terpenoid backbone, and the diverse terpenoid compounds are then produced by hydroxylation, dehydrogenation, acylation, or glycosylation (Dudareva et al., 2004; Pichersky et al., 2006) of the backbone. The five-carbon compounds, isopentenyl diphosphate (IPP) and dimethylallyl diphosphate (DMAPP), are added head to tail to produce terpenoids (Berthelot et al., 2012; Laskovics & Poulter, 1981). At first, the condensation of IPP and DMAPP produces geranyl diphosphate (GPP), a monoterpene. Then, farnesyl diphosphate (FPP) and geranylgeranyl diphosphate (GGPP) are produced. Further, the head-to-head condensation of two molecules of FPP and GGPP produces squalene (triterpenoid) and phytoene (tetraterpenoid). The linear precursor molecules undergo further modifications (oxidation, acetylation) (Luthra et al., 1999; McGarvey & Croteau, 1995). Two spatially separated and connected pathways: The mevalonic acid (MVA) and methylerythritol phosphate (MEP) pathways (Vranová et al., 2013) produce the terpenoid precursors in plants. The MVA pathway is common and is found in bacteria (Smit & Mushegian, 2000), yeasts (Disch & Rohmer, 1998), and animals (Kovacs et al., 2002). The majority of gramnegative bacteria (Rohmer et al., 1993), cyanobacteria (Proteau, 1998), and green algae have an MEP pathway (Disch et al., 1998). Higher plants, the red alga Cyanidium caldarium, and the golden alga Ochromonas Danica utilize both MVA and MEP pathways (B M Lange et al., 1998; Markus & Croteau, 1999; Lichtenthaler, 1999). MEP pathway is localized in plastids, and the MVA pathway is distributed in the cytoplasm, ER, and peroxisomes (Vranová et al., 2013). Farnesyl

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway

69

diphosphate synthases elongate the IPP and DMAPP, produced by the MVA pathway. The step catalyzed by 3-hydroxy-3-methyl-glutaryl-CoA reductase is the rate-limiting step in the MVA pathway (Hemmerlin, 2013; Hemmerlin et al., 2012; Tholl, 2015; Vranová et al., 2013). Apart from the MVA and MEP pathway, plant genomes contain the isopentenyl phosphate kinase (IPK) gene (VanNice et al., 2014). IPK converts isopentenyl phosphate (IP) and dimethylallyl phosphate (DMAP) to IPP and DMAPP in the cytosol. The ubiquitous presence of IPK in the sequenced plant genomes suggests its essential role in terpenoid biosynthesis. The IPP and DMAPP of the MEP pathway originate from HMBPP by 4-hydroxy-3-methyl but-2-enyl diphosphate reductase (HDR) (Rohdich et al., 2002). The MEP pathway includes seven conserved enzymatic steps (Banerjee & Sharkey, 2014) that catalyzes the formation of 1-deoxy-D-xylulose 5-phosphate (DXP) by the enzyme 1-deoxy-D-xylulose-5-phosphate synthase (DXS), conversion of DXP to MEP by the enzyme 1-deoxy-D-xylulose-5-phosphate reductor isomerase (DXR), conversion of MEP to methylerythritol 2,4-cyclodiphosphate (MEcDP), conversion of MEcDP to hydroxymethyl butenyl diphosphate (HMBDP) by HMBDP synthase (HDS) and finally the reduction of HMDBP to IDP and DMADP by HMBDP reductase (HDR) (George et al., 2018; Martin et al., 2003; Sivy et al., 2011). The possession of both MVA and MEP pathways provides higher plants an added advantage to rise above the constraints of the sedentary lifestyle. The spatial distribution of the MEP pathway in plastids and MVA pathway in the cytoplasm helps optimize terpene biosynthesis based on Carbon and ATP flux. Utilizing the buffering capacity of two pathways, plants have diversified the terpenoid cafeteria to adapt to the complex soil and environmental conditions (Van Wezel and McDowall, 2011; Zhou et al., 2012). The regulatory role of light in isoprenoid biosynthesis is well established (Vranová et al., 2013), the MVA pathway genes are repressed by light (Rodríguez-Concepción, 2006). Along with a decrease in the accumulation of sitosterol land stigmasterol (Ghassemian et al., 2006). Sunlight stimulates the proliferation of MEP-pathway transcripts and promotes viatol chains and carotenoids (Cordoba et al., 2009; Ghassemian et al., 2006; RodríguezConcepción, 2010) in many plant species (Hemmerlin et al., 2012). In A. thaliana, light has a stimulatory role in genes encoding enzymes downstream to MEP-pathway, such as AtGGPPS11, AtPSY (carotenoid biosynthesis), AtHEMA1, AtCHLH, AtGUN4, and AtVTE3 (tocopherol and plastoquinone biosynthesis) (Ghassemian et al., 2006; Hsieh & Goodman, 2005; Meier et al., 2011; Rodríguez-Concepción, 2006; Stephenson et al., 2009;

70

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Toledo-Ortiz et al., 2010). The light-dependent stimulation of carotenoid and chlorophyll accumulation ultimately converts etioplasts into chloroplasts (Rodríguez-Concepción et al., 2004; Toledo-Ortiz et al., 2010) and differentiate the organelle equipped with the required amounts of phylloquinone, plastoquinone, and α-tocopherol required during autotrophy (Ghassemian et al., 2006). In Arabidopsis, a period of darkness represses the accumulation of MEP-pathway genes except for AtHDR (Hsieh & Goodman, 2005). MEPpathway enzyme activities are regulated post-translationally also (Ghassemian et al., 2006). The MVA- and MEP-pathway genes are regulated by diverse environmental and soil factors; however, the signaling mechanism and associated transcription factors are not known (Cordoba et al., 2009; Stermer et al., 1994; Tholl & Lee, 2011). The paralogs of regulatory genes are differentially deployed in both MVA pathway (e.g., HMGR) and the MEP pathway (e.g., DXS). A specific paralog assist in primary metabolite synthesis (photosynthetic pigments and phytosterols), while another paralog is deployed towards synthesis of secondary metabolites (Choi et al., 1992; Dos Santos et al., 2003; Walter et al., 2002). 3.2 ISOPRENOID COMPOUNDS OF IMPORTANCE Isoprenoid compounds have a vast range of metabolic functions in photosynthesis, respiration, growth, development, membrane permeability, and environmental stress defense (Hemmerlin et al., 2012; Vranová et al., 2013; Tholl, 2015) (Figure 3.1). Terpenoids include a wide range of compounds, including hormones and pigments (tocopherol, brassinosteroids, gibberellin), vital in plant growth and stress signaling (Tholl; Piironen et al., 2000). Plant terpenoids also encompass compounds of industrial importance (Ajikumar et al., 2008; Immethun et al., 2013; Tippmann et al., 2013) and are an important avenue for product-oriented research (Bian et al., 2017). Economically essential products include natural latex, natural drugs, flavoring agents, biofuels, fragrances, natural pigments, pesticides, and disinfectants (Bohlmann & Keeling, 2008). Most primary terpenoid compounds are associated with photosynthetic component processes, light harvesting, electron transport, ATP production, and quenching of triplet chlorophylls. Chlorophyll is a tetrapyrrole macrocycle containing Mg2+ and a phytol chain. The lightharvesting complexes (LHC) are protected from photodamages by linear and partially cyclic carotenes and their oxygenated carotenes (xanthophyll). Carotenes and xanthophylls also make fruits and flowers visually attractive

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway

71

(Rodríguez-Concepción, 2010). Another important destination of plant terpenoids is membrane sterol lipids and isoprenoid-derived plant hormones. Five major plant hormones are directly or indirectly derived from isoprenoids: viz. Gibberellins, abscisic acid (ABA), cytokinins, brassinosteroids, and strigolactones (Santner et al., 2009). Protein prenylation, which regulates many developmental processes require isoprenoid compounds farnesyl diphosphate (FPP) and GGPP (Crowell & Huizinga, 2009; Galichet & Gruissem, 2003) (Figure 3.1). Isoprene and mono- and sesquiterpenes are volatile and are produced by plants in response to environmental stimuli. The amount and composition of volatiles emitted are dependent on plant species and the environment. Isoprene emission is observed in plants exposed to high-temperature, ozone, and reactive oxygen species (ROS), and herbivores and has a stress-protective role (Affek & Yakir, 2002; Centritto et al., 2014; Laothawornkitkul et al., 2008; Loivamäki et al., 2008; Loreto et al., 2001; Francesco & Schnitzler, 2010; Francesco & Velikova, 2001; Sasaki et al., 2007; Vickers et al., 2009). Fosmidomycin, an MEP pathway inhibitor, down-regulates isoprene emission and enhances high temperature (HT) and ozone sensitivity and ROS accumulation (Francesco & Velikova, 2001; Sharkey et al., 2001; Velikova et al., 2006; Velikova & Loreto, 2005). Plants deloused in isoprene are tolerant to ozone and oxidative stress temperature stress (Loreto et al., 2001; Sharkey et al., 2001; Singsaas et al., 1997; Velikova et al., 2006). The physiological significance and mechanism of isoprene emission are not clear. Initially, isoprenes were thought to have a protective role in thylakoid membrane protection (Katja et al., 2007; Owen & Peñuelas, 2005; Sharkey & Singsaas, 1995; Singsaas & Sharkey, 1998, 2000; Velikova et al., 2011; Vickers et al., 2009), dissipation of excess energy trapped by photosynthetic pigments (Pollastri et al., 2014; Sanadze, 2010), ROS signaling, antioxidant defense and ozone quenching (Affek & Yakir, 2002; Francesco et al., 2001; Sharkey et al., 2008; Vickers, Gershenzon et al., 2009; Vickers et al., 2009). The membrane fluidity protection and ROS scavenging roles of isoprenes were refuted recently by Harvey et al. (2015). The physiological level of isoprene is unlikely to render membrane protection or ROS scavenging compared to other antioxidant compounds (Harvey et al., 2015; Harvey & Sharkey, 2016). Isoprene emission suppression in transgenic gray poplar (Katja et al., 2010) and exogenous application of isoprene in Arabidopsis (Harvey & Sharkey, 2016) showed that isoprene could induce alteration in gene networks, proteome (Vanzo et al., 2016), metabolome (Way et al., 2013), and metabolic fluxes (Katja et al., 2010; Ghirardo et al., 2014). ISPS converts

72

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

DMPP to isoprene and is essential for isoprene emission. In transgenic Arabidopsis overexpressing ISPS, the ATP-synthase activity was altered (Velikova et al., 2011) and confirmed the hypothesis that isoprenes interact with membrane-bound proteins and induce signaling events (Harvey & Sharkey, 2016). Similarly, in Arabidopsis plants fumigated with 20 μL L–1 of isoprene, genes associated with photosynthesis, flavonoid, and phenylpropanoid biosynthesis and stress protection were expressed affected (Harvey & Sharkey, 2016). Harvey & Sharkey (2016) suggested that isoprene serves as a signaling molecule mediating transcriptional regulation of stress tolerance. Arabidopsis transgenic lines overexpressing Eucalyptus globulus ISPS (Zuo et al., 2019) showed higher leaf chlorophyll and carotenoid contents. The expression of genes associated with plant hormones (gibberellic acid (GA) and jasmonic acid (JA)) and stress tolerance were changed by isoprene emission. As discussed earlier, isoprene regulates gene expression and act as a signaling molecule.

FIGURE 3.1  Schematic model showing the importance of terpenoids in plant metabolism and stress adaptation.

3.3 MODULATION OF TERPENOID METABOLISM BY ABIOTIC STRESSORS 3.3.1 MODULATION OF TERPENOID METABOLISM BY NUTRIENT DEFICIENCY AND TOXICITY Reports suggest the involvement of different nutrients in terpenoid abundance in the plant. For example, nitrogen (N) indirectly determines the carbon substrate requirement for isoprene synthesis (Ormeño & Fernandez, 2012). Nitrogen promotes isoprene, mono, and sesquiterpenoid emission in response to environmental stresses. Soil N and terpenoid storage (Sangwan et al., 2001) showed a direct relationship (Lerdau et al., 1995; Elena Ormeño et al., 2008)

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway

73

in many plant species. Phosphorus (P) is a component of terpenoid precursors (IPP and DMAPP: dimethylallyl pyrophosphate) and reducing equivalents ATP and NADPH required for terpenoid synthesis. In Quercus coccifera L (Niinemets et al., 2002), 28 moles of NADPH and 40 moles of ATP are required to synthesize monoterpenoids. Deficiency of P instigates the remobilization of P from membrane phospholipids and thus affects the membrane stability and can increase isoprene emission (Kobayashi et al., 2009). On the other hand, the increased isoprene emission was able to stabilize membrane bilayer Siwko et al. (2007) in response to heat stress and P deficiency. Herbivore, warming, and moderate N addition increased the periodic BVOC emission from Scots pine seedlings (Tiiva et al., 2018). Hoshika et al. (2020) investigated O3, soil N, and P’s combined effect on isoprene emission from Oxford poplar clones. O3 decreased the periodic isoprene emission in September due to the reduced net photosynthesis. Isoprene emission was positively correlated with leaf ABA content in poplar (Hoshika et al., 2020). Peñuelas et al. (2011) studied the nutrient and carbon-based secondary compounds (CBSC) in 86 species grown in Hawaii’s young soil forest or an old soil forest in Borneo. The nutrient content was higher in Hawaii than in Borneo, while the number of species containing terpenes was significantly, more significant in Borneo (97%) than in Hawaii (34%). The longest adaptation time in Borneo created an array of defense, allopathic, and interspecies relationships of plants. Carriero et al. (2016) reported that in silver birch (Betula pendula), the exposure to ozone and the dosage of N fertilizer, i.e., both had determinant effects on the emission of BVOC (biogenic volatile organic compounds) by a direct impact on emission rates and indirectly by affecting the leaf area. The α-pinene, β-pinene, limonene, ocimene, (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), and hexanal were the major BVOCs emitted by silver birch. While BVOC emission was increased by ozone treatment, there was a concomitant decrease in leaf area. The reverse was true in the case of N fertilization where leaf area was improved while the emission of α-pinene and β-pinene emission showed a decreasing trend. N fertilization augmented the emission of auimne, hexanal, and DMNT. Llusia et al. (2014) also reported that ozone and high soil N deprecated the emission of terpenes in O. compressus and T. striatum, which could be a determinant of the competitiveness of these plants. A perusal of the above discussion indicates that N has a significant role in the emission of BVOC in various plant species. In another recent study, Mu et al. (2019) analyzed the BVOC emission in response to N deposition (60 kg N ha–1) in Mediterranean shrubland (main species, Erica multiflora)

74

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

and a Mediterranean forest (main species, Quercus ilex). Drought stress and hot weather increased the isoprene emissions, while N fertilization increased the total terpene emissions and narrowed the terpene diversity (Kainulainen et al., 2000). In Rosmarinus officinalis plants there was a positive correlation among total terpenoid content and leaf N or P concentration (Bustamante et al., 2020). In potted in aspen and white oak trees, photon flux density (PFD) increased the isoprene emission, and leaf N content was positively correlated with isoprene emission (Litvak et al., 1996). 3.3.2 MODULATION OF TERPENOID METABOLISM BY TEMPERATURE STRESS IN PLANTS 3.3.2.1 HIGH-TEMPERATURE STRESS Several climate models have predicted a rise in global air temperature by the end of the 21st century (Yáñez-Serrano et al., 2019). Extreme HT or heat stress is defined as an increase in temperature beyond optimal functioning, which causes irreversible damage to plant growth development (Wahid et al., 2007). Further, the severity of high-temperature stress depends on intensity, duration, and tolerance to elevated temperature. In general, plants have developed several mechanisms to fight heat stress, e.g., Scavenging of ROS through the production of Antioxidants, production of heat socking protein (HSP), Osmolytes, polyamines, phenolics compounds, etc. (Dietz et al., 2016; Wahid et al., 2007). Under high-temperature stress, tolerant plants maintain better thylakoid membrane stability which helps to protect photosynthetic mechanics and thus allows higher CO2 fixation under elevated temperature (Niinemets, 2018; Rennenberg et al., 2006; Zhang & Sharkey, 2009). Further, isoprene and monoterpene Volatile isoprenoids play an essential role against oxidative stress (Holopainen & Gershenzon, 2010). These volatiles minimize the level of damaging ROS and thus improve heat tolerance (Affek & Yakir, 2002; Francesco & Fares, 2007; Francesco & Velikova, 2001; Sharkey et al., 2008). However, it requires a very high Carbon number and off course, energetic Cost (Harvey et al., 2015). There are reports that volatiles like isoprene may play an essential role in stabilizing cell membrane and its integrated Proteins (Katja et al., 2007; Josep and Munné-Bosch, 2005; Sharkey & Yeh, 2001; Singsaas et al., 1997; Velikova et al., 2011). Moreover, a fascinating role of isoprene in signaling to modulate plant gene expression has also been documented by earlier workers (Harvey & Sharkey, 2016; Zuo et al., 2019). Environmental factors like solar radiation and

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway

75

temperature, affect isoprenoid biosynthesis by affecting the photosynthesis of plants (Harley et al., 1996; Russell et al., 1992). High light intensity and HT stress stimulate isoprene formation and protect photosynthetic machinery (Sharkey & Singsaas, 1995). There are reports demonstrating that isoprene protects plants against oxidative stress (Affek & Yakir, 2002; Loreto et al., 2001; Francesco & Velikova, 2001; Josep & Munné-Bosch, 2005; Velikova et al., 2005). Though the protective mechanism of isoprene is not yet precise, it is explained that isoprene is embedded in the organelle membrane and increases the membrane’s stability by preventing membrane lipid desaturation under oxidative stress (Owen & Peñuelas, 2005). Yáñez-Serrano et al. (2019) investigated the role of isoprene emission in two contrasting tropical species, i.e., Ficus Benjamina and Pachira Aquatica, under heat stress. They found that Ficus Benjamina was more heat tolerant because of the higher constitutive emission of isoprene under heat stress. A similar report was also reported in two-hybrid populous clones, Nanlin 1388 (relatively high drought tolerance) and Nanlin 895 (relatively high thermotolerance) by Sun et al. (2020). Werner et al. (2020) found that HT stress redirects the proportion of significant metabolite into VOC (volute organic compound) synthesis pathway at the cost of reactions involve primary metabolism and thus exhibits their importance in stress protection. Volatile isoprene is mainly emitted from several broad leaves temperate and tropical live species (Arneth et al., 2008; Guenther et al., 2006; Alex et al., 1995) and plays a vital role in the managing of oxidative stress (Harper & Unger, 2018; Mentel et al., 2013; Wilkinson et al., 2009). Further, isoprene emission is more responsive to temperature than photosynthate activity (Lantz et al., 2019) and higher isoprene emission takes place above 45°C. The Vmax of ISPS has a peak of optimum between 42°C and 45°C (Lehning et al., 1999; Russell et al., 1992; Morfopoulos et al., 2013). Michaelis–Menten constant (KM) of ISPS for DMADP is sensitive to temperature between 30°C and 40°C even though the effect is less than the turnover rate (Lantz et al., 2019). It has been confirmed by conducting prolonged heat experiments that the isoprene emission is more in the thermotolerant genotype. Another approach noted that Poplar transgenic plants with ISPS silencing showed little or no isoprene emission (Katja et al., 2007). Moderately raised temperature reduces a quick increase in the heat and light tolerance of photosystem-II in plants like potato (Havaux & Tardy, 1996). Interestingly exposure of potato leaves to strong light for a short period significantly provoke the enhancement in the stability of photosystem-II (PS-II) to heat stress. As a result, thermotolerance of PS-II could be enhanced either directly through a conformational change of PS-II

76

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

(Light-Harvesting PS-II) (Non-photo Chemical quenching) or indirectly via a carotenoid dependent modulation of membrane lipid fluidity. Pollastri et al. (2014) reported that chloroplasts of isoprene emitting leaves dissipate less energy as heat than chloroplast of non-emitting leaves under HT (28–37°C) as evidenced by NPQ valve isoprene emission found maximum when the foliar temperature was between 30°C and 35°C and NPQ valve was quenched approx. 20%. Kumar et al. (2020a) also reported that the heat-tolerant genotype had a high value of zeaxanthin pigment, Fv/Fm rate, NPQ, photosynthetic rate, chlorophylls, total carotenoids, and low lipid peroxidation as compared to sensitive plants under heat stress conditions. A higher level of Zeaxanthin and a low value of violaxanthin in heat-tolerant genotypes and association of NPQ with heat tolerance indicates that the zeaxanthin cycle is involved in heat-tolerance of chickpea. Further, they also reported that the bioregulator’s application enhanced the tolerance and yield in chickpea by modulating the zeaxanthins cycle (Kumar et al., 2020b). 3.3.2.2 LOW TEMPERATURE STRESS Exposure of plants to temperatures below 15°C and above 0°C is referred to as low temperature or chilling stress, while exposure to temperature below 0°C is known as freezing stress. Low temperature stress reduces the CO2 fixation and stomatal conductance, which results in the disruption of photosynthesis and electron transport through the thylakoid membrane (Allen & Ort, 2001; Hussain et al., 2018). The reduction in photosynthesis leads to excess energy in PS-I and PS-II and leads to photoinhibition (Baker, 2008). This excess energy can induce overproduction of ROS like superoxide anion, hydroxyl anion and hydrogen peroxide (H2O2) that result in severe oxidative damage (Gill & Tuteja, 2010). Low temperature stress disrupts cell membrane structure and cause cellular electrolyte leakage (Oustric et al., 2017; Wang et al., 2017). To cope with the chilling or low temperature stress, plants have developed a complex defense system that includes enzymatic and non-enzymatic antioxidant molecules to avoid or decrease the chilly injuries. The mechanism of cold tolerance is associated with enhancement in the antioxidant system (Agurla et al., 2018; Hussain et al., 2018; Oustric et al., 2017; Santini et al., 2013). Zhang et al. (2017) reported that candidate gene in the terpenoid biosynthesis pathway is involved in the cold stress response of Santalum album. Gene expression analysis using qRTPCR showed a peak in the accumulation of SOCBF2 is 4.5-fold more than control leaves and roots following 12 h and 24 h of cold stress, respectively. A crucial role in increasing

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway

77

cold tolerance is played by the CBF-dependent pathway. The finding that terpene synthase genes (TSGS) are induced by cold stress provides a clue as to how to stimulate santalol biosynthesis and accumulation of essential oils. It has been found that growth at low temperature considerably alters the pigment composition in plants like maize, the significant decrease in levels of chlorophylls and beta-carotene was accompanied by the accumulation of large amounts of de-epoxy dixanthophylls, zeaxanthin, and anthraxanthinin. The chilling tolerant maize genotype had a lower constant of xanthophyll cycle carotenoids and less of their xanthophyll carotenoid cycle pool in the form of zeaxanthin, which indicated the involvement of zeaxanthin cycle in cold tolerance in Zea mays (Haldimann, 1998). 3.3.3 MODULATION OF TERPENOID METABOLISM BY WATER STRESS IN PLANTS 3.3.3.1 DROUGHT In the current climate change Scenario, all living organisms suffer from water scarcity, predominantly plants, because they are sessile. Drought is a spell during which an area or region experienced below-normal precipitation. Drought adversely affects a variety of physiological and biological responses at cellular and whole-plant level. Several classes protect against oxidation stress among the MEP pathway products, including carotenoid, tocopherols, and isoprene. The formation of these components might be favored under conditions leading to oxidative stress, including HT, High light and low water supply (Perreca et al., 2020). Among isoprenoids, phytol, and alpha-tocopherol in Brachypodium distaclyon were enhanced during the easy phase of drought vs. thriving water condition (Ahkami et al., 2019; Guo et al., 2018; Mundim & Pringle, 2018; Selmar, 2008). Meanwhile, a meta-analysis of secondary metabolite isoprenoids generally increases during drought (Mundim & Pringle, 2018). Plant isoprene emission is well documented for abiotic stress tolerance, particularly during HT and drought episodes. Current studies have confirmed that transformation at the genetic level in context is isoprene emission causes a cascade of cellular modification that includes known signaling pathways and that provide adaptive survival mechanisms (Russell et al., 2021). Isoprene emission remains high even under severe water stress (Brilli et al., 2013; Fang et al., 1996; Fortunati et al., 2008; Lantz et al., 2019). The reduced severity of water stress enhanced isoprene’s role in resilience to abiotic stress during droughts

78

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

(Arab et al., 2016; Marino et al., 2017; Ryan et al., 2014; Tattini et al., 2014). Perreca et al. (2020) studied the effect of moderate and severe drought on MEP Pathway function in the conifer Picea glauca. Mild drought stress reduced the photosynthesis by more than 70%, metabolic flux through the MEP pathway was declined by 37% only. One deoxy D-xylulose-5 phosphate synthase (DXS) was reduced by about 50%, supporting the crucial role of this enzyme’s regular pathway metabolic flux. Besides the decrease in MEP pathway flux and intermediate pools, there was no noticeable decline in most major MEP pathway products under drought, suggesting that the pathway is somehow buffered against this stress. The resilience of the MEP pathway under drought may be a consequence of the importance of metabolites formed under stress conclusion. Frey et al. (2012) reported that carotenoid cleavage catalyzed by the nine cis epoxies Carotenoid dehydrogenase (NCED) constitutes a crucial step in regulating ABA biosynthesis. This enzyme encodes five genes, out of which NCED3 plays a crucial role in regulating ABA biosynthesis in response to drought. Elena Ormeño et al. (2020) examined the effect of exogenous isoprene (20 ppbv) on photosynthesis rate, stomatal conductance and production of H2O2 in leaves of Acer monspessulamium submitted to three watery treatments (optimal, moderate water stress and severe water stress). Furthermore, these results exhibit that Acer monspessulamium showed a net photosynthesis increase (+30%) and a relative leaf H2O2 decrease when saplings were exposed to an enriched isoprene atmosphere compared to isoprene-free conditions under moderate water deficit. The physiological importance of isoprene was not observed under optimal watering or severe water stress. In plants concurrently experiencing water and heat stress, stomata closure reduces latent heat and exacerbates sensible heat load (Tattini et al., 2015), in particular, hydrophilic isoprene emitters steeply close stomata even at moderate drought to avoid tissue dehydration (Brilli et al., 2007; Tattini et al., 2015; Velikova et al., 2016). In all cases, isoprene emitting lines showed reduced depression of photosynthesis and more minor oxidative damage than the non-emitting line when exposed to drought (Jud et al., 2016; Ryan et al., 2014). Mahdavi et al. (2020) investigates that volatiles predominantly consisting of monoterpenes and sesquiterpenes serve as antimicrobial, antiseptic, and antioxidant in phytomedicine. They also play a crucial role in plants as secondary metabolites via their potential role against herbivores, attracting pollinators, and abiotic stress tolerance. Different environmental factors, including drought, affected plant volatiles. The volatile composition changed due to the effect of prolonged water deficit stress. It was studied on the sensitive and tolerant

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway

79

thyme plant cultivars (T. Vulgaris Var. Wagner and T. Vulgaris Var. Varico3, respectively). Volatile sampling and morpho-physiological parameters such as soil moisture, water potential, shoot dry weight, photosynthetic rate, and water content measurements were performed on one-month-old plants after water withholding at 4-day intervals until the plants wilted. The tolerant and sensitive plants had different responses at physiological and volatile levels. The most stress-induced changes in the plants’ physiological traits occurred in the photosynthetic rates. The tolerant plants maintained their photosynthesis similar to the control ones until the 8th day of the drought stress. While the analysis of the volatile compounds (VOCs) of the sensitive thyme plants displayed the same pattern for almost all of them, in the tolerant plants, the comparison of the habit of changes in the tolerant plants revealed that the changes could be classified into three separate groups. Experimental and theoretical studies showed that the most determinant compounds involved in drought stress adaptation included α-phellandrene, O-cymene, γ-terpinene, and β-caryophyllene. Overall, it can be concluded that in the sensitive plant’s trade-off between growth and defense, the tolerant ones simultaneously activate their stress response mechanism and continue their development. 3.3.3.2 FLOODING/EXCESS WATER STRESS Partial or absolute particular soil waterlogging prevents carbon gain and growth leads to the risk of premature plant death in terrestrial plants. Temporal flooding in areas with flat topography and abundant or seasonally distributed precipitation is currently a significant plant stress factor in many temperate countries in the North hemisphere. Besides this, elevated sea level further increases the flooding stress danger in the Northern hemisphere temperate forest (Canziani & Parry, 2007). One of the main effects of the flood is lower oxygen availability in the submerged plant part and develop the anoxic condition will lead to reduced ATP production and consequently inhibition of root metabolism. The soil flooding also modifies soil PH and Soil redox potential, further altering plant metabolism and growth (Pezeshki, 2001). Plants exhibit considerable variation in the acclimation potential and tolerance to soil waterlogging and the interspecific variation in flooding resistance and responsible for differences in species abundance and distribution in flood-prone ecosystems worldwide (Jackson et al., 2009). Anoxic condition elicits many physiological stress responses, including a reduction in photosynthesis rate and stomatal conductance (Jackson, 2002). Elicitation

80

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

of emissions of marker compounds of anaerobic metabolism ethanol and acetaldehyde (Atkinson et al., 2008; Rottenberger et al., 2008), and production of a series of volatile stress marker compounds such as methanol (Holzinger et al., 2000), lipoxygenase (LOX) pathway products (Agarwal & Grover, 2006) and nitric oxide (NO) (Dat et al., 2004; Dordas et al., 2004). However, so far, the cause-effect relationships in decline in photosynthetic rates and stomatal conductance are not fully understood (Ehlert et al., 2009; Jackson, 2002), and the components of flooding‐driven signaling pathway are still under extensive investigation (Ehlert et al., 2009; Sairam et al., 2008; Yordanova & Popova, 2007). Furthermore, quantitative relationships between species waterlogging tolerance and immediate stress responses have been developed in only a few studies (Ranney & Bir, 1994.; Rätsch & Haase, 2007). However, such relationships are needed to gain insight into forest ecosystem responses to flooding (Dat et al., 2004). Copolovici & Niinemets (2010) reported that in seedlings of temperate deciduous tree species Alnus glutinosa, Populus tremula, and Quercus rubra (from highest to lowest waterlogging tolerance) throughout sustained root zone waterlogging of up to three weeks. In all species, waterlogging initially resulted in reductions in net assimilation and stomatal conductance and enhanced emissions of ethanol, acetaldehyde, NO, LOX products, and methanol, followed by complete or partial recovery depending on process and species. Strong negative correlations between g(s) and internal NO concentration and NO flux, valid within and across species, were observed throughout the experiment. Isoprene emission capacity was not related to waterlogging tolerance. More minor waterlogging tolerant species had a more significant reduction and smaller acclimation capacity in foliage physiological potentials and more significant emission bursts of volatile stress marker compounds. 3.3.4 MODULATION OF TERPENOID METABOLISM BY LIGHT STRESS IN PLANTS Katja Behnke, Loivamäki et al. (2010) investigated the effect of combined transient temperature and light stress (sun fleck). It comparably analyzed photosynthetic gas exchange in grey poplar, which has been genetically modified (GM) in isoprene emission capacity. Overall, we demonstrate that for poplar leaves, the ability to emit Isoprene is crucial to maintain photosynthesis when exposed to sunflecks. Net CO2 assimilation and electron

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway

81

transport rates were strongly impaired in the sun fleck-treated non-isoprene emitting poplars. Similar impairment was not detected when the leaves were exposed to high light (light dots) only. Within 10 h non-isoprene emitting poplars recovered from sun fleck-related impairment as indicated by chlorophyll fluorescence and microarray analysis. Unstressed leaves of nonisoprene emitting poplars had higher ascorbate contents and higher contents of malondialdehyde (MDA) than wild type. Microarray analyses revealed lipid and chlorophyll degradation processes in the non-isoprene emitting poplars. Thus, there is evidence for adjusting the antioxidative system in the non-isoprene emitting poplars even under normal growth conditions (Lantz et al., 2019). Light availability has a significant effect on the capacity for isoprene emission from leaves. The ability for isoprene emission is typically measured with the leaf at 30°C and 1,000 μmol–2 s–1 photosynthetic photon flux density. Using these standard conditions, long‐term effects on the ability of the leaf to make isoprene can be distinguished from the short‐term effects of these same parameters on the rate of isoprene emission. Low light has a much more potent inhibitory effect on the capacity for isoprene emission than the capacity for CO2 fixation (Hanson & Sharkey, 2001). A similar result was observed in mature trees where the gradient in isoprene emission capacity from top to bottom of the canopy was much steeper than the gradient in photosynthetic capacity (Harley et al., 1996; R K Monson et al., 1994; Sharkey et al., 1996). Isoprene emission is light-dependent (Sanadze & Kalandadze, 1966; Tingey et al., 1979); the weak dependence is similar to CO2 fixation except that isoprene emission can continue to increase with light at higher light intensity than CO2 fixation (Lerdau & Keller, 1997). The light dependence is presumed to result from the availability of high-energy intermediates such as ferredoxin, NADPH, ATP, and CTP. When an inhibitor blocks photosynthetic electron transport, isoprene emission stops (Garcia et al., 2019). It is presumed that the MEP pathway is more dependent on reductant than ATP compared with CO2 fixation. The ratio of ATP per NADPH for CO2 fixation is 1.5:1 (or more if photorespiration is considered), whereas, for isoprene production from CO2, it is 1.4:1 (Sharkey & Yeh, 2001). Nevertheless, the ATP supply also plays an important role. When isoprene emission and metabolites were measured under various conditions, the relationship between isoprene emission rate and ATP had an r2 of 0.8 to 0.9. In contrast, the relationship with phosphoglyceric acid, ribulose bisphosphate, and triose phosphates had r2 values of 0.55 or less in both oak leaves and velvet bean (Loreto & Sharkey, 1993). When plants are subjected to darkness, the production of DMADP stops instantaneously (Weise et al., 2013).

82

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

All are remaining DMADP is rapidly converted to isoprene (Z. Li et al., 2011; Russell & Fall, 1989; Rasulov et al., 2009, 2011). 3.3.5 MODULATION OF TERPENOID METABOLISM BY OZONE IN PLANTS Tropospheric O3 is one of the major global air pollutants, with current background concentrations in the Northern Hemisphere being approximately 20–45 ppb. Its impact is expected to become even more critical in the future due to increasing emissions of O3 precursors, nitrogen oxides (NOx), and volatile organic compounds (VOCs) in the atmosphere (Sitch et al., 2007; Vingarzan, 2004). Vickers, Gershenzon et al. (2009) suggested that volatile isoprenoids, especially isoprene, can react directly with ozone, either in planta or at the leaf surface, thus decreasing ozone levels and potentially mitigating oxidative damage caused by the leaf (Loreto et al., 2001; Loreto & Velikova, 2001). In highly oxidizing, humid atmospheric environments, isoprene does react with ozone (Sauer et al., 1999); similar conditions might occur at the leaf boundary layer and in the intercellular spaces of the mesophyll tissue when ozone is present. However, only monoterpenes have been experimentally demonstrated to scavenge a significant amount of ozone in the boundary layer (Fares et al., 2008). The reaction between ozone and isoprene is relatively slow, and direct removal of ozone in this way is insufficient to result in the observed protection of fumigated tissues (Fares et al., 2008). Furthermore, ozonolysis of isoprene in humid environments results in H2O2 production (Sauer et al., 1999). The photosynthetic apparatus of leaves in which isoprene emission was inhibited by fosmidomycin became more susceptible to damage by ozone than in isoprene-emitting leaves. Three days after ozone fumigation, the necrotic leaf area was significantly higher in isoprene-inhibited leaves than in isoprene-emitting leaves. Isoprene-inhibited leaves also accumulated high nitric oxide (NO) amounts, as detected by epifluorescence light microscopy. The results confirm that oxidative stresses activate biosynthesis and emission of chloroplastic isoprenoid, bringing further evidence supporting an antioxidant role for these compounds. It is suggested that, in nature, the simultaneous quenching of NO and ROS by Isoprene may be a very effective mechanism to control dangerous compounds formed under abiotic stress conditions while simultaneously attenuating the induction of the hypersensitive response leading to cellular damage and

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway

83

death. Li et al. (2017) investigated photosynthetic characteristics and VOC emissions in Phaseolus vulgaris following acute ozone exposure (600 nmol mol–1 for 30 min) under illumination and darkness and after priming 200 nmol mol–1 O3 for 30 min. Methanol and LOX pathway product emissions were induced rapidly, followed by moderate emissions of methyl salicylate (MeSA). Stomatal conductance before acute exposure was lower in darkness and after low O3 priming than in light and without priming. After low O3 priming, no MeSA and lower LOX emissions were detected under acute exposure. Loreto et al. (2001) found that plants sensitive to ozone and unable to emit isoprene become resistant to acute and short exposure to ozone if they are fumigated with exogenous isoprene. While isoprene-emitting plants that are sensitive to ozone do not suffer damage when exposed to ozone. Isoprene-induced ozone resistance is associated with the maintenance of photochemical efficiency and with low energy dissipation, as indicated by fluorescence quenching. This suggests that isoprene effectively stabilizes thylakoid membranes. However, when isoprene reacts with ozone within the leaves or in a humid atmosphere, it quenches the ozone concentration to levels that are less or non-toxic for plants. Thus, protection from ozone in plants fumigated with isoprene may be due to a direct ozone quenching rather than to an induced resistance at the membrane level. Irrespective of the mechanism, isoprene is one of the most effective antioxidants in plants. 3.3.6 MODULATION OF TERPENOID METABOLISM BY SALINITY STRESS IN PLANTS Soil salinity is a major edaphic factor that limits crop productivity worldwide. Recent reports suggest the involvement of terpenoid metabolism in the plant’s response to salinity. Zhang et al. (2018) investigated the production of volatile compounds in salinity-stressed tomato (Lycopersicum esculentum) plants. GC-MS coupled with solid-phase microextraction (SPME) indicated that salinity stress widely altered the composition and quantity of volatiles. RNASEq analysis identified approximately 7,200 differentially expressed genes (DEGs), out of which 6,200 were down-regulated, and 1,208 were up-regulated after exposure to NaCl. Around 18 DEGs associated with volatile biosynthesis were identified, among which the expression of genes regulating the abundance of eight volatile compounds (IPI, GPS, TPS, etc.) was altered by salinity. Biogenic volatile organic compound (BVOC) emissions were analyzed in salt-sensitive (Populus × canescens (Aiton) Sm.) and

84

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

salt-tolerant (Populus euphratica Oliv.) poplar plants in response to undersalinity, high-temperature, and high light treatments (Behnke et al., 2013). The combination of salt and highlight aggravated the isoprene emission of both species. 13CO2 labeling indicated that in salinity-stressed Populus × canescens leaves, the ‘alternative’ carbon sources were used for isoprene biosynthesis as photosynthesis was compromised. The stress-protective role of isoprene was also confirmed as the non-isoprene-emitting leaves were sensitive to HT and released a burst of BVOCs in response to high-temperature episodes. Francesco & Delfine (2000) evaluated Eucalyptus species and found them as one of the highest isoprene emitting plants. In response to transient salinity, isoprene emission was significantly affected, while during recovery, sudden isoprene emission and a concomitant increase in photosynthetic performance were observed. The highest isoprene emission was noted when the plants were exposed to simultaneous HTs (40–45°C) and salt stress. Stress-induced activation of alternative non-photosynthetic pathways of isoprene synthesis is temperature-dependent and involves a thylakoid-bound ISPS. Teuber et al. (2008) studied the impact of salt stress and nitrogen forms on the isoprene emission of salt‐sensitive grey poplar (Populus × canescens) plants. Salt stress significantly decreased the DMADP content in leaves, probably due to restricted availability of photosynthates for DMADP biosynthesis; however, the isoprene emission is maintained by other carbon sources. Valifard et al. (2019) reported that in salt-stressed Salvia mirzayanii plants, the expression of cineole synthase one gene (SmCin1) increased 11-fold. In response to salt stress, the content of significant terpenoids, α-terpinyl acetate, 1,8-cineole, and linalyl acetate also showed a progressive increase. 1,8-cineole is the major component of S. mirzayanii essential oil; hence, the improved resource allocation towards its synthesis in salt-stressed plants can help in the development of a new chemotype of S. mirzayanii an important medicinal plant. 3.4 CONCLUSION Terpenoids or isoprenoids compounds are naturally occurring and highly divergent class plant secondary metabolites. In plants, the sedentary lifestyle necessitates the use of diverse compounds for stress defense and signaling. Terpenoid compounds suit this requirement invariably by being produced by two flexible and environmentally regulated pathways: the MVA and MEP pathways in plants. In response to the plant’s requirement, the paralogs of genes are employed for producing primary metabolites (photosynthetic

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway

85

pigments and phytosterols), or secondary metabolites (Figure 3.1). The identification of signaling mechanisms and transcription factors regulating the genes associated with both the pathways is an interesting future research avenue. Isoprene is a prominent terpenoid compound which is volatile and is produced by the action of the enzyme ISPS (Table 3.1). The amount and composition of volatiles emitted are dependent on plant species and the environment. Isoprene emission is observed in plants exposed to hightemperature, ozone, and ROS, and herbivores and has a stress-protective role. Plants treated with exogenous isoprene are tolerant to ozone and oxidative stress temperature stresses. The inhibitor and transgenic (overexpression /suppression) based studies have proven that isoprene emission has stress protective role against a wide range of stresses. The physiological and molecular signaling mechanism of isoprene emission is another area of interest. Isoprene emission during stress responses also coordinates hormone signaling in plants (ABA, GA, and JA). The detailed discussion on the role of terpenoid compounds perception and signaling of different stresses viz. nutrient deficiency, HT, low temperature, drought, flooding, and ozone underscores the importance of terpenoids in stress protection. TABLE 3.1  Role of Terpenoids in Abiotic Stress Tolerance of Plants Sl. Terpenoid No. 1. Isoprene emission

Plant sp.

Stress

Eucalyptus spp.

Salinity tolerance

2.

Isoprene

Quercus ilex

3.

Isoprene

Ficus benjamina

4.

High Zeaxanthin and Cicer arietinum low violaxanthin Isoprene Poplar Exogenous Isoprene Acer monspessulamium Isoprene fumigation Arabidopsis thaliana Total leaf terpenoid Rosmarinus officinalis Isoprene emission Aspen and white oak

5. 6. 7. 8. 9.

References

Francesco & Delfine (2000) Ozone quenching Loreto et al. (2001); Loreto & Velikova (2001). ROS scavenging un- Yáñez-Serrano et al. der high temperature (2019) Heat tolerance Kumar et al. (2020) High light tolerance Katja et al. (2010) Water deficit Elena et al. (2020) tolerance Stress protection Harvey & Sharkey (2016) High leaf N and P Bustamante et al. content (2020) High N content Litvak et al. (1996)

86

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

KEYWORDS • dimethylallyl diphosphate • geranyl diphosphate • isopentenyl diphosphate • methylerythritol phosphate • mevalonic acid • terpene synthase

REFERENCES Affek, H. P., & Yakir, D., (2002). Protection by isoprene against singlet oxygen in leaves. Plant Physiology, 129(1), 269LP–277. https://doi.org/10.1104/pp.010909. Agarwal, S., & Grover, A., (2006). Molecular biology, biotechnology and genomics of flooding associated low O2 stress response in plants. Critical Reviews in Plant Sciences, 25(1), 1–21. https://doi.org/10.1080/07352680500365232. Agurla, S., Gahir, S., Munemasa, S., Murata, Y., & Raghavendra, A. S., (2018). In: IwayaInoue, M., Sakurai, M., & Uemura, M., (eds.), Mechanism of Stomatal Closure in Plants Exposed to Drought and Cold Stress BT - Survival Strategies in Extreme Cold and Desiccation: Adaptation Mechanisms and Their Applications (pp. 215–232). Springer Singapore. https://doi.org/10.1007/978-981-13-1244-1_12. Ahkami, A. H., Wang, W., Wietsma, T. W., Winkler, T., Lange, I., Jansson, C., Lange, B. M., & McDowell, N. G., (2019). Metabolic shifts associated with drought-induced senescence in Brachypodium. Plant Science, 289, 110278. https://doi.org/https://doi.org/10.1016/j. plantsci.2019.110278. Ajikumar, P. K., Tyo, K., Carlsen, S., Mucha, O., Phon, T. H., & Stephanopoulos, G., (2008). Terpenoids: Opportunities for biosynthesis of natural product drugs using engineered microorganisms. Molecular Pharmaceutics, 5(2), 167–190. https://doi.org/10.1021/ mp700151b. Allen, D. J., & Ort, D. R., (2001). Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends in Plant Science, 6(1), 36–42. https://doi.org/10.1016/ s1360-1385(00)01808-2. Arab, L., Kreuzwieser, J., Kruse, J., Zimmer, I., Ache, P., Alfarraj, S., Al-Rasheid, K. A. S., et al., (2016). Acclimation to heat and drought—Lessons to learn from the date palm (Phoenix dactylifera). Environmental and Experimental Botany, 125, 20–30. https://doi.org/https:// doi.org/10.1016/j.envexpbot.2016.01.003. Arneth, A., Monson, R. K., Schurgers, G., Niinemets, Ü., & Palmer, P. I., (2008). Why are estimates of global terrestrial isoprene emissions so similar (and why is this not so for monoterpenes)? Atmos. Chem. Phys., 8(16), 4605–4620. https://doi.org/10.5194/ acp-8-4605-2008.

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway

87

Atkinson, C. J., Harrison-Murray, R. S., & Taylor, J. M., (2008). Rapid flood-induced stomatal closure accompanies xylem sap transportation of root-derived acetaldehyde and ethanol in Forsythia. Environmental and Experimental Botany, 64(2), 196–205. https://doi.org/https:// doi.org/10.1016/j.envexpbot.2008.02.001. Baker, N. R., (2008). Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annual Review of Plant Biology, 59(1), 89–113. https://doi.org/10.1146/annurev. arplant.59.032607.092759. Banerjee, A., & Sharkey, T. D., (2014). Methylerythritol 4-phosphate (MEP) pathway metabolic regulation. Natural Product Reports, 31(8), 1043–1055. https://doi.org/10.1039/ C3NP70124G. Behnke, K., Ehlting, B., Teuber, M., Bauerfeind, M., Louis, S., Hänsch, R., Polle, A., et al., (2007). Transgenic, non-isoprene emitting poplars don’t like it hot. The Plant Journal, 51(3), 485–499. https://doi.org/https://doi.org/10.1111/j.1365-313X.2007.03157.x. Behnke, K., Ghirardo, A., Janz, D., Kanawati, B., Esperschütz, J., Zimmer, I., SchmittKopplin, P., et al., (2013). Isoprene function in two contrasting poplars under salt and sunflecks. Tree Physiology, 33(6), 562–578. https://doi.org/10.1093/treephys/tpt018. Behnke, K., Kaiser, A., Zimmer, I., Brüggemann, N., Janz, D., Polle, A., Hampp, R., et al., (2010). RNAi-mediated suppression of isoprene emission in poplar transiently impacts phenolic metabolism under high temperature and high light intensities: A transcriptomic and metabolomic analysis. Plant Molecular Biology, 74(1, 2), 61–75. Behnke, K., Loivamäki, M., Zimmer, I., Rennenberg, H., Schnitzler, J. P., & Louis, S., (2010). Isoprene emission protects photosynthesis in sunfleck exposed grey poplar. Photosynthesis Research, 104(1), 5–17. https://doi.org/10.1007/s11120-010-9528-x. Berthelot, K., Estevez, Y., Deffieux, A., & Peruch, F., (2012). Isopentenyl diphosphate isomerase: A checkpoint to isoprenoid biosynthesis. Biochimie, 94(8), 1621–1634. https:// doi.org/https://doi.org/10.1016/j.biochi.2012.03.021. Bian, G., Deng, Z., & Liu, T., (2017). Strategies for terpenoid overproduction and new terpenoid discovery. Current Opinion in Biotechnology, 48, 234–241. https://doi.org/ https://doi.org/10.1016/j.copbio.2017.07.002. Bohlmann, J., & Keeling, C. I., (2008). Terpenoid biomaterials. The Plant Journal, 54(4), 656–669. https://doi.org/https://doi.org/10.1111/j.1365-313X.2008.03449.x. Brilli, F., Barta, C., Fortunati, A., Lerdau, M., Loreto, F., & Centritto, M., (2007). Response of isoprene emission and carbon metabolism to drought in white poplar (Populus alba) saplings. New Phytologist, 175(2), 244–254. https://doi.org/https://doi. org/10.1111/j.1469-8137.2007.02094.x. Brilli, F., Tsonev, T., Mahmood, T., Velikova, V., Loreto, F., & Centritto, M., (2013). Ultradian variation of isoprene emission, photosynthesis, mesophyll conductance, and optimum temperature sensitivity for isoprene emission in water-stressed Eucalyptus citriodora saplings. Journal of Experimental Botany, 64(2), 519–528. https://doi.org/10.1093/jxb/ ers353. Bustamante, M. Á., Michelozzi, M., Barra, C. A., Grenni, P., Verbokkem, J., Geerdink, P., Safi, C., & Nogues, I., (2020). Effects of soil fertilization on terpenoids and other carbonbased secondary metabolites in Rosmarinus officinalis plants: A comparative study. Plants (Basel, Switzerland), 9(7). https://doi.org/10.3390/plants9070830. Canziani, O. F., & Parry, M. L., (2007). Climate Change 2007: Impacts, Adaptation, and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (IPCC).

88

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Carriero, G., Brunetti, C., Fares, S., Hayes, F., Hoshika, Y., Mills, G., Tattini, M., & Paoletti, E., (2016). BVOC responses to realistic nitrogen fertilization and ozone exposure in silver birch. Environmental Pollution (Barking, Essex: 1987), 213, 988–995. https://doi. org/10.1016/j.envpol.2015.12.047. Centritto, M., Haworth, M., Marino, G., Pallozzi, E., Tsonev, T., Velikova, V., Nogues, I., & Loreto, F., (2014). Isoprene emission aids recovery of photosynthetic performance in transgenic Nicotiana tabacum following high intensity acute UV-B exposure. Plant Science, 226, 82–91. https://doi.org/https://doi.org/10.1016/j.plantsci.2014.06.004. Choi, D., Ward, B. L., & Bostock, R. M., (1992). Differential induction and suppression of potato 3-hydroxy-3-methylglutaryl coenzyme A reductase genes in response to Phytophthora infestans and to its elicitor arachidonic acid. The Plant Cell, 4(10), 1333– 1344. https://doi.org/10.1105/tpc.4.10.1333. Copolovici, L., & Niinemets, U., (2010). Flooding induced emissions of volatile signaling compounds in three tree species with differing waterlogging tolerance. Plant, Cell and Environment, 33(9), 1582–1594. https://doi.org/10.1111/j.1365-3040.2010.02166.x. Cordoba, E., Salmi, M., & León, P., (2009). Unravelling the regulatory mechanisms that modulate the MEP pathway in higher plants. Journal of Experimental Botany, 60(10), 2933–2943. https://doi.org/10.1093/jxb/erp190. Crowell, D. N., & Huizinga, D. H., (2009). Protein isoprenylation: The fat of the matter. Trends in Plant Science, 14(3), 163–170. https://doi.org/10.1016/j.tplants.2008.12.001. Dat, J. F., Capelli, N., Folzer, H., Bourgeade, P., & Badot, P. M., (2004). Sensing and signaling during plant flooding. Plant Physiology and Biochemistry, 42(4), 273–282. https://doi.org/ https://doi.org/10.1016/j.plaphy.2004.02.003. Dietz, K. J., Turkan, I., & Krieger-Liszkay, A., (2016). Redox- and reactive oxygen speciesdependent signaling into and out of the photosynthesizing chloroplast. Plant Physiology, 171(3), 1541 LP–1550. https://doi.org/10.1104/pp.16.00375. Disch, A., & Rohmer, M., (1998). On the absence of the glyceraldehyde 3-phosphate/pyruvate pathway for isoprenoid biosynthesis in fungi and yeasts. FEMS Microbiology Letters, 168(2), 201–208. https://doi.org/10.1111/j.1574-6968.1998.tb13274.x. Disch, A., Schwender, J., Müller, C., Lichtenthaler, H. K., & Rohmer, M., (1998). Distribution of the mevalonate and glyceraldehyde phosphate/pyruvate pathways for isoprenoid biosynthesis in unicellular algae and the cyanobacterium Synechocystis PCC 6714. The Biochemical Journal, 333(2), 381–388. https://doi.org/10.1042/bj3330381. Dordas, C., Hasinoff, B. B., Rivoal, J., & Hill, R. D., (2004). Class-1 hemoglobins, nitrate and NO levels in anoxic maize cell-suspension cultures. Planta, 219(1), 66–72. https://doi. org/10.1007/s00425-004-1212-y. Dos Santos, C. V., Letousey, P., Delavault, P., & Thalouarn, P., (2003). Defense gene expression analysis of Arabidopsis thaliana parasitized by Orobanche ramosa. Phytopathology®, 93(4), 451–457. https://doi.org/10.1094/PHYTO.2003.93.4.451. Dudareva, N., Pichersky, E., & Gershenzon, J., (2004). Biochemistry of plant volatiles. Plant Physiology, 135(4), 1893LP–1902. https://doi.org/10.1104/pp.104.049981. Ehlert, C., Maurel, C., Tardieu, F., & Simonneau, T., (2009). Aquaporin-mediated reduction in maize root hydraulic conductivity impacts cell turgor and leaf elongation even without changing transpiration. Plant Physiology, 150(2), 1093LP–1104. https://doi.org/10.1104/ pp.108.131458.

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway

89

Fang, C., Monson, R. K., & Cowling, E. B., (1996). Isoprene emission, photosynthesis, and growth in sweetgum (Liquidambar styraciflua) seedlings exposed to short- and long-term drying cycles. Tree Physiology, 16(4), 441–446. https://doi.org/10.1093/treephys/16.4.441. Fares, S., Loreto, F., Kleist, E., & Wildt, J., (2008). Stomatal uptake and stomatal deposition of ozone in isoprene and monoterpene emitting plants. Plant Biology (Stuttgart, Germany), 10(1), 44–54. https://doi.org/10.1055/s-2007-965257. Fortunati, A., Barta, C., Brilli, F., Centritto, M., Zimmer, I., Schnitzler, J. P., & Loreto, F., (2008). Isoprene emission is not temperature-dependent during and after severe droughtstress: A physiological and biochemical analysis. The Plant Journal: For Cell and Molecular Biology, 55(4), 687–697. https://doi.org/10.1111/j.1365-313X.2008.03538.x. Frey, A., Effroy, D., Lefebvre, V., Seo, M., Perreau, F., Berger, A., Sechet, J., et al., (2012). Epoxy carotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members. The Plant Journal, 70(3), 501–512. https://doi.org/https://doi.org/10.1111/j.1365-313X.2011.04887.x. Galichet, A., & Gruissem, W., (2003). Protein farnesylation in plants--conserved mechanisms but different targets. Current Opinion in Plant Biology, 6(6), 530–535. https://doi. org/10.1016/j.pbi.2003.09.005. Garcia, S., Jardine, K., Souza De, V. F., Souza De, R. A. F., Duvoisin, Jr. S., & Gonçalves De, J. F. C., (2019). Reassimilation of leaf internal CO2 contributes to isoprene emission in the neotropical species inga edulis mart. In: Forests (Vol. 10, No. 6). https://doi.org/10.3390/ f10060472. George, K. W., Thompson, M. G., Kim, J., Baidoo, E. E. K., Wang, G., Benites, V. T., Petzold, C. J., et al., (2018). Integrated analysis of isopentenyl pyrophosphate (IPP) toxicity in isoprenoid-producing Escherichia coli. Metabolic Engineering, 47, 60–72. https://doi.org/ https://doi.org/10.1016/j.ymben.2018.03.004. Ghassemian, M., Lutes, J., Tepperman, J. M., Chang, H. S., Zhu, T., Wang, X., Quail, P. H., & Lange, B. M., (2006). Integrative analysis of transcript and metabolite profiling data sets to evaluate the regulation of biochemical pathways during photomorphogenesis. Archives of Biochemistry and Biophysics, 448(1, 2), 45–59. https://doi.org/10.1016/j.abb.2005.11.020. Ghirardo, A., Wright, L. P., Bi, Z., Rosenkranz, M., Pulido, P., Rodríguez-Concepción, M., Niinemets, Ü., et al., (2014). Metabolic flux analysis of plastidic isoprenoid biosynthesis in poplar leaves emitting and nonemitting isoprene. Plant Physiology, 165(1), 37LP–51. https://doi.org/10.1104/pp.114.236018. Gill, S. S., & Tuteja, N., (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48(12), 909– 930. https://doi.org/https://doi.org/10.1016/j.plaphy.2010.08.016. Guenther, A., Hewitt, C. N., Erickson, D., Fall, R., Geron, C., Graedel, T., Harley, P., et al., (1995). A global model of natural volatile organic compound emissions. Journal of Geophysical Research: Atmospheres, 100(D5), 8873–8892. https://doi.org/https://doi. org/10.1029/94JD02950. Guenther, A., Karl, T., Harley, P., Wiedinmyer, C., Palmer, P. I., & Geron, C., (2006). Estimates of global terrestrial isoprene emissions using MEGAN (model of emissions of gases and aerosols from nature). Atmos. Chem. Phys., 6(11), 3181–3210. https://doi.org/10.5194/ acp-6-3181-2006. Guo, R., Shi, L., Jiao, Y., Li, M., Zhong, X., Gu, F., Liu, Q., et al., (2018). Metabolic responses to drought stress in the tissues of drought-tolerant and drought-sensitive wheat genotype seedlings. AoB Plants, 10(2). https://doi.org/10.1093/aobpla/ply016.

90

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Haldimann, P., (1998). Low growth temperature-induced changes to pigment composition and photosynthesis in Zea mays genotypes differing in chilling sensitivity. Plant, Cell and Environment, 21(2), 200–208. https://doi.org/https://doi. org/10.1046/j.1365-3040.1998.00260.x. Hanson, D. T., & Sharkey, T. D., (2001). Effect of growth conditions on isoprene emission and other thermotolerance-enhancing compounds. Plant, Cell and Environment, 24(9), 929–936. https://doi.org/https://doi.org/10.1046/j.1365-3040.2001.00744.x. Harley, P., Guenther, A., & Zimmerman, P., (1996). Effects of light, temperature and canopy position on net photosynthesis and isoprene emission from sweetgum (Liquidambar styraciflua) leaves. Tree Physiology, 16(1, 2), 25–32. https://doi.org/10.1093/ treephys/16.1-2.25. Harper, K. L., & Unger, N., (2018). Global climate forcing driven by altered BVOC fluxes from 1990 to 2010 land cover change in maritime Southeast Asia. Atmos. Chem. Phys., 18(23), 16931–16952. https://doi.org/10.5194/acp-18-16931-2018. Harvey, C. M., & Sharkey, T. D., (2016). Exogenous isoprene modulates gene expression in unstressed Arabidopsis thaliana plants. Plant, Cell and Environment, 39(6), 1251–1263. https://doi.org/https://doi.org/10.1111/pce.12660. Harvey, C. M., Li, Z., Tjellström, H., Blanchard, G. J., & Sharkey, T. D., (2015). Concentration of isoprene in artificial and thylakoid membranes. Journal of Bioenergetics and Biomembranes, 47(5), 419–429. https://doi.org/10.1007/s10863-015-9625-9. Havaux, M., & Tardy, F., (1996). Temperature-dependent adjustment of the thermal stability of photosystem II in vivo: Possible involvement of xanthophyll-cycle pigments. Planta, 198(3), 324–333. https://doi.org/10.1007/BF00620047. Hemmerlin, A., (2013). Post-translational events and modifications regulating plant enzymes involved in isoprenoid precursor biosynthesis. Plant Science: An International Journal of Experimental Plant Biology, 203, 204, 41–54. https://doi.org/10.1016/j. plantsci.2012.12.008. Hemmerlin, A., Harwood, J. L., & Bach, T. J., (2012). A raison d’être for two distinct pathways in the early steps of plant isoprenoid biosynthesis? Progress in Lipid Research, 51(2), 95–148. https://doi.org/10.1016/j.plipres.2011.12.001. Holopainen, J. K., & Gershenzon, J., (2010). Multiple stress factors and the emission of plant VOCs. Trends in Plant Science, 15(3), 176–184. https://doi.org/https://doi.org/10.1016/j. tplants.2010.01.006. Holzinger, R., Sandoval-Soto, L., Rottenberger, S., Crutzen, P. J., & Kesselmeier, J., (2000). Emissions of volatile organic compounds from Quercus ilex L. measured by proton transfer reaction mass spectrometry under different environmental conditions. Journal of Geophysical Research: Atmospheres, 105(D16), 20573–20579. https://doi.org/https://doi. org/10.1029/2000JD900296. Hoshika, Y., Brilli, F., Baraldi, R., Fares, S., Carrari, E., Zhang, L., Badea, O., & Paoletti, E., (2020). Ozone impairs the response of isoprene emission to foliar nitrogen and phosphorus in poplar. Environmental Pollution, 267, 115679. https://doi.org/https://doi.org/10.1016/j. envpol.2020.115679. Hsieh, M. H., & Goodman, H. M., (2005). The Arabidopsis IspH homolog is involved in the plastid nonmevalonate pathway of isoprenoid biosynthesis. Plant Physiology, 138(2), 641LP–653. https://doi.org/10.1104/pp.104.058735. Hussain, H. A., Hussain, S., Khaliq, A., Ashraf, U., Anjum, S. A., Men, S., & Wang, L., (2018). Chilling and drought stresses in crop plants: Implications, cross talk, and potential

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway

91

management opportunities. In: Frontiers in Plant Science (Vol. 9, p. 393). https://www. frontiersin.org/article/10.3389/fpls.2018.00393 (accessed on 18October 2022). Immethun, C., Hoynes-O’Connor, A., Balassy, A., & Moon, T. A. E. S., (2013). Microbial production of isoprenoids enabled by synthetic biology. In: Frontiers in Microbiology (Vol. 4, p. 75). https://www.frontiersin.org/article/10.3389/fmicb.2013.00075 (accessed on 18 October 2022). Jackson, M. B., (2002). Long‐distance signaling from roots to shoots assessed: The flooding story. Journal of Experimental Botany, 53(367), 175–181. https://doi.org/10.1093/ jexbot/53.367.175. Jackson, M. B., Ishizawa, K., & Ito, O., (2009). Evolution and mechanisms of plant tolerance to flooding stress. Annals of Botany, 103(2), 137–142. https://doi.org/10.1093/aob/mcn242. Jud, W., Vanzo, E., Li, Z., Ghirardo, A., Zimmer, I., Sharkey, T. D., Hansel, A., & Schnitzler, J. P., (2016). Effects of heat and drought stress on post-illumination bursts of volatile organic compounds in isoprene-emitting and non-emitting poplar. Plant, Cell and Environment, 39(6), 1204–1215. https://doi.org/https://doi.org/10.1111/pce.12643. Kainulainen, P., Utriainen, J., Holopainen, J. K., Oksanen, J. A. R. I., & Holopainen, T., (2000). Influence of elevated ozone and limited nitrogen availability on conifer seedlings in an open-air fumigation system: Effects on growth, nutrient content, mycorrhiza, needle ultrastructure, starch and secondary compounds. Global Change Biology, 6(3), 345–355. https://doi.org/https://doi.org/10.1046/j.1365-2486.2000.00310.x. Kobayashi, K., Awai, K., Nakamura, M., Nagatani, A., Masuda, T., & Ohta, H., (2009). Type-B monogalactosyldiacylglycerol synthases are involved in phosphate starvation-induced lipid remodeling and are crucial for low-phosphate adaptation. The Plant Journal: For Cell and Molecular Biology, 57(2), 322–331. https://doi.org/10.1111/j.1365-313X.2008.03692.x. Kovacs, W. J., Olivier, L. M., & Krisans, S. K., (2002). Central role of peroxisomes in isoprenoid biosynthesis. Progress in Lipid Research, 41(5), 369–391. https://doi. org/10.1016/s0163-7827(02)00002-4. Kumar, P., Yadav, S., & Singh, M. P., (2020). Possible involvement of xanthophyll cycle pigments in heat tolerance of chickpea (Cicer arietinum L.). Physiology and Molecular Biology of Plants, 26(9), 1773–1785. https://doi.org/10.1007/s12298-020-00870-7. Lange, B. M., & Croteau, R., (1999). Isopentenyl diphosphate biosynthesis via a mevalonateindependent pathway: Isopentenyl monophosphate kinase catalyzes the terminal enzymatic step. Proceedings of the National Academy of Sciences, 96(24), 13714LP–13719. https:// doi.org/10.1073/pnas.96.24.13714. Lange, B. M., Wildung, M. R., McCaskill, D., & Croteau, R., (1998). A family of transketolases that directs isoprenoid biosynthesis via a mevalonate-independent pathway. Proceedings of the National Academy of Sciences of the United States of America, 95(5), 2100–2104. https://doi.org/10.1073/pnas.95.5.2100. Lantz, A. T., Allman, J., Weraduwage, S. M., & Sharkey, T. D., (2019). Isoprene: New insights into the control of emission and mediation of stress tolerance by gene expression. Plant, Cell and Environment, 42(10), 2808–2826. https://doi.org/https://doi.org/10.1111/pce.13629. Laothawornkitkul, J., Paul, N. D., Vickers, C. E., Possell, M., Taylor, J. E., Mullineaux, P. M., & Hewitt, C. N., (2008). Isoprene emissions influence herbivore feeding decisions. Plant, Cell and Environment, 31(10), 1410–1415. https://doi.org/https://doi. org/10.1111/j.1365-3040.2008.01849.x. Laskovics, F. M., & Poulter, C. D., (1981). Prenyltransferase: Determination of the binding mechanism and individual kinetic constants for farnesylpyrophosphate synthetase by rapid

92

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

quench and isotope partitioning experiments. Biochemistry, 20(7), 1893–1901. https://doi. org/10.1021/bi00510a027. Lehning, A., Zimmer, I., Steinbrecher, R., Brüggemann, N., & Schnitzler, J. P., (1999). Isoprene synthase activity and its relation to isoprene emission in Quercus robur L. leaves. Plant, Cell and Environment, 22(5), 495–504. https://doi.org/https://doi. org/10.1046/j.1365-3040.1999.00425.x. Lerdau, M., & Keller, M., (1997). Controls on isoprene emission from trees in a subtropical dry forest. Plant, Cell and Environment, 20(5), 569–578. https://doi.org/https://doi. org/10.1111/j.1365-3040.1997.00075.x. Lerdau, M., Matson, P., Fall, R., & Monson, R., (1995). Ecological controls over monoterpene emissions from Douglas-fir (Pseudotsuga menziesii). Ecology, 76(8), 2640–2647. https:// doi.org/10.2307/2265834. Li, S., Harley, P. C., & Niinemets, Ü., (2017). Ozone-induced foliar damage and release of stress volatiles is highly dependent on stomatal openness and priming by low-level ozone exposure in Phaseolus vulgaris. Plant, Cell and Environment, 40(9), 1984–2003. https:// doi.org/https://doi.org/10.1111/pce.13003. Li, Z., Ratliff, E. A., & Sharkey, T. D., (2011). Effect of temperature on postillumination isoprene emission in oak and poplar. Plant Physiology, 155(2), 1037 LP–1046. https://doi. org/10.1104/pp.110.167551. Lichtenthaler, H. K., (1999). The 1-deoxy-d-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 47–65. https://doi.org/10.1146/annurev.arplant.50.1.47. Litvak, M. E., Loreto, F., Harley, P. C., Sharkey, T. D., & Monson, R. K., (1996). The response of isoprene emission rate and photosynthetic rate to photon flux and nitrogen supply in aspen and white oak trees. Plant, Cell and Environment, 19(5), 549–559. https://doi.org/ https://doi.org/10.1111/j.1365-3040.1996.tb00388.x. Llusia, J., Bermejo-Bermejo, V., Calvete-Sogo, H., & Peñuelas, J., (2014). Decreased rates of terpene emissions in Ornithopus compressus L. and Trifolium striatum L. by ozone exposure and nitrogen fertilization. Environmental Pollution, 194, 69–77. https://doi.org/ https://doi.org/10.1016/j.envpol.2014.06.038. Loivamäki, M., Mumm, R., Dicke, M., & Schnitzler, J. P., (2008). Isoprene interferes with the attraction of bodyguards by herbaceous plants. Proceedings of the National Academy of Sciences, 105(45), 17430 LP–17435. https://doi.org/10.1073/pnas.0804488105. Loreto, F., & Delfine, S., (2000). Emission of isoprene from salt-stressed Eucalyptus globulus leaves. Plant Physiology, 123(4), 1605 LP –1610. https://doi.org/10.1104/pp.123.4.1605. Loreto, F., & Fares, S., (2007). Is ozone flux inside leaves only a damage indicator? Clues from volatile isoprenoid studies. Plant Physiology, 143(3), 1096 LP–1100. https://doi. org/10.1104/pp.106.091892. Loreto, F., & Schnitzler, J. P., (2010). Abiotic stresses and induced BVOCs. Trends in Plant Science, 15(3), 154–166. https://doi.org/https://doi.org/10.1016/j.tplants.2009.12.006. Loreto, F., & Sharkey, T. D., (1993). On the relationship between isoprene emission and photosynthetic metabolites under different environmental conditions. Planta, 189(3), 420– 424. https://doi.org/10.1007/BF00194440. Loreto, F., & Velikova, V., (2001). Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiology, 127(4), 1781 LP–1787. https://doi.org/10.1104/ pp.010497.

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway

93

Loreto, F., Fischbach, R. J., Schnitzler, J. P., Ciccioli, P., Brancaleoni, E., Calfapietra, C., & Seufert, G., (2001). Monoterpene emission and monoterpene synthase activities in the Mediterranean evergreen oak Quercus ilex L. grown at elevated CO2 concentrations. Global Change Biology, 7(6), 709–717. https://doi.org/https://doi. org/10.1046/j.1354-1013.2001.00442.x. Loreto, F., Mannozzi, M., Maris, C., Nascetti, P., Ferranti, F., & Pasqualini, S., (2001). Ozone quenching properties of isoprene and its antioxidant role in leaves. Plant Physiology, 126(3), 993–1000. https://doi.org/10.1104/pp.126.3.993. Luthra, R., Luthra, P. M., & Kumar, S., (1999). Redefined role of mevalonate–isoprenoid pathway in terpenoid biosynthesis in higher plants. Current Science, 76(2), 133–135. http:// www.jstor.org/stable/24101222. Mahdavi, A., Moradi, P., & Mastinu, A., (2020). Variation in terpene profiles of Thymus vulgaris in water deficit stress response. Molecules (Basel, Switzerland), 25(5). https://doi. org/10.3390/molecules25051091. Marino, G., Brunetti, C., Tattini, M., Romano, A., Biasioli, F., Tognetti, R., Loreto, F., et al., (2017). Dissecting the role of isoprene and stress-related hormones (ABA and ethylene) in Populus nigra exposed to unequal root zone water stress. Tree Physiology, 37(12), 1637– 1647. https://doi.org/10.1093/treephys/tpx083. Martin, V. J. J., Pitera, D. J., Withers, S. T., Newman, J. D., & Keasling, J. D., (2003). Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nature Biotechnology, 21(7), 796–802. https://doi.org/10.1038/nbt833. McGarvey, D. J., & Croteau, R., (1995). Terpenoid metabolism. The Plant Cell, 7(7), 1015– 1026. https://doi.org/10.1105/tpc.7.7.1015. Meier, S., Tzfadia, O., Vallabhaneni, R., Gehring, C., & Wurtzel, E. T., (2011). A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana. BMC Systems Biology, 5, 77. https://doi.org/10.1186/1752-0509-5-77. Mentel, T. F., Kleist, E., Andres, S., Dal Maso, M., Hohaus, T., Kiendler-Scharr, A., Rudich, Y., et al., (2013). Secondary aerosol formation from stress-induced biogenic emissions and possible climate feedbacks. Atmos. Chem. Phys., 13(17), 8755–8770. https://doi. org/10.5194/acp-13-8755-2013. Monson, R. K., & Fall, R., (1989). Isoprene emission from aspen leaves. Plant Physiology, 90(1), 267 LP–274. https://doi.org/10.1104/pp.90.1.267. Monson, R. K., Harley, P. C., Litvak, M. E., Wildermuth, M., Guenther, A. B., Zimmerman, P. R., & Fall, R., (1994). Environmental and developmental controls over the seasonal pattern of isoprene emission from aspen leaves. Oecologia, 99(3), 260–270. https://doi. org/10.1007/BF00627738. Monson, R. K., Jaeger, C. H., Adams, W. W., Driggers, E. M., Silver, G. M., & Fall, R., (1992). Relationships among isoprene emission rate, photosynthesis, and isoprene synthase activity as influenced by temperature. Plant Physiology, 98(3), 1175 LP–1180. https://doi. org/10.1104/pp.98.3.1175. Monson, R. K., Weraduwage, S. M., Rosenkranz, M., Schnitzler, J. P., & Sharkey, T. D., (2021). Leaf isoprene emission as a trait that mediates the growth-defense tradeoff in the face of climate stress. Oecologia. https://doi.org/10.1007/s00442-020-04813-7. Morfopoulos, C., Prentice, I. C., Keenan, T. F., Friedlingstein, P., Medlyn, B. E., Peñuelas, J., & Possell, M., (2013). A unifying conceptual model for the environmental responses

94

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

of isoprene emissions from plants. Annals of Botany, 112(7), 1223–1238. https://doi. org/10.1093/aob/mct206. Mu, Z., Llusià, J., Liu, D., Ogaya, R., Asensio, D., Zhang, C., & Peñuelas, J., (2019). Profile of foliar isoprenoid emissions from Mediterranean dominant shrub and tree species under experimental nitrogen deposition. Atmospheric Environment, 216, 116951. https://doi.org/ https://doi.org/10.1016/j.atmosenv.2019.116951. Mundim, F. M., & Pringle, E. G., (2018). Whole-plant metabolic allocation under water stress. In: Frontiers in Plant Science (Vol. 9, p. 852). https://www.frontiersin.org/article/10.3389/ fpls.2018.00852. Niinemets, Ü., (2018). When leaves go over the thermal edge. Plant, Cell and Environment, 41(6), 1247–1250. https://doi.org/https://doi.org/10.1111/pce.13184. Niinemets, Ü., Seufert, G., Steinbrecher, R., & Tenhunen, J. D., (2002). A model coupling foliar monoterpene emissions to leaf photosynthetic characteristics in Mediterranean evergreen Quercus species. New Phytologist, 153(2), 257–275. https://doi.org/https://doi. org/10.1046/j.0028-646X.2001.00324.x. Ormeño, E., & Fernandez, C., (2012). Effect of soil nutrient on production and diversity of volatile terpenoids from plants. Current Bioactive Compounds, 8(1), 71–79. Ormeño, E., Baldy, V., Ballini, C., & Fernandez, C., (2008). Production and diversity of volatile terpenes from plants on calcareous and siliceous soils: Effect of soil nutrients. Journal of Chemical Ecology, 34(9), 1219–1229. https://doi.org/10.1007/s10886-008-9515-2. Ormeño, E., Viros, J., Mévy, J. P., Tonetto, A., Saunier, A., Bousquet-Mélou, A., & Fernandez, C., (2020). Exogenous isoprene confers physiological benefits in a negligible isoprene emitter (Acer monspessulanum L.) under water deficit. In: Plants (Vol. 9, No. 2). https:// doi.org/10.3390/plants9020159. Oustric, J., Morillon, R., Luro, F., Herbette, S., Lourkisti, R., Giannettini, J., Berti, L., & Santini, J., (2017). Tetraploid Carrizo citrange rootstock (Citrus sinensis Osb. ×Poncirus trifoliata L. Raf.) enhances natural chilling stress tolerance of common clementine (Citrus clementina Hort. ex Tan). Journal of Plant Physiology, 214, 108–115. https://doi.org/ https://doi.org/10.1016/j.jplph.2017.04.014. Owen, S. M., & Peñuelas, J., (2005). Opportunistic emissions of volatile isoprenoids. Trends in Plant Science, 10(9), 420–426. https://doi.org/https://doi.org/10.1016/j. tplants.2005.07.010. Peñuelas, J., & Munné-Bosch, S., (2005). Isoprenoids: An evolutionary pool for photoprotection. Trends in Plant Science, 10(4), 166–169. https://doi.org/https://doi. org/10.1016/j.tplants.2005.02.005. Peñuelas, J., Sardans, J., Llusia, J., Owen, S. M., & Niinemets, Ü., (2011). Lower P contents and more widespread terpene presence in old Bornean than in young Hawaiian tropical plant species guilds. Ecosphere, 2(4), art45. https://doi.org/https://doi.org/10.1890/ ES10-00185.1. Perreca, E., Rohwer, J., González-Cabanelas, D., Loreto, F., Schmidt, A., Gershenzon, J., & Wright, L. P., (2020). Effect of drought on the methylerythritol 4-phosphate (MEP) pathway in the isoprene emitting conifer Picea glauca. In Frontiers in Plant Science (Vol. 11, p. 1535). https://www.frontiersin.org/article/10.3389/fpls.2020.546295 (accessed on 18 October 2022). Pezeshki, S. R., (2001). Wetland plant responses to soil flooding. Environmental and Experimental Botany, 46(3), 299–312. https://doi.org/https://doi.org/10.1016/ S0098-8472(01)00107-1.

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway

95

Pichersky, E., Noel, J. P., & Dudareva, N., (2006). Biosynthesis of plant volatiles: Nature diversity and ingenuity. Science, 311(5762), 808 LP–811. https://doi.org/10.1126/ science.1118510. Piironen, V., Lindsay, D. G., Miettinen, T. A., Toivo, J., & Lampi, A. M., (2000). Plant sterols: Biosynthesis, biological function and their importance to human nutrition. Journal of the Science of Food and Agriculture, 80(7), 939–966. https://doi.org/https://doi.org/10.1002/ (SICI)1097-0010(20000515)80:73.0.CO;2-C (accessed on 18 October 2022). Pollastri, S., Tsonev, T., & Loreto, F., (2014). Isoprene improves photochemical efficiency and enhances heat dissipation in plants at physiological temperatures. Journal of Experimental Botany, 65(6), 1565–1570. https://doi.org/10.1093/jxb/eru033. Proteau, P. J., (1998). Biosynthesis of phytol in the Cyanobacterium Synechocystis sp. UTEX 2470:  Utilization of the non-mevalonate pathway. Journal of Natural Products, 61(6), 841– 843. https://doi.org/10.1021/np980006q. Ranney, T. G., & Bir, R. E., (n.d.). Comparative flood tolerance of birch rootstock. Journal of the American Society for Horticultural Science Jashs, 119(1), 43–48. https://doi. org/10.21273/JASHS.119.1.43. Rasulov, B., Copolovici, L., Laisk, A., & Niinemets, Ü., (2009). Postillumination isoprene emission: In vivo measurements of dimethylallyldiphosphate pool size and isoprene synthase kinetics in aspen leaves. Plant Physiology, 149(3), 1609 LP–1618. https://doi. org/10.1104/pp.108.133512. Rasulov, B., Hüve, K., Laisk, A., & Niinemets, Ü., (2011). Induction of a longer-term component of isoprene release in darkened aspen leaves: Origin and regulation under different environmental conditions. Plant Physiology, 156(2), 816 LP–831. https://doi. org/10.1104/pp.111.176222. Rätsch, G., & Haase, K., (2007). Anatomic prerequisites for internal root aeration of three tree species of the Amazonian inundation forest. Amazoniana, 19(3, 4), 185–198. Rennenberg, H., Loreto, F., Polle, A., Brilli, F., Fares, S., Beniwal, R. S., & Gessler, A., (2006). Physiological responses of forest trees to heat and drought. Plant Biology, 8(5), 556–571. https://doi.org/https://doi.org/10.1055/s-2006-924084. Rodríguez-Concepción, M., (2006). Early steps in isoprenoid biosynthesis: Multilevel regulation of the supply of common precursors in plant cells. Phytochemistry Reviews, 5(1), 1–15. https://doi.org/10.1007/s11101-005-3130-4. Rodríguez-Concepción, M., (2010). Supply of precursors for carotenoid biosynthesis in plants. Archives of Biochemistry and Biophysics, 504(1), 118–122. https://doi.org/10.1016/j. abb.2010.06.016. Rodríguez-Concepción, M., Forés, O., Martinez-García, J. F., González, V., Phillips, M. A., Ferrer, A., & Boronat, A., (2004). Distinct light-mediated pathways regulate the biosynthesis and exchange of isoprenoid precursors during Arabidopsis seedling development. The Plant Cell, 16(1), 144–156. https://doi.org/10.1105/tpc.016204. Rohdich, F., Hecht, S., Gärtner, K., Adam, P., Krieger, C., Amslinger, S., Arigoni, D., Bacher, A., & Eisenreich, W., (2002). Studies on the nonmevalonate terpene biosynthetic pathway: Metabolic role of IspH (LytB) protein. Proceedings of the National Academy of Sciences, 99(3), 1158 LP–1163. https://doi.org/10.1073/pnas.032658999. Rohmer, M., Knani, M., Simonin, P., Sutter, B., & Sahm, H., (1993). Isoprenoid biosynthesis in bacteria: A novel pathway for the early steps leading to isopentenyl diphosphate. The Biochemical Journal, 295(2), 517–524. https://doi.org/10.1042/bj2950517.

96

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Rottenberger, S., Kleiss, B., Kuhn, U., Wolf, A., Piedade, M. T. F., Junk, W., & Kesselmeier, J., (2008). The effect of flooding on the exchange of the volatile C2-compounds ethanol, acetaldehyde and acetic acid between leaves of Amazonian floodplain tree species and the atmosphere. Biogeosciences, 5(4), 1085–1100. https://doi.org/10.5194/bg-5-1085-2008. Ryan, A. C., Hewitt, C. N., Possell, M., Vickers, C. E., Purnell, A., Mullineaux, P. M., Davies, W. J., & Dodd, I. C., (2014). Isoprene emission protects photosynthesis but reduces plant productivity during drought in transgenic tobacco (Nicotiana tabacum) plants. New Phytologist, 201(1), 205–216. https://doi.org/https://doi.org/10.1111/nph.12477. Sairam, R. K., Kumutha, D., Ezhilmathi, K., Deshmukh, P. S., & Srivastava, G. C., (2008). Physiology and biochemistry of waterlogging tolerance in plants. Biologia Plantarum, 52(3), 401. https://doi.org/10.1007/s10535-008-0084-6. Sanadze, G. A., & Kalandadze, A. N., (1966). Light and temperature curves of the evolution of C5H8. Fiziol. Rast, 13, 458–461. Sanadze, G. A., (2010). Photobiosynthesis of isoprene as an example of leaf excretory function in the light of contemporary thermodynamics. Russian Journal of Plant Physiology, 57(1), 1–6. https://doi.org/10.1134/S1021443710010012. Sangwan, N. S., Farooqi, A. H. A., Shabih, F., & Sangwan, R. S., (2001). Regulation of essential oil production in plants. Plant Growth Regulation, 34(1), 3–21. https://doi. org/10.1023/A:1013386921596. Santini, J., Giannettini, J., Pailly, O., Herbette, S., Ollitrault, P., Berti, L., & Luro, F., (2013). Comparison of photosynthesis and antioxidant performance of several Citrus and Fortunella species (Rutaceae) under natural chilling stress. Trees, 27(1), 71–83. Santner, A., Calderon-Villalobos, L. I. A., & Estelle, M., (2009). Plant hormones are versatile chemical regulators of plant growth. Nature Chemical Biology, 5(5), 301–307. https://doi. org/10.1038/nchembio.165. Sasaki, K., Saito, T., Lämsä, M., Oksman-Caldentey, K. M., Suzuki, M., Ohyama, K., Muranaka, T., et al., (2007). Plants utilize isoprene emission as a thermotolerance mechanism. Plant and Cell Physiology, 48(9), 1254–1262. https://doi.org/10.1093/pcp/ pcm104. Sauer, F., Schäfer, C., Neeb, P., Horie, O., & Moortgat, G. K., (1999). Formation of hydrogen peroxide in the ozonolysis of isoprene and simple alkenes under humid conditions. Atmospheric Environment, 33(2), 229–241. https://doi.org/https://doi.org/10.1016/ S1352-2310(98)00152-6. Selmar, D., (2008). Potential of salt and drought stress to increase pharmaceutical significant secondary compounds in plants. Agricultural Research in Volkenrode, 58(1, 2), 139. Sharkey, T. D., & Singsaas, E. L., (1995). Why plants emit isoprene. Nature, 374(6525), 769. https://doi.org/10.1038/374769a0. Sharkey, T. D., & Yeh, S., (2001). Isoprene emission from plants. Annual Review of Plant Physiology and Plant Molecular Biology, 52(1), 407–436. https://doi.org/10.1146/annurev. arplant.52.1.407. Sharkey, T. D., Chen, X., & Yeh, S., (2001). Isoprene increases thermotolerance of fosmidomycin-fed leaves. Plant Physiology, 125(4), 2001 LP–2006. https://doi.org/10.1104/ pp.125.4.2001. Sharkey, T. D., Singsaas, E. L., Vanderveer, P. J., & Geron, C., (1996). Field measurements of isoprene emission from trees in response to temperature and light. Tree Physiology, 16(7), 649–654. https://doi.org/10.1093/treephys/16.7.649.

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway

97

Sharkey, T. D., Wiberley, A. E., & Donohue, A. R., (2008). Isoprene emission from plants: Why and how. Annals of Botany, 101(1), 5–18. https://doi.org/10.1093/aob/mcm240. Singsaas, E. L., & Sharkey, T. D., (1998). The regulation of isoprene emission responses to rapid leaf temperature fluctuations. Plant, Cell and Environment, 21(11), 1181–1188. https://doi.org/https://doi.org/10.1046/j.1365-3040.1998.00380.x. Singsaas, E. L., & Sharkey, T. D., (2000). The effects of high temperature on isoprene synthesis in oak leaves. Plant, Cell and Environment, 23(7), 751–757. https://doi.org/ https://doi.org/10.1046/j.1365-3040.2000.00582.x. Singsaas, E. L., Lerdau, M., Winter, K., & Sharkey, T. D., (1997). Isoprene increases thermotolerance of isoprene-emitting species. Plant Physiology, 115(4), 1413 LP–1420. https://doi.org/10.1104/pp.115.4.1413. Sitch, S., Cox, P. M., Collins, W. J., & Huntingford, C., (2007). Indirect radiative forcing of climate change through ozone effects on the land-carbon sink. Nature, 448(7155), 791–794. https://doi.org/10.1038/nature06059. Sivy, T. L., Fall, R., & Rosenstiel, T. N., (2011). Evidence of isoprenoid precursor toxicity in Bacillus subtilis. Bioscience, Biotechnology, and Biochemistry, advpub, 1111022722. https://doi.org/10.1271/bbb.110572. Siwko, M. E., Marrink, S. J., De Vries, A. H., Kozubek, A., Schoot, U. A. J. M., & Mark, A. E., (2007). Does isoprene protect plant membranes from thermal shock? A molecular dynamics study. Biochimica et Biophysica Acta (BBA) - Biomembranes, 1768(2), 198–206. https://doi.org/https://doi.org/10.1016/j.bbamem.2006.09.023. Smit, A., & Mushegian, A., (2000). Biosynthesis of isoprenoids via mevalonate in Archaea: The lost pathway. Genome Research, 10(10), 1468–1484. https://doi.org/10.1101/gr.145600. Stephenson, P. G., Fankhauser, C., & Terry, M. J., (2009). PIF3 is a repressor of chloroplast development. Proceedings of the National Academy of Sciences, 106(18), 7654 LP–7659. https://doi.org/10.1073/pnas.0811684106. Stermer, B. A., Bianchini, G. M., & Korth, K. L., (1994). Regulation of HMG-CoA reductase activity in plants. Journal of Lipid Research, 35(7), 1133–1140. Sun, Z., Shen, Y., & Niinemets, Ü., (2020). Responses of isoprene emission and photochemical efficiency to severe drought combined with prolonged hot weather in hybrid Populus. Journal of Experimental Botany, 71(22), 7364–7381. https://doi.org/10.1093/jxb/eraa415. Tarkowská, D., & Strnad, M., (2018). Isoprenoid-derived plant signaling molecules: Biosynthesis and biological importance. Planta, 247(5), 1051–1066. https://doi. org/10.1007/s00425-018-2878-x. Tattini, M., Loreto, F., Fini, A., Guidi, L., Brunetti, C., Velikova, V., Gori, A., & Ferrini, F., (2015). Isoprenoids and phenylpropanoids are part of the antioxidant defense orchestrated daily by drought stressed Platanus × acerifolia plants during Mediterranean summers. New Phytologist, 207(3), 613–626. https://doi.org/https://doi.org/10.1111/nph.13380. Tattini, M., Velikova, V., Vickers, C., Brunetti, C., DI Ferdinando, M., Trivellini, A., Fineschi, S., et al., (2014). Isoprene production in transgenic tobacco alters isoprenoid, non-structural carbohydrate and phenylpropanoid metabolism, and protects photosynthesis from drought stress. Plant, Cell and Environment, 37(8), 1950–1964. https://doi.org/https:// doi.org/10.1111/pce.12350. Teuber, M., Zimmer, I., Kreuzwieser, J., Ache, P., Polle, A., Rennenberg, H., & Schnitzler, J. P., (2008). VOC emissions of grey poplar leaves as affected by salt stress and different N sources. Plant Biology, 10(1), 86–96. https://doi.org/https://doi. org/10.1111/j.1438-8677.2007.00015.x.

98

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Tholl, D., & Lee, S., (2011). Terpene specialized metabolism in Arabidopsis thaliana. The Arabidopsis Book, 9, e0143. https://doi.org/10.1199/tab.0143. Tholl, D., (2015). Biosynthesis and biological functions of terpenoids in plants. Advances in Biochemical Engineering/Biotechnology, 148, 63–106. https://doi. org/10.1007/10_2014_295. Tiiva, P., Häikiö, E., & Kasurinen, A., (2018). Impact of warming, moderate nitrogen addition and bark herbivory on BVOC emissions and growth of Scots pine (Pinus sylvestris L.) seedlings. Tree Physiology, 38(10), 1461–1475. https://doi.org/10.1093/treephys/tpy029. Tingey, D. T., Manning, M., Grothaus, L. C., & Burns, W. F., (1979). The influence of light and temperature on isoprene emission rates from live oak. Physiologia Plantarum, 47(2), 112–118. https://doi.org/https://doi.org/10.1111/j.1399-3054.1979.tb03200.x. Tippmann, S., Chen, Y., Siewers, V., & Nielsen, J., (2013). From flavors and pharmaceuticals to advanced biofuels: Production of isoprenoids in Saccharomyces cerevisiae. Biotechnology Journal, 8(12), 1435–1444. https://doi.org/https://doi.org/10.1002/biot.201300028. Toledo-Ortiz, G., Huq, E., & Rodríguez-Concepción, M., (2010). Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors. Proceedings of the National Academy of Sciences of the United States of America, 107(25), 11626–11631. https://doi.org/10.1073/pnas.0914428107. Valifard, M., Mohsenzadeh, S., Kholdebarin, B., Rowshan, V., Niazi, A., & Moghadam, A., (2019). Effect of salt stress on terpenoid biosynthesis in Salvia mirzayanii: From gene to metabolite. The Journal of Horticultural Science and Biotechnology, 94(3), 389–399. https://doi.org/10.1080/14620316.2018.1505443. Van, W. G. P., & McDowall, K. J., (2011). The regulation of the secondary metabolism of Streptomyces: New links and experimental advances. Natural Product Reports, 28(7), 1311–1333. https://doi.org/10.1039/c1np00003a. VanNice, J. C., Skaff, D. A., Keightley, A., Addo, J. K., Wyckoff, G. J., & Miziorko, H. M., (2014). Identification in Haloferax volcanii of phosphomevalonate decarboxylase and isopentenyl phosphate kinase as catalysts of the terminal enzyme reactions in an archaeal alternate mevalonate pathway. Journal of Bacteriology, 196(5), 1055 LP–1063. https://doi. org/10.1128/JB.01230-13. Vanzo, E., Merl-Pham, J., Velikova, V., Ghirardo, A., Lindermayr, C., Hauck, S. M., Bernhardt, J., et al., (2016). Modulation of protein S-nitrosylation by isoprene emission in poplar. Plant Physiology, 170(4), 1945 LP–1961. https://doi.org/10.1104/pp.15.01842. Velikova, V., & Loreto, F., (2005). On the relationship between isoprene emission and thermotolerance in Phragmites australis leaves exposed to high temperatures and during the recovery from a heat stress. Plant, Cell and Environment, 28(3), 318–327. https://doi. org/https://doi.org/10.1111/j.1365-3040.2004.01314.x. Velikova, V., Brunetti, C., Tattini, M., Doneva, D., Ahrar, M., Tsonev, T., Stefanova, M., et al., (2016). Physiological significance of isoprenoids and phenylpropanoids in drought response of Arundinoideae species with contrasting habitats and metabolism. Plant, Cell and Environment, 39(10), 2185–2197. https://doi.org/10.1111/pce.12785. Velikova, V., Loreto, F., Tsonev, T., Brilli, F., & Edreva, A., (2006). Isoprene prevents the negative consequences of high temperature stress in Platanus orientalis leaves. Functional Plant Biology, 33(10), 931–940. https://doi.org/10.1071/FP06058. Velikova, V., Pinelli, P., Pasqualini, S., Reale, L., Ferranti, F., & Loreto, F., (2005). Isoprene decreases the concentration of nitric oxide in leaves exposed to elevated ozone. The New Phytologist, 166(2), 419–425. https://doi.org/10.1111/j.1469-8137.2005.01409.x.

Terpenoid Production Through Mevalonate and Methylerythritol Phosphate Pathway

99

Velikova, V., Várkonyi, Z., Szabó, M., Maslenkova, L., Nogues, I., Kovács, L., Peeva, V., et al., (2011). Increased thermostability of thylakoid membranes in isoprene-emitting leaves probed with three biophysical techniques. Plant Physiology, 157(2), 905 LP–916. https:// doi.org/10.1104/pp.111.182519. Vickers, C. E., Gershenzon, J., Lerdau, M. T., & Loreto, F., (2009). A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nature Chemical Biology, 5(5), 283–291. https://doi.org/10.1038/nchembio.158. Vickers, C. E., Possell, M., Cojocariu, C. I., Velikova, V. B., Laothawornkitkul, J., Ryan, A., Mullineaux, P. M., & Nicholas, H. C., (2009). Isoprene synthesis protects transgenic tobacco plants from oxidative stress. Plant, Cell and Environment, 32(5), 520–531. https:// doi.org/10.1111/j.1365-3040.2009.01946.x. Vingarzan, R., (2004). A review of surface ozone background levels and trends. Atmospheric Environment, 38(21), 3431–3442. https://doi.org/https://doi.org/10.1016/j. atmosenv.2004.03.030. Vranová, E., Coman, D., & Gruissem, W., (2013). Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annual Review of Plant Biology, 64, 665–700. https:// doi.org/10.1146/annurev-arplant-050312-120116. Wahid, A., Gelani, S., Ashraf, M., & Foolad, M. R., (2007). Heat tolerance in plants: An overview. Environmental and Experimental Botany, 61(3), 199–223. https://doi.org/https:// doi.org/10.1016/j.envexpbot.2007.05.011. Walter, M. H., Hans, J., & Strack, D., (2002). Two distantly related genes encoding 1-deoxyd-xylulose 5-phosphate synthases: Differential regulation in shoots and apocarotenoidaccumulating mycorrhizal roots. The Plant Journal: For Cell and Molecular Biology, 31(3), 243–254. https://doi.org/10.1046/j.1365-313x.2002.01352.x. Wang, K., Yin, X. R., Zhang, B., Grierson, D., Xu, C. J., & Chen, K. S., (2017). Transcriptomic and metabolic analyses provide new insights into chilling injury in peach fruit. Plant, Cell and Environment, 40(8), 1531–1551. https://doi.org/https://doi.org/10.1111/pce.12951. Way, D. A., Ghirardo, A., Kanawati, B., Esperschütz, J., Monson, R. K., Jackson, R. B., SchmittKopplin, P., & Schnitzler, J. P., (2013). Increasing atmospheric CO2 reduces metabolic and physiological differences between isoprene- and non-isoprene-emitting poplars. New Phytologist, 200(2), 534–546. https://doi.org/https://doi.org/10.1111/nph.12391. Weise, S. E., Li, Z., Sutter, A. E., Corrion, A., Banerjee, A., & Sharkey, T. D., (2013). Measuring dimethylallyl diphosphate available for isoprene synthesis. Analytical Biochemistry, 435(1), 27–34. https://doi.org/https://doi.org/10.1016/j.ab.2012.11.031. Werner, C., Fasbender, L., Romek, K. M., Yáñez-Serrano, A. M., & Kreuzwieser, J., (2020). Heat waves change plant carbon allocation among primary and secondary metabolism altering CO2 assimilation, respiration, and VOC emissions. In: Frontiers in Plant Science (Vol. 11, p. 1242). https://www.frontiersin.org/article/10.3389/fpls.2020.01242 (accessed on 18October 2022). Wilkinson, M. J., Monson, R. K., Trahan, N., Lee, S., Brown, E., Jackson, R. B., Polley, H. W., et al., (2009). Leaf isoprene emission rate as a function of atmospheric CO2 concentration. Global Change Biology, 15(5), 1189–1200. https://doi.org/https://doi. org/10.1111/j.1365-2486.2008.01803.x. Yáñez-Serrano, A. M., Mahlau, L., Fasbender, L., Byron, J., Williams, J., Kreuzwieser, J., & Werner, C., (2019). Heat stress increases the use of cytosolic pyruvate for isoprene biosynthesis. Journal of Experimental Botany, 70(20), 5827–5838. https://doi.org/10.1093/ jxb/erz353.

100

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Yazaki, K., Arimura, G. I., & Ohnishi, T., (2017). “Hidden” terpenoids in plants: Their biosynthesis, localization and ecological roles. Plant and Cell Physiology, 58(10), 1615– 1621. https://doi.org/10.1093/pcp/pcx123. Yordanova, R. Y., & Popova, L. P., (2007). Flooding-induced changes in photosynthesis and oxidative status in maize plants. Acta Physiologiae Plantarum, 29(6), 535–541. Zhang, J., Zeng, L., Chen, S., Sun, H., & Ma, S., (2018). Transcription profile analysis of Lycopersicum esculentum leaves, unravels volatile emissions and gene expression under salinity stress. Plant Physiology and Biochemistry: PPB, 126, 11–21. https://doi. org/10.1016/j.plaphy.2018.02.016. Zhang, R., & Sharkey, T. D., (2009). Photosynthetic electron transport and proton flux under moderate heat stress. Photosynthesis Research, 100(1), 29–43. https://doi.org/10.1007/ s11120-009-9420-8. Zhang, X., Teixeira Da, S. J. A., Niu, M., Li, M., He, C., Zhao, J., Zeng, S., et al., (2017). Physiological and transcriptomic analyses reveal a response mechanism to cold stress in Santalum album L. leaves. Scientific Reports, 7, 42165. https://doi.org/10.1038/srep42165. Zhou, Z., Gu, J., Li, Y. Q., & Wang, Y., (2012). Genome plasticity and systems evolution in Streptomyces. BMC Bioinformatics, 13(10), S8. https://doi. org/10.1186/1471-2105-13-S10-S8. Zuo, Z., Weraduwage, S. M., Lantz, A. T., Sanchez, L. M., Weise, S. E., Wang, J., Childs, K. L., & Sharkey, T. D., (2019). Isoprene acts as a signaling molecule in gene networks important for stress responses and plant growth. Plant Physiology, 180(1), 124–152. https:// doi.org/10.1104/pp.18.01391.

PART II Individual Secondary Metabolites in Tolerance

CHAPTER 4

Role of Diverse Classes of Terpenoids in Tolerance Against Different Environmental Stresses NEHAN SHAMIM,1 ANAMIKA PAUL,1 MARYAM HAGHIGHI,2 and NILANJAN CHAKRABORTY1*

Scottish Church College, Department of Botany, Kolkata – 700006, West Bengal, India

1

Department of Horticulture, College of Agriculture, Isfahan University of Technology, Iran

2

*

Corresponding author. E-mail: [email protected]

ABSTRACT Terpenoids are an important class of structurally diverse plant metabolites synthesized from C-5 precursor units (isopentyl pyrophosphate (IPP) and dimethylallyl pyrophosphate (DMPP)). These precursors are produced by two alternative pathways, i.e., cytosolic mevalonate pathway (MVA) and plastidial methylerythritol phosphate pathway (MEP). Based on the number of carbon atoms, terpenoids can be classified into hemiterpenoids, monoterpenoids, sesquiterpenoids, diterpenoids, triterpenoids, tetraterpenoids, and polyterpenoids. The majority of the terpenoids produced are common to all plants, while some of them are species-specific. Terpenoids are known for their role as accessory pigments, phytoalexins, allelopathic agents, pheromones, repellents, and attractants in plant-insect or plant-animal interaction. Their accumulation in plants is known to be affected upon encountering various biotic and abiotic stresses. Terpenoids such as zealexins are elicited Biology and Biotechnology of Environmental Stress Tolerance in Plants: Secondary Metabolites in Environmental Stress Tolerance, Volume 1. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

104

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

in response to fungal infection, whereas citral induces senescence. Moreover, the induction of terpenoid production is one of the primary defense mechanisms in plants responding to herbivory attacks. This chapter provides a comprehensive account of the critical roles of terpenoids in plants in response to various environmental stresses. 4.1 INTRODUCTION Plants in their surroundings are exposed to various abiotic (radiation, salinity, floods, drought, extremes of temperature, heavy metals, etc.) and biotic (attacks by multiple pathogens such as fungi, bacteria, oomycetes, nematodes, and herbivores) stress factors. The encounter of plants with such environmental stress causes them immense damage and reduces crop yield. Abiotic stress alone can cause a 50–70% decrease in crop productivity. As plants are static in nature, to deal with biotic or abiotic stress, they possess defense responses that include cell wall reinforcement by deposition of lignin, induction of defense genes, generation of reactive oxygen species (ROS), and production of defense compounds. The defense response of plants to cope with adversity can be categorized into morphological changes, physiological changes, and synthesis of secondary metabolites (Naik & Al-Khayri, 2016; Poloni & Schirawski, 2014; Yadav et al., 2021). Secondary metabolites defend the plants against various herbivores, pathogenic microorganisms, and several abiotic stresses, thereby helping the plant persist under adverse conditions. The different secondary metabolite found in plants includes alkaloids, terpenoids, phenols, nitrogen (N), and sulfur (S) containing compounds (Anjum et al., 2011; Chaves, 2002). These terpenoids are the most critical and structurally diverse metabolites (Block et al., 2018). They are synthesized in cytosol and plastid and are stored in specialized secretory structures such as resin ducts, laticifers, and trichomes found on the surface of the leaves (Langenheim, 1994). The terpenoids are made up of isoprene units. Thus, they are also known as isoprenoids. Based on the number of carbon atoms, they can be classified into hemiterpenoids (C5), monoterpenoids (C10), sesquiterpenoids (C15), diterpenoids (C20), triterpenoids (C30), tetraterpenoids (C40), and polyterpenoids (C>40). The monoterpenoids and sesquiterpenoids are the significant components of the essential oil. The essential oils play a crucial role as repellent and antioxidant compounds, helping the plant cope with infestation, predation, and oxidative stress (Grabmann, 2015). Essential oils such as eucalyptol,

Role of Diverse Classes of Terpenoids in Tolerance

105

perillaldehyde, limonene, menthol, carvone, thymol, α-terpineol are monoterpenoids (Boncan et al., 2020). Whereas β-caryophyllene, humulene (α-caryophyllene), and farnesol are sesquiterpenoids. Abscisic acid (ABA) is also a sesquiterpenoid plant hormone involved in the closure of stomata in response to drought stress (Grabmann, 2015). Terpenoids are characteristically diverse, aromatic, volatile, or nonvolatile toxic compounds produced by plants. These metabolite features help the plant in mediating various ecological interactions and communications (Aharoni, 2003). Moreover, they are also known to play a significant role in the defense and development of the plant (Block et al., 2018). Due to the ecological significance of the terpenoid and its role in defense against environmental stress factors, several efforts have been made to modify the terpenoid production in plants (Aharoni et al., 2005; Block et al., 2018; Boncan et al., 2020). The major techniques used for altering the secondary metabolite production in plants include elicitation, metabolic engineering, and genetic transformation (Kowalczyk et al., 2020). Elicitors are low molecular weight compounds that, when applied in small quantities to plants, enhance the biosynthesis of secondary metabolites and other defense-related compounds. This enhancement in the production of metabolites upon application of trace amounts of elicitors is known as elicitation (Halder et al., 2019). Metabolic engineering is in vitro manipulation of the genes encoding the rate-limiting enzymes in the biosynthetic pathway by overexpression or silencing. This approach involves blocking or increasing the metabolic flux to introduce a new metabolic way in the plant to improve the accumulation of secondary metabolites or reduce unwanted compounds’ production (Kowalczyk et al., 2020). Genetic transformation refers to the use of various systems that causes the integration of a foreign gene into an organism’s genome (Jouanin et al., 1993). Terpene (terpenoid) synthases (TPSs) is an important enzyme that is involved in synthesizing the backbone of specialized terpenoids such as ABA and precursors of gibberellic acid (GA) (Falara et al., 2011; Trapp & Croteau, 2001). The elucidation of the terpenoid biosynthetic pathway with various enzymes involved and identification of TPS genes has made metabolic and genetic engineering for upregulating the terpenoid content in plants quite feasible (Aharoni et al., 2005; Falara et al., 2011; Trapp & Croteau, 2001). A detailed account of the biosynthetic pathway of terpenoids has been discussed below, after which we will focus on the role of terpenoids in defense against various environmental stress.

106

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

4.2 BIOSYNTHESIS OF TERPENOIDS Terpenoids are synthesized from C-5 precursor units which are isopentyl pyrophosphate (IPP) and dimethylallyl pyrophosphate (DMAPP). These precursors are produced by two alternative pathways, i.e., cytosolic mevalonate pathway (MVA) and plastidial methylerythritol phosphate pathway (MEP) (Keeling & Bohlmann, 2008). The MEP begins with the formation of 1-deoxy-D-xylulose 5-phosphate (DXP) caused by the condensation of pyruvic acid and glyceraldehyde-3-phosphate (G3P) with the help of the enzyme 1-deoxy-D-xylulose 5-phosphate synthase (DXS) (Singh & Sharma, 2014; Weisner & Jomaa, 2013). The upregulation of DXS enzyme is Arabidopsis elevated the levels of chlorophylls, carotenoids, and ABA in the plant (Estévez et al., 2001). After the synthesis of DXP, it is reduced to 2-C-methyl-D-erythritol 4-phosphate (MEP) by the enzyme 1-deoxy-Dxylulose 5-phosphate reductoisomerase (DXR) (Singh & Sharma, 2014; Weisner & Jomaa, 2013). In transgenic peppermint plant overexpressing DXR enzyme there is a 50% increase in the essential oil yield (Mahmoud & Croteau, 2001). The next step involves the joining of MEP and 4-cytidine 5-phosphate that leads to the formation of 4-cytidine 5’-diphospho-2-Cmethyl-D-erythriol (CDP-ME). The reaction is catalyzed by the enzyme 2-C-methyl-D-erythritol-4-phosphate-cytidyltransferase (MCT). Eventually the enzyme 4-diphosphocytidyl-2-C-methyl-d-erythritol kinase (CMK) catalyzes the conversion CDP-ME to 4-cytidine-5’-diphospho-2-C-methylD-erythritol-2-phosphate (CD-ME2P). The production of methylerythritol cyclodiphosphate (ME-cPP) from CD-ME2P is catalyzed by the enzyme 2-C-methyl-D-erythritol-2,4-cyclodiphosphate (MDS). The enzyme 4-hydroxy-3-methylbut-2-enyl-diphosphate synthase (HDS) produces (E)-4-hydroxy-3-3-methylbut-2-enyl diphosphate (HMBPP) from ME-cPP. Conversion of HMBPP to mixture an isopentyl pyrophosphate (IPP) and dimethylallyl diphosphate (DMAPP) is catalyzed by (E)-4-hydroxy-3methylbut-2-enyl diphosphate reductase (HDR) (Singh & Sharma, 2014; Weisner & Jomaa, 2013). Contrary to MEP the MEV pathway starts in the cytosol with the condensation of three molecules of acetyl CoA by the enzyme acetoacetyl CoA acetyltransferase (ACCT) resulting in the formation of acetoacetyl CoA (AcAc.CoA). The production of 3-hydroxyl-3methyl glutaryl CoA (HMG-CoA) from acetoacetyl CoA is catalyzed by the enzyme 3-hydroxyl-3-methyl glutaryl CoA synthase (HMGS). The production of mevalonic acid (MVA) from HMG-CoA is caused by the enzyme 3-hydroxyl-3-methyl glutaryl CoA reductase (HMGR) (Singh & Sharma,

Role of Diverse Classes of Terpenoids in Tolerance

107

2014). The reaction catalyzed by HMGR could be a rate-limiting step as the overexpression of the genes encoding the enzyme in tobacco resulted in up to a tenfold increase in the isoprenoid accumulation in the plant (Chappell et al., 1995). MVA is phosphorylated by the enzyme mevalonate kinase (MK) to produce mevalonate-5-phosphate (MVP). The mevalonate pyrophosphate (MVPP) is produced from MVP by the enzyme phosphomevalonate kinase (PMK). Isopentyl pyrophosphate (IPP) is produced by decarboxylation of mevalonate pyrophosphate by the enzyme diphosphomevalonate decarboxylase (MVD). Later IPP is isomerized to DMAPP with the help of the enzyme isopentyl diphosphate isomerase (IDI). The synthesized IPP and DMAPP undergoes subsequent condensation by the action of the enzyme prenyl transferase (PT) to produce terpenoid precursors which are acyclic and achiral isoprenyl diphosphate intermediates such as geranyl pyrophosphate (GPP), geranylgeranyl pyrophosphate (GGPP), farnesyl pyrophosphate (FPP), and farnesol farnesyl pyrophosphate (FFPP) in MEP and MVA pathway, respectively. These precursors are acted upon by terpene synthase that results in the production of various terpenoids (Boncan et al., 2020; Karlic & Varga, 2017). Once synthesized the terpenoids may undergo further transformation due to the action of the many enzymes present in different organelles. The non-volatile (phytohormones and pigments) and volatile products (hemiterpenes, monoterpenes, sesquiterpenes, diterpenes, and triterpenes) are formed as a result of the transformations (Glas et al., 2012). The schematic representation of the MEP and MVA pathway is given in Figure 4.1. 4.3 ROLE OF DIVERSE CLASSES OF TERPENOIDS IN RESPONSE TO TOLERANCE AGAINST DIFFERENT ENVIRONMENTAL STRESS Terpenoids accumulation in plants is known to be affected upon encountering various biotic and abiotic stresses. They play a significant role in thermotolerance and in quenching oxidative stress. Moreover, they are also known as accessory pigments (carotenoids), phytoalexins, antioxidant, allelopathic agents, pheromones, repellents, and attractants in plant-insect or plantanimal interaction (Aharoni et al., 2005; Ding et al., 2017; Vaughan et al., 2015). Apart from this, biosynthesis of terpenoids is also induced in response to wounding, where they play a role in sealing the wound (Grassmann et al., 2002). The role played by terpenoids in response to stress has been depicted in Figure 4.2.

108

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

FIGURE 4.1  The biosynthetic pathway of terpenoids in plants. Note: G3P: Glyceraldehyde-3-phosphate; DXS: 1-deoxy-D-xylulose 5-phosphate synthase; DXP: 1-deoxy-D-xylulose 5-phosphate; DXR: 1-deoxy-D-xylulose 5-phosphate reductoisomerase; MEP: 2-C-methyl-D-erythritol 4-phosphate; MCT: 2-C-methyl-D-erythritol4-phosphate-cytidyltransferase; CDP-ME: 4-cytidine 5’-diphospho-2-C-methyl-D-erythriol; CMK: 4-diphosphocytidyl-2-C-methyl-d-erythritol kinase; CD-ME2P: 4-cytidine-5’-diphospho-2-C-methyl-D-erythritol-2-phosphate; MDS: 2-C-methyl-D-erythritol-2,4-cyclodiphosphate; ME-cPP: methylerythritol cyclodiphosphate; HDS: 4-hydroxy-3-methylbut-2-enyldiphosphate synthase; HMBPP: (E)-4-hydroxy-3-3-methylbut-2-enyl diphosphate; HDR: (E)-4-hydroxy-3-methylbut-2-enyl diphosphate reductase; IPP: Isopentyl pyrophosphate; IDI: isopentyl diphosphate isomerase; DMAPP: dimethylallyl diphosphate; PT: Prenyl transferase; GPP: Geranyl pyrophosphate; GGPP: Geranylgeranyl pyrophosphate; ACCT: acetoacetyl CoA acetyltransferase; AcAc.CoA: acetoacetyl CoA; HMGS: 3-hydroxyl-3-methyl glutaryl CoA synthase; HMG-CoA: 3-hydroxyl-3-methyl glutaryl CoA; HMGR: 3-hydroxyl-3-methyl glutaryl CoA reductase; MVA: mevalonic acid; MK: mevalonate kinase; PMK: phosphomevalonate kinase; MVPP: mevalonate pyrophosphate; MVD: diphosphomevalonate decarboxylase; FPP: farnesyl pyrophosphate; FFPP: Farnesyl farnesyl pyrophosphate.

4.3.1 TERPENOID AS STRESS HORMONE Among various abiotic stress, drought is known to cause a severe decrease in crop productivity (Yadav et al., 2021). Drought stress is the trigger for synthesizing various monoterpenoids, diterpenoids, and sesquiterpenoids to overcome adversity (Chaves, 2002). As drought intensifies, water availability

Role of Diverse Classes of Terpenoids in Tolerance

109

FIGURE 4.2  The various role played by terpenoids in response to stress [round shape represents the role of terpenoids and rectangular shape depicts the mode of action].

decreases, and it is further accompanied by loss of cell turgor, high salinity, oxidative stress, and osmotic stress. One of the immediate responses of plants against drought is stomatal closure (Wilkinson & Davies, 2010). It has been proposed that the dehydrating roots send chemical signals to stomata in the form of ABA, which promotes stomatal closure and prevents water loss by transpiration (Chaves, 2002). 4.3.1.1 BIOSYNTHESIS OF ABA ABA is a C-15 sesquiterpenoid and a critical plant hormone involved in various plant growth and development processes and has an essential role in adapting environmental stress factors. The phytohormone promotes seed dormancy, abscission, and senescence, inhibiting germination and delaying floral induction. In addition of these ABA is also known to function in coordination with other hormones such as gibberellins, auxin, and brassinosteroids to regulate the elongation of primary root and suppress the formation of lateral roots, thereby maintaining the root growth and architecture (Antoni et

110

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

al., 2012). ABA is not just found in plants but also in certain phytopathogenic fungi. It is synthesized in plants through the carotenoid pathway, which is also called the indirect pathway. Whereas, in phytopathogenic fungi, it is synthesized via the mevalonate pathway that is the direct pathway. In plants, the subsequent condensations of isopentyl diphosphate (IPP) and DMADP produced by plastidial MEP leads to sequential production of geranyl diphosphate, farnesyl diphosphate, geranylgeranyl diphosphate (GGGP), phytoene, ζ-carotene (zeta-carotene), lycopene and β-carotene. When β-carotene is acted upon by β-carotene hydrolase (BCH) it results in the formation of zeaxanthin which is a C-40 precursor of ABA (Danquah et al., 2014; Finkelstein, 2013). ABA biosynthesis is initiated in the plastid with the conversion of zeaxanthin to all-trans-violaxanthin catalyzed by the enzyme zeaxanthin epoxidase (ZEP). The aba1 (Arabidopsis) mutants have a wilty phenotype (due to excessive water loss) and exhibit characters such as deficiency in ABA synthesis, a decrease in violaxanthin and neoxanthin content but an increase in zeaxanthin accumulation in leaves all of which implies that the ABA locus of Arabidopsis encodes ZEP (Rock & Zeevaart, 1991). The overexpression of BCH genes in transgenic Arabidopsis thaliana led to a twofold increase in violaxanthin content of leaves with enhanced tolerance of the plant to drought stress (Davison et al., 2002). The all-trans-violaxanthin can be converted to 9’-cis-neoxanthin through all-trans-neoxanthin by the enzymes neoxanthin synthase (NSY) and 9-cis-epoxycarotenoid forming isomerase (NCEI). In an alternative pathway, all-trans-violaxanthin is directly converted to 9’-cis-violaxanthin by an unknown isomerase. Then the oxidative cleavage of the 9’-cis-neoxanthin or 9’-cis-violaxanthin by the 9-cis-epoxycarotenoid dioxygenase (NCED) leads to production of C-15 xanthoxin (Taylor et al., 2005). In water-stressed leaves of Phaseolus vulgaris, a significant increase in PvNCED1 mRNA and protein levels was observed with a subsequent elevation in ABA accumulation. Moreover, in transgenic wild tobacco, the constitutive expression of PvNCED1 resulted in an increase in the accumulation of ABA and its catabolite phaseic acid (Qin & Zeevaart, 1999; Qin & Zeevaart, 2002) Xanthoxin acts as a growth inhibitor and its production is the rate-limiting step in ABA biosynthesis. Further, xanthoxin is transported to cytosol where it is converted to abscisic aldehyde (ABAld) by an ABA-specific short-chain dehydrogenase/reductase (AS-SDR) (Finkelstein, 2013; Taylor et al., 2005). The ABAld is eventually converted to ABA by ABA-aldehyde oxidase (AAO). In wilty tomato mutants, flacca, and sitiens impaired at the last step of ABA synthesis have a higher proportion of ABAld converted to alcohol instead of ABA (Taylor

Role of Diverse Classes of Terpenoids in Tolerance

111

et al., 1988). The ABA-deficient mutant of Arabidiopsis has wilty phenotype due to mutation in aldehyde oxidase 3 (AA03) gene, which is responsible for encoding the AAO enzyme (Seo et al., 2000). ABA conjugation and its catalytic hydroxylation are the two pathways of catabolism through which the stress hormone levels are maintained. The hydroxylation of ABA at 8’ position catalyzed by cytochrome P450 monooxygenase encoded by CYP707 results in phaseic acid (PA) production. Further, the enzyme PA reductase catalyzes the conversion of PA to dihydrophaseic acid (DPA) (Gillard & Walton, 1976; Kushiro et al., 2004). In the other pathway, ABA glycosyltransferase causes the conjugation of ABA to ABA-glucosyl ester (ABA-GE), an inactive form of ABA stored in apoplast and vacuoles. As the environment changes, the enzyme β-glucosidase rapidly transforms ABA-GE to ABA (Danquah et al., 2014). The schematic representation of ABA biosynthesis has been shown in Figure 4.3.

FIGURE 4.3  Biosynthesis of ABA in plants. Note: ZEP: zeaxanthin epoxidase; NSY: neoxanthin synthase; NCEI: 9-cis-epoxycarotenoid forming isomerase; NCED: 9-cis-epoxycarotenoid dioxygenase; AS-SDR: ABA-specific short-chain dehydrogenase/reductase; ABAld: abscisic aldehyde; AAO: ABA-aldehyde oxidase; ABA: abscisic acid.

112

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

4.3.1.1.1 ABA Perception and Signaling The major breakthrough in our understanding of ABA signaling was the discovery of PYRABACTIN RESISTANCE1 (PYR1)/PYR1-like (PYL)/ regulatory components of ABA receptors (RCAR) proteins. PYR1/PYL/ RCAR belongs to a family of START domain proteins that act as ABA receptors. These receptors are involved in the ABA signal transduction that induces the expression of ABA-responsive genes. The ABA-responsive genes contain cis-elements known as ABA-responsive elements (ABRE) or a combination of ABRE with a coupling element (CE) which have ACGT cores in their promoter regions. The expression of ABRE-dependent genes is regulated by basic-domain leucine zipper (bZIP), ABRE-binding protein (AREB), and ABRE-binding factors (ABFs). In the Arabidopsis genome, AREB1/ABF, AREB2/ABF4, and ABF3 are among the AREB/ ABF subfamily of bZIP transcription factors induced by drought stress. It has been observed that areb1, areb2, and abf3 triple mutant have reduced tolerance towards drought. The other significant factors involved in ABA signaling include the sucrose non-fermenting protein-1 related kinases 2 (SnRK2s) and group A type 2C protein phosphatases (PP2Cs). The former is a positive regulator, while the latter functions as a negative regulator of the signaling pathway. The cloning of PYR1 and PYLs of Arabidopsis have revealed that they disrupt the functioning of PP2Cs such as ABA-insensitive 1 and 2 (ABAI1 and ABAI2) and hypersensitive to ABA1 (HAB1) (Antoni et al., 2012; Park et al., 2009; Raghavendra et al., 2010). In the absence of stress, the SnRK2s are maintained in a dephosphorylated state through their physical interaction with PP2Cs. Upregulation of endogenous ABA during drought stress is perceived by PYR/RCAR. This causes the ABA-PYR/ RCAR complex to interact with PP2Cs and inhibit its phosphatase activity, thereby activating SnRK2s. The activated SnRK2s phosphorylates AREB/ ABFs resulting in the induction of ABA-responsive genes (Nakashima & Shinozaki, 2013). 4.3.1.1.2 ABA Induced Stomatal Closure The closure of stomata is induced by the ABA-mediated activation of the anion channel on the guard cells. During low concentrations of ABA, the PP2Cs keeps the S-type anion channel (SLAC1) on guard cells in an inactive and dephosphorylated state. The perception of ABA by PYL/PYR/RCAR due to increased concentration inhibits the PP2Cs mediated inactivation of

Role of Diverse Classes of Terpenoids in Tolerance

113

SLAC1 on guard cells. The SnRK2s phosphorylates SLAC1 and NADPH oxidase (NADPHox) respiratory burst oxidase (Rboh), which plays a prominent role in the production of ROS and the formation of nitric oxide (NO) (Laxalt et al., 2016). Among the various intermediates involved in the stomatal closure, Nitric oxide (NO) is equally essential. It acts as a signaling molecule mediating the ABA-induced closure of stomata. Application of exogenous NO in the form of NO donors such as sodium nitroprusside (SNP) induced stomatal closure in species such as Vicia faba, Salpichroa origanifolia and Trandescantia sp. (Garcia-Mata & Lamattina, 2001). Whereas NO scavengers such as 2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (PTIO) or 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline (cPTIO) are capable of reversing the effects of the NO donor substances (Neill et al., 2002; Neill et al., 2008). It has been demonstrated that NO is produced in the guard cells of pea and Arabidopsis in response to ABA. Still, the treatment of these plants with PTIO inhibits stomatal closure and facilitates the removal of NO. NO is produced due to the enzymatic activity of nitrate reductase (NR). The guard cells of Arabidopsis mutants which have significantly reduced NR activity, do not synthesize NO, and ABA-induced stomatal closure is not seen in such mutants. Although careful observation proved that ABA does prevent the opening of the stomata in such mutants. NO is known to promote the production of a secondary lipid messenger, phosphatidic acid (PA). PA produce due to the actions of phospholipase C (PLC) causes the hydrolysis of phosphatidylinositol 4,5 bisphosphate (PIP2) into diacylglycerol and inositol polyphosphates (InsPPs). The phosphorylation of diacylglycerol-by-diacylglycerol kinase (DAG) results in the production of PA. The PA formed binds to Rboh, causing its activation, and simultaneously it also inhibits PP2C and K+ influx ion channels on the guard cells. Whereas InsPPs formed is water-soluble, it diffuses to the cytosol, consequently promoting the release of calcium (Ca) stored in the stomatal guard cells (Desikan et al., 2002; Distéfano et al., 2007). The elevated levels of ABA increase cyclic ADP ribose (cADPR), and InsPPs further activates additional calcium channels in the tonoplast (Dittrich et al., 2019; Himmelbach et al., 2003; Macrobbie, 1992). Substantial evidence confirms an increase in the cytosolic concentration of Ca2+ in the guard cells of the plants treated with exogenous ABA. Ca2+ acts as an intracellular messenger in ABA signaling, and the activation of the calcium channel depends on ATP hydrolysis. Upon perceiving calcium ions, the calcium sensor proteins such as calcineurin B-like proteins (CBLs) activates CBL interacting protein kinases (CIPKs). The CBLs and CIPKs in association and coordination with each other,

114

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

regulate several downstream events, which leads to stomatal closure (Edel & Kudla, 2016; Laxalt et al., 2016). The influx of calcium initiates intracellular Ca2+ oscillations and promotes the further release of Ca2+ from the vacuoles. The rise in intracellular Ca2+ blocks K+ influx channels and facilitates Cl– outward channels on the plasma membrane, causing membrane depolarization. The plasma membrane proton pump is inhibited by an ABA-induced increase in cytosolic calcium concentration, and a rise in intracellular pH further depolarizes the membrane, leading to stomata closure (Dittrich et al., 2019; Himmelbach et al., 2003; Macrobbie, 1992). 4.3.1.1.3  Role of ABA in Cold Acclimatization Cold stress or low temperatures is a significant stress factor that can disrupt the plant cells’ normal metabolism, thereby limiting the plant’s growth and productivity. Chilling stress can cause the inhibition of various physiological and biochemical processes of the plant, leading to the accumulation of toxic compounds in plants. In contrast, in freezing stress, ice crystals form within the plant cell, leading to membrane damage followed by cell death (Shi & Yang, 2014). In plants increase in freezing tolerance involves changes in proteins, sugars, enzymes, and gene expression. It has been suggested that ABA plays a role in acclimatization to cold stress (Gilmour & Thomashow, 1991). The experiment conducted by Chen and his colleagues in 1979 was one of the earliest works on the theory. They observed that the exogenous application of ABA to stem cultivated plants and the leaf callus of Solanum sp. induced freezing resistance in the majority of the samples. Similar results were obtained when the cell suspension culture of Triticum aestivum L. cv Norstar was treated with ABA. There is evidence that ABA’s exogenous application did increase freezing tolerance in a wide range of plants such as tobacco, alfalfa, and Arabidopsis. Moreover, there are reports of elevation in the endogenous levels of ABA in response to cold stress (Chen et al., 1983). Based on these works, Chen et al. (1983) concluded that the exposure of plants to cold temperatures results in an increase in the endogenous levels of ABA in plants which in turn is responsible for triggering the synthesis of proteins that induces freezing tolerance in plants. Gilmour & Thomashow (1991) demonstrated that ABA-deficient mutants were impaired in freezing tolerance. Moreover, the overexpression of TaSnRK2.3 (a novel SnRK2 member found in wheat) in Arabidopsis resulted in enhanced tolerance to drought, salinity, and cold

Role of Diverse Classes of Terpenoids in Tolerance

115

stress (Tian et al., 2013). On the other hand, the downregulation of PP2Cs in transgenic Arabidopsis accelerated acclimatization to cold stress (Tähtiharju & Palva, 2002). In plants, acclimatization to cold stress is achieved due to the expression of cold-regulated genes. The important cor genes of Arabidopsis include responsive to dehydration (rd), cold-regulated (cor), low-temperature induced (lti), and early responsive to dehydration (erd) (Viswanathan & Zhu, 2002). The characterization of rd29A of Arabidopsis thaliana led to identifying ABRE cis-elements in the promoter region of the genes (YamaguchiShinozaki & Shinozaki, 1993). The C-repeat binding factors (CBFs) genes, also known as dehydration-responsive element binding factors (DREBs), play a central role in acclimatizing cold stress. CBF1, CBF2, and CBF4 are apetala2/ethylene-responsive factors (AP2/ERF). The CBF1 and CBF3 are not induced in response to ABA (Shi & Yang, 2014), whereas the expression of CBF4 is induced in response to ABA and drought not cold. The transgenic plants overexpressing CBF4 are more tolerant to drought and freezing stress (Haake, 2002). All of this evidence indicates that the dehydration associated with cold-stress results in an increase in the endogenous levels of ABA, leading to the induction of cold-responsive genes through ABRE cis-elements but the major molecular mechanism as to how ABA increases freezing tolerance is still unknown (Viswanathan & Zhu, 2002). 4.3.2 TERPENOIDS IN RESPONSE TO OXIDATIVE STRESS/ TERPENOIDS AS ANTIOXIDANTS Solar energy absorption is the prerequisite for photosynthesis, but there is a need for the thermal dissipation of this energy. The excess energy, if not dissipated, would result in the plant being subjected to oxidative stress. Drought, high-intensity light, and salt stress can cause oxidative stress to persist, which is hazardous to plants. Oxidative stress refers to complicated physiological and chemical parameters. The oxidation and antioxidation reactions are imbalanced, so overproduction of ROS happens (Bartosz, 1997; Demidchik, 2015). ROS is a collective term used for partially reduced intermediates of atmospheric oxygen (O2) which were earlier recognized as toxic by-products of aerobic metabolism. Although after years of research, it has become apparent that ROS has high biological significance to living cells and is involved in various developmental processes of plants. Moreover, ROS also functions as an eminent signaling molecule in response to biotic and abiotic stress. Similarly, in humans, nearly 1–3% of the O2

116

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

consumed by the body is converted into different ROS, which is involved in killing microbial pathogens, cell signaling, and induction of apoptosis. The primary sites of ROS production in plants are chloroplast, mitochondria, peroxisomes, endoplasmic reticulum, cell membrane, and apoplast (Das & Roychoudhury, 2014; Grabmann, 2015; Khoshbakht et al., 2017). The increase in ROS production due to biotic and abiotic stresses occurs through distinct pathways. In response to biotic stress, specific ROS-producing enzymes are activated, such as NADPH oxidase and cell wall peroxidases. On the other hand, abiotic stress causes an elevation in ROS production through the impairment of photosynthetic and respiratory electron transport pathways (Haghighi et al., 2014). The various ROS crucial for the induction of oxidative stress includes the free radicals such as superoxide anion (O2–), hydroxyl radical (OH–), and non-radicals such as hydrogen peroxide (H2O2) and singlet oxygen species (1O2) (Pogány et al., 2006). Singlet oxygen (1O2) is the common name for triplet oxygen generated by the reaction of chlorophyll in the triplet state. It has a half-life of 1 μs and plays a significant role in the upregulation of genes involved in providing defense against photo-oxidative stress, whereas its overproduction results in oxidation of DNA, polyunsaturated fatty acids (PUFA), and proteins. The superoxide anion (O2–) is a powerful reducing agent that has a half-life of 1 μs, mainly produced as a result of mitochondrial electron transport chain (ETC) and by thylakoid-localized PSI during non-cyclic ETC. It can react with a double bond containing iron-sulfur (Fe-S) clusters of proteins and cause electron leaks from the carriers in mitochondrial ETC. H2O2 is a weak oxidant mainly produced by the dismutation of the superoxide radical. With a half-life of 1 millisecond, H2O2 can oxidize proteins and can produce hydroxyl radical (OH–) by reacting with superoxide anion (O2–) in a Fe-catalyzed reaction (Fenton reaction). Hydroxyl radical (OH–) is the most reactive and toxic ROS with a half-life of 1 nanosecond. It is mainly produced due to the Fenton reaction occurring in the stroma due to the decomposition of ozone (O3) in the apoplast. The hydroxyl radical is highly reactive with proteins, DNA, lipids, and other macromolecules. The excessive accumulation of OH– results in cell death. Moreover, it can pair with O2– and react with NO, resulting in the production of reactive nitrogen species (RNSs), peroxynitrite (ONOO–), and alkyl peroxynitrite (ROONO). Conclusively, many harmful effects of overproduction of ROS happen in plants like increased oxidative reactions, damage to proteins and DNA, lipid peroxidation, and peroxidation of PUFA of cell membrane turn lead to damage of different cellular components and enzyme inhibition, electron leak, and cell death. To keep the production of

Role of Diverse Classes of Terpenoids in Tolerance

117

ROS under control, the plants possess antioxidants or ROS scavengers, such as superoxide dismutase (SOD), catalase (CAT), ascorbic acid, tocopherols, uric acid, and terpenoids. In this chapter, we will focus on the role of terpenoids as antioxidants. The most potent terpenoid antioxidant includes the carotenoids and the various mono-, di-, and sesquiterpenoid essential oils produced in the plants (Graßmann, 2015; Motamedi et al., 2019). Carotenoids are pigment compounds widely distributed in plants, algae, fungi, and bacteria. They function as an accessory pigment in plants and are often referred to antenna molecule which absorbs light between 450 nm and 570 nm of the visible spectrum. Carotenoids belong to the significant group of tetraterpenoids formed by the conjugation of two C20 units. Till now, more than 600 carotenoids have been isolated from nature. In addition to functioning as accessory pigments, the carotenoids play a significant role as antioxidants. It has been approximated that each carotenoid can quench up to 1,000 singlet oxygen molecules. The major carotenoids found in plants are β-carotene, lutein, violaxanthin, neoxanthin, and xanthophylls. Carotenoids are located close to the chlorophylls, where they transfer the radiant energy absorbed by them to the chlorophyll molecules, protecting them against photooxidation and bleaching (Grabmann, 2015). The β-carotene protects the photosynthetic apparatus by quenching the singlet oxygen formed via chlorophyll in the triplet state. This quenching is facilitated by the nine double bonds in β-carotene (Choudhary & Behera, 2001). Similarly, lycopene also quenches the singlet oxygen, but its quenching rate is higher than that of β-carotene. The higher rates of scavenging correspond to the presence of β-ionone ring at one end of lycopene. The glutathione, sulfonyl, and nitrogen dioxide radical can also be quenched by β-carotene (Conn et al., 1991; Di Mascio et al., 1989). The transgenic calli of Ipomoea batatas with suppressed β-carotene hydroxylase gene showed higher β-carotene content, a high antioxidant capacity, and increased tolerance to salt stress (Kim et al., 2012). Similar results were published by Kang et al. (2017). The suppression β-carotene hydroxylase gene in transgenic sweet potato resulted in an up to the 16-fold increase in β-carotene content compared to the non-transgenic line. The increase in β-carotene content was accompanied by higher levels of chlorophyll and conferred enhanced tolerance of the plant towards abiotic stress. Lutein is a vital plant carotenoid, and in some plants, it accounts for more than 50% of the total carotenoid content. The enzyme lycopene ε cyclase (LYC-ε) is involved in the carotenoid biosynthetic pathway as it catalyzes the formation of lutein from α-carotene. The overexpression of LYC-ε gene from Lycium chinense in Arabidopsis thaliana

118

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

enhanced tolerance to stress (Song et al., 2016). Similar overexpression of LYC-ε in Apium graveolens resulted in higher lutein content and increased tolerance to salt stress (Yin et al., 2020). Zeaxanthin causes the dissipation of excessive excitation energy by causing non-photochemical quenching (NPQ) of chlorophyll fluorescence. Moreover, in comparison to lutein, the quenching ability of zeaxanthin is two times more effective, possibly due to the presence of conjugated double bond in zeaxanthin (Choudhary & Behera, 2001; Everett et al., 1996). A broad range of essential oils also serves as antioxidants in response to oxidative stress (Grabmann, 2015). In plants such as Rosmarimus officinalis (rosemary) and Mentha spicata (spearmint), an increase in the levels of monoterpenoids in response to mild or severe water stress has been reported. In spearmint, limonene, and carvone are the main monoterpenoids, and a 50% increase in their content in severely stressed plants was observed. Whereas in rosemary, α-pinene and camphor were the major compounds formed, and more than 100-fold increase in the content of these compounds in severely stressed plants was noted (Delfine et al., 2005). Oregano (Origanum vulgare) is a world-famous flavoring herb, the essential oils of which is known to contain various monoterpenoids and sesquiterpenoids such as carvacrol, thymol, linalyl acetate, (E)-βcaryophyllene, germacrene D, bi-cyclogermacrene, β-caryophyllene oxide (Morshedloo et al., 2017). Morshedloo et al. (2017) conducted experiments by subjecting two different subspecies of oregano to water stress. They observed a subsequent increase in the essential oil content of Origanum vulgare subsp. gracile, whereas no significant increase in the essential oil content of Origanum vulgare sub sp. virens was noted. Although an increase in (E)-β-caryophyllene content in Origanum vulgare sub sp. virens subjected to water stress were reported suggesting its possible role in water stress attenuation. The cucurbitacins are well known for their role as a repellent, and their role in water stress has also been established. It has been reported that the concentration of cucurbitacin in a wilted cucumber is twice as much as in a non-wilted cucumber. To some extent, this can form the basis for the correlation of accumulation cucurbitacins in plants with drought stress (Kano & Goto, 2003). Furthermore, Mashilo et al. (2018) performed experiments with a few Lagernaria siceraria (bottle gourd) varieties to decipher the relationship of accumulation of cucurbitacin E and I with drought tolerance. Their results hypothesized that the accumulation of cucurbitacins was most probably have osmolytes role in regulating the stomatal conductance and

Role of Diverse Classes of Terpenoids in Tolerance

119

transpiration rates to maintain the plant water balance in photosynthesis. They also suggested an antioxidant role of cucurbitacin against various ROS such as superoxide anion (O2–), hydroxyl radical (OH–), H2O2 and singlet oxygen species (1O2). 4.3.3 TERPENOID AS REPELLANTS Terpenoids can directly target insect pests by acting as toxins and deterrents, or the volatile terpenoid may attract the arthropods that prey on the pest infesting the plant (Block et al., 2018; Boncan et al., 2020; Sharma et al., 2017). The chemical analysis of such volatiles from plants infested by pests showed that the terpenoids produced by plants attract the pests’ predators (Takabayashi et al., 1994). The probable mechanism by which terpenoids act as a toxin to pests includes inhibiting ATP synthase, alkylation of nucleophiles, and interference with molting (Langenheim, 1994). The direct and indirect defense response mediated by volatile plant terpenoids is often associated with the presence of glandular trichomes. The glandular trichomes act as a physical hindrance, toxins (for predators), and feeding repellents. Terpenoids are metabolites found in the glandular trichomes and various other flavonoids, phenylpropenes, methyl ketones, acyl sugars, and defensive proteins (Glas et al., 2012). The feeding or walking of insects disrupts glandular trichomes, which in turn induces a jasmonic acid (JA) signaling cascade and other defense genes (Sharifi-Rad et al., 2017). In some cases, after coming in contact with air, the water-soluble exudates of the glandular hair change into a black insoluble material. Eventually, the black insoluble substance gets precipitated in the aphid’s limbs, impeding its movement. Further accumulation of the material causes the aphid to become immobilized and starved to death (Gibson, 1971). The sesquiterpenoid leucosceptroids present in the glandular trichomes of Leucosceptrum canum exhibits antifeedant activity against beet armyworm Spodoptera exigua and cotton bollworm Helicoverpa armigera (Lou et al., 2010). In a few Solanum species, the glandular hair produces the sesquiterpenes 7-epizingiberene and R-curcumeme, which repellents to Bemisia tabaci (Silverleaf whiteflies) (Bleeker et al., 2011; Glas et al., 2012). Gibson & Pickett (1983) reported that the sesquiterpenoid (E)-β-farnesene present in the glandular trichomes of Solanum berthautii (Wild potato) has the potential to repel Myzus persicae (aphids) even if they are at a distance of nearly 1–3 mm from the leaves. Moreover, (E)-β-farnesene attracts Diaeretiella rapae, a

120

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

parasitoid to M. persicae (Beale et al., 2006). The infestation of lima beans with spider mite Tetranychus urticae induces the terpenoids (E)-β-ocimene and linalool, which attracts the predatory mites Phytoseiulus persimilis and Neoseiulus californicus (Sharma et al., 2017; Shimoda et al., 2005). Quite often, the phenomenon of enticement of the parasitoid begins with the herbivore egg deposition. The deposition of eggs of Pieris brassicae on the black mustard plant induces the production of volatiles with high amounts of (Z)-3-hexen-1-ol that significantly increased the attraction of parasitoid Cotesia glomerata to the plant (Pashalidou et al., 2014). Similarly, the oviposition on needles of Pinus sylvestris by the pine sawfly Diprion pini causes the release of volatiles, the odor of which lures the eulophid egg parasitoid Chrysonotomyia ruforum. This oviposition can trigger the systematic release of volatiles from the needles adjacent to those bearing the eggs (Hilker et al., 2002). In the elm plant (Ulmus minor) the deposition of the egg by Xanthogaleruca luteola causes the emission of terpenoids such as (E)-2,6-dimethyl-6,8-nonadien-4-one, (E)-2,6-dimethyl-2,6,8-nonatrien-4-one, and (R,E)-2,3-epoxy-2,6-dimethyl-6,8-nonadiene that attracts Oomyzus gallerucae parasitoid to the plant (Wegener & Schulz, 2002). It has been demonstrated that on being infested with S. exigua (beet armyworm) the maize seedlings released large amounts of volatiles containing (Z)-3-hexenal, (E)-2-hexenal, (Z)-3-hexen-1-ol, (Z)-3-hexen-1-yl acetate, linalool, (3E)-4,8-dimethyl-1,3,5-nonatriene, indole, α-trans-bergamotene, (E)-β-farnesene, (E)-nerolidol and (3E, 7E)-4,8,12-trimethyl-1,3,7,11tridecatetraene and the blend of which lures Cotesia marginiventris which is a parasitoid on S. exigua (Turlings et al., 1990; Turlings et al., 1991). In response to feeding maize root by the larvae of naive Diabrotica virgifera virgifera, the root of the plant releases (E)-β-caryophyllene, which attracts an entomopathogenic nematode which is parasitoid towards the attacking organism (Rasmann et al., 2005). Kauralexins found in maize are known to exhibit antifeedant activity against Ostrinia nubilais (European corn borer) (Schmelz et al., 2011). Cucurbitacins are a group of oxygenated tetracyclic triterpenoids produced widely in Cucurbitaceae. They are known for their bitterness and toxicity towards various pathogens, pests, animals, and humans (Ferguson & Metcalf, 1985; Chen et al., 2005). The bitter variety of cucumber that is the varieties in which cucurbitacins are present exhibits a pronounced resistance towards spider mite T. urticae (Gould, 1978). The resistance of Cucumis sativus to spider mite is associated with cucurbitacin C as it is the only cucurbitacin that has been identified in the plant (Balkema-Boomstra

Role of Diverse Classes of Terpenoids in Tolerance

121

et al., 2003). The eudesmane type sesquiterpenoids show a broad spectrum of biological activities by functioning as plant growth regulators and antifeedant, antifungal, and antibacterial compounds. One such terpenoid is β-costic acid produced in various medicinal and aromatic plants and maize. It is known to inhibit the growth of Fusarium graminearum, F. verticilloides, Rhizopus microsporus, Aspergillus parasiticus, and Cochliobolus heterostrophus (Ding et al., 2017). Eugenol, caryophyllene oxide, α-pinene, α-humulene and α-phellandrene are terpenoids found in cinnamon and clove. They are known to show toxic effects against the pest Sitophilus granaries (Boncan et al., 2020; Plata-Rueda et al., 2018). Similar findings have been reported from Cymbopogon citratus whose essential oil components such as citral and geranyl acetate exhibited insecticidal activity against the peanut beetle Ulomoides dermestoides (PlataRueda et al., 2020). The terpenoid (E)-β-caryophyllene is concerned with attracting the Cotesia sesamiae, a larval parasitoid of the stem borer Chilo partellus. Along with an increase in the (E)-β-caryophyllene content in response to infestation of a maize plant by the stem borer, a subsequent elevation in the transcript levels of terpene synthase 23 (TSP23) was also noted as the enzyme catalyzes the last reaction in the biosynthetic pathway of (E)-β-caryophyllene (Tamiru et al., 2017). Transgenic lines of Arabidopsis thaliana overexpressing maize TSP10 increased the attractiveness of Cotesia marginiventris to these plants (Schnee et al., 2006). Similar results were obtained when maize TSP8 was expressed in Arabidopsis. Moreover, it was observed that the collective expression of maize TPS10, TPS8, and TPS5 resulted in transgenic plants that were more attractive to C. marginiventris than the plants expressing these genes individually (Fontana et al., 2011). Similarly, transgenic chrysanthemum-producing linalool potentially repelled western flower thrips Frankliniella occidentalis (Aharoni et al., 2005). The A. thaliana plants overexpressing linalool significantly repelled aphids M. persicae (Aharoni, 2003). The repellent and toxic terpenoids can be used as biopesticides and bioinsecticides to control the crop damage by the herbivore. In 2018 Oliveira and his co-workers successfully trapping Bemisia tabaci (whitefly) using geraniol encapsulated in chitosan/gum Arabic nanoparticles. This nanoparticle technology can encapsulate potential terpenoids for trapping pests and insects (Boncan et al., 2020). The various terpenoids which play a role in defending the plant from pest infestation with their mode of action is given in Table 4.1.

Terpenoid

Target Pest

Mode of Action

References

Zea mays L.

(Z)-3-hexenal, (E)-2-hexenal, (Z)-3hexen-1-ol, (Z)-3-hexen-1-yl acetate, linalool, (E)-β-farnesene, (E)-nerolidol (E)-β-caryophyllene

Spodoptera exigua

Attracts parasitoid Cotesia marginiventris.

Turlings et al. (1990, 1991)

Diabrotica virgifera virgifera Chilo partellus

Attracts parasitoid.

Rasmann et al. (2005)

Attract parasitoid Cotesia sesamiae Toxic towards the pest Toxic to insect

Tamiru et al. (2017)

Kauralexins Linalool

Ostrinia nubilais Myzus persicae

(Z)-3-hexen-1-ol

Pieris brassicae

Solanum berthaultii Hawkes

(E)-β-farnesene

M. persicae

Cinnamomum sp. and Syzygium aromaticum (L.) Merr. and L.M. Perry Cucumis sativus L.

Eugenol, caryophyllene oxide, α-pinene, α-humulene and α-phellandrene

Sitophilus granaries

Toxic to pest

Cucurbitacin C

Tetranychus urticae

Deters the pest

Spodoptera exigua Helicoverpa armigera

Deters feeding of the insect

Arabidopsis thaliana (L.) Heynh Brassica nigra L.

Leucosceptrum canum Leucosceptroids Sm.

Attracts the egg parasitoid Cotesia glomerata Attract parasitoid Diaeretiella rapae

Schmelz et al. (2011) Aharoni (2003) Pashalidou et al. (2014) Beale et al. (2006); Gibson & Pickett (1983) Boncan et al. (2020); Plata-Rueda et al. (2018) Balkema-Boomstra et al. (2003); Gould (1978) Lou et al. (2010)

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Plant Name

122

TABLE 4.1  List of Few Plant Terpenoids with Their Mode of Action and Target Pests

Plant Name

Terpenoid

Target Pest

Phaseolus lunatus L.

(E)-β-ocimene

T. urticae

Pinus sylvestris L.

Volatiles (identity under investigation)

Ulmus minor Mill.

(E)-2,6-dimethyl-6,8-nonadien-4-one, (E)-2,6-dimethyl-2,6,8-nonatrien-4-one and (R,E)-2,3-epoxy-2,6-dimethyl-6,8nonadiene

Mode of Action

Attract predator mites Phytoseiulus persimilis and Neoseiulus californicus Attracts the Diprion pini egg parasitoid Chrysonotomyia ruforum Xanthogaleruca luteola Attract parasitoid Oomyzus gallerucae

References Sharma et al. (2017); Shimoda et al. (2005)

Hilker et al. (2002)

Wegener & Schulz (2002)

Role of Diverse Classes of Terpenoids in Tolerance

TABLE 4.1  (Continued)

123

124

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

4.3.4 TERPENOIDS AS PHYTOALEXINS In the year 1940, Müller and Borger performed an experiment showing that the prior inoculation of a potato tuber with the incompatible strain of Phytophthora infestans resulted in the development of resistance in the tuber against a compatible strain of Phytophthora infestans and Fusarium sp. This made them hypothesize that the presence of a nonspecific substance was responsible for developing resistance against the compatible strain of pathogen. The nonspecific substance was named as phytoalexins. Phytoalexins can be defined as a low-molecular-weight antimicrobial compound, the accumulation of which increases in plants in response to attack by pathogens (Hammerschmidt, 1999). Chemically phytolaexins can be phenolics, terpenoids, furanoacetylenes, steroid glycoalkaloids, sulfur-containing compounds, and indoles (Jeandet, 2015). In most of the plant species, certain diterpenoids and sesquiterpenoids function as phytoalexins (Cheng et al., 2007). Phytoalexins such as capsidiol, gossypol, ipomeamarone, phytuberin, lubimin, and rishitin are sesquiterpenoids, whereas carbene, momilactones, and oryzalexins are diterpenoids (Huang, 2001). The non-volatile terpenoid phytoalexins such as zealexins, dolabralexins, and kauralexins possess antimicrobial and antifeedant activity (Block et al., 2018). For phytoalexins, only one mode of action is highly unlikely due to diversity in its chemical structure. However, most of the effects are on membrane integrity and respiration of the attacking microbe (Huang, 2001). Perrin & Bottomley (1962) were the first to isolate a phytoalexin from the pods of Pisum sativum inoculated with the Monilinia fruticola which named as pisatin after its crystallization and characterization. Ever since the isolation of pisatin, efforts have been made to elucidate various other phytoalexins’ biosynthesis, structure, and biological activity (Jeandet, 2015). The biosynthesis of these terpenoids is triggered upon encounter with pathogens or elicitor treatment. Such stimulation results in the activation of various enzymes involved in the acetatemevalonate pathway (Huang, 2001). Nearly 14 polycyclic diterpenoids have been identified in Oryza sativa. They are categorized into four types, i.e., momilactones A and B, oryzalexins A-F oryzalexin S and phytocassanes A-E. They are synthesized from geranylgeranyl diphosphate (GGDP) via intermediate hydrocarbon precursors such as 9β-pimara-7, 15-diene, stemar-13-ene, ent-sandatacopimaradiene, and ent-cassa-12,15-diene. It has been found that rice leaves accumulate all the phytoalexins with anti-microbial activity in response to inoculation with blast fungus Magnaporthe grisea or ultraviolet irradiation (Cheng et al., 2007). Among the non-volatile terpenoids produced

Role of Diverse Classes of Terpenoids in Tolerance

125

by maize in response to the biotic attack are kauralexins, labdane-related diterpenoids, and zealexins which are sesquiterpenoids. Biosynthesis of kauralexins involves bi-cyclization of GGDP by ent-copalyl diphosphate synthase into ent-copalyl diphosphate which is further converted to entkaurene by ent-kaurene synthases. The maize kauralexins A1–A3 includes ent-kauran-17-oic acid, ent-kauran-17, 19-dioic acid and ent-kaur-19-al17-oic acid. The maize kauralexins B1–B3 includes ent-kaur-15-en-17-oic acid, ent-kaur-15-en-17, 19-dioic acid and ent-kaur-15-en-19-al-17-oic acid (Block et al., 2018). Kauralexins in maize has been found to exhibit antifeedant activity against Ostrinia nubilais (European corn borer) and antifungal activity against Colletotrichum graminicola, Rhizopus microsporus, and Fusarium graminearum (Schmelz et al., 2011). Zealexins are nonvolatile acidic sesquiterpenoids that are specifically induced by fungal inoculation. The accumulation of zealexins escalates upon infection with pathogens such as Cochliobolus heterostrophus, Fusarium graminearum, Rhizopus microsporus, Colletotrichum sublineolum and Aspergillus flavus (Block et al., 2018; Christensen et al., 2017; Huffaker et al., 2011). Sorghum is an important cereal crop like maize and paddy, which, although it is high heat and drought tolerant, is susceptible to attack by various pathogens. In response to infection with Colletotrichum sublineolum there is accumulation of two distinct 3-deoxyanthocyanidin phytoalexins in infected cells of Sorghum bicolor, namely, apigeninidin (2-(4-hydrophenyl) benzopyrilium chloride) and luteolinidin, which are responsible for hindering the proliferation and spread of fungal hyphae (Poloni & Schirawski, 2014). Moreover, Stonecipher et al. (1993) observed that apigeninidin also prevents the growth of Bacillus cereus, Staphylococcus aurens, Staphylococcus epidermidis, Streptococcus faecalis, Escherichia coli, Serratia marcescens, and Shigella flexneri. In Capsicum annuum inoculation with Phytophthora capsici resulted in the accumulation of capsidiol in the necrotic area, which inhibited the further growth of the pathogen (Egea et al., 1996). Gossypol is an eminent sesquiterpenoid that functions as phytoalexins in cotton plants, with δ-cadinene synthase being the major enzyme involved in its synthesis (Lou et al., 2001). The mRNA level of δ-cadinene synthase was significantly induced in the stem of the cotton plant infected with Verticillium dahliae (Alchanati et al., 1998). Similarly, the expression of a cytochrome P450 monooxygenase catalyzes the formation of an intermediate in gossypol biosynthesis, increased in Gossypium arboreum upon treatment with the suspension culture Verticillium dahliae. Consequently, the accumulation of gossypol in the sub-epidermal

126

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

glands of aerial tissues and root epidermal cells of the plant also increased (Lou et al., 2001). In sweet potato (Ipomoea batatas), inoculation with Ceratocystis fimbriata induced Ipomea marone production in the plant’s root tissues. Casbene found in Ricinus communis is an antifungal diterpenoid elicited upon attack by Rhizopus stolonifer and few other fungi (Sitton & West, 1975). The elicitation of thorn apple (Datura stramonium) with spore suspension of Penicillium chrysogenum and sonicate Phytophthora infestans mycelium induced the formation of rishitin and lubimin (Whitehead et al., 1990). The list of important terpenoid phytoalexins produced by certain plants has been listed in Table 4.2. 4.3.5 TERPENOIDS IN RESPONSE TO WOUNDING The induction of terpenoids biosynthesis in plants can also be associated with the mechanical injury caused by many potential pests, pathogens, and animals. Mechanical damage of any type may induce the emission of specific monoterpenoids and sesquiterpenoids as volatiles. In conifers, the accumulation of terpenoid oleoresin in the epithelial cells around the cortical and trauma-associated resin duct acts as a defense mechanism (Bohlmann & Keeling, 2008). Oleoresin is a viscous and odoriferous liquid composed of distinct terpenoid compounds (Keeling & Bohlmann, 2006b). The insect feeding, fungal inoculation, and mechanical damage trigger the activation of epithelial cells lining the resin ducts, resulting in specialized traumatic resin ducts in the xylem. In conifers, oleoresin terpenoids are stored in axial and radial resin ducts that may be constitutive (essential) or induced (induced upon injury). Chemically oleoresin consists of monoterpenes and diterpenoid resin acid in nearly the same proportions. Still, the composition of oleoresin changes according to the environmental stress that the plant has to cope with survival. The terpenoid oleoresin can be a deterrent or toxic to pests and pathogens (Keeling & Bohlmann, 2006a; Zulak & Bohlmann, 2010). In response to wounding, the terpenoids function as a solvent and vehicle for resin acids. It has been observed that the oleoresin flows out at the injury site with resin acids crystallization at the same point due to oxidative polymerization, thus entombing the insect. The sequence of events eventually leads to the sealing of the wound, which further acts as a mechanical barrier towards the invading pests and inhibits pathogens’ entry (Grassmann et al., 2002; Kreuzwieser et al., 1999). The oxidation of diterpene synthase products by the activity of cytochrome P450-dependent monooxygenases

Plant Name Zea mays L.

Oryza sativa L. Sorghum bicolor (L.) Moench Gossypium arboreum L. Capsicum annuum L. Ipomoea batatas (L.) Lam Ricinus communis L. Datura stramonium L.

Phytoalexin Kauralexins, Zealexins

Action Against Ostrinia nubilais, Colletotrichum graminicola, Rhizopus microsporus and Fusarium graminearum, Cochliobolus heterostrophus, Fusarium graminearum, Rhizopus microsporus, Colletotrichum sublineolum and Aspergillus flavus Momilactones, oryzalexins, Magneportha grisea or ultraviolet irradiation and phytocassanes Apigeninidin and Bacillus cereus, Staphylococcus aurens, Staphylococcus luteolinidin epidermidis, Streptococcus faecalis, Escherichia coli, Serratia marcescens and Shigella flexneri Gossypol Verticillium dahliae

References Block et al. (2018); Christensen et al. (2017); Huffaker et al. (2011); Schmelz et al. (2011) Cheng et al. (2007)

Capsidiol

Phytophthora capsici

Poloni & Schirawski (2014); Stonecipher et al. (1993) Alchanati et al. (1998); Lou et al. (2001) Egea et al. (1996)

Ipomeamarone

Ceratocystis fimbriata

Huang (2001)

Casbene

Rhizopus stolonifer and few other fungi

Sitton & West (1975)

Rishitin and Lubimin

Penicillium chrysogenum and sonicate Phytophthora infestans mycelium

Whitehead et al. (1990)

Role of Diverse Classes of Terpenoids in Tolerance

TABLE 4.2  Role of Phytoalexins Against Pathogens

127

128

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

(P450s) results in the formation of diterpenoid resin acids. The P450s are a large class of heme-containing enzymes that cleaves atmospheric O2 by utilizing NAPDH or NADP. To this date, only one P450 gene involved in diterpenoid resin acid biosynthesis in conifers has been characterized that is CYP720B of loblolly pine (Pinus taeda). The transcript levels of P450s of CYP720B group and TPS enzyme are upregulated in response to insect attack (Keeling & Bohlmann, 2006a, b; Zulak & Bohlmann, 2010). The attack on Sitka spruce (Picea sitchensis) by white pine weevil (Pissodes strobi), one of the most destructive insect pests, elevated the transcription of various TPS genes in the plant, specifically the monoTPS gene, along with an increase in the levels of volatile terpenoid emission. The weevil attack induced the formation of axial terpenoid resin ducts in the stems of Sitka spruce (Miller et al., 2005). Moreover, the exogenous application of defense hormones such as methyl jasmonate (MeJA) can also augment the transcript levels of TPS and P450 enzymes. The application of a solution of MeJA to the soil of Douglas-fir (Pseudotsuga menziesii) seedlings results in the formation of traumatic resin duct in roots. In response to this elicitation the stems of Douglas-fir exhibit a significant increase in the content of monoterpenoids such as linalool, camphene, myrcene, tricyclene, β-phellandrene α- and β-pinene whereas in roots an increase in few sesquiterpenoids such as α-humulene, (E)-caryophyllene, germacrene D, and longifolene have been noted (Huber et al., 2005). Similar results were seen in Norway spruce (Picea abies) and Sitka spruce, where spraying MeJA elicited the formation of traumatic resin ducts and accumulation of mono- and diterpenoids in the stems of the two conifers (Martin et al., 2002; Miller et al., 2005). Apart from MeJA the application of JA to plants such as A. thaliana also resulted in upregulation of specific TPS (Aharoni, 2003). The terpenoids (Z)-3-hexen1-ol and (Z)-3-hexenyl acetate, also called green leaf volatiles, are produced in response to herbivory attacks. These compounds are the volatile components of the blend released by lima bean upon physical damage caused by an infestation by a spider mite (Shimoda et al., 2005). 4.4 CONCLUSION The terpenoids are known to play a role in various biological processes of the plant, especially in defense against stress. The multiple terpenoids may function as accessory pigments, phytoalexins, repellents, and as constituents of oleoresin and essential oils. Emission of volatile terpenoids and the

Role of Diverse Classes of Terpenoids in Tolerance

129

production of non-volatile terpenoids have great significance in countering biotic and abiotic stress. The terpenoids functioning as repellents can be used as biopesticides and bioinsecticides. Moreover, the nanoencapsulation of terpenoids can serve as a promising system for pest management in sustainable agriculture. Two of the most novel findings were identifying the terpenoid phytoalexin found in maize and rice. The elucidation of the regulating mechanism of phytoalexin in commercially important food crops and other species is a prerequisite for developing strategies to improve disease resistance in plants. In addition, a better knowledge of the mode of action of phytoalexin is also required. Essential oils with mono- and sesquiterpenoids as their constituents are unique as they play a dual role in plants. These essential oils do not just show toxicity towards pests but can also act as an antioxidant. The carotenoids exhibit exceptional singlet oxygen quenching potential. The characterization of mutant plants with increased tolerance to oxidative stress due to upregulation or suppression of enzymes involved in the carotenoid biosynthetic pathway might provide useful information for increasing crop productivity in a warmer climate. Although the role of ABA in regulating ion channels and stomatal closure has been elucidated, its role in mediating cold response in plants is still controversial. Whether or not the critical components of the ABA signaling pathway are involved in regulating cold-regulated genes is yet to be elucidated. The alteration of the terpenoid biosynthetic pathway did produce transgenic plants with improved resistance to stress. However, to increase the crop yield to feed the growing human population, a better understanding of the factors controlling the regulation of enzymes involved in terpenoid metabolism is needed. KEYWORDS • • • •

abscisic acid antioxidant isopentyl pyrophosphate phytoalexins

• repellents • stomatal closure • terpenoids against stresses

130

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

REFERENCES Aharoni, A., (2003). Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell, 15, 2866–2884. Aharoni, A., Jongsma, M., & Bouwmeester, H., (2005). Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci., 10, 594–602. Alchanati, I., Patel, J. A. A., Liu, J., Benedict, C. R., Stipanovic, R. D., Bell, A. A., Cui, Y., & Magill, C. W., (1998). The enzymatic cyclization of nerolidyl diphosphate by δ-cadinene synthase from cotton stele tissue infected with Verticillium dahlia. Phytochemistry, 47, 961–967. Anjum, S. A., Xiao, X., Wang, L., Saleem, M. F., Man, C., & Lei, W., (2011). Morphological, physiological and biochemical responses of plants to drought stress. Afr. J. Agric. Res., 6, 2026–2032. Antoni, R., Guzman, M. G., Rodriguez, L., Llobet, M. P., Pizzio, G. A., Fernandez, M. A., Winne, N. D., et al., (2012). Pyrabactin resistance1-like8 plays an important role for the regulation of abscisic acid signaling in root. Plant Physiol., 161, 931–941. Balkema-Boomstra, A. G., Zijlstra, S., Verstappen, F. W. A., Inggamer, H., Mercke, P. E., Jongsma, M. A., & Bouwmeester, H. J., (2003). Role of cucurbitacin c in resistance to spider mite (Tetranychus urticae) in cucumber (Cucumis sativus L.). J. Chem. Ecol., 29, 225–235. Bartosz, G., (1997). Oxidative stress in plants. Acta Physiol. Plant, 19, 47–64. Beale, M. H., Birkett, M. A., Bruce, T. J. A., Chamberlain, K., Field, L. M., Huttly, A. K., Martin, J. L., et al., (2006). Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior. PNAS., 103, 10509–10513. Block, A. K., Vaughan, M. M., Schmelz, E. A., & Christensen, S. A., (2018). Biosynthesis and function of terpenoids defense compounds in maize (Zea mays). Planta, 249, 21–30. Bohlmann, J., & Keeling, C. I., (2008). Plant terpenoids. Wiley Encyclopedia of Chemical Biology. Boncan, D. A. T., Tsang, S. S. K., Lee, C., Lee, I. H. T., Lam, H. M., Chan, T. F., & Hui, J. H. L., (2020). Terpenes and terpenoids in plants: Interactions with environment and insects. Int. J. Mol. Sci., 21, 1–19. Chappell, J., Wolf, F., Proulx, J. C., Cuellar, R., & Saunders, C., (1995). Is the reaction catalyzed by 3-hydroxy-3-methylglutaryl coenzyme A reductase a rate-limiting step for the isoprenoid biosynthesis in plants? Plant Physiol., 109, 1337–1343. Chaves, M. M., (2002). Hoe plants cope with water stress in the field? Photosynthesis and growth. Ann. Bot., 89, 907–916. Chen, H. H., Gavinlertvatana, P., & Li, P. H., (1979). Cold acclimation of stem-cultured plants and leaf callus of Solanum species. Bot. Gaz., 104, 142–147. Chen, H. H., Li, P. H., & Brenner, M. L., (1983). Involvement of abscisic acid in potato cold acclimation. Plant Physiol., 71, 362–365. Chen, J. C., Chiu, M. H., Nie, R. L., Cordell, G. A., & Qiu, S. X., (2005). Cucurbitacins and cucurbitane glycosides: Structures and biological activities. Nat. Pro. Rep., 22, 386–399. Chen, T. H. H., & Gusta, L. V., (1983). Abscisic acid-induced freezing resistance in cultured plant cells. Plant Physiol., 73, 71–75. Cheng, A. X., Lou, Y. G., Mao, Y. B., Lu, S., Wang, L. J., & Chen, X. Y., (2007). Plant terpenoids: Biosynthesis and ecological functions. J. Integr. Plant Biol., 49, 179–186.

Role of Diverse Classes of Terpenoids in Tolerance

131

Choudhary, N., & Behera, R., (2001). Photoinhibition of photosynthesis: Role of carotenoids in photoprotection of chloroplast constituents. Photosynthetica, 39, 481–488. Christensen, S. A., Huffaker, A., Sims, J., Hunter, C. T., Block, A., Vaughan, M. M., Willett, D., et al., (2017). Fungal and herbivore elicitation of the novel maize sesquiterpnoid, zealexin A4, is attenuated by elevated CO2. Planta, 247, 863–873. Conn, P. F., Schalch, W., & Truscott, T. G., (1991). The singlet oxygen and carotenoid interaction. J. Photochem. Photobiol. B: Biol., 11, 41–47. Danquah, A., Zelicourt, A., Colcombet, J., & Hirt, H., (2014). The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol. Adv., 32, 40–52. Davison, P. A., Hunter, C. N., & Horton, P., (2002). Overexpression of β-carotene hydrolase enhances stress tolerance in Arabidopsis. Nature, 418, 203–206. Delfine, S., Loreto, F. P., Ponelli, P., Tognetti, R., & Alvino, A., (2005). Isoprenoids content and photosynthetic limitations in rosemary and spearmint plants under water stress. Agric. Ecosyst. Environ., 106, 243–252. Demidchik, V., (2015). Mechanisms of oxidative stress in plants: From classical chemistry to cell biology. Environ. Exp. Bot., 109, 212–228. Desikan, R., Griffiths, R., Hancock, J., & Neill, S., (2002). A new role for an old enzyme: Nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. PNAS., 99, 16314–16318. Di Mascio, P., Kaiser, S., & Sies, H., (1989). Lycopene as the most efficient biological carotenoid singlet oxygen quencher. Arch. Biochem. Biophys., 274, 532–538. Ding, Y., Huffaker, A., Köllner, T. G., Weckwerth, P., Robert, C. A. M., Spencer, J. L., Lipka, A. E., & Schmelz, E. A., (2017). Selinene volatiles are essential precursors for maize defense promoting fungal pathogen resistance. Plant Physiol., 175, 1455–1468. Distéfano, A. M., García-Mata, C., Lamattina, L., & Laxalt, A. M., (2007). Nitric oxideinduced phosphatidic acid accumulation: A role for phospholipase C and D in stomatal closure. Plant Cell & Environ., 31, 187–194. Dittrich, M., Mueller, H. M., Bauer, H., Peirats-Llobet, M., Rodriguez, P. L., Geilfus, C. M., Carpentier, S. C., et al., (2019). The role of Arabidopsis ABA receptors from the PYR/ PYL/RCAR family in stomatal acclimation and closure signal integration. Nat. Plants, 5, 1002–1011. Edel, K. H., & Kudla, J., (2016). Integration of calcium and ABA signaling. Curr. Opin. Plant Biol., 33, 83–91. Egea, C., Alcazar, M. D., & Candela, M. E., (1996). Capsosiol: Its role in resistance of Capsicum annuum to Phytophthora capsici. Physiol. Plant, 98, 737–742. Estévez, J. M., Cantero, A., Reindl, A., Reichler, S., & Leόn, P., (2001). 1-Deoxy-d-xylulose5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J. Biol. Chem., 276, 22901–22909. Everett, S. A., Dennis, M. F., Patel, K. B., Maddix, S., Kundu, S. C., & Willson, R. L., (1996). Scavenging of nitrogen dioxide, thiyl, and sulfonyl free radicals by the nutritional antioxidant-carotene. J. Biol. Chem., 27, 3988–3994. Falara, V., Akhatr, T. A., Nguyen, T. T. H., Spyropoulou, E. A., Bleeker, P. M., Schauvinhold, I., Matsuba, Y., et al., (2011). The tomato terpene synthase gene family. Plant Physiol., 157, 770–789. Ferguson, J. E., & Metcalf, R. L., (1985). Cucurbitacins. J. Chem. Ecol., 11, 311–318. Finkelstein, R., (2013). Abscisic acid synthesis and response. The Arabidopsis Book, 11, 1–36.

132

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Fontana, A., Held, M., Fantaye, C. A., Turlings, T. C., Degenhardt, J., & Gershenzon, J., (2011). Attractiveness of constitutive and herbivore-induced sesquiterpene blends of maize to the parasitic wasp Cotesia marginiventris (Cresson). J. Chem. Ecol., 37, 582–591. Garcia-Mata, C., & Lamattina, L., (2001). Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol., 128, 790–792. Gibson, R. W., & Pickett, J. A., (1983). Wild potato repels aphids by release of aphid alarm pheromone. Nature, 302, 608, 609. Gibson, R. W., (1971). Glandular hairs providing resistance to aphids in certain wild potato species. Ann. Appl. Biol., 68, 113–119. Gillard, D. F., & Walton, D. C., (1976). Abscisic acid metabolism by a cell-free preparation from Echinocystis lobata liquid endosperm. Plant Physiol., 58, 790–795. Gilmour, S. J., & Thomashow, M. F., (1991). Cold acclimation and cold-regulated gene expression in ABA mutants of Arabidopsis thaliana. Plant Mol. Biol., 17, 1233–1240. Glas, J., Schimmel, B., Alba, J., Ecobar-Bravo, R., Schuurink, R., & Kant, M., (2012). Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. Int. J. Mol. Sci., 131, 17077–17103. Gould, F., (1978). Resistance of cucumber varieties to Tetranychus urticae: Genetic and environmental determinants. J. Econ. Entomol., 71, 680–683. Graßmann, J., (2015). Terpenoids as plant antioxidants. Vitam. Horm., 72, 505–535. Grassmann, J., Hippeli, S., & Elstner, E. F., (2002). Plant’s defense and its benefits for animals and medicine: Role of phenolics and terpenoids in avoiding oxygen stress. Plant Physiol. Biochem., 40, 471–478. Haake, V., (2002). Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol., 130, 639–648. Haghighi, M., Abolghasemi, R., & Teixeira, S. J. A., (2014). Low and high temperature stress affect the growth characteristics of tomato in hydroponic culture with Se and nano-Se amendment. Sci. Hortic., 178, 231–240. Halder, M., Sarkar, S., & Jha, S., (2019). Elicitation: A biotechnological tool for enhanced production of secondary metabolites in hairy root cultures. Eng. Life Sci., 19, 880–895. Hammerschmidt, R., (1999). Phytoalexins: What have we learned after 60 years? Annu. Rev. Phytopathol., 37, 285–306. Hilker, M., Kobs, C., Varama, M., & Schrank, K., (2002). Insect egg deposition induces Pinus sylvestris to attract egg parasitoids. J. Exp. Biol., 205, 455–461. Himmelbach, A., Yang, Y., & Grill, E., (2003). Relay and control of abscisic acid signaling. Curr. Opin. Plant Biol., 6, 470–479. Huang, J. S., (2001). Accumulation of phytoalexins as a resistance mechanism. Plant Pathogenesis and Resistance, 525–621. Huber, D. P. W., Philippe, R. N., Madilao, L. L., Sturrock, R. N., & Bohlmann, J., (2005). Changes in anatomy and terpene chemistry in roots of Douglas-fir seedlings following treatment with methyl jasmonate. Tree Physiol., 25, 1075–1083. Huffaker, A., Kaplan, F., Vaughan, M. M., Dafoe, N. J., Ni, X. Z., Rocca, J. R., & Alborn, H., (2011). Tet al., Novel acidic sesquiterpenoids constitute a dominant class of pathogeninduced phytoalexins in maize. Plant Physiol., 156, 2082–2097. Jeandet, P., (2015). Phytoalexins: Current progress and future prospects. Molecules, 20, 2770–2774. Jouanin, L., Brasileiro, A. C. M., Leplé, J. C., Pilate, G., & Cornu, D., (1993). Genetic transformation: A short review of methods and their applications, results and perspectives for forest trees. Ann. Sci., 50, 325–336.

Role of Diverse Classes of Terpenoids in Tolerance

133

Kang, L., Ji, C. Y., Kim, S. H., Ke, Q., Park, S. C., Kim, S. H., Lee, H. U., et al., (2017). Suppression of the β-carotene hydrolase gene increases β-carotene content and tolerance to abiotic stress in transgenic sweetpotato plants. Plant Physiol. Biochem., 117, 24–33. Kano, Y., & Goto, H., (2003). Relationship between the occurrence of bitter fruit in cucumber (Cucumis sativus L.) and the contents of total nitrogen, amino acid nitrogen, protein and HMG-CoA reductase activity. Sci. Hortic., 98, 1–8. Karlic, H., & Varga, F., (2017). Mevalonate pathway. Encyclopedia of Cancer, 2, 445–457. Keeling, C. I., & Bohlmann, J., (2006a). Diterpene resin acids in conifers. Phytochemistry, 67, 2415–2423. Keeling, C. I., & Bohlmann, J., (2006b). Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defense of conifers against insects and pathogens. New Phytol., 170, 657–675. Khoshbakht, D., Asghari, M. R., & Haghighi, M., (2017). Influence of foliar application of polyamines on growth, gas exchange characteristics, and chlorophyll fluorescence in Bakraii citrus under saline conditions. Photosynthetica, 56, 731–742. Kim, S. H., Ahn, Y. O., Ahn, M. J., Lee, H. S., & Kwak, S. S., (2012). Down-regulation of β-carotene hydrolase increases β-carotene and total carotenoids enhancing salt stress tolerance in transgenic cultured cells of sweetpoatato. Phytochemistry, 74, 69–78. Kowalczyk, T., Wieczfinska, J., Skała, E., Śliwiński, T., & Sitarek, P., (2020). Transgenesis as a tool for the efficient production of selected secondary metabolites from in vitro plant cultures. Plants, 9, 1–21. Kreuzwieser, J., Schnitzler, J. P., & Steinbrecher, R., (1999). Biosynthesis of organic compounds emitted by plants. Plant Biol., 1, 1647–1656. Kushiro, T., Okamoto, M., Nakabayashi, K., Yamagishi, K., Kitamura, S., Asami, T., Hirai, N., et al., (2004). The Arabidopsis cytochrome P450 CYP707A encodes ABA 8ʹ-hydrolases: Key enzymes in ABA catabolism. EMBO, 23, 1647–1656. Langenheim, J. H., (1994). Higher plant terpenoids: A phytocentric overview of their ecological roles. J. Chem. Ecol., 20, 1223–1280. Laxalt, A. M., Garcia-Mata, C., & Lamattina, L., (2016). The dual role of nitric oxide in guard cells: Promoting and attenuating the ABA and phospholipid-derived signals leading to the stomatal closure. Front. Plant Sci., 7, 1–3. Lou, P., Wang, Y. H., Wang, G. D., Essenberg, M., & Chen, X. Y., (2001). Molecular cloning and functional identification of (+)-δ-cadiene-8-hydrolase, a cytochrome P450 monooxygenase (CYP706B1) of cotton sesquiterpene biosynthesis. Plant J., 28, 95–104. Lou, S. H., Lou, Q., Niu, X. M., Xie, M. J., Zhao, X., Schneider, B., Gershenzon, J., & Li, S. H., (2010). Glandular trichomes of Leucosceptrum canum harbor defensive sesterterpenoids. Angew. Chem. Int. Ed., 122, 4573–4577. McRobbie, E. A. C., (1992). Calcium and ABA-induced stomatal closure. Philos. Trans. R. Soc. B: Biol. Sci., 338, 5–18. Mahmoud, S. S., & Croteau, R. B., (2001). Metabolic engineering of essential oil yield and composition in mint by altering expression of deoxy xylulose phosphate reductoisomerase and menthofuran synthase. PNAS., 98, 8915–8920. Martin, D. M., Tholl, D., Gershenzon, J., & Bohlmann, J., (2002). Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid metabolism in developing xylem of Norway spruce stems. Plant Physiol., 129, 1003–1018. Mashilo, J., Odindo, A. O., Shimelis, H. A., Musenge, P., Tesfay, S. Z., & Magwaza, L. S., (2018). Photosynthetic response of bottle gourd [Lagenaria siceraria (Molina) Standl.] to

134

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

drought stress: Relationship between cucurbitacins accumulation and drought tolerance. Sci. Hortic., 231, 133–143. Miller, B., Madilao, L. L., Ralph, S., & Bohlmann, J., (2005). Insect-induced conifer defense. White pine weevil and methyl jasmonate induce traumatic resinosis, de novo formed volatile emissions, and accumulation of terpenoid synthase and octadecanoid pathway transcripts in Sitka spruce. Plant Physiol., 137, 369–382. Morshedloo, M. R., Craker, L. E., Salami, A., Nazeri, V., Sang, H., & Maggi, F., (2017). Effect of prolonged water stress on essential oil content, compositions and gene expression patterns of mono- and sesquiterpene synthesis in two oregano (Origanum vulgare L.) subspecies. Plant Physiol. Biochem., 111, 119–128. Motamedi, M., Haghighi, M., & Goli, A., (2019). Physiological changes of sweet and hot peppers in vegetative and reproductive growth stages treated by Ca and H2O2 under unforeseen heat stresses. Sci. Hortic., 249, 306–313. Naik, P. M., & Al-Khayri, J. M., (2013). Abiotic and biotic elicitors—Role in secondary metabolites production through in vitro culture of medicinal plants. In: Shanker, A. K., & Shanker, C., (eds.), Abiotic and Biotic Stress in Plants—Recent Advances and Future Perspectives (pp. 247–277). IntechOpen: Croatia. Nakashima, K., Yamaguchi-Shinozaki, K. ABA signaling in stress-response and seed development. Plant Cell Rep., 32, 959–970. Neill, S. J., Desikan, R., Clarke, A., & Hancock, J. T., (2002). Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol., 128, 13–16. Neill, S., Barros, R., Bright, J., Desikan, R., Hancock, J., Harrison, J., Morris, P., et al., (2008). Nitric oxide, stomatal closure and abiotic stress. J. Exp. Bot., 59, 165–176. Park, S. Y., Fung, P., Nishimura, N., Jensen, D. R., Fujii, H., Zhao, Y., Lumba, S., et al., (2009). Abscisic acid inhibits type 2C protein phosphatise via the PYR/PYL family of START proteins. Science, 324, 1068–1071. Pashalidou, F. G., Gols, R., Berkhout, B. W., Weldegergis, B. T., Van, L. J. J. A., Dickie, M., & Fatouros, N. E., (2014). To be in time: Egg deposition enhances plant detection of young caterpillars by parasitoids. Oecologia, 177, 477–486. Perrin, D. R., & Bottomley, W., (1962). Studies on phytoalexin V. The structure of pisatin from Pisum sativum L. J. Am. Chem. Soc., 84, 1919–1922. Plata-Rueda, A., Campos, J. M., Rolim, G. D. S., Martínez, L. C., Dos, S. M. H., Fernandes, F. L., Serrão, J. E., & Zanuncio, J. C., (2018). Terpenoid constituents of cinnamom and clove essential oils cause toxic effects and behavior repellancy response on granary weevil, Sitophilus granarius. Ecotoxicol. Environ. Saf., 156, 263–270. Plata-Rueda, A., Martínez, L. C., Da Silva, R. G., Coelho, R. P., Dos, S. M. H., De Souza, W. T., Zanuncio, J. C., & Serrão, J. E., (2020). Insecticidal and repellent activities of Cymbopogon citratus (Poaceae) essential oil and its terpenoids (citral and geranyl acetate) against Ulomoides dermestoides. Crop Prot., 137, 1–21. Pogány, M., Harrach, B. D., Hafeez, Y. M., Barna, B., Kiraly, Z., & Paldi, E., (2006). Role of reactive oxygen species in abiotic and biotic stresses in plants. Acta Phytopathol. Entomolo. Hung., 41, 23–35. Poloni, A., & Schirawski, J., (2014). Red card for pathogens: Phytoalexins in sorghum and maize. Molecules, 19, 9114–9133. Qin, X., & Zeevaart, J. A. D., (1999). The 9-cis-epoxycarotenoid cleavage reaction is the key regulator step of abscisic acid biosynthesis in water-stressed bean. PNAS., 96, 15354–15361.

Role of Diverse Classes of Terpenoids in Tolerance

135

Qin, X., & Zeevaart, J. A. D., (2002). Overexpression of a 9-cis-epoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. Plant Physiol., 128, 544–551. Raghavendra, A. S., Gonugunta, V. K., Christmann, A., & Grill, E., (2010). ABA perception and signaling. Trends Plant Sci., 15, 395–401. Rasmann, S., Köllner, T. G., Degenhardt, J., Hiltpold, I., Toepfer, S., Kuhlmann, U., Gershenzon, J., & Turlings, T. C. J., (2005). Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature, 434, 732–737. Rock, C. D., & Zeevaart, J. A., (1991). The aba mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. PNAS., 88, 7496–7499. Schmelz, E. A., Kaplan, F., Huffaker, A., Dafoe, N. J., Vaughan, M. M., Ni, X., Rocca, J. R., et al., (2011). Identity, regulation and activity of inducible diterpenoid phytoalexin in maize. PNAS., 108, 5455–5460. Schnee, C., Kollner, T. G., Held, M., Turlings, T. C. J., Gershenzon, J., & Degenhardt, J., (2006). The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. PNAS., 103, 1129–1134. Seo, M., Peeters, A. J. M., Koiwai, H., Oritani, T., Marion-Poll, A., Zeevaart, J. A. D., Koorneef, M., et al., (2000). The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyzes the final step in abscisic acid biosynthesis in leaves. PNAS., 97, 12908–12913. Sharifi-Rad, J., Sureda, A., Tenore, G. C., Daglia, M., Sharifi-Rad, M., Valussi, M., Tundis, R., et al., (2017). Biological activities of essential oils: From plant chemoecology to traditional healing systems. Molecules, 22, 70. Sharma, E., Anand, G., & Kapoor, R., (2017). Terpenoids in plants and arbuscular mycorrhizareinforced defiance against herbivorous insect. Ann. Bot., 119, 791–801. Shi, Y., & Yang, S., (2014). ABA regulation of the cold stress response in plants. In: Zhang, D. P., (ed.), Abscisic Acid: Metabolism, Transport and Signaling (pp. 337–363). Springer: Netherlands. Shimoda, T., Ozawa, R., Sano, K., Yano, E., & Tabkabayashi, J., (2005). The involvement of volatile infochemicals from spider mites and from food plants in prey location of generalist predatory mite Neoseiulus californicus. J. Chem. Ecol., 31, 2019–2032. Singh, B., & Sharma, R. A., (2014). Plant terpenes: Defense responses, phylogenetic analysis, regulation and clinical applications. 3 Biotech, 5, 129–151. Sitton, D., & West, C. A., (1975). Casbene: An antifungal diterpene produced in cell-free extracts of Ricinus communis seedlings. Phytochemistry, 14, 1921–1925. Song, X., Diao, J., Ji, J., Wang, G., Li, Z., Wu, J., Josine, T. L., & Wang, Y., (2016). Overexpression of lycopene ε-cyclase gene from Lycium chinense confers tolerance to chilling stress in Arabidopsis thaliana. Gene, 576, 395–403. Stonecipher, L. L., Hurley, P. S., & Netzly, D. H., (1993). Effect of apigeninidin on the growth of selected bacteria. J. Chem. Ecol., 19, 1021–1027. Tähtiharju, S., & Palva, T., (2002). Antisense inhibition of protein phosphatise 2C accelerates cold acclimation in Arabidopsis thaliana. Plant J., 26, 461–470. Takabayashi, J., Dickie, M., & Posthumus, M. A., (1994). Volatile herbivore-induced terpenoids in plant-mite interactions: Variation caused by biotic and abiotic factors. J. Chem. Ecol., 20, 1329–1354. Tamiru, A., Bruce, T. J. A., Richter, A., Woodcock, C. M., Midega, C. A. O., Degenhardt, J., Kelemu, S., et al., (2017). A maize landrace that emits defense volatiles in response

136

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

to herbivore eggs possess a strongly inducible terpene synthase gene. Ecol. Evol., 7, 2835–2845. Taylor, I. B., Linforth, R. S. T., Al-Naieb, R. J., Bowman, W. R., & Marples, B. A., (1988). The wilty tomato mutants flacca and sitiens are impaired in the oxidation of ABA-aldehyde to ABA. Plant Cell Environ., 11, 739–745. Taylor, I. B., Sonneveld, T., Bugg, T. D. H., & Thompson, A. J., (2005). Regulation and manipulation of the biosynthesis of abscisic acid, including the supply of xanthophyll precursors. J. Plant Growth Regul., 24, 253–273. Tian, S., Mao, X., Zhang, H., Chen, S., Zhai, C., Yang, S., & Jing, R., (2013). Cloning and characterization of TaSnRK2.3, a novel SnRK2 gene in common wheat. J. Exp. Bot., 64, 2063–2080. Trapp, S. C., & Croteau, R. B., (2001). Genomic organization of plant terpene synthases and molecular evolutionary implications. Genetics, 158, 811–832. Turlings, T. C., Tumlinson, J. H., & Lewis, W. J., (1990). Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science, 250, 1251–1253. Turlings, T. C., Tumlinson, J. H., Heath, R. R., Proveaux, A. T., & Doolittle, R. E., (1999). Isolation and identification of allelochemicals that attract the larval parasitoid, Cotesia marginiventris (Cresson), to the microhabitat of one of its hosts. J. Chem. Ecol., 17, 2235–2251. Vaughan, M. M., Christensen, S., Schmelz, E. A., Huffaker, A., Mcauslane, H. J., Alborn, H. T., Romero, M., et al., (2015). Accumulation of terpenoid phytoalexins in maize roots is associated with drought tolerance. Plant Cell Environ., 38, 2195–2207. Viswanathan, C., & Zhu, J. K., (2002). Molecular genetics analysis of cold-regulated gene transcription. Philos. Trans. R. Soc. B: Biol. Sci., 357, 877–886. Wegener, R., & Schulz, S., (2002). Identification and synthesis of homoterpenoids emitted from elm leaves after elicitation by beetle eggs. Tetrahedron, 58, 315–319. Weisner, J., & Jomaa, H., (2013). 1-Deoxy-d-xylulose 5-phosphate pathway. Encyclopedia of Malaria, 1–12. Whitehead, I., Atkinson, A., & Threlfall, D., (1990). Studies on the biosynthesis and metabolism of the phytoalexin lubimin and related compounds in Datura stramonium L. Planta, 182, 81–88. Wilkinson, S., & Davies, W. J., (2010). Drought, ozone, ABA and ethylene: New insights from cell to plant to community. Plant Cell Environ., 33, 510–525. Yadav, B., Jogawat, A., Rahman, M. S., & Narayan, O. M., (2021). Secondary metabolites in drought stress of crop plants: A review. Gene Rep., 23, 1–14. Yamaguchi-Shinozaki, K., & Shinozaki, K., (1993). Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Mol. Gen. Genet., 236, 331–340. Zulak, K. G., & Bohlmann, J., (2010). Terpenoid biosynthesis and specialized vascular cells of conifer defense. J. Integr. Plant Biol., 52, 86–97.

CHAPTER 5

Terpenoids in Plant Tolerance Against Different Environmental Stress ANWESHA CHATTERJEE and HARSHATA PAL*

Amity Institute of Biotechnology, Amity University, Major Arterial Road (South-East), Action Area II, Newtown, Kolkata – 700135, West Bengal, India *

Corresponding author. E-mail: [email protected]

ABSTRACT Plant secondary metabolites are types of organic molecules synthesized by plants that are not directly responsible for the overall growth and development of the plant but are required for their interaction with the environment. These organic molecules are produced in response to stress. Terpenes are possibly the largest as well as the most diverse class of secondary metabolites built up from isoprene units and are simple hydrocarbons, while terpenoids are modified forms of terpenes with oxygen-containing functional groups which are biologically active. Apart from the basic medical applications, diverse classes of terpenoids are responsible for chemical interaction and protection of the plant from abiotic and biotic stress conditions. Emerging tools and resources in the field of plant biotechnology have allowed researchers to study the terpenoid biosynthesis pathway and genes in order to develop strategies to control stress and build resiliency in plants. Results obtained by scientists while studying the effects of biotic and abiotic stress during terpenoid emission accumulate information regarding the sensitivity and interaction of terpenoids breaking new ground in the field of plant stress biology. In this chapter, we briefly describe the classification of terpenoids and broadly discuss their role in tolerance against various environmental Biology and Biotechnology of Environmental Stress Tolerance in Plants: Secondary Metabolites in Environmental Stress Tolerance, Volume 1. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

138

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

stresses, which will come up with the significance of terpenoids as a major class of plant secondary metabolite. 5.1 INTRODUCTION Plant cells undergo various metabolic pathways in order to produce chemical compounds known as secondary metabolites. They are potent regulators of proper growth and defense mechanism in plants. The plant secondary metabolites for stress tolerance are broadly classified into terpenoids, alkaloids, flavonoids, and phenolics. Terpenoids are the most diverse class and have significant functions in stress biology (Gershenzon & Dudareva, 2007). Terpenes are synthesized from isopentenyl pyrophosphate (IPP, a five-carbon isoprene unit) formed via mevalonic acid (MVA) pathway and its functional isomer dimethylallyl pyrophosphate (DMAPP) formed via methylerythritol 4-phosphate pathway. Subsequent condensation of IPP and DMAPP produces geranyl pyrophosphate (GPP), a 10-carbon compound forming the precursor of monoterpenes. A 5-carbon is added next to GPP to form farnesyl pyrophosphate (FPP), a 15-carbon compound which forms the precursor of sesquiterpenes (15 carbon). Subsequent addition of one carbon results to the formation of geranylgeranyl diphosphate (GGPP) as a precursor of diterpenes (20 carbon). Dimerization of FPP produce triterpenes (30 carbon) and dimerization of GGPP leads to the production of tetraterpenes (40 carbon) (Figure 5.1). Whereas polyterpenes are polymers consisting of a large number of isopentyl units. Terpenes are simple hydrocarbons whereas terpenoids are terpenes with oxygen moiety (Nagel et al., 2019). The major classes of terpenes and their properties are described in Table 5.1.

FIGURE 5.1  Outline of terpene biosynthesis.

Class Monoterpene

Isoprene Carbon Common Unit Atom Examples 2 10 •  α-pinene •  Limonene

Function in Plants

References

Prevents conifer species around the world from insects like bark beetle.

Adams et al. (2011)

•  Myrcene Sesquiterpene 3

15

•  Linalool •  Abscisic acid •  Nerolidol

Diterpene

4

20

•  Abietic acid •  Phorbol •  Gibberellin

Triterpene

6

30

•  Phytol •  Sterol •  Limnoid

Mazid et al. (2011); Abscisic acid helps in seed maintenance and also regulates Zhao et al. (2020) plant’s response to water stress, nerolidol regulates plant interaction during cold stress. Abietic acid releases resins which blocks the entry of feeding Mazid et al. (2011) insects, phorbol irritates skin of the predator thereby protecting the plant, gibberellin is a plant hormone responsible for plant growth and development and phytol takes part in photosynthesis. Acts as antiherbivore compounds by exerting various toxic effects by releasing chemical agents.

Mazid et al. (2011)

•  Azadirachtin Tetraterpene

8

40

•  Phytoecdysones •  Carotene Responsible for photosynthesis and also protects plants from Misawa (2010) solar oxidation of chlorophyll molecules. •  Xanthophyll

Polyterpene

>8

>40

•  Rubber

Terpenoids in Plant Tolerance Against Different Environmental Stress

TABLE 5.1  Classification of Terpenes

Possess wound healing property and provides defense against Mazid et al. (2011) herbivores. 139

140

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

The diversity of terpenes occurs by the action of terpene synthase enzymes and various precursors of terpene biosynthesis. Various chemical rearrangements including carbonation driven cyclization and elimination reactions in the precursor compounds give rise to numerous structurally distinct terpenes. Researchers also found the presence of multi-substrate terpene synthases in plants which control the terpene production depending on environmental fluctuations (Pazouki & Niinemetst, 2016; Christianson, 2017; Karunanithi & Zerbe, 2019). Scientists reported seven clades (a-h) that forms the plant terpene synthase family that evolved from triterpene synthase and prenyl transferase enzymes via gene duplication or rearrangement of various proteins which led to the formation of huge terpene synthase gene families where changes in an active site might have an effect on the terpene emission profile ultimately resulting in molecular evolution of the plant terpene synthase family (Muchlinski et al., 2019). 5.2 IDENTIFICATION AND CHARACTERIZATION OF TERPENE SYNTHASE GENES (TSGS) IN PLANTS Terpene synthases are responsible for the biosynthesis of various terpenes that are associated with plant growth and interaction. They act as gatekeepers and generates terpenoid diversity by undergoing a series of reactions resulting in the formation of a huge number of hydrocarbons. Enzymatic analysis showed seven clades or subclass of terpene synthase genes (TSGS) pointing out lineage – specific evolution of the genes belonging to families of variable size. They form the plant terpene synthase family originating from pre-existing triterpene synthase and prenyl transferase like enzymes via repeated gene duplication and other molecular events. A minor alteration in the active site of terpene synthase enzymes also leads to the production of chemically diverse terpenes in various plant species (Chen et al., 2011; Karunanithi & Zerbe, 2019). Limited information regarding the occurrence of TSGs has led the scientists to perform genome wide identification of TSGs. A scientific study revealed the characterization of Terpene synthases from spearmint and basil genome and along with other data, the scientists concluded that the terpene synthases might have originated from isoprenyl diphosphate synthase genes (Jiang et al., 2019). Scientists documented the assembly of TSGS and cytochrome P450 genes in eudicots and monocots, resulting in different patterns of new metabolic pathways (Boutanaev et al., 2015). Such metabolic gene

Terpenoids in Plant Tolerance Against Different Environmental Stress

141

clusters and gene duplication are involved in the evolution of plant secondary metabolite biosynthetic genes (Tohge & Fernie, 2020). Scientists identified a family of 44 monoterpene and sesquiterpene synthases while studying the emission of terpenes in switchgrass when emitting volatiles in order to protect themselves from stress and demonstrated overall response of terpene metabolism in switchgrass family (Muchlinski et al., 2019). In a different study, scientists identified new TSGS called MTPSLs (microbial terpene synthase-like genes) present in a wide variety of non-seed plants but not in seeded plant or green algae and are acquired by plants from microorganisms through horizontal gene transfer (Jia et al., 2018). Scientists also reported characterization and phylogenetic analysis of all known terpene synthases from Pinus species which helped the scientists to obtain the evolutionary history of the TSGS involved in terpenoid metabolism and specifically isolation of mono terpene synthases from Pinus nigra for the first time (Alicandri et al., 2020). About 69 putatively functional TSGS were annotated in grapevine and about 29 potentially functional TSGS were annotated in tomato which demonstrated the importance of terpene metabolism and biochemical functions of the TSGS that are responsible for bringing out the organoleptic properties in the said fruits (Martin et al., 2010; Falara et al., 2011). Scientists also characterized terpene profiles of cannabis and revealed different cannabis terpene synthase genes (CsTPS) with differential expressions responsible for the biosynthesis of monoterpenes and sesquiterpenes as well as their diversification (Booth et al., 2020). Scientists identified two cytochrome P450 monooxygenase genes CYP88D6 and CYP72A154 that takes part in the biosynthesis of glycyrrhizin, a triterpenoid. They also revealed that CYP72A63 of Medicago truncatula was able to catalyze the oxidation of triterpene b-amyrin, thereby revealing a genetic tool for the production of triterpenes (Seki et al., 2011). A similar study revealed that a multifunctional enzyme CYP76C1 catalyzes oxidation of linalool whose emission protects the plants from biotic stress (Boachon et al., 2015). Scientists identified and characterized eight terpene synthase genes (FhTPS) which are responsible for the release of volatile terpenes in two different cultivars of Freesia × hybrida and the obtained result can be utilized while modifying the genes responsible for introducing fragrance in flowers (Gao et al., 2018). Another study showed identification of three TSGS responsible for the biosynthesis of monoterpene geraniol from orchid genome of which DoGES1 was highly expressed. The findings paved the way for genetic modification of genes causing fragrance in different species of orchids (Zhao et al., 2020).

142

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

A recent study showed complete functional analysis of the terpene synthase family in tomato. The terpenes produced by the biochemical activities of TSGS are involved in the processes responsible for the growth and development of the plant and also other interactions giving insights towards genetic modifications (Zhou & Pichersky, 2020). Another recent study showed the evolution and diversity of terpene synthase clades in the Poaceae or grass family. It consists of five clades consisting of TSGS responsible for the biosynthesis of various terpenes via complex pathways in grass family crops like maize, wheat, rice, and sorghum (Luck et al., 2020). Terpenoids, although having a major role in plant growth, isoprenoids are dedicated to mediating defense against environmental stresses. When plants come in contact with an external pathogen like microorganisms, they cope up with a defense mechanism that includes structures like thorns, trichomes as well they release phytochemicals with antimicrobial properties. These phytochemicals are often called phytoalexins and are of low molecular weight (Singh & Sharma, 2015). The diverse classes of terpenoids, including mainly hemiterpenes, monoterpenes, sesquiterpenes as well as some diterpenes play a vital role in interacting with the environment. These terpenes are referred to as Volatile terpenes (VT) and are stored in specialized plant tissues like various secretory channels. The storage, emission, and overall functionality of these terpenes depend on their chemical properties as well as biotic and abiotic environmental factors. Scientists suggested that some terpenes undergo glycosylation when stored followed by hydrolysis upon exposure to stress and are finally released to the atmosphere (Yazaki et al., 2017). Therefore, it is strongly believed that terpene emission is directly associated with plant-pathogen or plant-animal interactions (Boncan et al., 2020). 5.3 ACTION OF TERPENES IN ABIOTIC STRESS Abiotic stresses like high salinity, high or low temperature, drought, UV radiations as well as heavy metal pollution are harmful for the growth and development of plants, ultimately resulting into reduction of crop yield around the world. However, most plants have generalized defense mechanism against abiotic stresses. Under stressful conditions, a network of signaling molecules like stress hormones, reactive oxygen species (ROS), and transcription factors come into play. Terpenoids, the diverse class of plant secondary

Terpenoids in Plant Tolerance Against Different Environmental Stress

143

metabolite play an important role in mitigating a variety of abiotic stress and ensure proper development of the plant. Scientists proposed that different classes of terpenoids interact with oxidants either inside the cell or on the outer leaf surface and also by causing alteration in ROS signaling (Vickers et al., 2009; Sewelam et al., 2016; Blande et al., 2014). Reports say that volatile terpenes along with phytohormones, takes part in the stress induced plant senescence. Deviation in the actual biosynthetic pathway induces volatile terpene accumulation which along with certain phytohormones causing plant senescence and abscission (Korankye et al., 2017). 5.3.1 DROUGHT ASSOCIATED TERPENES AND TERPENOIDS According to researchers, drought stress can influence terpenoid emission in plants cultivated in the nearby areas of the Mediterranean Sea. They followed the rates of monoterpene and sesquiterpene emission during a drought treatment in Citrus sinesis (orange fruit) and subsequently its recovery. The emitted terpenoids from orange consisted mainly of sesquiterpene beta-caryophyllene and monoterpene trans-P-ocimene under drought stress (Hansen & Seufert, 1999). In another study, scientists found that severe drought in two conifer species (Pinus sylvestris and Picea abies) increased the emission of monoterpenes and oleoresins which is a complex mixture of diverse class of terpenes and affected the growth of both the woods (Turtola et al., 2003). Much later to this report, scientists studied the pattern of terpenoid (Zealexins and kauralexins) accumulation in maize root in response to drought stress and also concluded that mutant AN2 (deficient in kauralexin) was more prone to be sensitive towards drought (Vaughan et al., 2015). Scientists revealed that under drought condition wine grape increased the emission of phenylpropanoids, monoterpenes, and tocopherols and potentially effected the plant as a result of transcriptional regulation of terpenoid genes (Savoi et al., 2016). Douglas fir, when under moderate drought conditions showed abundant terpenoid accumulation in the needles and when moderately stressed showed increased terpenoid emission in the roots forming a defense mechanism (Kleiber et al., 2017). A recent study on Thyme plant showed accumulation of volatile terpenoids predominantly α-phellandrene, O-cymene, γ-terpinene and β-caryophyllene during water deficit for a longer time period in sensitive and tolerant thyme cultivars which showed different patterns of stress-induced changes in various characters but ultimately the plant growth continued (Mahdavi et al., 2020).

144

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

5.3.2 SALINITY ASSOCIATED TERPENES AND TERPENOIDS A study on Artemisia annua revealed that the total content of monoterpenoids and sesquiterpenoids increased when exposed to sodium chloride (NaCl) salinity (Yadav et al., 2017). Emission of three terpenes (Z)-beta-ocimene, 2-carene and beta-phellandrene increased in a variety of tomato plant under salt stress (Tomescu et al., 2017). Major terpenoids, α-terpinyl acetate, 1,8-cineole and linalyl acetate increased in Salvia mirzayanii under excess salt stress while the scientists aimed to isolate and characterized cineole synthase 1 gene (SmCin1) involved in the biosynthesis of major terpenoids (Valifard et al., 2019). All these volatile emissions ensured the growth or survival of these plant under stress. 5.3.3 TEMPERATURE ASSOCIATED TERPENES AND TERPENOIDS Quercus ilex when exposed to a higher temperature, monoterpene emission increased providing membrane stability and protecting other cellular processes (Loreto et al., 1998). A study revealed that heat-priming in Achillea millefolium improved heat tolerance and enhanced terpenoid, benzenoid, and phenolics accumulation in the plant (Liu et al., 2020). According to another study, mutation in a particular gene that regulates isoprenoid synthesis in grapevine plant, led to a strong increase in monoterpene emission upon heat stress (Bertamini et al., 2019). Scientists found that silver birch and European aspen when exposed to increased nighttime temperature showed increased emission of several monoterpenes and sesquiterpenes, which improved tolerance (Ibrahim et al., 2010). 5.3.4 UV RADIATION ASSOCIATED TERPENES AND TERPENOIDS Grindelia chiloensis is a native plant of Patagonia (Argentina) where the atmosphere is exposed to solar UV irradiance. Scientists reported increased accumulation of resins in leaf and leaf thickens when exposed to UV radiation. Chemical and structural changes protect the plant from UV radiation (Zavala & Ravetta, 2002). Studies demonstrated that UV radiation increased terpene accumulation in cantaloupe tissues (Beaulieu, 2007). Scientists underwent solid-phase microextraction–gas chromatography-mass spectrometry (SPME–GC–MS) and revealed that when rice seedlings are exposed to UV-B radiation the concentration of terpenes increased and the mixture comprised

Terpenoids in Plant Tolerance Against Different Environmental Stress

145

of limonene, sabinene, myrcene, α-terpinene, β-ocimene, γ-terpinene, and α-terpinolene (Lee et al., 2015). Researchers conducted a study on Flourensia cernua to determine the concentrations of secondary metabolites when under stress. The volatile terpene concentration was higher in the plants exposed to UV rays than those of in shaded area (Estell et al., 2016). 5.3.5 HEAVY METAL ASSOCIATED TERPENES AND TERPENOIDS Scientists studied Ocimum basilicum and Mentha spicata under greenhouse conditions and were exposed to heavy metals like lead, copper, and cadmium (Cd). The gas chromatography-mass spectrometry (GC-MS) analysis revealed the enhancement of linalool and essential oils in case of Ocimum basilium whereas Mentha spicata showed no significant change in terpenoid concentrations (Kunwar et al., 2015). Tanacetum parthenium when exposed to heavy metals like cadmium and copper affected the terpene profile variation in order to form chemical defense under heavy metal stress (Hojati et al., 2017). 5.4 ACTION OF TERPENES IN BIOTIC STRESS Biotic stress is a major cause of crop destruction in agriculture. It is caused by living organisms like insects, bacteria, virus, fungi, nematodes, and other land animals that feed on plants. Plants respond to these stresses by means of defense mechanisms. Role of terpenes and terpenoids in plant defense against various pathogens is currently an important topic of research. Terpenes act as pathogen inhibitors in plant-living organism interaction and ensure protection. Terpenoids are considered as an extensively studied plant secondary metabolite in order to identify their role as insecticide, pesticide, antimicrobial, and weed control agents (Ninkuu et al., 2021). 5.4.1 TERPENES AS INSECTICIDES AND PESTICIDES Terpenes have the ability to act as deterrents to insects and pests. Although terpenoids are released as a mixture of volatile organic compounds, it is the particular proportion and blends of terpene to which herbivores are sensitive to (Sharma et al., 2017). The host plant produces terpenes in glandular trichomes or epidermis in order to trap insects and activates several mechanisms that can disrupt the lifecycle of the insects (Glas et al., 2012). Cyclopentanoid, a derivative of monoterpenoid cause degradation of protein

146

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

and nucleotides causing the insects to suffer nutrient deficit. It also hampers the proper regulation of biochemical pathways responsible for their growth and development (Park et al., 2010; War et al., 2018). A natural harmless monoterpene pyrethroids and methylcyclopentanoid showed insecticidal properties against moth, bees, wasps, ants, cockroaches, beetles, etc., and are used commercially as repellents (Lybrand et al., 2020). White-backed plant hopper attack was prevented by diterpene momilactone A in rice plant (Zhao et al., 2018). (E)-β-caryophyllene is produced in maize attracted enemies to fight herbivores like corn rootworm. β-1,3-glucan laminarin reduced the attack of tea green leaf hopper, a harmful pest for green tea (Chiriboga et al., 2017; Xin et al., 2019). A study showed that essential oils from cannabis were effective against aphids and mosquito larvae, tobacco cutworms, housefly as well as adult mosquitoes (Winnacker & Rieger, 2015). Diterpene rhizathalene released from the roots of Arabidopsis showed defense against root fungus gnat that feeds on the host plant (Vaughan et al., 2013). Eugenol, caryophyllene oxide, α-pinene, α-humulene, and α-phellandrene present in the essential oil from clove and cinnamon showed antiherbivore activity against adult grain weevil (Plata-Rueda et al., 2018). Overexpression of β-ocimene induced defense responses against potato aphid in tomato plants (Cascone et al., 2015). Combined effects of terpenes from volatile organic compounds elicited the attack of Ostrinia nubilais, a worldwide pest of maize (Solé et al., 2010). Scientists used neem oil, orange oil and essential oil from Chenopodium sp. as biopesticides and found them to be effective against two aphids Myzus persicae and Aphis gossypii on ornamental crops grown under greenhouse condition (Smith et al., 2018). Upon biotic stress condition, Mentha aquatica L. showed emission of (+)-menthofuran which acted as toxic agent to Chrysolina herbacea due to upregulation of menthofuran synthase gene (Zebelo et al., 2011). Combination of terpenes from volatile organic compounds released by host plant attracted and repelled Orseolia oryzivora, a major pest of rice in Africa (Ogah et al., 2017). Terpenes released from Eucalyptus grandis showed resistance against gall wasp that causes severe damage to the host plant (Naidoo et al., 2018). 5.4.2 TERPENES AS ANTIMICROBIAL AGENTS Phytoalexins are chemical agents released from a plant surface when it comes in contact with an external parasite and ultimately inhibits the growth

Terpenoids in Plant Tolerance Against Different Environmental Stress

147

of that parasite. Terpenes released as volatiles often act as phytoalexins and shows antimicrobial activity. There are plenty of literature supporting the role of terpenoids as phytoalexins that inhibits the growth of harmful bacteria, virus, and fungi (Mahizan et al., 2019). (E)-β-caryophyllene inhibited the growth of Pseudomonas on Solanaceae and Arabidopsis by activating defense pathways (Huang et al., 2012). Another sesquiterpene capsidiol inhibited virulence spread by different species of microorganisms in Nicotiana sp. (Song et al., 2019). Diterpenes like momilactone A and B, phytocassanes A to F, oryzalexin A to F and oryzalexin S played defense activities against various pathogens that are responsible for causing plant diseases. Several diterpenes are also responsible for inhibiting the growth of microorganisms causing bacterial leaf spot disease (Lu et al., 2018; Wang et al., 2018). Phytocassanes A-D, sclareol, and cis-abienol are reported to have antimicrobial properties and prevents plants from diseases (Umemura et al., 2003; Seo et al., 2012). Epoxydolabranol and zealexin released from the roots of maize plant inhibited the growth of pathogens (Mafu et al., 2018; Christensen et al., 2018; Huffaker et al., 2011). Phytoalexins, momilactones A and B, and phytocassanes A-E in rice plant induced defense mechanism that restricted the growth of blast fungus (Hasegawa et al., 2010). Monoterpenes α-thujene, α-pinene, sabinene, myrcene, α-terpene, and (S)-limonene, cyclosativene, α-copaene, and β-elemene as well as γ-Terpinene inhibited the infection of Xanthomonas that cause bacterial blight in rice (Lee et al., 2016; Yoshitomi et al., 2016). Scientists studied gene regulatory pathway of terpene synthesis and identified a sesquiterpene responsible for inhibiting the growth of fungi causing soybean rust (Parmezan et al., 2020). Sesquiterpene capsidiol 3-acetate acted against Potato virus in Nicotiana benthamiana (Li et al., 2015). Terpenoids were extracted from the fungal isolates from the fruits of Annona muricata and are reported to be effective against various types of bacteria (Abdel-Rahman et al., 2019). A study showed that R-limonene, S-limonene, myrcene, sabinene, α-pinene and β-elemene enhanced the activity of antibiotics ethambutol, isoniazid, and rifampicin against Mycobacterium tuberculosis (Sieniawska et al., 2017). Eugenol, terpineol, carveol, citronellol, and geraniol showed bactericidal effects against diverse class of pathogens (Guimarães et al., 2019). Terpenoids such as α-pinene, limonene, myrcene, geraniol, linalool, nerol, and terpineol were reported to have antibacterial properties functional against various food borne pathogens opening avenues for studying natural compounds for use in the field of food biotechnology (Wang et al., 2019).

148

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

5.4.3 TERPENES AS WEEDICIDES Allelopathic activity in plants is a common method to survive alone, eradicating all the possibilities for weeds to grow. The plants release allelochemicals that are toxic in nature and negatively effects the other plants growing nearby by hindering cell division and other molecular signaling mechanisms which saves the plants from water or nutrient deficit that directly effects their growth and development (Scognamiglio et al., 2013). Scientists have reported the allelopathic activity of various terpenes that acts as controls the growth of unwanted neighboring plants. Studies showed that monoterpenes like citronellal, linalool, and cineole restrained weed germination. Other studies also revealed that monoterpenes also inhibited seed sprouting, radical elongation, cell proliferation and DNA synthesis (Chon & Nelson, 2010; De Martino et al., 2010; Abd-Elgawad et al., 2021). Several reports support that apart from monoterpenes, various sesquiterpenes and diterpenes also acts as phytotoxic agents against unwanted plants. Roots of Pinus halepensis released caryophyllene which inhibited the growth of weeds (Santonja et al., 2019). Diterpene momilactone A and momilactone B from the roots of rice plant inhibited the growth of Lepidium sativum, Cyperus difformis L, Leptochloa chinenesis, Amaranthus retroflexus, Cyperus difform, mustard, varieties of cabbage and lettuce, wild grasses like Echinochloa colonum and Phleum pratense and also Arabidopsis by affecting germination and various signaling pathways responsible for proper DNA synthesis (Toyomasu et al., 2014; Xu et al., 2012; Kato-Noguchi et al., 2013; Kato-Noguchi et al., 2012; Kato Noguchi & Ota, 2013; Mirmostafaee et al., 2020). Momilactones A, B, and E from rice husk showed inhibitory effects on various invasive weeds (Quan et al., 2019). 5.5 OTHER USES OF TERPENES Apart from the role of different classes of terpenes in stress tolerance, there are some other important functions of terpene that are discussed below. 5.5.1 TERPENES AS POLLINATOR ATTRACTANTS Floral scents are generally responsible for pollinator visitation in plants to carry out reproduction. Several terpenoids released during floral patterning in the form of volatiles are responsible for odor that attracts the pollinators. It is

Terpenoids in Plant Tolerance Against Different Environmental Stress

149

reported that the quality and quantity of monoterpenes linalool, limonene, and β-pinene at different floral stages of fig plant enhanced the attractiveness of the plant that certainly invited pollinator Ceratosolen solmsi marchali (Chen & Song, 2008). Monoterpenes D-limonene, β-myrcene and E-β-ocimene have been reported to be emitted as floral volatiles in two different species of Mimulus that attracts bumblebee and hummingbird as pollinators with their natural scent (Byers et al., 2014). 5.5.2 MEDICINAL AND THERAPEUTIC USES OF TERPENES Apart from its role in growth, development, and stress tolerance, terpenes are natural compound of huge medicinal importance. One of the most widely studied sources of terpene with medicinal properties is Cannabis. It contains properties like anticancer, anti-inflammatory, antimicrobial, and other therapeutic characters (Cox-Georgian et al., 2019). Some of the recent discoveries on the medicinal properties of some common terpenes are shown in Table 5.2. TABLE 5.2  Recent Studies on the Therapeutic Potential of Plant Terpenes Terpene Pinene Caryophyllene Paclitaxel Limonene Thymoquinone Andrographolide Hyperforin

Source Pine trees Murrya koenigii Yew trees Pinecones Black cumin Andrographis paniculata Hypericum perforatum Valeriana wallichii

Combined terpene extracts – Combined monoterpene extracts

Function Antimalarial Antimalarial Anticancer Anticancer Anticancer Antidiabetic

References Boyom et al. (2011) Kamaraj et al. (2017) Efferth et al. (2008) Palareti et al. (2016) Majdalawieh et al. (2017) Brahmachari (2017)

Antidepressant

Jang et al. (2008)

Antidepressant

Jang et al. (2008); Pliego Zamora et al. (2016) Pliego Zamora et al. (2016)

Antiviral

5.6 METABOLIC ENGINEERING OF TERPENOIDS IN PLANTS Plant stresses, both biotic and abiotic causes loss in crop production worldwide. Scientists are working in this field to prevent the loss that would increase food production and serve the ever-growing human population.

150

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

They are identifying the cause as well as investigating various processes in order to overcome the challenge of food scarcity. Genetic engineering came into play to maintain the growth and survival of plants under stressful conditions. Phytohormones and plant secondary metabolites are proven to be important targets for metabolic engineering in order to produce stress tolerant plants (Wani et al., 2016). 5.6.1 TERPENOIDS FORMING DEFENSE AGAINST HERBIVORES Terpenoid synthesis in plants is regulated by terpene synthase (TPS) which plays a major role in plant response to stress. Scientists have targeted various TPS genes and applied modifications that resulted in novel varieties of plants that are tolerant towards various stresses. An example of such modification includes transformation of Petunia plant with TPS (S-limonene synthase) gene from Clarika breweri that increased the production of linalool that formed natural repellent for aphids (Lücker et al., 2001). Modification of FaNES1 (Fragaria ananassa Nerolidol Synthase 1) gene of strawberry and its expression in potato catalyzed the formation of S-linalool thereby increasing its level (Aharoni et al., 2006). It was also seen that FaNES1 in mitochondria of transgenic Arabidopsis lead higher sesquiterpene nerolidol production rather than FaNES1 in plastid (Aharoni et al., 2003). 4,8-dimethyl-1,3(E),7-nonatriene is a homoterpene derivative of nerolidol that also contributed in trapping insects (Bouwmeester et al., 1999). Another successful work involved overexpression of Terpene synthase 10 gene in Arabidopsis, thereby increasing the quantity of sesquiterpenes similar to that of the volatile organic compounds from maize accountable for defending themselves against herbivores. These transgenic Arabidopsis release odors that attract female Cotesia marginiventris, which locates the attackers, thereby mediating defense against herbivore attack in the plant (Schnee et al., 2006). 5.6.2 TERPENOIDS IMPROVING FRUIT FLAVOR AND AROMA Scientists were also able to identify and silence various biosynthetic genes in order to produce scented compounds (Abbas et al., 2017). Overexpression of linalool synthase gene in tomato fruit was the first successful experiment in improving fruit flavor and aroma (Lewinsohn et al., 2001; Abbas et al., 2017).

Terpenoids in Plant Tolerance Against Different Environmental Stress

151

5.6.3 MONOTERPENE METABOLISM IN TRANSGENIC PLANTS Scientists also created transgenic Dianthus caryophyllus (Carnation) by expressing linalool synthase gene from Clarkia breweri which resulted in the production of monoterpene linalool and linalool oxide which is not a character of wild type Carnation plant (Lavy et al., 2002). A study also revealed transformation of transgenic tobacco by Limonene-3-hydroxylase isolated from mint that produced three lemon monoterpene synthase genes producing (+)-limonene, γ-terpinene and (–)-β-pinene which finally emitted (+)-transisopiperitenol and further modification of this compound produced terpenes like 1,3,8-p-menthatriene, 1,5,8-p-menthatriene, p-cymene, and isopiperitenone (Lücker et al., 2004). Similarly in another study, Mentha arvensis and Mentha piperita were transformed with neomycin phosphotransferase gene and a 4S-limonene synthase from Mentha spicata where modification of monoterpene levels was observed (Diemer et al., 2001). 5.6.4 TERPENOIDS INVITING POLLINATORS Terpenes attracts a huge number of pollinators. Scientists showed that genetically modified (GM) eggplant with cry3Bb contained high levels of terpenes like (+)-limonene, Z-jasmone, p-cymene, α-pinene, and (–)-limonene, and explained increased arrival of pollinator bumblebee (Bombus terrestris) (Arpaia et al., 2011). 5.6.5 TERPENOIDS AS BIOHERBICIDES A study revealed terpenoids that attract herbivores can also function as bioherbicide agents that control weed growth in agricultural fields. Scientists found out that Altica cyanea females are attracted by elevated emissions of terpenoids like α-pinene, linalool oxide, geraniol, and phytol from damaged Ludwigia octovalvis (Jacq.) Raven (Onagraceae), a rice-field weed (Mitra et al., 2017). Recently scientists from nanotechnology background are using encapsulated terpenoids to trap insects. A recent example is entrapping Bemisia tabaci by geraniol encapsulated in chitosan/gum Arabic nanoparticles (De Oliveira et al., 2018). The detailed study on the role of terpenoids as bioherbicides or antiherbivore is already discussed.

152

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

5.6.6 PHARMACEUTICAL TERPENOID PRODUCTION Terpenoids are natural products that have curative effects on diseases like cancer, cardiovascular disease, malaria, Alzheimer’s disease. Agrobacterium mediated transformation methods are used in biosynthesis of pharmaceutical terpenoids by overexpression of terpenoid synthase genes as well as suppression of other pathways (Lu et al., 2016). Other studies showed sesquiterpene lactone, artemisinin released from Artemisia annua L. is an important anti-malarial drug and are effective against other viral and parasitic diseases (Weathers et al., 2011). Scientists showed that Artemisinin production can be increased with the help of Jasmonic acid (JA) responsive AP2 family transcription factors (Yu et al., 2012) (Figure 5.2).

FIGURE 5.2  Outline of plant – terpene interaction.

5.7 CONCLUSION Plants have the ability to survive and reproduce naturally in the environment fighting against all odds. The plant secondary metabolites act as their major weapon to protect themselves from enemies. Terpenes are the largest group of secondary metabolites released from the surface of the plants in order to alleviate stressful situations. Plant terpenes are drawing the attention of a huge number of botanists for understanding the patterns of interaction and applying them in the field of biotechnology. The beneficial role of terpenes in biotic and abiotic stresses and a very little or no hazardous properties has allowed the scientists to move forward with the study of ecological

Terpenoids in Plant Tolerance Against Different Environmental Stress

153

resilience. Scientists are also emphasizing on the diverse biological functions of terpenoids leading to the production of quality products that directly benefit mankind. Despite having numerous scientific data, understanding the patterns associated with communication of plant and environment is still ambiguous in nature. This chapter includes a critical review of terpene and its functions that would be advantageous for the investigators as it would help them to gain a superficial knowledge regarding the subject before diving into the depths of their research. KEYWORDS • • • • • • •

abiotic stress biotic stress geranyl pyrophosphate isoprene secondary metabolites terpenes terpenoids

REFERENCES Abbas, F., Ke, Y., Yu, R., Yue, Y., Amanullah, S., Jahangir, M. M., & Fan, Y., (2017). Volatile terpenoids: Multiple functions, biosynthesis, modulation and manipulation by genetic engineering. Planta, 246(5), 803–816. Abd-Elgawad, A. M., El Gendy, A. E. N. G., Assaeed, A. M., Al-Rowaily, S. L., Alharthi, A. S., Mohamed, T. A., Nassar, M. I., et al., (2021). Phytotoxic effects of plant essential oils: A systematic review and structure-activity relationship based on chemometric analyses. Plants, 10(1), 1–16. Abdel-Rahman, T., Hussein, A. S., Beshir, S., Hamed, A. R., Ali, E., & El-Tanany, S. S., (2019). Antimicrobial activity of terpenoids extracted from Annona muricata seeds and its endophytic Aspergillus Niger strain SH3 either singly or in combination. Open Access Maced. J. Med. Sci., 7(19), 3127–3131. Adams, A. S., Boone, C. K., Bohlmann, J., & Raffa, K. F., (2011). Responses of bark beetleassociated bacteria to host monoterpenes and their relationship to insect life histories. J. Chem. Ecol., 37(8), 808–817. Aharoni, A., Giri, A. P., Deuerlein, S., Griepink, F., De Kogel, W. J., Verstappen, F. W. A., Verhoeven, H. A., et al., (2003). Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell, 15(12), 2866–2884.

154

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Aharoni, A., Jongsma, M. A., Kim, T. Y., Ri, M. B., Giri, A. P., Verstappen, F. W. A., Schwab, W., & Bouwmeester, H. J., (2006). Metabolic engineering of terpenoid biosynthesis in plants. Phytochem Rev., 5(1), 49–58. Alicandri, E., Paolacci, A. R., Osadolor, S., Sorgonà, A., Badiani, M., & Ciaffi, M., (2020). On the evolution and functional diversity of terpene synthases in the Pinus species: A review. J. Mol. Evol., 88(3). Springer US. Arpaia, S., De Cristofaro, A., Guerrieri, E., Bossi, S., Cellini, F., Leo, G. M. D., Germinara, G. S., et al., (2011). Foraging activity of bumblebees (Bombus terrestris L.) on Bt-expressing eggplants. Arthropod-Plant Interact., 5(3), 255–261. Beaulieu, J. C., (2007). Effect of UV irradiation on cut cantaloupe: Terpenoids and esters. J. Food Sci., 72(4), 272–281. Bertamini, M., Grando, M. S., Zocca, P., Pedrotti, M., Lorenzi, S., & Cappellin, L., (2019). Linking monoterpenes and abiotic stress resistance in grapevines. BIO Web of Conferences, 13, 01003. Blande, J. D., Holopainen, J. K., & Niinemets, Ü., (2014). Plant volatiles in polluted atmospheres: Stress responses and signal degradation. Plant Cell Environ., 37(8), 1892–1904. Boachon, B., Junker, R. R., Miesch, L., Bassard, J. E., Höfer, R., Caillieaudeaux, R., Seidel, D. E., et al., (2015). CYP76C1 (cytochrome P450)-mediated linalool metabolism and the formation of volatile and soluble linalool oxides in Arabidopsis flowers: A strategy for defense against floral antagonists. Plant Cell, 27(10), 2972–2990. Boncan, D. A. T., Tsang, S. S. K., Li, C., Lee, I. H. T., Lam, H. M., Chan, T. F., & Hui, J. H. L., (2020). Terpenes and terpenoids in plants: Interactions with environment and insects. Int. J. Mol. Sci., 21(19), 1–19. Booth, J. K., Yuen, M. M. S., Jancsik, S., Madilao, L. L., Page, J. E., & Bohlmann, J., (2020). Terpene synthases and terpene variation in Cannabis sativa. Plant Physiol., 184(1), 130–147. Boutanaev, A. M., Moses, T., Zi, J., Nelson, D. R., Mugford, S. T., Peters, R. J., & Osbourn, A., (2015). Investigation of terpene diversification across multiple sequenced plant genomes. Proceedings of the National Academy of Sciences of the United States of America, 112(1), E81–E88. Bouwmeester, H. J., Verstappen, F. W. A., Posthumus, M. A., & Dicke, M., (1999). Spider mite-induced (3S)-(E)-nerolidol synthase activity in cucumber and lima bean. The first dedicated step in acyclic C11-homoterpene biosynthesis. Plant Physiol., 121(1), 173–180. Boyom, F. F., Ngouana, V., Kemgne, E. A. M., Zollo, P. H. A., Menut, C., Bessiere, J. M., Gut, J., & Rosenthal, P. J., (2011). Antiplasmodial volatile extracts from Cleistopholis patens Engler & Diels and Uvariastrum pierreanum Engl. (Engl. & Diels) (Annonaceae) growing in Cameroon. Parasitol. Res., 108(5), 1211–1217. Brahmachari, G., (2017). Andrographolide: A molecule of antidiabetic promise. Discovery and Development of Antidiabetic Agents from Natural Products: Natural Product Drug Discovery, 1, 1–27. Byers, K. J. R. P., Bradshaw, H. D., & Riffell, J. A., (2014). Three floral volatiles contribute to differential pollinator attraction in monkeyflowers (Mimulus). J. Exp. Biol., 217(4), 614–623. Cascone, P., Iodice, L., Maffei, M. E., Bossi, S., Arimura, G. I., & Guerrieri, E., (2015). Tobacco overexpressing β-ocimene induces direct and indirect responses against aphids in receiver tomato plants. J. Plant Physiol., 173, 28–32.

Terpenoids in Plant Tolerance Against Different Environmental Stress

155

Chen, C., & Song, Q., (2008). Responses of the pollinating wasp Ceratosolen solmsi marchali to odor variation between two floral stages of Ficus hispida. J. Chem. Ecol., 34(12), 1536–1544. Chen, F., Tholl, D., Bohlmann, J., & Pichersky, E., (2011). The family of terpene synthases in plants: A mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant Journal, 66(1), 212–229. Chiriboga, M. X., Campos-Herrera, R., Jaffuel, G., Röder, G., & Turlings, T. C. J., (2017). Diffusion of the maize root signal (E)-β-caryophyllene in soils of different textures and the effects on the migration of the entomopathogenic nematode Heterorhabditis megidis. Rhizosphere, 3, 53–59. Chon, S. U., & Nelson, C. J., (2010). Allelopathy in Compositae plants. A review. Agron. Sustain Dev., 30(2), 349–358. Christensen, S. A., Huffaker, A., Sims, J., Hunter, C. T., Block, A., Vaughan, M. M., Willett, D., et al., (2018). Fungal and herbivore elicitation of the novel maize sesquiterpenoid, zealexin A4, is attenuated by elevated CO2. Planta, 247(4), 863–873. Christianson, D. W., (2017). Structural and chemical biology of terpenoid cyclases. Chem. Rev., 117(17), 11570–11648. Cox-Georgian, D., Ramadoss, N., Dona, C., & Basu, C., (2019). Therapeutic and medicinal uses of terpenes. Medicinal Plants: From Farm to Pharmacy, 333–359. De Martino, L., Mancini, E., De Almeida, L. F. R., & De Feo, V., (2010). The anti-germinative activity of twenty-seven monoterpenes. Molecules, 15(9), 6630–6637. De Oliveira, J. L., Campos, E. V. R., Pereira, A. E. S., Nunes, L. E. S., Da Silva, C. C. L., Pasquoto, T., Lima, R., et al., (2018). Geraniol encapsulated in chitosan/gum Arabic nanoparticles: A promising system for pest management in sustainable agriculture. J. Agric. Food Chem., 66(21), 5325–5334. Diemer, F., Caissard, J. C., Moja, S., Chalchat, J. C., & Jullien, F., (2001). Altered monoterpene composition in transgenic mint following the introduction of 4S-limonene synthase. Plant Physiol. Biochem., 39(7, 8), 603–614. Efferth, T., Kahl, S., Paulus, K., Adams, M., Rauh, R., Boechzelt, H., Hao, X., Kaina, B., & Bauer, R., (2008). Phytochemistry and pharmacogenomics of natural products derived from traditional Chinese medicine and Chinese Materia medica with activity against tumor cells. Mol. Cancer Ther., 7(1), 152–161. Estell, R. E., Fredrickson, E. L., & James, D. K., (2016). Effect of light intensity and wavelength on concentration of plant secondary metabolites in the leaves of Flourensia cernua. Biochem. Syst. Ecol., 65, 108–114. Falara, V., Akhtar, T. A., Nguyen, T. T. H., Spyropoulou, E. A., Bleeker, P. M., Schauvinhold, I., Matsuba, Y., et al., (2011). The tomato terpene synthase gene family. Plant Physiol., 157(2), 770–789. Gao, F., Liu, B., Li, M., Gao, X., Fang, Q., Liu, C., Ding, H., Wang, L., & Gao, X., (2018). Identification and characterization of terpene synthase genes accounting for volatile terpene emissions in flowers of Freesia × hybrida. J. Exp. Bot., 69(18), 4249–4265. Gershenzon, J., & Dudareva, N., (2007). The function of terpene natural products in the natural world. Nat. Chem. Biol., 3(7), 408–414. Glas, J. J., Schimmel, B. C. J., Alba, J. M., Escobar-Bravo, R., Schuurink, R. C., & Kant, M. R., (2012). Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. Int. J. Mol. Sci., 13(12), 17077–17103.

156

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Guimarães, A. C., Meireles, L. M., Lemos, M. F., Guimarães, M. C. C., Endringer, D. C., Fronza, M., & Scherer, R., (2019). Antibacterial activity of terpenes and terpenoids present in essential oils. Molecules, 24(13), 1–12. Hansen, U., & Seufert, G., (1999). Terpenoid emission from Citrus sinensis (L.) OSBECK under drought stress. Phys. Chem. Earth, Part B: Hydrology, Oceans and Atmosphere, 24(6), 681–687. Hasegawa, M., Seo, I. M. S., Lmai, T., Koga, J., Okada, K., Yamane, H., & Ohashi, Y., (2010). Phytoalexin accumulation in the interaction between rice and the blast fungus. Mol. Plant Microbe Interact., 23(8), 1000–1011. Hojati, M., Modarres-Sanavy, S. A. M., Enferadi, S. T., Majdi, M., Ghanati, F., Farzadfar, S., & Pazoki, A., (2017). Cadmium and copper-induced changes in growth, oxidative metabolism and terpenoids of Tanacetum parthenium. Environ. Sci. Pollut. Res., 24(13), 12261–12272. Huang, M., Sanchez-Moreiras, A. M., Abel, C., Sohrabi, R., Lee, S., Gershenzon, J., & Tholl, D., (2012). The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen. New Phytol., 193(4), 997–1008. Huffaker, A., Kaplan, F., Vaughan, M. M., Dafoe, N. J., Ni, X., Rocca, J. R., Alborn, H. T., et al., (2011). Novel acidic sesquiterpenoids constitute a dominant class of pathogen-induced phytoalexins in maize. Plant Physiol., 156(4), 2082–2097. Ibrahim, M. A., Mäenpää, M., Hassinen, V., Kontunen-Soppela, S., Malec, L., Rousi, M., Pietikäinen, L., et al., (2010). Elevation of night-time temperature increases terpenoid emissions from Betula pendula and Populus tremula. J. Exp. Bot., 61(6), 1583–1595. Jang, M. H., Piao, X. L., Kim, J. M., Kwon, S. W., & Park, J. H., (2008). Inhibition of cholinesterase and amyloid-beta aggregation by resveratrol oligomers from Vitis amurensis. Phytother Res., 22(4), 544–549. Jia, Q., Köllner, T. G., Gershenzon, J., & Chen, F., (2018). MTPSLs: New terpene synthases in nonseed plants. Trends Plant Sci., 23(2), 121–128. Jiang, S. Y., Jin, J., Sarojam, R., & Ramachandran, S., (2019). A comprehensive survey on the terpene synthase gene family provides new insight into its evolutionary patterns. Genome Biol. Evol., 11(8), 2078–2098. Kamaraj, C., Balasubramani, G., Siva, C., Raja, M., Balasubramanian, V., Raja, R. K., Tamilselvan, S., et al., (2017). Ag nanoparticles synthesized using β-caryophyllene isolated from Murraya koenigii: Antimalarial (Plasmodium falciparum 3D7) and anticancer activity (A549 and HeLa cell lines). J. Clust. Sci., 28(3), 1667–1684. Karunanithi, P. S., & Zerbe, P., (2019). Terpene synthases as metabolic gatekeepers in the evolution of plant terpenoid chemical diversity. Front. Plant Sci., 10, 1–23. Kato, N. H., & Ota, K., (2013). Biological activities of rice allelochemicals momilactone A and B. J. Rice Res., 1(2), 1–5. Kato-Noguchi, H., Ota, K., & Kujime, H., (2012). Absorption of momilactone A and B by Arabidopsis thaliana L. and the growth inhibitory effects. J. Plant Physiol., 169(15), 1471–1476. Kato-Noguchi, H., Ota, K., Kujime, H., & Ogawa, M., (2013). Effects of momilactone on the protein expression in Arabidopsis germination. Weed Biol. Manag., 13(1), 19–23. Kleiber, A., Duan, Q., Jansen, K., Junker, L. V., Kammerer, B., Rennenberg, H., Ensminger, I., et al., (2017). Drought effects on root and needle terpenoid content of a coastal and an interior Douglas fir provenance. Tree Physiol., 37(12), 1648–1658.

Terpenoids in Plant Tolerance Against Different Environmental Stress

157

Korankye, E. A., Lada, R., Asiedu, S., & Caldwell, C., (2017). Plant senescence: The role of volatile terpene compounds (VTCs). Am. J. Plant Sci., 08(12), 3120–3139. Kunwar, G., Pande, C., Tewari, G., Singh, C., & Kharkwal, G. C., (2015). Effect of heavy metals on terpenoid composition of Ocimum basilicum L. and Mentha spicata L. J. Essent. Oil-Bear. Plants, 18(4), 818–825. Lavy, M., Zuker, A., Lewinsohn, E., Larkov, O., Ravid, U., Vainstein, A., & Weiss, D., (2002). Linalool and linalool oxide production in transgenic carnation flowers expressing the Clarkia breweri linalool synthase gene. Mol. Breed., 9(2), 103–111. Lee, G. W., Chung, M. S., Kang, M., Chung, B. Y., & Lee, S., (2016). Direct suppression of a rice bacterial blight (Xanthomonas oryzae pv. oryzae) by monoterpene (S)-limonene. Protoplasma, 253(3), 683–690. Lee, G. W., Lee, S., Chung, M. S., Jeong, Y. S., & Chung, B. Y., (2015). Rice terpene synthase 20 (OsTPS20) plays an important role in producing terpene volatiles in response to abiotic stresses. Protoplasma, 252(4), 997–1007. Lewinsohn, E., Schalechet, F., Wilkinson, J., Matsui, K., Tadmor, Y., Nam, K. H., Amar, O., et al., (2001). Enhanced levels of the aroma and flavor compound S-linalool by metabolic engineering of the terpenoid pathway in tomato fruits. Plant Physiol., 127(3), 1256–1265. Li, R., Tee, C. S., Jiang, Y. L., Jiang, X. Y., Venkatesh, P. N., Sarojam, R., & Ye, J., (2015). A terpenoid phytoalexin plays a role in basal defense of Nicotiana benthamiana against Potato virus X. Sci. Rep., 5, 1–6. Liu, B., Zhang, L., Rusalepp, L., Kaurilind, E., Sulaiman, H. Y., Püssa, T., & Niinemets, Ü., (2020). Heat priming improved heat tolerance of photosynthesis, enhanced terpenoid and benzenoid emission and phenolics accumulation in Achillea millefolium. Plant Cell Environ., 44, 2365–2385. Loreto, F., Förster, A., Dürr, M., Csiky, O., & Seufert, G., (1998). On the monoterpene emission under heat stress and on the increased thermotolerance of leaves of Quercus ilex L. fumigated with selected monoterpenes. Plant Cell Environ., 21(1), 101–107. Lu, X., Tang, K., & Li, P., (2016). Plant metabolic engineering strategies for the production of pharmaceutical terpenoids. Front. Plant Sci., 7, 1–11. Lu, X., Zhang, J., Brown, B., Li, R., Rodríguez-Romero, J., Berasategui, A., Liu, B., et al., (2018). Inferring roles in defense from metabolic allocation of rice diterpenoids. Plant Cell, 30(5), 1119–1131. Luck, K., Chen, X., Norris, A. M., Chen, F., Gershenzon, J., & Köllner, T. G., (2020). The reconstruction and biochemical characterization of ancestral genes furnish insights into the evolution of terpene synthase function in the Poaceae. Plant Mol. Biol., 104(1, 2), 203–215. Lücker, J., Bouwmeester, H. J., Schwab, W., Blaas, J., Van, D. P. L. H. W., & Verhoeven, H. A., (2001). Expression of clarkia s-linalool synthase in transgenic petunia plants results in the accumulation of s-linalyl-β-d-glucopyranoside. Plant J., 27(4), 315–324. Lücker, J., Schwab, W., Franssen, M. C. R., Van, D. P. L. H. W., Bouwmeester, H. J., & Verhoeven, H. A., (2004). Metabolic engineering of monoterpene biosynthesis: Two-step production of (+)-trans-isopiperitenol by tobacco. Plant J., 39(1), 135–145. Lybrand, D. B., Xu, H., Last, R. L., & Pichersky, E., (2020). How plants synthesize pyrethrins: Safe and biodegradable insecticides. Trends Plant Sci., 25(12), 1240–1251. Mafu, S., Ding, Y., Murphy, K. M., Yaacoobi, O., Addison, J. B., Wang, Q., Shen, Z., et al., (2018). Discovery, biosynthesis and stress-related accumulation of dolabradiene-derived defenses in maize. Plant Physiol., 176(4), 2677–2690.

158

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Mahdavi, A., Moradi, P., & Mastinu, A., (2020). Variation in terpene profiles of Thymus vulgaris in water deficit stress response. Molecules, 25(5), 1–19. Mahizan, N. A., Yang, S., Moo, C. L., Song, A. A. L., Chong, C. M., Chong, C. W., Abushelaibi, A., et al., (2019). Terpene derivatives as a potential agent against antimicrobial resistance (AMR) pathogens. Molecules, 24(2631), 1–21. Majdalawieh, A. F., Fayyad, M. W., & Nasrallah, G. K., (2017). Anti-cancer properties and mechanisms of action of thymoquinone, the major active ingredient of Nigella sativa. Crit. Rev. Food Sci. Nutr., 57(18), 3911–3928. Martin, D. M., Aubourg, S., Schouwey, M. B., Daviet, L., Schalk, M., Toub, O., Lund, S. T., & Bohlmann, J., (2010). Functional annotation, genome organization and phylogeny of the grapevine (Vitis vinifera) terpene synthase gene family based on genome assembly, FLcDNA cloning, and enzyme assays. BMC Plant Biol., 10(226). Mazid, M., Khan, T. A., & Mohammad, F., (2011). Role of secondary metabolites in defense mechanisms of plants. Biology and Medicine, 3(2), 232–249. Mirmostafaee, S., Azizi, M., & Fujii, Y., (2020). Study of allelopathic interaction of essential oils from medicinal and aromatic plants on seed germination and seedling growth of lettuce. Agronomy, 10(2). Misawa, N., (2010). Carotenoids, 1(20), 733–752. Elsevier. Mitra, S., Karmakar, A., Mukherjee, A., & Barik, A., (2017). The role of leaf volatiles of Ludwigia octovalvis (Jacq.) raven in the attraction of Altica cyanea (weber) (Coleoptera: Chrysomelidae). J. Chem. Ecol., 43(7), 679–692. Muchlinski, A., Chen, X., Lovell, J. T., Köllner, T. G., Pelot, K. A., Zerbe, P., Ruggiero, M., et al., (2019). Biosynthesis and emission of stress-induced volatile terpenes in roots and leaves of switchgrass (Panicum virgatum L.). Front. Plant Sci., 10, 1–16. Nagel, R., Schmidt, A., & Peters, R. J., (2019). Isoprenyl diphosphate synthases: The chain length determining step in terpene biosynthesis. Planta, 249(1), 9–20. Naidoo, S., Christie, N., Acosta, J. J., Mphahlele, M. M., Payn, K. G., Myburg, A. A., & Külheim, C., (2018). Terpenes associated with resistance against the gall wasp, Leptocybe invasa, in Eucalyptus grandis. Plant Cell Environ., 41(8), 1840–1851. Ninkuu, V., Zhang, L., Yan, J., Fu, Z., Yang, T., & Zeng, H., (2021). Biochemistry of terpenes and recent advances in plant protection. Int. J. Mol. Sci., 22(11). Ogah, E. O., Smart, L. E., Woodcock, C. M., Caulfield, J. C., Birkett, M. A., Pickett, J. A., Nwilene, F. E., & Bruce, T. J., (2017). Electrophysiological and behavioral responses of female African rice gall midge, Orseolia oryzivora Harris and Gagné, to host plant volatiles. J. Chem. Ecol., 43(1), 13–16. Palareti, G., Legnani, C., Cosmi, B., Antonucci, E., Erba, N., Poli, D., Testa, S., & Tosetto, A., (2016). Comparison between different D-dimer cutoff values to assess the individual risk of recurrent venous thromboembolism: Analysis of results obtained in the DULCIS study. Clin Lab Haematol., 38(1), 42–49. Park, K. S., Kim, B. H., & Chang, I. M., (2010). Inhibitory potencies of several iridoids on cyclooxygenase-1, cyclooxygenase-2 enzymes activities, tumor necrosis factor-α and nitric oxide production in vitro. Evid. Based Complementary Altern. Med., 7(1), 41–45. Parmezan, T. R., Júnior, S. L. B., De Carvalho, K., De Aquino, M., Birkett, M., Pickett, J., De Oliveira, N. E., et al., (2020). Transcriptional profile of genes involved in the production of terpenes and glyceollins in response to biotic stresses in soybean. Genet. Mol. Biol., 43(4), 1–12.

Terpenoids in Plant Tolerance Against Different Environmental Stress

159

Pazouki, L., & Niinemetst, U., (2016). Multi-substrate terpene synthases: Their occurrence and physiological significance. Front. Plant Sci., 7, 1–16. Plata-Rueda, A., Campos, J. M., Da Silva, R. G., Martínez, L. C., Dos, S. M. H., Fernandes, F. L., Serrão, J. E., & Zanuncio, J. C., (2018). Terpenoid constituents of cinnamon and clove essential oils cause toxic effects and behavior repellency response on granary weevil, Sitophilus granarius. Ecotoxicol. Environ. Saf., 156, 263–270. Pliego, Z. A., Edmonds, J. H., Reynolds, M. J., Khromykh, A. A., & Ralph, S. J., (2016). The in vitro and in vivo antiviral properties of combined monoterpene alcohols against West Nile virus infection. Virology, 495, 18–32. Santonja, M., Bousquet-Mélou, A., Greff, S., Ormeño, E., & Fernandez, C., (2019). Allelopathic effects of volatile organic compounds released from Pinus halepensis needles and roots. Ecol. Evol., 9(14), 8201–8213. Savoi, S., Wong, D. C. J., Arapitsas, P., Miculan, M., Bucchetti, B., Peterlunger, E., Fait, A., et al., (2016). Transcriptome and metabolite profiling reveals that prolonged drought modulates the phenylpropanoid and terpenoid pathway in white grapes (Vitis vinifera L.). BMC Plant Biol., 16(1), 1–17. Schnee, C., Köllner, T. G., Held, M., Turlings, T. C. J., Gershenzon, J., & Degenhardt, J., (2006). The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proceedings of the National Academy of Sciences of the United States of America, 103(4), 1129–1134. Scognamiglio, M., D’Abrosca, B., Esposito, A., Pacifico, S., Monaco, P., & Fiorentino, A., (2013). Plant growth inhibitors: Allelopathic role or phytotoxic effects? Focus on Mediterranean biomes. Phytochem. Rev., 12(4), 803–830. Seki, H., Sawai, S., Ohyama, K., Mizutani, M., Ohnishi, T., Sudo, H., Fukushima, E. O., et al., (2011). Triterpene functional genomics in licorice for identification of CYP72A154 involved in the biosynthesis of glycyrrhizin. Plant Cell, 23(11), 4112–4123. Seo, S., Gomi, K., Kaku, H., Abe, H., Seto, H., Nakatsu, S., Neya, M., et al., (2012). Identification of natural diterpenes that inhibit bacterial wilt disease in tobacco, tomato and Arabidopsis. Plant Cell Physiol., 53(8), 1432–1444. Sewelam, N., Kazan, K., & Schenk, P. M., (2016). Global plant stress signaling: Reactive oxygen species at the crossroad. Front. Plant Sci., 1–21. Sharma, E., Anand, G., & Kapoor, R., (2017). Terpenoids in plant and arbuscular mycorrhizareinforced defense against herbivorous insects. Ann. Bot., 119(5), 791–801. Sieniawska, E., Swatko-Ossor, M., Sawicki, R., Skalicka-Woźniak, K., & Ginalska, G., (2017). Natural terpenes influence the activity of antibiotics against isolated Mycobacterium tuberculosis. Med Princ Pract., 26(2), 108–112. Singh, B., & Sharma, R. A., (2015). Plant terpenes: Defense responses, phylogenetic analysis, regulation and clinical applications. 3 Biotech, 5(2), 129–151. Smith, G. H., Roberts, J. M., & Pope, T. W., (2018). Terpene based biopesticides as potential alternatives to synthetic insecticides for control of aphid pests on protected ornamentals. Crop Prot., 110, 125–130. Solé, J., Sans, A., Riba, M., & Guerrero, A., (2010). Behavioral and electrophysiological responses of the European corn borer Ostrinia nubilalis to host-plant volatiles and related chemicals. Physiol. Entomol., 35(4), 354–363. Song, N., Lan, M., Wang, W., Sun, H., Wang, L., Baldwin, I. T., & Wu, J., (2019). An ERF2like transcription factor regulates production of the defense sesquiterpene capsidiol upon Alternaria alternata infection. J. Gerontol. A Biol. Sci. Med. Sci., 1–11.

160

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Tohge, T., & Fernie, A. R., (2020). Co-regulation of clustered and neo-functionalized genes in plant-specialized metabolism. Plants, 9(5), 1–11. Tomescu, D., Şumǎlan, R., Copolovici, L., & Copolovici, D., (2017). The influence of soil salinity on volatile organic compounds emission and photosynthetic parameters of Solanum lycopersicum L. varieties. Open Life Sci., 12(1), 135–142. Toyomasu, T., Usui, M., Sugawara, C., Otomo, K., Hirose, Y., Miyao, A., Hirochika, H., et al., (2014). Reverse-genetic approach to verify physiological roles of rice phytoalexins: Characterization of a knockdown mutant of OsCPS4 phytoalexin biosynthetic gene in rice. Physiol. Plant., 150(1), 55–62. Turtola, S., Manninen, A. M., Rikala, R., & Kainulainen, P., (2003). Drought stress alters the concentration of wood terpenoids in Scots pine and Norway spruce seedlings. J. Chem. Ecol., 29(9), 1981–1995. Umemura, K., Ogawa, N., Shimura, M., Koga, J., Usami, H., & Kono, T., (2003). Possible role of phytocassane, rice phytoalexin, in disease resistance of rice against the blast fungus Magnaporthe grisea. Biosci. Biotechnol. Biochem., 67(4), 899–902. Valifard, M., Mohsenzadeh, S., Kholdebarin, B., Rowshan, V., Niazi, A., & Moghadam, A., (2019). Effect of salt stress on terpenoid biosynthesis in Salvia mirzayanii: From gene to metabolite. J. Hortic. Sci. Biotechnol., 94(3), 389–399. Van, Q. N., Xuan, T. D., Tran, H. D., & Dieu, T. N. T., (2019). Inhibitory activities of momilactones A, B, E, and 7-Ketostigmasterol isolated from rice husk on paddy and invasive weeds. Plants, 8(6). Vaughan, M. M., Christensen, S., Schmelz, E. A., Huffaker, A., Mcauslane, H. J., Alborn, H. T., Romero, M., et al., (2015). Accumulation of terpenoid phytoalexins in maize roots is associated with drought tolerance. Plant Cell Environ., 38(11), 2195–2207. Vaughan, M. M., Wang, Q., Webster, F. X., Kiemle, D., Hong, Y. J., Tantillo, D. J., Coates, R. M., et al., (2013). Formation of the unusual semivolatile diterpene rhizathalene by the Arabidopsis class I terpene synthase TPS08 in the root stele is involved in defense against belowground herbivory. Plant Cell, 25(3), 1108–1125. Vickers, C. E., Gershenzon, J., Lerdau, M. T., & Loreto, F., (2009). A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat. Chem. Biol., 5(5), 283–291. Wang, C. Y., Chen, Y. W., & Hou, C. Y., (2019). Antioxidant and antibacterial activity of seven predominant terpenoids. Int. J. Food Prop., 22(1), 230–238. Wang, W., Li, Y., Dang, P., Zhao, S., Lai, D., & Zhou, L., (2018). Rice secondary metabolites: Structures, roles, biosynthesis, and metabolic regulation. Molecules, 23(12). Wani, S. H., Kumar, V., Shriram, V., & Sah, S. K., (2016). Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J., 4(3), 162–176. War, A. R., Taggar, G. K., Hussain, B., Taggar, M. S., Nair, R. M., & Sharma, H. C., (2018). Special issue: Using non-model systems to explore plant-pollinator and plant-herbivore interactions: Plant defense against herbivory and insect adaptations. AoB Plants, 10(4), 1–19. Weathers, P. J., Arsenault, P. R., Covello, P. S., McMickle, A., Teoh, K. H., & Reed, D. W., (2011). Artemisinin production in Artemisia annua: Studies in planta and results of a novel delivery method for treating malaria and other neglected diseases. Phytochem Rev., 10(2), 173–183. Winnacker, M., & Rieger, B., (2015). Recent progress in sustainable polymers obtained from cyclic terpenes: Synthesis, properties, and application potential. ChemSusChem, 8(15), 2455–2471.

Terpenoids in Plant Tolerance Against Different Environmental Stress

161

Xin, Z., Cai, X., Chen, S., Luo, Z., Bian, L., Li, Z., Ge, L., & Chen, Z., (2019). A disease resistance elicitor laminarin enhances tea defense against a piercing herbivore Empoasca (Matsumurasca) onukii matsuda. Sci. Rep., 9(1), 1–13. Xu, M., Galhano, R., Wiemann, P., Bueno, E., Tiernan, M., Wu, W., Chung, I. M., et al., (2012). Genetic evidence for natural product-mediated plant-plant allelopathy in rice (Oryza sativa). New Phytol., 193(3), 570–575. Yadav, R. K., Sangwan, R. S., Srivastava, A. K., & Sangwan, N. S., (2017). Prolonged exposure to salt stress affects specialized metabolites-artemisinin and essential oil accumulation in Artemisia annua L.: Metabolic acclimation in preferential favor of enhanced terpenoid accumulation accompanying vegetative to reproductive phase transition. Protoplasma, 254(1), 505–522. Yazaki, K., Arimura, G. I., & Ohnishi, T., (2017). “Hidden” terpenoids in plants: Their biosynthesis, localization and ecological roles. Plant Cell Physiol., 58(10), 1615–1621. Yoshitomi, K., Taniguchi, S., Tanaka, K., Uji, Y., Akimitsu, K., & Gomi, K., (2016). Rice terpene synthase 24 (OsTPS24) encodes a jasmonate-responsive monoterpene synthase that produces an antibacterial γ-terpinene against rice pathogen. J. Plant Physiol., 191, 120–126. Yu, Z. X., Li, J. X., Yang, C. Q., Hu, W. L., Wang, L. J., & Chen, X. Y., (2012). The jasmonateresponsive AP2/ERF transcription factors AaERF1 and AaERF2 positively regulate artemisinin biosynthesis in Artemisia annua L. Mol. Plant., 5(2), 353–365. Zavala, J. A., & Ravetta, D. A., (2002). The effect of solar UV-B radiation on terpenes and biomass production in Grindelia chiloensis (Asteraceae), a woody perennial of Patagonia, Argentina. Plant Ecol., 161(2), 185–191. Zebelo, S., Bertea, C. M., Bossi, S., Occhipinti, A., Gnavi, G., & Maffei, M. E., (2011). Chrysolina herbacea modulates terpenoid biosynthesis of Mentha aquatica L. PLoS One, 6(3). Zhao, C., Yu, Z., Teixeira Da, S. J. A., He, C., Wang, H., Si, C., Zhang, M., et al., (2020). Functional characterization of a Dendrobium officinale geraniol synthase doGES1 involved in floral scent formation. Int. J. Mol. Sci., 21(19), 1–15. Zhao, M., Cheng, J., Guo, B., Duan, J., & Che, C. T., (2018). Momilactone and related diterpenoids as potential agricultural chemicals. J. Agric. Food Chem., 66(30), 7859–7872. Zhao, M., Zhang, N., Gao, T., Jin, J., Jing, T., Wang, J., Wu, Y., et al., (2020). Sesquiterpene glucosylation mediated by glucosyltransferase UGT91Q2 is involved in the modulation of cold stress tolerance in tea plants. New Phytol., 226(2), 362–372. Zhou, F., & Pichersky, E., (2020). The complete functional characterization of the terpene synthase family in tomato. New Phytol., 226(5), 1341–1360.

CHAPTER 6

Role of Anthocyanin in Plants to Survive Against Environmental Stresses

SUPRAVA NATH,1 SUBHASHISA PRAHARAJ,2 SAGAR MAITRA,2* AKBAR HOSSAIN,3 TANMOY SHANKAR,2 BISWAJIT PRAMANICK,4 MAHUA BANERJEE,5 BISHAL MUKHERJEE,6 DINKAR JAGANNATH GAIKWAD,2 MASINA SAIRAM,2 and RAJESH SHRIRAM KALASARE2

University of Agricultural Sciences, Bangalore – 560065, Karnataka, India

1

Centurion University of Technology and Management, Odisha – 761211, India

2

Bangladesh Wheat and Maize Research Institute, Dinajpur – 5200, Bangladesh

3

Dr. Rajendra Prasad Central Agricultural University, Pusa, Samastipur, Bihar – 848125, India

4

Palli Siksha Bhavana, Visva-Bharati, Sriniketan – 731204, West Bengal, India

5

Bidhan Chandra Krishi Viswavidyalaya, Mohanpur – 741252, West Bengal, India

6

*

Corresponding author. E-mail: [email protected]

ABSTRACT Abiotic and biotic stresses are major limiting factors in crop production. To minimize the impact of stress, plants adapt many mechanisms. Anthocyanin pigments have been found to play an important role in both biotic and abiotic Biology and Biotechnology of Environmental Stress Tolerance in Plants: Secondary Metabolites in Environmental Stress Tolerance, Volume 1. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

164

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

stress tolerance. In addition to their role to impart color to the vegetative tissues and fruits, it also improves plants tolerance against different stresses. The color imparted by anthocyanin helps plants in attracting pollinators, thus helps in fertilization. It also helps in further seed dispersal. The role of anthocyanin as photo protectant is worth noting. Anthocyanin also helps reduce the negative impact of different stresses because of their antioxidant activity. In addition to stress tolerance, anthocyanin pigments have also been found to improve human health. Considering all these benefits, anthocyanin pigments can be included as an important train in different breeding program that targets stress tolerance and nutraceutical benefits. 6.1 INTRODUCTION Anthocyanins are a group of flavonoids consisting of a large number of secondary metabolites (Liu et al., 2018). These glycosylated polyphenolic compounds are found in multiple colors, such as red, orange, purple, etc. (Tanaka & Ohmiya, 2008). Anthocyanin pigments have multiple roles in plants that include attracting pollinators, protection against biotic and abiotic stresses, etc. (Liu et al., 2018; Moustaka et al., 2020; Chalker-Scott, 1999). In addition to their role in imparting attractive colors, it has also been found to show beneficial health impact (Lila, 2004; Ghosh & Konishi, 2007; Pojer et al., 2013). The commonly found anthocyanins in plants are derivatives of pelargonidin, cyanidin, delphinidin, peonidin, petunidin, and malvidin (Liu et al., 2018). The anthocyanin content in plants depends on the amount of anthocyanin produced and the amount that is degraded. Considering the fact that, anthocyanin has an important role in imparting stress tolerance they can offer great promise in adaptation to climate change. Changing climate has increased the risk of abiotic stress incidents. Abiotic stress, such as flooding, heat stress, drought stress, etc., causes a huge loss in crop production. Anthocyanins have been found to improve tolerance against stresses, most notably against drought stress and high light stress (Li et al., 2017; Hughes et al., 2010; Trojak et al., 2017). The stress tolerance ability imparted by anthocyanin is mostly due to its antioxidant activity. The antioxidant activity largely depends on the extent of B-ring hydroxylation. Hydroxylation of B-ring enhances antioxidant activity (Liu et al., 2018). Anthocyanin also acts as a photo-protectant and protects the photosynthetic apparatus of plants against excessive light (Steyn et al., 2002; Gould et al., 2018; Merzlyak & Chivkunova, 2000). Accumulation of

Role of Anthocyanin in Plants to Survive Against Environmental Stresses

165

anthocyanin in young tissues has been reported to be a protective mechanism against photoinhibition and photobleaching (Liu et al., 2018). In addition to the role of anthocyanin in abiotic stress tolerance, anthocyanin has also been found to provide biotic stress tolerance (Liu et al., 2018). The color imparted by anthocyanin pigments has been found to reduce pest attacks in crops like tobacco, tomato, etc. These benefits provided by anthocyanin should be considered while selecting traits in a breeding program for biotic stress tolerance. The Important roles of anthocyanin are presented in Figure 6.1. Apart from stress tolerance, one important property of anthocyanin worth noting is its beneficial role in human health. Anthocyanins have many beneficial roles with respect to human health. Anthocyanin may reduce many chronic diseases (Liu et al., 2018). For example, a type of anthocyanin found in solanaceous vegetables called delphinidin derivatives have a role in reducing vascular inflammation and reduce thrombosis (Watson & Schonlau, 2015). Similarly, inhibition of many forms of cancer has been reported due to anthocyanin (Liu et al., 2018). Considering all the benefits of anthocyanin in plants as well as human health, it must be studied in detail and extensively. In this chapter, an attempt has been made to discuss the role of anthocyanin in plants tolerance to environmental stresses.

FIGURE 6.1  Important roles of anthocyanin.

166

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

6.2 STRUCTURE The chemical structure of anthocyanin plays a dominant role in determining their potential activities. Owing to specific chemical structures, anthocyanins are one electron deficient, which makes them extremely reactive towards reactive oxygen species (ROS) thus, considered as naturally present antioxidants. Various anthocyanin structures have been reported from a diverse group of plant species (De pascual et al., 2008). From the point of chemical configuration, anthocyanins are glycosides of anthocyanidins (Herborne & Smith, 1972). Anthocyanidins are common plant pigments, the sugar-free counterparts of anthocyanin molecules and are based on a single basic core structure, the flavylium ion with various groups substituted for its hydrogen atoms. More than 600 different types of anthocyanins are present, which is due to variation in the basic anthocyanidin skeleton and variation in substitution sites of anthocyanidin molecules for different subsidiary groups. Aurantinidin, cyaniding, delphinidin, europinidin, malvidin, peonidin, petunidin, and rosinidin are various types of anthocyanidins that constitute anthocyanin. The anthocyanins basic chromophore is the 7-hydroxyflavylium ion which is naturally present and usually has hydroxyl substituents at positions 3 and 5 which are glycosylated constantly and occasionally respectively, and the B-ring or 2-phenyl has single or additional methoxy or hydroxy substituent (Bridle & Timberlake, 1997). Naturally present anthocyanins in which the methoxy group substitutes the 7-hydroxy groups are uncommon. Commonly, a large number of anthocyanins occurs which differ primarily in the alternative pattern in the B-ring and the sugar nature and other additional molecules that make up the glycosylated segment (Andersen & Markham, 2005). Both naturally occurring and artificial anthocyanins vary in colors from yellow to purple and this variation depends upon so many factors such as the type of substituents present in the B-ring, the pH, the state of accumulation of the anthocyanins and complex formation in presence of metal cations (Kamiloglu et al., 2015). The chemical composition of anthocyanins are glycosides and anthocyanidins, acylglycosides, and the aglycones flavyliums (2-phenylbenzopyrilium) varied in the diverse methoxyl (–OCH3) and hydroxyl (–OH) replacement in the central arrangement. The flavylium ion, center of the anthocyanidin molecule, has the C6-C3-C6 flavonoid structure, surrounded by three different rings such as A ring (Fused aromatic ring), B ring (phenyl component) and C ring (heterocyclic benzopyran ring) (Bridle & Timberlake, 1997). The structure of the anthocyanin has been presented in Figure 6.2.

Role of Anthocyanin in Plants to Survive Against Environmental Stresses

167

FIGURE 6.2  Structure of anthocyanin.

Based on the chemical composition, anthocyanin is classified into two broad groups; one is a flavonoid (concerned to isoflavone/ flavone, C15H10O2) and another one is phenolics (phenol, C6H5OH) (Wink, 1999). Anthocyanins are glycosides of polyhydroxy and polyhydroxy derived of 2-phenylbenzopyrilium or flavylium salts (Jiang et al., 2021). Among various anthocyanidins, major six anthocyanidins upon methylation produce most of the anthocyanin and 90% of the anthocyanins are produced from three methylated anthocyanidins such as malvidin, peonidin, and petunidin (Mazza & Francis, 1995). In detail, flavonoids are secondary metabolites belonging to the phenylpropanoids class. These flavonoids impart color change in varieties of flowers, fruits, seeds, and leaves.

6.3 FUNCTIONS Anthocyanins are ubiquitous in plant kingdoms especially in seeded plants and are stored in vacuoles. Major phenolic substances, e.g., pro-anthocyanidins and flavonols are produced in fruits at the time of commencement of fruit development and these substances produce anthocyanins at the time of fruit ripening (Jaakola, 2013). Betalains, the derivative of tyrosine, are a subgroup of flavonoids, a class of phenolics secondary metabolites

168

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

present extensively in a wide range of plant species and involved in various developmental functions (Tanaka et al., 2008). Anthocyanins being a rich source of carotenoids, flavonoids, and nutraceutical compounds, play an important role in balanced nutrition and aid in fitness (Oki et al., 2016). Anthocyanins are light in color and highly soluble in water and for these properties, used for coloring of various fruits and vegetables as a replacement of synthetic color (Wrolstad, 2004). These are water soluble pigments present in flowers and fruits of many plant species and act as attractants for insects and animals for pollination and seed dispersal (Lo Piero et al., 2005). Anthocyanin pigments scavenge free radicle molecules thus acting as natural antioxidant and also protect the plant from various pathogens, attract the pollinators for pollination and protect the plant cells against various abiotic and biotic stresses such as protection from UV (ultraviolet) radiation, heat stress, cold stress, water stress and pathogenic microbes (Rasmussen et al., 2005). In plants, the crucial function of anthocyanin pigments is to protect the cell membrane and tissues from various ROS such as O2–, OH–, H2O2, which are produced in electron transport chain (ETC) and damage membrane configuration and alter cell metabolism. Short wave ultraviolet-B radiation is harmful for the plants as it inhibits various physiological processes such as photosynthesis, transport of nutrient and water and it has been found anthocyanins play an important role in protection of plants against this harmful radiation (Oancea & Oprean, 2011). Phenolic component of anthocyanins is dependable for antioxidant actions, i.e., capacity to search various ROS such as singlet oxygen, superoxide, peroxide, hydroxyl radical and hydrogen peroxide (H2O2) and for this reason these pigments have been regarded as strong inhibitors and novel antioxidants to lipid peroxidation as compared to other antioxidants (Kurutas, 2016). Phenolics also have various important functions in plants such as nutrient uptake, activation of enzymes, photosynthesis, and synthesis of protein. Phenolics production is enhanced under various stresses thus considered as indicator of stress. In flowers, color imparted by the anthocyanin pigment helps to attract pollinators for pollination while in fruits, coloration helps in seed dispersal by attracting various herbivorous animals. Anthocyanins protect the plant from extreme high as well as low temperatures by countering ROSs. In tomato plants, anthocyanins help to lower the cell death in leaves, thus protecting the plant (Oki et al., 2016).

Role of Anthocyanin in Plants to Survive Against Environmental Stresses

169

Anthocyanins protect the plant from incoming harmful ultraviolet radiation by getting accumulated in the epidermal cell layer of leaves and stems and absorbing light in the UV region and allowing photosynthetically active radiation to pass throughout uninterrupted. In this way, the plant maintains its normal growth and development unaffected by UV-B radiation. 6.4 ROLE OF ANTHOCYANIN IN STRESS TOLERANCE Under open conditions, growing plants are susceptible to a wide range of biotic and abiotic stresses. Biotic stresses are those stresses caused by living organisms which include various harmful microorganisms such as bacteria, fungi, viruses, and nematodes. Abiotic stresses include soil moisture stress, salinity, heat stress, cold stress, drought stress and deficiency or toxicity of nutrients, etc. Under these environmental stresses, plants are triggered to produce various secondary metabolites, which help the plant to overcome the stress period. Anthocyanin pigment is a such secondary metabolite that is produced in response to stress and protects the plant. Anthocyanin pigments have been found to provide tolerance against different stresses, mostly due to their anti-oxidative activity. 6.4.1 DROUGHT STRESS Moisture stress otherwise known as drought stress is one of the crucial abiotic stresses that significantly affect agricultural crop productivity. Drought stress affects normal plant growth and development through several processes, such as causing morphological changes (reduced leaf expansion, increased depth of roots), oxidative stress (production of ROS such as O2–, OH–, H2O2 in ETC which damages membrane configuration and alters cell metabolism) and closure of stomata which reduces CO2 entry into the plants thus reducing net photosynthesis (Farooq et al., 2017). Germination and emergence are hampered due to drought stress as it negatively impacts the hydrolysis of seed reserves and also by reducing the plumule length (Sedghi et al., 2013). Under water stress conditions, there is ABA synthesis in the roots which acts as a signaling system that the shoot receives and stomata get closed (Bhargava Sawant, 2013). As a result of which CO2 entry into the leaves is restricted, this reduces the amount of photosynthates to be produced. Other reasons for the reduced rate of photosynthesis under drought stress is due to reduced chlorophyll content in leaves, leaf expansion, the number of

170

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

leaves produced and disintegration of membrane structures (Keyvan, 2010). Both cell division and cell elongation are affected under moisture deficit as there is a failure of maintenance of turgidity of the cells. Cell division takes place when the cell attains a particular size and due to loss of turgor under drought stress, that particular size is not achieved. Soil supplied nutrients can be taken up by the plants only when sufficient soil water allows mass flow and diffusion of nutrients to the roots. Along with this soil water affects the solubility of the nutrients which is necessary for the nutrient uptake. As moisture stress hinders these processes, it also affects the nutrient uptake and movement by the plants making them hungry along with thirsty. In leguminous crops, water stress reduces the biological nitrogen fixation by reducing the activity of Rhizobium sp. and content of leg hemoglobin. Under water stress conditions, synthesis of plant growth promoting hormones, e.g., auxin, gibberellin, and cytokinin is reduced, whereas growth retarding hormones, e.g., ABA and ethylene are synthesized inside the plant in more quantity. In plants, significant alterations in major physiological and biochemical processes occurs due to decreased growth and development which is induced by drought (Aimar et al., 2011). In response to drought stress, various secondary metabolites are produced in the plants to evade from the injurious effect of drought. Various medicinal plants, e.g., Catharanthus roseus (Madagascar periwinkle), Hypericum perforatum (Perforate St John’s-wort) and Artemisia annua (Sweet wormwood) reported to increase the accumulation of secondary metabolites in response to moisture stress (Azhar et al., 2011). Significant reduction in photosynthates production along with the consequent increase in secondary metabolites accumulation such as hypericin, hyperforin, and pseudohypericin have been reported in drought induced Hypericum perforatum (Zobayed et al., 2007). Along with enhanced production of secondary metabolites, moisture stress resulted in improving the quality of important secondary metabolites such as artemisinin in Artemisia annua and quercetin, betulinic acid and rutin in Hypericum brasiliense (Goatweed). Phenols are a group of secondary metabolites which are also a part of anthocyanins that help the plant to overcome drought stress mainly by two processes such as pigmentation and providing defense against injurious ROS. Almost all tissues adapt this mechanism to evade drought stress. However, in the tissues such as juvenile leaves where synthesis of these secondary metabolites is not possible as a line of defense, solute concentration in the vacuole is increased (Curtis et al., 1996). As a result of which leaf osmotic

Role of Anthocyanin in Plants to Survive Against Environmental Stresses

171

potential decreases letting the plant to maintain its turgidity under reduced water potential conditions during drought stress. Anthocyanins are pigments having a crucial role in protecting the plants under moisture stress. Accumulation of anthocyanin is associated with the production of varieties of osmolytes which act as antioxidants and protect the plant from various ROS (Sperdouli & Moustakas, 2012). Light screening activity of these pigments that is the elimination of UV-B radiation without hindrance in absorption in visible radiation also acts as a kind of antioxidant. Anthocyanins have the properties to reduce the excitation pressure of the photons coming from the sun thus they modify the light quantity as well as quality perceived by the plant canopy under stress conditions (Landi et al., 2015). Considering this modulation property of anthocyanin pigments, it has been reported that these pigments could be the potential driver for the shift from growth mode metabolism to resilience mode metabolism (Steyn et al., 2002). As a result of which there is changes in morphological, physiological, and biochemical processes occurring inside the plants which help the plant to overcome drought stress where competition among the plants is very high and resources particularly water is limited. Under moisture stress, there is over-accumulation of anthocyanin in the leaves which is associated with a remarkable metabolic shift in terms of non-structural carbohydrates and amino acids (Cirillo et al., 2021). Starch reserves which were already present in plants are diverted to provide carbon molecules for the synthesis of secondary metabolites, which play a major role in osmotic adjustments. This results in reducing cell water potential and helps in leaf expansion under stress conditions. Thus, anthocyanins are regarded as the novel physiological inducers of resilience and adaptation owing to their light screening properties when the plant is subjected to drought stress. So many instances are there where the accumulation of anthocyanin help to overcome drought stress. ‘Pretty purple’ variety of pepper provides more resistance against moisture stress compared to green cultivars (Bahler et al., 1991). With increased levels of anthocyanins, ornamental plants such as Photinia and Cotius are more resistant to drought stress (Knox, 1989). Anthocyanin accumulation in Populus shoots is associated with drought tolerance (Wettstein-Westersheim & Minelli, 1962). Resurrection plants accumulate three to four times more anthocyanins and show enhanced tolerance to moisture stress (Sherwin & Farrant, 1998). Leaves of Rhododendron, Viburnum, and Mahonia which contain anthocyanin are more drought-tolerant due to

172

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

maintenance of lower water content than that of their green counterparts (Kaku et al., 1992). 6.4.2 HIGH LIGHT STRESS Each plant has a specific light absorption capacity by its photosynthetic apparatus and exposure of the plants to the light intensity above the light saturation point is regarded as high light stress. It is that excess part of light beyond that utilized by the plant for photosynthesis. When the ratio of photon flux density (PFD) to the rate of photosynthesis is high, it results in high light stress and this ratio increases either due to reduced photosynthesis or increased photon flux density. Photo-inhibition is the inhibition in the activity of Photo systemII (PS-II) due to high irradiance and this occurs due to an imbalance between the rate of photodamage to PS-II and the rate of repair of those damaged PS-II. Under high light intensity, the production of ROS increases, which inactivates PS-II. During this process, oxygen concentration increases, and CO2 concentration decreases as a result of which electron from the reduced ferredoxin molecule is transferred to the molecular oxygen, which results in the production of reactive superoxide anions. Production of these reactive superoxide anions leads to photo-oxidative damage to photosynthetic apparatus, lipid peroxidation of thylakoid membranes of chloroplast and photooxidation of proteins. Along with this, increased light intensity is associated with high temperature (HT) which results in increased transpirational loss of water and loss of turgidity of plant cells. With the closure of stomata, there is less uptake of CO2 from the atmosphere which leads to a reduced rate of photosynthesis. Respiration continues with reduced photosynthesis leading to lesser availability of photosynthesis or carbohydrates for plant growth and development. As light is the driving force for photosynthesis, photoinhibition due to high light intensity is unavoidable. However, photoinhibition is reduced to some extent by various photoprotective processes such as strategic leaf and chloroplast movements, detoxification of reactive ROS by various antioxidants, non-radiative dissipation of absorbed excitation energy, utilization of excess incident light by a set of alternative electron acceptors and repairing mechanism to prevent photodamages. Under antioxidant activities to detoxify reactive ROS, both enzymatic, as well as non-enzymatic antioxidant system, operates in the plants. Various enzymes such as catalase (CAT), superoxide dismutase (SOD), peroxidase, and ascorbate, etc., comes under the enzymatic antioxidant system.

Role of Anthocyanin in Plants to Survive Against Environmental Stresses

173

The non-enzymatic antioxidant system includes ascorbic acid, β-carotene, α-tocopherol and glutathione, etc. (Allen & Tresini, 2000; Foyer et al., 1994). In addition, anthocyanins also act as antioxidants to scavenge ROS under photo-oxidative stress (Duthie & Crozier, 2000; Gould et al., 2002). When plants are exposed to high light stress, enhanced accumulation of anthocyanin pigment is reported (Chalker-Scott, 1999). Anthocyanin protects the plant from high light stress mainly by two mechanisms. In the first mechanism, these pigments act as a shield to protect the chloroplast from excess absorbed light energy by absorbing green light themselves and reducing the excitation energy of photons. Anthocyanin pigments accumulated in the epidermis layer of vacuoles of maize (Zea mays L.) plant is reported to absorb nearly 43% of incident solar radiation (Pietrini & Massacci, 1998). Secondly, these anthocyanins which belong to polyphenols serve as antioxidants due to specific chemical structures and protect the plant from excess light stress by detoxifying the ROS produced during the photooxidation process. The antioxidant capacity of various types of anthocyanin is measured using the automated oxygen radical absorbance. Following this procedure, it has been reported that the antioxidant capacity of cyaniding-3-glucoside (one type of anthocyanin) to scavenge singlet oxygen was 3.5 times more than α-tocopherol (Wang et al., 1997). Anthocyanin extracted from purple sweet potato and used in tobacco resulted in providing protection against ROS and subsequent damage to photosynthetic apparatus. 6.4.3 SALT STRESS Anthocyanins have also been found to provide salt stress tolerance (Chutipaijit et al., 2011; Kim et al., 2017). The high content of anthocyanin and proline have been found to improve salt stress tolerance in Indica rice (Chutipaijit et al., 2011). Salt tolerance in Brassica napus due to high anthocyanin accumulation has also been reported (Kim et al., 2017). Anthocyanin content varies with salt stress in many plant species (Chunthaburee et al., 2016) which can serve as an indicator of salt stress. Increased accumulation of anthocyanin has been found to improve plant growth under low nitrate and high salt stress conditions due to active nitrate metabolism modulation (Truong et al., 2018). The antioxidative role of anthocyanin may also reduce the negative impact of high salt stress.

174

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

6.4.4 HEAVY METAL STRESS Like many other stresses, anthocyanin has also been found to provide tolerance against heavy metal stress. Anthocyanin has been found to protect wheat seedlings against cadmium stress (Shoeva & Khlestkina, 2018). Anthocyanin accumulation brought about by the overexpression of RsMYB1 transcription factor has been found to improve heavy metal stress tolerance in petunia (Ai et al., 2018). The antioxidant activity of anthocyanin helps in scavenging ROS such as superoxide, hydroxyl radical, etc., thus protecting heavy metal stress (Dai et al., 2012). Anthocyanins are also known for their role in the chelation of metallic pollutants (Dai et al., 2012). 6.5 FUTURE SCOPE 1. The role of anthocyanin in human health needs to be studied. The mechanism by which they improve human health should be further investigated. 2. Anthocyanin, being a pigment responsible for imparting multiple stress tolerance and nutraceutical property can be included in different breeding programs. 3. Relation between anthocyanin content and their variation concerning different stresses can be studied. Any strong correlation between anthocyanin content and stress can be used as an indicator for stress assessment. 6.6 CONCLUSION Biotic and abiotic stresses, being one of the most important limiting factors of crop productivity needs to be addressed for achieving food security. Plants have multiple mechanisms by which they adapt to stress conditions. The role of anthocyanin plant stress tolerance is one of the important stress tolerance mechanisms. Anthocyanin has an important role in providing drought and light stress tolerance. It also provides tolerance against other stresses through their antioxidant activity. Through their antioxidant activity, they can scavenge different superoxide radicals and hence protect the membranes from damage. In addition to abiotic stresses, anthocyanin also provides tolerance against different biotic stresses. The coloration of vegetative tissues due to the presence of anthocyanin repels certain pests, thus providing a

Role of Anthocyanin in Plants to Survive Against Environmental Stresses

175

competitive advantage to plant. Plants with anthocyanin can be considered as a useful trait against stress tolerance and can be used in future breeding programs. KEYWORDS • • • • • •

anthocyanin crop productivity drought stress light stress photon flux density reactive oxygen species

REFERENCES Ai, T. N., Yun, B. W., Lim, S. H., & Kim, C. K., (2018). Overexpression of RsMYB1 enhances anthocyanin accumulation and heavy metal stress tolerance in transgenic petunia. Front. Plant Sci., 9, 1388. Aimar, D., Calafat, M., Andrade, A. M., Carassay, L., Abdala, G. I., & Molas, M. L., (2011). Drought tolerance and stress hormones: From model organisms to forage crops. Plants Environ., 10(6), 137–164. Allen, R. G., & Tresini, M., (2000). Oxidative stress and gene regulation. Free Radic. Biol. Med., 28(3), 463–499. Andersen, O. M., & Markham, K. R., (2005). Flavonoids: Chemistry, Biochemistry and Applications. CRC Press. Azhar, N., Hussain, B., Ashraf, M. Y., & Abbasi, K. Y., (2011). Water stress-mediated changes in growth, physiology and secondary metabolites of desi ajwain (Trachyspermum ammi L.). Pak. J. Bot., 43(9), 15–19. Bahler, B. D., Steffen, K. L., & Orzolek, M. D., (1991). Morphological and biochemical comparison of a purple-leafed and a green-leafed pepper cultivar. Hort. Sci., 26(6), 736. Bhargava, S., & Sawant, K., (2013). Drought stress adaptation: Metabolic adjustment and regulation of gene expression. Plant Breed., 132(1), 21–32. Bridle, P., & Timberlake, C. F., (1997). Anthocyanins as natural food colors—Selected aspects. Food Chem., 58(1, 2), 103–109. Chalker‐Scott, L., (1999). Environmental significance of anthocyanins in plant stress responses. J. Photochem. Photobiol., 70(1), 1–9. Chunthaburee, S., Sakuanrungsirikul, S., Wongwarat, T., Sanitchon, J., Pattanagul, W., & Theerakulpisut, P., (2016). Changes in anthocyanin content and expression of anthocyanin

176

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

synthesis genes in seedlings of black glutinous rice in response to salt stress. Asian J. Plant Sci., 15(3, 4), 56–65. Chutipaijit, S., Cha-um, S., & Sompornpailin, K., (2011). High contents of proline and anthocyanin increase protective response to salinity in ‘Oryza sativa’ L. spp. ‘indica’. Aust. J. Crop Sci., 5(10), 1191–1198. Cirillo, V., D’Amelia, V., Esposito, M., Amitrano, C., Carillo, P., Carputo, D., & Maggio, A., (2021). Anthocyanins are key regulators of drought stress tolerance in tobacco. Bio., 10(2), 139. Curtis, J. D., Lersten, N. R., & Lewis, G. P., (1996). Leaf anatomy, emphasizing unusual ‘concertina’ mesophyll cells, of two east African legumes (Caesalpinieae, Caesalpinioideae, Leguminosae). Ann. Bot., 78(1), 55–59. Dai, L. P., Dong, X. J., & Ma, H. H., (2012). Antioxidative and chelating properties of anthocyanins in Azolla imbricata induced by cadmium. Pol. J. Environ. Stud., 21(4). De Pascual-Teresa, S., & Sanchez-Ballesta, M. T., (2008). Anthocyanins: From plant to health. Phytochem. Rev., 7(2), 281–299. Duthie, G., & Crozier, A., (2000). Plant-derived phenolic antioxidants. Curr. Opin. Lipidol., 11(1), 43–47. Farooq, M., Gogoi, N., Barthakur, S., Baroowa, B., Bharadwaj, N., Alghamdi, S. S., & Siddique, K. H. M., (2017). Drought stress in grain legumes during reproduction and grain filling. J. Agron. Crop Sci., 203(2), 81–102. Foyer, C. H., Lelandais, M., & Kunert, K. J., (1994). Photooxidative stress in plants. Physiol. Plantarum, 92(4), 696–717. Ghosh, D., & Konishi, T., (2007). Anthocyanins and anthocyanin-rich extracts: Role in diabetes and eye function. Asia Pac. J. Clin. Nutr., 16(2). Gollop, R., Even, S., Colova‐Tsolova, V., & Perl, A., (2002). Expression of the grape dihydroflavonol reductase gene and analysis of its promoter region. J. Exp. Bot., 53(373), 1397–1409. Gould, K. S., Jay-Allemand, C., Logan, B. A., Baissac, Y., & Bidel, L. P., (2018). When are foliar anthocyanins useful to plants? Re-evaluation of the photoprotection hypothesis using Arabidopsis thaliana mutants that differ in anthocyanin accumulation. Environ. Exp. Bot., 154, 11–22. Gould, K. S., McKelvie, J., & Markham, K. R., (2002). Do anthocyanins function as antioxidants in leaves? Imaging of H2O2 in red and green leaves after mechanical injury. Plant. Cell Envin., 25(10), 1261–1269. Harborne, J. B., & Smith, D. M., (1972). Flavonoid pigments and plant phylogeny: The case of the hand-flower tree Chiranthodendron pentadactylon. Zeitschrift für Naturforschung B, 27(2), 210–210. Hughes, N. M., Reinhardt, K., Feild, T. S., Gerardi, A. R., & Smith, W. K., (2010). Association between winter anthocyanin production and drought stress in angiosperm evergreen species. J. Exp. Bot., 61(6), 1699–1709. Jaakola, L., (2013). New insights into the regulation of anthocyanin biosynthesis in fruits. T. Plant Sci., 18(9), 477–483. Jiang, X., Sun, J., & Bai, W., (2021). Anthocyanins in food. In: Xiao, J., Sarker, S. D., & Asakawa, Y., (eds.), Handbook of Dietary Phytochemicals. Springer, Singapore. https://doi. org/10.1007/978-981-15-4148-3_13.

Role of Anthocyanin in Plants to Survive Against Environmental Stresses

177

Kaku, S., Iwaya-Inoue, M., & Toki, K., (1992). Anthocyanin influence on water proton NMR relaxation times and water contents in leaves of evergreen woody plants during the winter. Plant Cell Physiol., 33(2), 131–137. Kamiloglu, S., Capanoglu, E., Grootaert, C., & Van, C. J., (2015). Anthocyanin absorption and metabolism by human intestinal CaCo2 cells—A review. Int. J. Mol. Sci., 16(9), 21555–21574. Keyvan, S., (2010). The effects of drought stress on yield, relative water content, proline, soluble carbohydrates and chlorophyll of bread wheat cultivars. J. Anim. Plant Sci., 8(3), 1051–1060. Kim, J., Lee, W. J., Vu, T. T., Jeong, C. Y., Hong, S. W., & Lee, H., (2017). High accumulation of anthocyanins via the ectopic expression of AtDFR confers significant salt stress tolerance in Brassica napus L. Plant Cell Rep., 36(8), 1215–1224. Knox, G. W., (1989). Water use and average growth index of five species of container grown woody landscape plants. J. Env. Hort., 7(4), 136–139. Kurutas, E. B., (2016). The importance of antioxidants which play the role in cellular response against oxidative/nitrosative stress: Current state. Nutr J., 15(1), 71. doi: 10.1186/s12937016-0186-5. PMID: 27456681; PMCID: PMC4960740. Landi, M., Tattini, M., & Gould, K. S., (2015). Multiple functional roles of anthocyanins in plant-environment interactions. Environ. Exp. Bot., 119, 4–17. Li, P., Li, Y. J., Zhang, F. J., Zhang, G. Z., Jiang, X. Y., Yu, H. M., & Hou, B. K., (2017). The Arabidopsis UDP‐glycosyltransferases UGT79B2 and UGT79B3, contribute to cold, salt and drought stress tolerance via modulating anthocyanin accumulation. Plant J., 89(1), 85–103. Lila, M. A., (2004). Anthocyanins and human health: An in vitro investigative approach. J. Biomed. Biotec., (5), 306. Liu, Y., Tikunov, Y., Schouten, R. E., Marcelis, L. F., Visser, R. G., & Bovy, A., (2018). Anthocyanin biosynthesis and degradation mechanisms in solanaceous vegetables: A review. Front. Chem., 6, 52. Lo Piero, A. R., Puglisi, I., Rapisarda, P., & Petrone, G., (2005). Anthocyanins accumulation and related gene expression in red-orange fruit induced by low temperature storage. J. Agric. Food Chem., 53(23), 9083–9088. Mazza, G., & Francis, F. J., (1995). Anthocyanins in grapes and grape products. Crit. Rev. Food Sci. Nutr., 35(4), 341–371. Merzlyak, M. N., & Chivkunova, O. B., (2000). Light-stress-induced pigment changes and evidence for anthocyanin photoprotection in apples. J. Photochem. Photobiol. B, Biol., 55(2, 3), 155–163. Moustaka, J., Tanou, G., Giannakoula, A., Adamakis, I. D. S., Panteris, E., Eleftheriou, E. P., & Moustakas, M., (2020). Anthocyanin accumulation in poinsettia leaves and its functional role in photo-oxidative stress. Environ. Exp. Bot., 175, 104065. Oancea, S., & Oprean, L., (2011). Anthocyanins, from biosynthesis in plants to human health benefits. Acta Universitatis Cinbinesis, Series E: Food Technol., 15(1). Oki, T., Kano, M., Watanabe, O., Goto, K., Boelsma, E., Ishikawai, F., & Suda, I., (2016). Effect of consuming a purple-fleshed sweet potato beverage on health-related biomarkers and safety parameters in Caucasian subjects with elevated levels of blood pressure and liver function biomarkers: A 4-week, open-label, non-comparative trial. Biosci. Microb. Food H., 2015–2026.

178

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Pietrini, F., & Massacci, A., (1998). Leaf anthocyanin content changes in Zea mays L. grown at low temperature: Significance for the relationship between the quantum yield of PS II and the apparent quantum yield of CO2 assimilation. Photosyn. Res., 58(3), 213–219. Pojer, E., Mattivi, F., Johnson, D., & Stockley, C. S., (2013). The case for anthocyanin consumption to promote human health: A review. Compr. Rev. Food Sci. Food Saf., 12(5), 483–508. Rasmussen, S. E., Frederiksen, H., Struntze, K. K., & Poulsen, L., (2005). Dietary proanthocyanidins: Occurrence, dietary intake, bioavailability, and protection against cardiovascular disease. Mol. Nutr. Food Res., 49(2), 159–174. Sedghi, M., Hadi, M., & Toluie, S. G., (2013). Effect of nano zinc oxide on the germination parameters of soybean seeds under drought stress. Ann. West Univ. Timis. Ser. Biol., 16(2), 73. Sherwin, H. W., & Farrant, J. M., (1998). Protection mechanisms against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscosa. Plant Growth Regul., 24(3), 203–210. Shoeva, O. Y., & Khlestkina, E. K., (2018). Anthocyanins participate in the protection of wheat seedlings against cadmium stress. Cereal Res. Commun., 46(2), 242–252. Sperdouli, I., & Moustakas, M., (2012). Interaction of proline, sugars, and anthocyanins during photosynthetic acclimation of Arabidopsis thaliana to drought stress. J. Plant Physiol., 169(6), 577–585. Steyn, W. J., Wand, S. J. E., Holcroft, D. M., & Jacobs, G., (2002). Anthocyanins in vegetative tissues: A proposed unified function in photoprotection. New Phytol., 155(3), 349–361. Tanaka, Y., & Ohmiya, A., (2008). Seeing is believing: Engineering anthocyanin and carotenoid biosynthetic pathways. Curr. Opin. Biotechnol., 19(2), 190–197. Tanaka, Y., Sasaki, N., & Ohmiya, A., (2008). Biosynthesis of plant pigments: Anthocyanins, betalains and carotenoids. Plant J., 54(4), 733–749. Trojak, B., Zullino, D., & Achab, S., (2017). Role of anthocyanins in high-light stress response. World Sci. News, 81(2), 150–168. Truong, H. A., Lee, W. J., Jeong, C. Y., Trịnh, C. S., Lee, S., Kang, C. S., Cheong, Y. K., et al., (2018). Enhanced anthocyanin accumulation confers increased growth performance in plants under low nitrate and high salt stress conditions owing to active modulation of nitrate metabolism. J. Plant Physic., 231, 41–48. Wang, R., Hashimoto, K., Fujishima, A., Chikuni, M., Kojima, E., Kitamura, A., Shimohigoshi, M., & Watanabe, T., (1997). Light-induced amphiphilic surfaces. Natr., 388(6641), 431, 432. Watson, R., & Schönlau, F., (2015). Nutraceutical and antioxidant effects of a delphinidinrich maqui berry extract delphinol: A review. Minerva Cardioangiol., 63, 1–11. Retrieved from: http://www.ncbi.nlm.nih.gov/pubmed/25892567 (accessed on 18 October 2022). Wettstein-Westersheim, W., & Minelli, H., (1962). Breeding intersectional Populus hybrids. Allg. Forst Z., 73(2). Wink, M., (1999). Functions of Plant Secondary Metabolites and Their Exploitation in Biotechnology (p. 3). Taylor Francis. Wrolstad, R. E., (2004). Anthocyanin pigments—Bioactivity and coloring properties. J. Food Sci., 69(5), C419–C425. Zobayed, S. M. A., Afreen, F., & Kozai, T., (2007). Phytochemical and physiological changes in the leaves of St. John’s wort plants under a water stress condition. Environ. Exp. Bot., 59(2), 109–116.

CHAPTER 7

Role of Carotenoids in Tolerance Against Different Environmental Stress BHUPINDER DHIR

School of Sciences, Indira Gandhi National Open University, New Delhi, India

ABSTRACT Carotenoids are metabolites that play vital functions in plants. They provide protection to plants against strong light, dissipation of excess energy and control the harvesting of light by antenna chlorophyll molecules. In abiotic stress conditions, carotenoids protect the photosynthetic apparatus by oxidative damage caused due to photooxidation and extreme temperature. Free radical scavenging property of carotenoids protects the membranes from lipid peroxidation and helps in the stabilization of membrane lipid bilayers. Singlet oxygen, a reactive oxygen species (ROS) produced under stress conditions, oxidize carotenoids to synthesize derivatives (electrophile species) that helps in acclimation to stress by inducing changes in gene expression. The products of carotenoids oxidation act mainly as antioxidants. The activities such as light harvesting, scavenging of singlet oxygen species and dissipation of excess energy establish the role of carotenoids as molecules of immense importance in plants exposed to stress. 7.1 INTRODUCTION Carotenoids are yellow, orange, and red color pigments synthesized in bacteria, fungi, algae, and plants (Sandmann, 2001). Carotenoids are lipophilic Biology and Biotechnology of Environmental Stress Tolerance in Plants: Secondary Metabolites in Environmental Stress Tolerance, Volume 1. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

180

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

isoprenoids or terpenoids which are composed of eight isoprene units. Majority of carotenoids are derived from the linear tetraterpene phytoene (DellaPenna & Pogson, 2006; Ruiz-Sola & Rodriguez-Concepcion, 2012). Carotenoids are grouped into two categories – oxygenated xanthophylls which include lutein, zeaxanthin, violaxanthin; and unoxygenated carotenes which include α-carotene, β-carotene, and lycopene (Zaripheh & Erdman, 2002). Carotenoids are synthesized and localized in the plastids of higher plants. Their accumulation occurs primarily in the thylakoid membranes of chloroplasts, senescing leaves, chromoplasts of ripening fruits and flower petals. In some plants, carotenoids have also been found to be present in the amyloplasts of plant storage tissues (such as maize seeds and potato tubers). Carotenoids found in plant chloroplasts mainly include lutein, zeaxanthin, antheraxanthin, violaxanthin, and neoxanthin. Lutein, violaxanthin, and neoxanthin are essential components of the light-harvesting antennae. They absorb photons, transfer the energy to chlorophyll and assist in the harvesting of light. The presence of carotenoids such as capsanthin, capsorubin, bixin, rocetin, citraurin in chromoplasts has also been reported. Carotenoids play a role in many biological processes of plants. These include photosynthesis, photomorphogenesis, photoprotection, and development. Carotenoids form essential components of the photosynthetic apparatus. They are integrated into light-harvesting complexes (LHC) along with chlorophyll. The physiological roles played by them mainly include photoprotection and light harvesting (Croce et al., 1999a, b; Ashraf et al., 2019). Carotenoids also associate in production of phytohormones, including ABA and strigolactone. Their roles as antioxidants, accessory light-harvesting pigments, agents of attraction for pollinators and agents that help in seed dispersal are also known. Recent studies have shown that carotenoids play a role in tackling environment stress. 7.2 MAJOR ROLES OF CAROTENOIDS IN PLANTS 7.2.1 PHOTOSYNTHESIS Carotenoids form an important component of the photosystems. They are bound in discrete pigment-protein complexes known as LHCII trimeric complex (Demmig-Adams & Adams, 2006; Li et al., 2009b). They absorb light in the range of the spectral region and transfer energy to chlorophyll,

Role of Carotenoids in Tolerance Against Different Environmental Stress

181

initiating the photochemical events of photosynthesis (Polívka & Frank, 2010). Photosynthesis generates highly reactive intermediates/species (ROS). These reactive oxygen species (ROS) affect the photosynthetic rate by causing oxidative damage to the photosynthetic apparatus (Niyogi, 1999). Carotenoids function as photoprotectants by quenching ROS, thereby preventing oxidative damage. Non-photochemical quenching (NPQ) and dissipation of excess light and heat are some other roles of carotenoids (Demmig-Adams et al., 1996; Croce et al., 1999b; Niyogi, 1999). 7.2.2 PHOTOMORPHOGENESIS During photomorphogenesis, carotenoids are produced in a coordinated manner. They help in the formation of thylakoid membranes which form an important component of photosynthetic apparatus (Welsch et al., 2000). Hence carotenoids are essential for the development of chloroplasts (Rodrı’guez-Villalo’n et al., 2009). 7.2.3 PHOTOPROTECTION Photoprotective properties of carotenoids include quenching of triplet chlorophyll (3Chl*) and singlet oxygen (1O2) (Triantaphylides & Havaux, 2009). 1O2 is the ROS produced in photosynthetic organisms during strong illumination (Triantaphylides et al., 2008; Gonzalez-Perez et al., 2011). The plants deficient in carotenoids are sensitive and suffer from extensive photodamage. The dihydroxy carotenoid zeaxanthin plays a role in the dissipation of light energy. Zeaxanthin is formed from β-carotene by hydroxylation and acts serves as a substrate in the biosynthesis of many other important xanthophylls. 7.2.4 OTHER ROLES Carotenoids act as precursors of apocarotenoids which are the oxidative and enzymatic cleavage products of carotenoids. The formation of apocarotenoids is initiated by oxidative reactions catalyzed by enzymes. The formation of apocarotenoids can also take place during exposure or

182

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

non-enzymatic attack of carotenoids to ROS. Apocarotenoids play a role in various biological processes in plants, such as the formation of photosystems and light-harvesting antenna complexes that play a role in photosynthesis, photoprotection, and regulation of growth and development (Cazzonelli & Pogson, 2010b; Ruiz-Sola & Rodrı’guez-Concepcio’na, 2012; Havaux, 2014). They also act as signaling molecules and have been implicated in the interactions of plants with their environment (Cazzonelli, 2011; Walter & Strack, 2011). 7.3 ROLE OF CAROTENOIDS IN MITIGATION OF STRESS An external factor that influences growth, productivity, reproductive capacity, or survival of plants in a negative manner is called stress (Buchanan et al., 2002). It is also defined as an external factor that negatively affects growth, development or productivity of plants. Plants require an optimal range of temperature, water their growth and survival. Scarcity or excess of water (flooding stress) can affect the growth and development of plants to a significant extent. Excess of water causes plant cells to swell and burst, whereas water deficit (too little water) cause drying of plant, leading to a condition called desiccation. Changes in temperature prove detrimental for the growth of plants. Very low temperature exposes plants to chilling stress. Low temperature affects the uptake of water and nutrients resulting in dehydration and starvation of the cell. On the contrary, extreme hot conditions alter the permeability of the cell wall and cell membranes due to damage and breakdown of proteins, and the process is called denaturation. Other stresses that affect plants include imbalance of nutrition or toxicity. High amounts of salt uptake by plants lead to cell desiccation. This is because the presence of high levels of salt outside a plant cell forces water to move out of the cell via the process of osmosis. Soil salinization also affects plants osmotic potential and hampers cellular functions such as photosynthesis and stomatal opening. Stress caused due to heat, high/low temperature, drought results in stomatal closing, disruption of electron transport system, damage to photosynthetic machinery and high generation of toxic active oxygen species. The stress exposure in plants triggers the role of antioxidant compounds and organic (compatible) solutes that play a vital role in the protection of photosynthetic machinery and other necessary metabolic activities/reactions. Plants exposed to oxidative stress caused by environmental stress show high

Role of Carotenoids in Tolerance Against Different Environmental Stress

183

activity of enzymatic and non-enzymatic antioxidant systems. Antioxidants such as ascorbic acid, tocopherol, glutathione, phenolics, flavonoids, and carotenoids induce tolerance against abiotic stress by scavenging ROS. ROS, especially singlet oxygen (1O2) is produced in the chloroplasts of plants exposed to environmental stress. Singlet oxygen reduces the photosynthetic capacity of plants and results in excessive absorption of light energy. Singlet oxygen is a strong electrophilic agent and adversely affects biological molecules such as lipids, proteins, and DNA. It also triggers a signaling cascade inducing programmed cell death (PCD). Carotenoids act as the first line of defense in plants against toxicity caused by singlet oxygen. They assist in quenching and scavenging of singlet oxygen. Carotenoids transfer excitation energy followed by thermal deactivation to provide protection against triplet chlorophylls. Carotenoids act as light harvesters and remove excess energy produced during stress conditions. Carotenoids act as accessory light‐harvesting pigments that extend the range of light absorbed by the photosynthetic apparatus in a very effective way. They provide protection to plants against overexcitation in strong light and help in removal of excess energy. The plants that do not produce carotenoids are photosensitive and suffer from extensive photodamage. The carotenoids influence the molecular dynamic of membranes, thereby inducing a protective role in plants. Signaling molecules and regulatory metabolites derived from carotenoids have been identified in plants (Havaux, 2014). β-cyclocitral derived from the oxidation of β-carotene is a reactive electrophilic species which is highly bioactive and help in adapting to stress condition by inducing changes in gene expression (D’Alessandro et al., 2019). Carotenoids are also associated with xanthophyll cycle (Nasir et al., 2015). The carotenoid zeaxanthin, synthesized via de novo synthesis in response to environmental stress or rapid enzymic de‐epoxidation of the carotenoid violaxanthin is involved in the dissipation excess of harmful excitation energy under stress conditions (Horton & Ruban, 2005; Jahns & Holzwarth, 2012; D’Alessandro et al., 2018). Plants show difference in their ability to produce zeaxanthin under stress conditions, and hence vary in their ability to protect the photosynthetic apparatus. Recent studies have demonstrated that dissipation of excess excitation energy and formation of zeaxanthin from violaxanthin in the light-harvesting are correlated. C Apocarotenoids act as precursors of the phytohormones abscisic acid (ABA) and strigolactones (SLs). Both ABA and strigolactones play a role in the abatement of abiotic stress in plants (Jia et al., 2017). Carotenoids help

184

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

in the production of phytohormones such as ABA, strigolactone, and other signaling molecules (e.g., blumenin and mycorradicin). Beta-carotene act as the substrate for biosynthesis of strigolactone (Matusova et al., 2005; Rani et al., 2008). Changes in β-carotene levels perturb strigolactone production. Strigolactones are a class of hormones which are basically terpenoid lactones that help in regulating branching of shoot (Gomez-Roldan et al., 2008; Umehara et al., 2008; Felemban et al., 2019). The strigolactone which are carotenoid-derived terpenoids act by three ways: (i) inhibiting branching of shoots by restricting growth of buds (Gomez-Roldan et al., 2008; Umehara et al., 2008); (ii) influencing growth of mycorrhizal hyphal which trigger symbiotic relationship in the root rhizosphere (Akiyama et al., 2005); and (iii) supporting germination of seeds of parasitic plants (Matusova et al., 2005). The hormone ABA is derived from the enzymatic oxidation of the xanthophylls neoxanthin (Nambara and Marion-Poll, 2005). ABA plays a role in modulation adaptive responses for plants in adverse environmental conditions at the gene level. Apocarotenoids are believed to act as signaling compounds for the regulation of root colonization by arbuscular mycorrhizal (AM) fungi (Strack & Fester, 2006). 7.4 ABATEMENT OF STRESS USING CAROTENOID-DERIVED SIGNALING MOLECULES Many new carotenoid-derived signaling molecules and regulatory metabolites have been identified in the recent years (Nisar et al., 2015; Uarrota et al., 2018). Apocarotenoid and volatile cyclocitral functions in regulating stress response. Apocarotenoids play a role in controlling the turnover of arbuscule in AM fungi during symbiosis and triggering hyphal branching in the rhizosphere (Giuliano et al., 2003; Akiyama et al., 2005). Carotenoid derivative, volatile β-cyclocitral, derived from the oxidation of β-carotene (Ramel et al., 2012a). It is a cleavage product and reactive electrophile species that induce changes in gene expression leading to acclimation to stress conditions (Wurtzela, 2019). The presence of β-Cyclocitral has been reported in plant species such as tomato, rice, parsley, tea, grape, and many trees (Tieman et al., 2012; Rodrigo et al., 2013; Tewari et al., 2015; Linde et al., 2016; Hinge et al., 2016; Chen et al., 2017; Ojha & Roy, 2018). Studies with of Arabidopsis showed that low concentrations of volatile β-cyclocitral modify the expression of genes in plants treated with high light

Role of Carotenoids in Tolerance Against Different Environmental Stress

185

conditions (Ramel et al., 2012b). β-carotene is localized very close to the primary site of 1O2 production in chloroplasts (i.e., the PSII reaction center), therefore its oxidation metabolites constitute primary sensors of light stress in plants. The genes induced by β-cyclocitral are related to cellular defense against stress. More than 80% of the genes affected by β-cyclocitral were identified as 1O2-responsive genes. β-cyclocitral stimulates 1O2-specific responses and activates acclimation to photooxidative stress. β-cyclocitral is an intermediate in the signaling of this ROS in Arabidopsis. An increase in light intensity causes a significant increase in the level of glycosylated β-cyclocitral (Mi et al., 2019b). β-cyclocitral increases the plant tolerance to photo-oxidative stress and initiates acclimation to high light conditions by triggering transcriptome reprograming (Ramel et al., 2012b). Apocarotenoid, volatile cyclocitral functions in regulating stress response and determining root architecture (Azzahra et al., 2019). Treatment with β-cyclocitral brings significant increases in lateral root branching. This happens because cell division in undifferentiated cells in meristems of lateral and primary roots gets stimulated. β-cyclocitral positively affects the growth of plants exposed to salt stress. Studies have indicated that application of β-cyclocitral eliminates the negative effect of salt on root growth and exerts a positive effect on the vigor of rice plants (Dickinson et al., 2019). Apocarotenoids are known to inhibit branching of shoots. They have been shown to positively influence the organisms of rhizosphere, mycorrhizal fungi so that root architectural changes necessary for symbiosis get mediated and resistance to harmful fungi is achieved (Al-Babili & Bouwmeester, 2015; Borghi et al., 2016; Decker et al., 2017; Stauder et al., 2018). Apocarotenoid signals control plant architecture. This was suggested when the architectural abnormalities were seen when carotenoid biosynthesis was blocked at certain steps or expression of carotenoid cleavage dioxygenase enzymes was removed (Hou et al., 2016). 7.5 CONCLUSION Carotenoids are compounds that play an important role in plants. They possess antioxidant properties and act as accessory pigment that plays a role in the light-harvesting system. Their role as light harvesters, quenchers, scavengers of singlet oxygen species, membrane stabilizers and dissipators of excess harmful energy during stress conditions is well established. Their Apocarotenoids generated by enzymatic cleavage of carotenoids perform

186

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

several bioactivities related to architecture, growth, development, and stress responses in plants. Oxidation products of carotenoids act as stress signal in plants. Carotenoids derivatives such as volatile β-cyclocitral derived from the oxidation of β-carotene play a role in gene expression leading to acclimation to stress conditions. β-cyclocitral acts a signal produced in high light conditions and induces defense mechanisms and acts alike as messenger involved in the 1O2 signaling pathway in plants. The diverse roles of carotenoids establish them as molecules of immense importance in the protection of plants against stress. A good understanding related to carotenoid biosynthesis and its functions in plants has been made, but a lot remains to be explored to highlight its role in imparting stress tolerance in plants. Bioactivities of apocarotenoids suggest a new method for creating or modifying plants required for agricultural and industrial needs. KEYWORDS • • • • • • •

antioxidant arbuscular mycorrhizal isoprenoids light-harvesting complexes non-photochemical quenching reactive oxygen species singlet oxygen

REFERENCES Akiyama, K., Matsuzaki, K. I., & Hayashi, H., (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature, 435, 824. Al-Babili, S., & Bouwmeester, H. J., (2015). Strigolactones, a novel carotenoid-derived plant hormone. Annu. Rev. Plant Biol., 66, 161–186. Ashraf, M. A., Riaz, M., Arif, M. S., Rasheed, R., Iqbal, M., Hussain, I., & Mubarik, M. S., (2019). The role of non-enzymatic antioxidants in improving abiotic stress tolerance in plants. Plant Tolerance to Environmental Stress. CRC Press, eBook ISBN9780203705315. Azzahra, F., Zaifuddin, M., Felemban, N. M. H., et al., (2019). Apocarotenoids in plant development and stress response. Frontiers in Plant Science, 10. Article 1168.

Role of Carotenoids in Tolerance Against Different Environmental Stress

187

Borghi, L., Liu, G. W., Emonet, A., Kretzschmar, T., & Martinoia, E., (2016). The importance of strigolactone transport regulation for symbiotic signaling and shoot branching. Planta, 243, 1351–1360. Buchanan, B. B., Schürmann, P., Wolosiuk, R. A., & Jacquot, J. P., (2002). The ferredoxin/ thioredoxin system: From discovery to molecular structures and beyond. Photosynthesis Research, 73, 215–222. Cazzonelli, C. I., & Pogson, B. J., (2010b). Source to sink: Regulation of carotenoid biosynthesis in plants. Trends Plant Sci., 15, 266–274. Cazzonelli, C. I., (2011). Carotenoids in nature: Insights from plants and beyond. Functional Plant Biology, 38, 833–847. Cazzonelli, C. I., Nisar, N., Hussain, D., Carmody, M. E., & Pogson, B. J., (2010a). Biosynthesis and regulation of carotenoids in plants micronutrients, vitamins and health benefits. In: Pua, E. C., & Davey, M. R., (eds.) Plant Developmental Biology–Biotechnological Perspectives (Vol. 2, pp. 117–137). Berlin, Heidelberg: Springer. Chen, W. K., Yu, K. J., Liu, B., Lan, Y. B., Sun, R. Z., Li, Q., et al., (2017). Comparison of transcriptional expression patterns of carotenoid metabolism in ‘Cabernet Sauvignon’ grapes from two regions with distinct climate. Journal of Plant Physiology, 213, 75–86. Croce, R., Remelli, R., Varotto, C., Brenton, J., & Bassi, R., (1999a). The neoxanthin binding site of the major light-harvesting complex (LHCII) from higher plants. Federation of European Biochemical Society Letters, 456, 1–6. Croce, R., Weiss, S., & Bassi, R., (1999b). Carotenoid-binding sites of the major lightharvesting complex II of higher plants. Journal of Biological Chemistry, 274, 29613–29623. D’Alessandro, S., Ksas, B., & Havaux, M., (2018). Decoding ß-cyclocitral-mediated retrograde signaling reveals the role of a detoxification response in plant tolerance to photooxidative stress. Plant Cell, 30, 2495–2511. D’Alessandro, S., Mizokami, Y., Légeret, B., & Havaux, M., (2019). The apocarotenoid β-cyclocitric acid elicits drought tolerance in plants. iScience, 19, 461–473. Decker, E. L., Alder, A., Hunn, S., Ferguson, J., Lehtonen, M. T., Scheler, B., Kerres, K. L., Wiedemann, G., Safavi-Rizi, V., Nordzieke, S., Balakrishna, A., Baz, L., et al., (2017). Strigolactone biosynthesis is evolutionarily conserved, regulated by phosphate starvation and contributes to resistance against phytopathogenic fungi in a moss, Physcomitrella patens. New Phytologist, 216, 455–468. DellaPenna, D., & Pogson, B. J., (2006). Vitamin synthesis in plants: Tocopherols and carotenoids. Annual Review Plant Biology, 57, 711–738. Demmig-Adams, B., & Adams, W. W., (2006). Photoprotection in an ecological context: The remarkable complexity of thermal dissipation. New Phytologist, 172, 11–21. Demmig-Adams, B., Gilmore, A. M., & Adams, III. W. W., (1996). In vivo function of carotenoids in higher plants. Journal of the Federation of American Societies for Experimental Biology, 10, 403–412. Dickinson, A. J., Lehner, K., Mi, J., Jia, K. P., Mijar, M., Dinneny, J., et al., (2019). β-cyclocitral is a conserved root growth regulator. Proceedings of National Academy of Sciences, 116, 10563–10567. Dickinson, A. J., Lehner, K., Mijar, M., & Benfey, P. N., (2019). β-cyclocitral is a natural root growth regulator. Proceedings of National Academy of Sciences U S A, 116, 10563–10567. Felemban, A., Braguy, J., Zurbriggen, M. D., & Al-Babili, S., (2019). Apocarotenoids involved in plant development and stress response. Front. Plant Science, 10, 1168.

188

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Giuliano, G., Al‐Babili, S., Von, L. J., (2003). Carotenoid oxygenases: Cleave it or leave it. Trends in Plant Science, 8, 145–149. Gomez-Roldan, V., Fermas, S., Brewer, P. B., et al., (2008). Strigolactone inhibition of shoot branching. Nature, 455, 189–194. González-Pérez, S., Gutiérrez, J., García-García, F., Osuna, D., Dopazo, J., Lorenzo, Ó., Revuelta, J. L., & Arellano, J. B., (2011). Early transcriptional defense responses in Arabidopsis cell suspension culture under high-light conditions. Plant Physiology, 156, 1439–1456. Havaux, M., (2014). Carotenoid oxidation products as stress signals in plants. Plant Journal, 79, 597–606. Horton, P., & Ruban, A. V., (2005). Molecular design of photosystem II light-harvesting antenna: Photosynthesis and photoprotection. Journal of Experimental Botany, 56, 365–373. Jahns, P., & Holzwarth, A. R., (2012). The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochimica et Biophysica Acta, 1817, 182–193. Li, F., Tzfadia, O., & Wurtzel, E. T., (2009a). The phytoene synthase gene family in the grasses. Plant Signal Behavior, 4, 208–211. Li, Z., Wakao, S., Fischer, B. B., & Niyogi, K. K., (2009b). Sensing and responding to excess light. Annual Review of Plant Biology, 60, 239–260. Linde, G., Gazim, Z., Cardoso, B., Jorge, L., Tešević, V., Glamoćlija, J., et al., (2016). Antifungal and antibacterial activities of Petroselinum crispum essential oil. Genetics and Molecular Research, 15, 1–11. Matusova, R., Rani, K., Verstappen, F. W., Franssen, M. C., Beale, M. H., & Bouwmeester, H. J., (2005). The strigolactone germination stimulants of the plant parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiology, 139, 920–934. Mi, J., Jia, K. P., Balakrishna, A., Feng, Q., & Al-Babili, S., (2019a). A highly sensitive SPE-derivatization-UHPLC-MS approach for quantitative profiling of carotenoid-derived dialdehydes from vegetables. Journal of Agricultural Food Chemistry, 67, 5899–5907. Mi, J., Jia, K. P., Balakrishna, A., Wang, J. Y., & Al-Babili, S., (2019b). An LC-MS profiling method reveals a route for apocarotene glycosylation and shows its induction by high light stress in Arabidopsis. Analyst, 144, 1197–1204. Nisar, N., Li, L., Lu, S., Khin, N. C., & Pogson, B. J., (2015). Carotenoid metabolism in plants. Molecular Plant, 8, 68–82. Niyogi, K. K., (1999). Photoprotection revisited: Genetics and molecular approaches. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 333–359. Ojha, P. K., & Roy, K., (2018). PLS regression-based chemometric modeling of odorant properties of diverse chemical constituents of black tea and coffee. RSC Advances, 8, 2293–2304. Polívka, T., & Frank, H. A., (2010). Molecular factors controlling photosynthetic light harvesting by carotenoids. Accounts of Chemical Research, 43, 1125–1134. Ramel, F., Birtic, S., Cuine, S., Triantaphylides, C., Ravanat, J. L., & Havaux, M., (2012a). Chemical quenching of singlet oxygen by carotenoids in plants. Plant Physiology., 158, 1267–1278. Ramel, F., Birtic, S., Ginies, C., Soubigou-Taconnat, L., Triantaphylides, C., & Havaux, M., (2012b). Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proceedings of National Academic Sciences USA. 109, 5535–5540. Rani, K., Zwanenburg, B., Sugimoto, Y., Yoneyama, K., & Bouwmeester, H. J., (2008). Biosynthetic considerations could assist the structure elucidation of host plant produced

Role of Carotenoids in Tolerance Against Different Environmental Stress

189

rhizosphere signaling compounds (strigolactones) for arbuscular mycorrhizal fungi and parasitic plants. Plant Physiology and Biochemistry, 46, 617–626. Rodrigo, M. J., Alquézar, B., Alós, E., Medina, V., Carmona, L., Bruno, M., et al., (2013). A novel carotenoid cleavage activity involved in the biosynthesis of Citrus fruit-specific apocarotenoid pigments. Journal of Experimental Botany, 64, 4461–4478. Rodriguez-Villalon, A., Gas, E., & Rodriguez-Concepcion, M., (2009a). Phytoene synthase activity controls the biosynthesis of carotenoids and the supply of their metabolic precursors in dark-grown Arabidopsis seedlings. Plant Journal, 60, 424–435. Ruiz-Sola, Á., & Rodríguez-Concepción, M., (2012). Carotenoid biosynthesis in Arabidopsis: A colorful pathway. Arabidopsis Book, 10, e0158. Sandmann, G., (2001). Carotenoid biosynthesis and biotechnological application. Archives of Biochemistry and Biophysics, 385, 4–12. Stauder, R., Welsch, R., Camagna, M., Kohlen, W., Balcke, G. U., Tissier, A., & Walter, M. H., (2018). Strigolactone levels in dicot roots are determined by an ancestral symbiosisregulated clade of the PHYTOENE SYNTHASE gene family. Frontiers of Plant Science, 9, 255. Strack, D., & Fester, T., (2006). Isoprenoid metabolism and plastid reorganization in arbuscular mycorrhizal roots. New Phytologist, 172, 22–34. Tewari, G., Mohan, B., Kishor, K., Tewari, L. M., & Nailwal, T. K., (2015). Volatile constituents of Ginkgo biloba L. leaves from Kumaun. Journal of Indian Chemical Society, 92, 1583–1586. 10.1080/0972060X.2014.958567. Triantaphylidès, C., & Havaux, M., (2009). Singlet oxygen in plants: Production, detoxification and signaling. Trends in Plant Science, 14, 219–228. Triantaphylides, C., Krischke, M., Hoeberichts, F. A., Ksas, B., Gresser, G., Havaux, M., Van, B. F., & Mueller, M. J., (2008). Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiology, 148, 960–968. Uarrota, V. G., Stefen, D. L. V., Leolato, L. S., Gindri, D. M., & Nerling, D., (2018). Revisiting carotenoids and their role in plant stress responses: From biosynthesis to plant signaling mechanisms during stress. Antioxidants and Antioxidant Enzymes in Higher Plants, 207–232. Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., et al., (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature, 11, 195–200. Walter, M. H., & Strack, D., (2011). Carotenoids and their cleavage products: Biosynthesis and functions. National Production Reproduction, 28, 663–692. Welsch, R., Beyer, P., Hugueney, P., Kleinig, H., & Von, L. J., (2000). Regulation and activation of phytoene synthase, a key enzyme in carotenoid biosynthesis, during photomorphogenesis. Planta, 211, 846–854. Wurtzela, E. T., (2019). Changing form and function through carotenoids and synthetic biology. Plant Physiology, 179, 830–843. Zaripheh, S., & Erdman, Jr. J. W., (2002). Factors that influence the bioavailability of xanthophylls. Journal of Nutrition, 132, 531S–534S.

CHAPTER 8

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance SHREYA NATH,1 ANISH NAG,2 SWARNALI DEY,3 RITA KUNDU,3 and SUBHABRATA PAUL1 School of Biotechnology, Presidency University (2nd Campus), Kolkata – 700156, West Bengal, India 1

Department of Life Sciences, CHRIST (Deemed to be University), Bangalore – 560029, Karnataka, India

2

Department of Botany, University of Calcutta, 35 Ballygunge Circular Road, Kolkata – 700019, West Bengal, India

3

*

Corresponding author. E-mail:

ABSTRACT Plants are invariably subjected to various environmental stresses that hinder their normal growth and development, which leads to decreased plant productivity and yield. To combat the detrimental effects of such abiotic and biotic stresses, plants have developed diverse mechanisms and one of the prominent ones includes the production of secondary metabolites like phenolic, alkaloids, terpenes, etc. Secondary metabolites serve as major components of the plant stress responses. Chalcones (1,3-diaryl-2-propen1-one) and coumarins (1,2-benzopyrone) are precursors of flavonoids, a common secondary metabolite of plants that provide a beneficial role during oxidative and biotic stress. Apart from protection, coumarins have certain roles in promoting or inhibiting plant growth, affecting cell division and differentiation and auxin metabolism. These compounds are also known to possess therapeutic properties such as anti-inflammatory, anti-microbial, Biology and Biotechnology of Environmental Stress Tolerance in Plants: Secondary Metabolites in Environmental Stress Tolerance, Volume 1. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

192

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

anti-cancer, and cytotoxic effects when isolated from plants. Besides, chalcones and coumarins have allelopathic effects and protect plants against herbivory. Owing to excellent ROS scavenging properties, chalcones, coumarins, and their derivatives are extensively employed as agents to alleviate adversities associated with abiotic stresses like osmotic, heat, and cold stress, and in defense against pathogen invasion. The application of these secondary metabolites to mitigate atrocities of environmental stress in plants is an interesting and concurrent area of investigation. This chapter highlights the structural and functional details of chalcones and coumarins and their implications in ameliorating environmental stress in plants. 8.1 INTRODUCTION Homeostatic conditions mean internal steady-state conditions which are optimal for all the physiological functions of organisms. Plant stress encompasses some malfunction in normal plant physiology due to a sudden shift of optimal environmental conditions to certain sub-optimal conditions that disrupt the initial homeostatic state. Nowadays, rapid urbanization, global warming, and ever-fluctuating climate disrupts the natural optimal condition for plant growth. Plants are most commonly exposed to both abiotic and biotic stress. Biotic stresses include invasion by several plant pathogens like viruses, bacteria, fungi, nematodes, etc., while abiotic stress components are most likely to be highintensity light, temperature, flood, drought, salinity, etc. Plant stress leads to various structural anomalies and physiological malfunctions in the plants that ultimately culminate into improper growth and concomitant yield loss. Over the years, efforts have been made consistently to find out plausible ways to combat such environmental stress and restore normal plant functions. Therefore, an adaptation of new strategies to mitigate the effect of such stress has become an important aspect of research in plant science. To date approaches like raising transgenic plants (Parvin et al., 2020), producing stress-tolerant varieties (Bita & Gerats, 2013), application of nanoparticles (Jalil & Ansari, 2019), and use of chemical compounds (Sako et al., 2021), fungicides (Parvin et al., 2020), biostimulants have been reported to mitigate plant stress. But all of the approaches have some sort of dismissive effect on human health due to their non-organic nature. The use of organic compounds, especially of plant origin has been favored compared to synthetic or chemical compounds, as the latter mostly leads to environmental degradation. On the other hand, transgenic crops have a negative reputation among the scientific community

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

193

because of uncontrolled genetic modification, socio-economic/bioethical issues, difficulties in crop management, etc. Therefore, the usage of the substance of plant origin to alleviate stress is more desirable. Researchers are continuously putting efforts into finding such substances of natural origin. Among them, chalcones and coumarins stand as one of the most propitious candidates in recent days due to their ability to alleviate both biotic and abiotic plant stress. In this chapter, we have attempted to elaborate on the various types of coumarins and chalcones that are naturally available, their biosynthetic pathways in plants, and how they help in ameliorating several abiotic and biotic stress incidences in plants. 8.2 CHALCONE Chalcone (1,3-diaryl-2-propane-1-one) or chalconoid, is present in several natural compounds like fruits, vegetables, tea leaves, etc. The name “chalcone” is derived from “chalcos” meaning “bronze,” as most of the naturally occurring chalcones have distinctive bronze or yellow color due to the presence of characteristic α,β-unsaturated double bond. Chalcone compound can exist in both cis and trans isomers with the trans isomer being thermodynamically more stable (Sahu et al., 2012). For many decades, chalcone compounds (both synthetic and naturally occurring) have grabbed the interest of many scientists due to their diverse biological activity starting from anti-inflammatory, antioxidant, anti-infective, anti-viral, anti-tumor, and anti-cancer properties (Ni et al., 2004; Sahu et al., 2012). Chalcones are also used for drug development for the treatment of digestive system-related diseases. Some chalcones have also been clinically tested for the treatment of cancer (Orlikova et al., 2011), cardiovascular diseases (Mahapatra & Bharti, 2016), and viral infections (Elkhalifa et al., 2021), etc. Due to its prominent role in the ROS scavenging mechanism, chalcone, and its derivative can be used to alleviate the adverse effects related to different abiotic and biotic stresses in plants. 8.2.1 STRUCTURE AND PROPERTIES Chalcones are 15 carbon-containing open-chain flavonoids with a C6-C3-C6 configuration. They are composed of two phenolic rings (A ring and B ring) connected by a highly electrophilic three-carbon α,β-unsaturated carbonyl structure. Their general chemical formula is C15H12O. The C-opening isoforms of chalcone are called dihydrochalcones and are abundant in leaves of apples (Malus domestica Brokh) and Aspalathus linearis (Del Rio et al., 2013; Yahyaa et al., 2017; Bramati et al., 2002). Due to the presence of

194

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

flavonoids, the leaves of Aspalathus are eaten as rubios tea. The biological activity of most of the chalcones is determined either by the characteristic α,β-unsaturated double bond or the presence and location of hydroxyl groups (Iwashina, 2000). Chalcones can exist in trans (E) and cis (Z) forms, however, the trans conformation is more stable thermodynamically (Evranos & Ertan, 2011). Owing to electron-pushing and electron-pulling functional groups on the benzene ring, chalcones can fluoresce (Zhuang et al., 2017). The absorption wavelength of 4-dimethylchalcone compounds is between 390 nm and 460 nm while the emission wavelength lies between 450 nm and 620 nm. Chalcones are generally aromatic ketone and enone (α,β-Unsaturated carbonyl compounds) with a molecular mass of 208.26 g·mol–1. The taste of chalcone glycosides and dihydrochalcones vary from very sweet, bitter to no taste at all (Taylor et al., 2014). 8.2.2 SOURCE AND SYNTHESIS Chalcones can either be obtained naturally from various plants or can be synthesized chemically in the laboratory in various ways. Naturally occurring chalcones can be found in two forms – chalcone-aglycones and O-glycosides. Chalcones are distributed in several families of dicotyledonous plants (Asteraceae, Moraceae, Fabaceae, and Aristolochiaceae), some monocotyledons (Poaceae, Amaryllidaceae, Xanthorrhoeaceae, Cyperaceae, Liliaceae, Zingiberaceae), gymnosperms (Cupressaceae, Pinaceae) and even pteridophytes (Platyzomataceae, Adiantaceae, Thelypteridaceae, Polypcdiaceae) (Iwashina, 2000). Table 8.1 summarizes the various chalcones that have been obtained from different plant parts. In higher plants, CHS initiates the biosynthesis of chalcones from p-coumaroyl-CoA (1 molecule) and malonyl-CoA (3 molecules). The aromatic B ring and the 3C bridge are formed by the conversion of L-phenylalanine (a product of the shikimic acid pathway) to p-coumaril-CoA (phenylpropanoid pathway). Later, the condensation of 3 molecules of malonyl-CoA (–C6) is followed by the formation of an A-ring. Once synthesized, chalcones can be used up in 3 ways in plant metabolism viz. to synthesize aurones; to produce glycoconjugates (which attributes to the yellow color in flowers) or produce naringenin by chalcone isomerase (CHI). Naringenin ultimately gives rise to anthocyanin through several metabolic changes. The latter pathway is the most followed one. In higher plants (except leguminous plants) CHI “type I” produces 5-hydroxyflavonenaringenin, which is the precursor of virtually all flavonoids (Díaz-Tielas et al., 2016).

Name of the Chalcone 2’,6’-dihydroxy-4’-methoxy-3’,5’-dimethyldihydrochalcone, and 4,4,6-trimethyl-2-(3-phenylpropionyl)-cyclohexane-1,3, 5-trione Rubone Bakuchalcone Mixtecacin 2’,6’-dihydroxy-4’-methoxydihydrochalcone and 2,4’,6’-trihydroxydihydrochalcone Xanthangelols B-E Hybrid flavan-chalcones, desmosflavans A & B, cardamonin, pinocembrin, and crysin Chalcone glycosides 4’-O-(6”-O-galloyl-β-d-glucopyranosyl)2’,4-dihydroxychalcone and 4’-O-(6”-O-galloyl-β-dglucopyranosyl)-2’-hydroxy-4-methoxychalcone;4’-O-β-dglucopyranosyl-2’-hydroxy-4-methoxychalcone 3,2’-dihydroxy-4,3’-dimethoxychalcone-4’-glucoside; 4’-O-(2”‘-O-caffeoyl)-2’,3’,3,4-tetrahydroxychalcone and 2’,4’,3-trihydroxy-3’,4-dimethoxychalcone 2’,3’-Dihydroxy-4’ 6’-dimethoxy-chalcone and its corresponding dihydrochalcone

Plant Source Myrica gale (Myricaceae)

Plant Parts Fruit

References Uyar et al. (1978)

Derris robusta (Fabaceae) Psoralea corylifolia (Fabaceae) Tephrosia woodii (Fabaceae) Linderaum bellata (Lauraceae)

Seed shell Seed Roots Leaf

Chibber et al. (1979) Yu (2005) Dominguez et al. (1983) Tanaka et al. (1984)

Angelica keiskei (Apiaceae) Desmoscochin chinensis (Annonaceae) Entada phaseoloides (Fabaceae)

Root Leaf

Baba et al. (1990) Bajgai et al. (2011)

Stem

Zhao et al. (2011)

Coreopsis lanceolate (Asteracese)

Flower

Shang et al. (2013)

Uvaria dulcis (Annonaceae)

Leaf

Chantrapromma et al. (2000)

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

TABLE 8.1  List of Various Chalcone Derivatives and Their Source from Different Plants Parts

195

196

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Besides, natural occurrence, chalcones can be chemically synthesized by condensation reaction via acid or base catalysis. Few synthetic strategies are discussed below: 1. Claisen-Schmidt Condensation: Condensation of Benzaldehyde and methyl ketone in presence of catalysts which can be either strong bases (sodium hydroxide or potassium hydroxide) or acids (Brønsted acids, Lewis acids like aluminum chloride, and solid acids) (Claisen, 1881). 2. Cross-Coupling Reaction: Two types of coupling reaction are suitable for chalcone synthesis: Suzuki coupling and Heck reaction. Suzuki coupling involves either cinnamoyl chloride coupling with phenylboronic acid or coupling of benzoyl chloride with phenylvinyl boronic acid (Miyaura et al., 1979). As chalcones are structurally stilbene, they can be synthesized by an arylboronic acid or aryl iodide reaction with an unsaturated ketone in the presence of a base and a palladium catalyst (known as classical Heck reaction) (Heck & Nolley, 1972). 3. Wittig Reaction: Possessing a suitable structural backbone of alkene for Wittig reaction, chalcone can be easily synthesized by incubating triphenyl benzoyl methylene phosphorene and benzaldehyde in benzene for 3 days of reflux or 30 h in tetrahydrofuran (THF) (Ramirez & Dershowitz, 1957). 8.2.3 POTENTIAL ROLES OF CHALCONES AGAINST ENVIRONMENTAL STRESS IN PLANTS The genetic code of enzymes involved in the biosynthesis of chalcones and their derivatives have been extensively studied and engineered to investigate the potential role of chalcones in plant stress biology (Figure 8.1). Chalcone synthase (CHS) (EC 2.3.1.74) governs the rate-limiting step in the biosynthesis of naringenin from chalcone and its expression level monitors downstream metabolism of flavonoids that regulates plants’ ability to combat external stresses. This enzyme, therefore, contributes starting materials for various plant metabolites, especially flavonoids, which in turn possess many crucial roles in plants (viz. acting as UV protectants, producing floral pigments and insect repellents) (Dao et al., 2011). Owing to its function, the molecular dissection of the CHS enzyme has been a fascinating area of research for

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

197

many biochemists and molecular biologists and extensive research revealed that CHS is a type III polyketide synthase enzyme (PKS). The enzyme is a homodimer made of monomers of 42–45 kDa molecular weight and having 2 independent active sites (Tropf et al., 1995). Several studies reported that the CHS is only present in an inactive form during normal situations, but on the arrival of different biotic elicitors and abiotic stimuli, CHS is activated, resulting in increased flavonoid biosynthesis. CHS mRNA though present in the cell at non-stressed conditions, but transcription of CHS is only activated under certain environmental stimuli. The half-life of the catalytically active and inactive forms of the enzyme is 6 hours and 18 hours respectively. Reports also reveal that active enzyme disintegrate more rapidly than inactive enzyme (Figure 8.2) (Schröder & Schäfer, 1980). Chalcones can be applied to mitigate diverse abiotic and biotic stress conditions in plants which have been discussed elaborately in this chapter (Figure 8.3).

FIGURE 8.1  Biosynthesis pathways of chalcones and coumarins. Source: Adapted from: Ono et al. (2006); Dao et al. (2011); Stringlis et al. (2019); Zhang et al. (2019).

198

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

FIGURE 8.2  CHS is a homodimer made of monomers of 42–45 kDa molecular weight and having two independent active sites. In the inactive form, it is present during normal conditions, but on the arrival of different biotic elicitors and abiotic stimuli, CHS is activated, resulting in increased flavonoid biosynthesis. CHS mRNA though present in the cell at non-stressed conditions, but transcription of CHS is only activated under certain environmental stimuli. The active CHS enzyme disintegrates more rapidly than the inactive form.

8.2.3.1 ROLES AGAINST ABIOTIC STRESS 8.2.3.1.1 Role Against High-Intensity Light or UV Stress Several studies reported that UV stress induces transcription of CHS genes. A photoreceptor-mediated mechanism regulates this process. The CHS promoter contains a regulatory motif known as G-box (nucleotide sequence CACGTG), which is important in visible light/UV light-mediated stress response alongside other domains that play a crucial role as core promoter elements and drives light-induced CHS transcription (Jenkins et

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

199

FIGURE 8.3  A summary depicting the potential roles of chalcone against various abiotic and biotic stress. Chalcone application against UV, cold, high temperature, drought, and salinity stress triggers stress-related and responsive genes and transcription factors that help to improve the antioxidant system through ROS homeostasis. Chalcone serves as fungicide, anti-viral, and allelopathic agents that minimize infection rate, spore germination and check the growth of weeds.

al., 2001). To further establish the role of light in CHS induction a study was performed where the NtCHS6 gene was isolated from common tobacco and its expression patterns were evaluated. It was documented that the gene expression decreased in tobacco leaves after 1 day of darkness and became nearly undetectable after 2 days. But as the dark-treated plants were kept in light for 2 days, the expression pattern rebounded to the same level as that of untreated control plants, which indicates the light dependency of NtCHS6 expression (Shuai et al., 2017). Exposure to high-intensity light or UV rays leads to the accumulation of a higher amount of CHS active enzyme, flavonoids, and other downstream phenolic compounds which play a protective role by rescuing cellular damage. The production of flavonoids can be linked to (at least in some parts) transcriptional induction of the CHS gene (Chappell & Hahlbrock, 1984). A massive increase in CHS enzyme activity (50-fold) was found after 24 h of high-intensity treatment in Arabidopsis thaliana (Feinbaum & Ausubel, 1988). Accumulated

200

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

anthocyanin was also evident visibly on those treated plants. In the case of a red turnip when UV-A was applied on the swollen hypocotyl, CHS gene was induced, and anthocyanin production was increased many folds (Zhou et al., 2007). Arabidopsis plants overexpressing CHS genes (CHS1, CHS2, CHS3) on exposure to high light treatment (200 μmol photons m–2 s–1), could survive for a longer period (25th day of treatment) and could also retain the photosynthetic capacity for a longer time. This could be due to up-regulation in anthocyanin biosynthesis genes like ANS (anthocyanidin synthase), DFR (dihydroflavonol 4-reductase) leading to greater accumulation of anthocyanins and ROS homeostasis. Whereas transgenic lines with deleted CHS genes died sooner when exposed to the same light stress. Thus, CHS-overexpression could be a useful strategy to mitigate high-intensity light stress (Zhang et al., 2018). Deschampsia antarctica, an antarctic grass, on exposure to artificial UV-B treatment, showed a difference in the amount of DaCHS1 transcripts. Such upregulation in CHS expression can be co-related to the presence of two flavonoids luteolin and tricin. It can be assumed that under UV stress those flavonoids are produced as a defense mechanism by plants (Cuadra et al., 2020). Similarly, Coelogyne ovalis Lindl. under UV-B irradiation (1,500 μJ/m2) revealed the highest expression of CoCHS mRNA after 2 hours of irradiation in leaf than the other parts of the plant body (root and pseudobulb). A similar increase in the transcript level of CoCHS mRNA in the leaf was also observed after the plants were exposed to 24 hours of the dark period (Singh & Kumaria, 2020). Thus, it is quite evident that high-intensity light or UV rays stimulate the CHS gene that results in the accumulation of different chalcones and their derivatives to protect photodamage. This property can hence be used for ensuring or reverting light-induced cellular damages in plants. 8.2.3.1.2 Role Against Chilling Stress Cold stress is the common type of stress faced by most of the crop plants grown in tropical and subtropical regions due to lack of acclimatization impairing plant growth and productivity. But plants grown at higher altitudes have a well-devised mechanism to combat such adverse conditions. Studies have suggested that these plants, in addition to several other adaptation strategies against cold stress, restrict the production of a myriad of secondary metabolites, specially belonging to chalcones. Pn021, PnCHS088, Pn270, PnCHS444, PnCHS768, and Pn847 were the six CHS

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

201

family genes identified in the Antarctic moss Pohlia nutans. When the plant was kept under low-temperature conditions, the expression levels of all the six P. nutans genes were reported to be downregulated (Yao et al., 2019). However, in some other cases, it is observed that the CHS expression is upregulated under cold stress in certain plants. Anthocyanin is an important class of flavonoids that mainly accumulate in stems and leaves under lowtemperature and changes in light intensity. Two main enzymes responsible for anthocyanin biosynthesis are phenylalanine ammonia-lyase (PAL) and CHS. Both CHS and PAL mRNA were found to be accumulated in the leaves of Arabidopsis under cold stress in a light-dependent manner (Leyva et al., 2020). Coelogyne ovalis Lindl. on cold treatment at 4°C showed the highest transcript level of CoCHS mRNA after 72 hours of treatment in leaf than the other parts of the plant body (root and pseudobulb) (Singh & Kumaria, 2020). So, it is quite evident that chalcones have the potential to protect from the adversities of chilling stress in plants. Further investigation is thus required to provide a comprehensive idea about the role of chalcones in mitigating cold stress-induced atrocities in plants and their application in agriculture. 8.2.3.1.3 Role Against High-Temperature Stress High temperature (HT) stress limits plant growth, metabolism, flower production, net productivity and fertilization success in various plants worldwide. Plants generally possess several acclimations, adaptive or avoidance mechanisms to cope with HT situations. Across the States, the flower color of Ipomoea purpurea is defined by the action of 2 polymorphic loci ‘W’ and ‘A.’ All the different genotypes can be identified according to the color of the corolla limb. When pollens from plants grown at either high or low temperature were put on the stigmas of the plants grown at HT, fertilization success was greatly reduced. But pollen from HT grown plants has reduced fertilization success compared to that of low temperature grown plants when the temperature of the stigma (maternal temperature) is low. However, interestingly, this was observed only in those plants which carry the recessive ‘aa’ gene. At the same time, these plants also produce lesser flower in low temperature and high light intensity. This observation made it to the conclusion that the CHS-D, which is expressed mainly in floral parts, is attributed to the ‘A’ locus. This CHS is the key enzyme for the production of chalcone which leads to the concomitant production

202

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

of flavonoids. Flavonoids may play a role in alleviating the effect of heat stress on fertilization success. Hence the plant which has the recessive gene could not produce the necessary secondary metabolites hence are unable to achieve fertilization success or produce a greater number of flowers (Coberly & Rausher, 2003). In eggplant (Solanum melongena L.) the peel color is responsible for its economic importance. The peel color of eggplant is determined by anthocyanin content which is in turn regulated by the expression patterns of CHS genes. 7 CHS putative genes (SmCHS1-7) show different expression patterns under heat stress conditions. Upon examining, it was observed that under 38°C and 45°C treatment, SmCHS5, SmCHS6, and SmCHS7 were continuously down-regulated, while SmCHS4 was up-regulated at the treatment of 38°C for 3 hours but showed little change at 45°C in peel (Wu et al., 2020). So, it can be asserted that chalcones have a well-defined role associated with high-temperature stress. 8.2.3.1.4 Role Against Drought Stress Due to climate change and uncertainty in the time and amount of precipitation, every year drought has become a common problem for crop plants that lead to major yield loss. Increased expression of CHS during drought stress can attribute to the role of chalcone in mitigating drought stress. Generally, CHS genes are highly expressed in floral organs which contain anthocyanin pigment. But sometimes they are expressed in other plant organs also. In those cases, they involve in the biosynthesis of other flavonoids which have different protective roles. NtCHS6 was strongly induced in leaves after drought stress, but in the normal condition, they showed a weak expression level in floral organs. This indicates NtCHS6 has a preventive role in drought stress. After analyzing the cis-elements of the promoter region, it was observed that NtCHS6 have 3 MYB recognition site (WAACCA, YAACKG, CNGTTR) and four MYC recognition site shaving same sequence (all the four sites having the similar sequence of CANNTG). All of these 7 sites are reported to be responsible for water stress response which further confirms the role of NtCHS6 to mitigate drought stress (Shuai et al., 2017). Transgenic Arabidopsis produced by overexpressing the CHS gene from Abelmoschus esculentus, showed augmented activity of enzymatic antioxidants [AtSOD (superoxide dismutase) and AtPOD (Peroxidase)] and marked

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

203

decrease in H2O2 and malondialdehyde (MDA) contents when exposed to osmotic stress by supplementing the media with 300 mM mannitol for 2 weeks (Wang et al., 2018). CHS gene over-expressed transgenic Nicotiana tabacum variety ‘K326’ seedlings on exposure to drought stress-induced through water deprivation for 14 days, showed remarkably higher relative water content (RWC) than the wild type plants. Both, leaf MDA and the H2O2 content were higher in the control plants than the transgenic plants, which signify the probable role of the CHS gene in abiotic stress mitigation through ROS homeostasis (Hu et al., 2019). 8.2.3.1.5 Role Against Salinity Stress Two Transgenic tobacco lines were generated either by overexpressing the EaCHS1 gene under CaMV (the cauliflower mosaic virus) 35S promoter (EaCHS-OE) and by silencing the EaCHS1 gene through RNAi (CHSRNAi). EaCHS1 is responsible for chalcone production in Eupatorium adenophorum. After that, the 10 days old transgenic plants were given salinity stress by growing them in MS (Murashige and Skoog medium) media supplemented with different concentrations of NaCl (0, 100, and 300 mM) for a week. After salt treatment, chlorophyll content and SOD and CAT activities were increased in the CHS gene overexpressed transgenic line. At the same time, MDA and H2O2 (hydrogen peroxide) content were decreased in the EaCHS-OE in comparison to the wild type and CHS-RNAi transgenic line. This result suggested that the EaCHS1 gene may take part in ROS homeostasis during salt stress (Lijuan et al., 2015). In another experiment transgenic Arabidopsis was produced by overexpressing the AeCHS gene from Abelmoschus esculentus. The transgenic seedlings were given salt stress by supplementing the media with 200 mM NaCl for 2 weeks. The H2O2 and MDA content in the leaves of salt-treated transgenic seedlings was lower than similar wild type ones. But the activity of AtSOD (Superoxide dismutase) and AtPOD (Peroxidase) is also upregulated in the transgenic lines after salinity stress. This indicates AeCHS gene mitigates ROS generation during salinity stress by activating antioxidant enzymes (Wang et al., 2018). Transgenic Arabidopsis plants overexpressing Chalcone-O-methyltransferase gene (pvChOMT) from Phaseolus vulgaris L. when subjected to salinity stress by gradually supplementing the media with different concentrations of NaCl, the transgenic plants showed better growth, wider leaf area, better root elongation, higher rates of seed germination,

204

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

greater RWC and increased proline accumulation in the leaves than the wild type plants. The expression profiles of different salt stress-related transcription factors like DREB2A (dehydration-responsive element-binding protein 2a), MYB2 (MYB domain protein 2), RD26 (responsive to desiccation 26) and genes like RAB18 (responsive to ABA 18), RD29B (responsive to desiccation 29B), P5CS1 (Delta1-pyrroline-5-carboxylate synthase 1), and P5CS2 (Delta1-pyrroline-5-carboxylate synthase 2) were also up-regulated in the transgenic lines (Niron & Türet, 2020). The findings hence elucidate the fact that chalcone-O-methyltransferase gene activity might alleviate salinity through upregulation of several downstream transcription factors and genes related to salt stress. Higher accumulation of CoCHS mRNA in the leaves and pseudobulbs of Coelogyne ovalis Lindl on exposure to salinity, also support the protective role of chalcones against salinityinduced stress (Singh & Kumaria, 2020). These findings thus validate the propitious role of chalcones in combating salinity stress by the maintenance of the antioxidant status of the plants and alteration in the accumulation of essential flavonoids and other crucial secondary metabolites. 8.2.3.2 ROLES AGAINST BIOTIC STRESS 8.2.3.2.1 Role as Fungicide Several naturally occurring chalcones and their derivatives are found to be toxic against a variety of plant fungal pathogens and appear to be more effective than commercially available fungicides. Colletotrichum falcatum, Curvularia pallescens, Ceratocystis paradoxa, Fusarium moniliforme, Periconia atropurpurea and Ustilago scitaminea are potential targets of chalcone compounds (Rao et al., 1994). Soybean cultivar Williams 82 over-expressing GmCHI1A (chalcone isomerase 1a) gene was isolated from Glycine max upon infection with Phytophthora sojae, exhibited lesser extension and length of disease lesion at the injection site and decrease in the accumulated biomass of the pathogen in the hairy roots than the control plants (empty vector-expressing hairy roots). Thus, over-expression of GmCHI1A can be beneficial in reducing the susceptibility of plants towards Phytophthora sojae (Zhou et al., 2018). Besides, several naturally occurring chalcones can be targeted as anti-fungal agents against a wide range of fungal pathogens (Table 8.2).

Name of Chalcone Compound 2’,4’-dihydroxy-3’-methoxychalcone

Plant Source Zuccagnia punctata

2’,3,4,4’-tetrahydroxy-3’-geranylchalcone 2’,4’-dihydroxy-3’,5’-dimethyl-6’-methoxychalcone and stercurensin

Artocarpus nobilis Myrica serrata

Fungal Target Biological Activity Fusarium verticillioides (MFC – 100 µg/ml) Growth inhibitor Fusarium graminearum sensustricto (MFC – 50 µg/ml) Cladosporium cladosporioides Cladosporium cucumerinum

Inhibit spore germination Acts as a growth inhibitor

References Jimenez et al. (2014) Jayasinghe et al. (2004) Gafner et al. (1996)

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

TABLE 8.2  List of Different Naturally Occurring Chalcone Derivatives, Their Source and Potential Role as Anti-Fungal Agents

205

206

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

8.2.3.2.2 Role as an Anti-Viral Agent Although the number of studies reporting antiviral property of chalcone is relatively scarce, few interesting ones suggest that chalcones are active against several plant viruses, including tomato ringspot virus (ToRSV) (Onyilagha et al., 1997; Malhotra et al., 1996), cauliflower mosaic virus (CaMV), and tobacco mosaic virus (TMV) (Zhou et al., 2018), etc., 2-hydroxychalcone can reduce the infection of ToRSVin Chenopodium quinoa (Malhotra et al., 1996). Later 21 different chalcones with a higher level of antiviral properties were found. Among them, 4 compounds-2’,3’,4’,4-tetrahydroxychalcone (69%), 4’,3,4-trimethoxychalcone (49%), 2\4’-dihydroxy-3,4,5-trimethoxychalcone (37%) and 2’,4’-dihydroxychalcone (52%) showed the best inhibitory effect against ToRSV when applied on leaves of Chenopodium quinoa (Onyilagha et al., 1997). Such antiviral activities are induced by hydroxylation at 2’,3’,4’ positions in the A-ring and at C-4’ positions in the B-ring. But it can be inhibited or lowered by C-5’ hydroxylation and methoxylation in the B-ring respectively (Onyilagha et al., 1997). 8.2.3.2.3 Role as Allelopathic Agents Owing to phytotoxic properties, chalcones are useful for weed control agents and selective herbicides. Several investigations led to the findings that chalcones have negative effects on the germination of Plantago lanceolata and Lactuca sativa; early root growth of Amaranthus retroflexus, Echinochloa crus-galli, P. lanceolate and development of adult Arabidopsis (DıazTielas et al., 2013). Kukulcanin B and heliannone A (chalcones isolated from sunflower), was reported to inhibit shoot growth and germination of Lycopersicon esculentum and Hordeum vulgare (Macías et al., 1997). The variation in the biological action of chalcones not only relies on the number and position of the free hydroxyl group present in each molecule but also on the concentration at which they were applied to the target plant. In Zea mays, 100 and 200 μM chalcone inhibited root growth and total fresh weight but no effect could be found at higher or lower concentrations (Chen et al., 2004). Chalcones are supposed to hinder the catalytic effect of 2 enzymes involved in the phenylpropanoid pathway, phenylalanine ammonia lyase (PAL) and 4-Coumarate CoA Ligase, both attributing to lignin production (Chen et al., 2004, 2011; Yun et al., 2009). As lignin biosynthesis is halted

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

207

due to chalcone application the normal growth and development of the plant is hampered. A low concentration of trans-chalcones (35 μM) was found to inhibit root growth of Arabidopsis seedlings by inducing PCD (Díaz-Tielas et al., 2012). Several detrimental effects such as loss of mitochondrial membrane potential and mitochondrial condensation, photosynthetic pigment and organellar degradation, activation of cell detoxification mechanisms (Golgi complex, vacuoles, and autophagosomes), and lipid accumulation have been documented in plants on the application of chalcones (Díaz-Tielas et al., 2012, 2016). In a study to check the effects of (E)-Chalcone on photosynthesis, seeds of Arabidopsis thaliana were treated with different concentrations of (E)-chalcone [0 μM (control), 35 μM (IC50) and 73 μM (IC80)]. It was documented that cotyledons were green at the beginning, but degreening started on the 5th day. With 35 μM (IC50) (E)-chalcone, the cotyledons became chlorotic on the 13th day of treatment. Transmission Electron Microscopy showed disruption of stromal and granal thylakoids and reduced number of grana per chloroplast which suggests that chalcone enhances photo-oxidation. Chalcone-treated plants are unable to dissipate heat produced during photo-oxidation as it also inhibits the carotenoids, xanthophylls, lutein, and β-carotene (Jahns & Holzwarth, 2012). Hence, the photosynthetic system begins more susceptible to light damage. Chalcone alters the pH gradient of the chloroplast (which disrupts the xanthophyll cycle. As a result, the photo-protective functions of xanthophylls were compromised (Díaz-Tielas et al., 2017). Very shortly after addition, chalcone triggers a rapid diffusion of membrane potential that may affect membrane permeability (Flickinger et al., 2010). Later effects of chalcone treatment include ROS accumulation as a result of photo-oxidation, pigment degradation, bleaching, and eventually cell death in Arabidopsis (Díaz-Tielas et al., 2012). Chalcone ‘okanin’ (2’,3’,4’,3,4 Pentahydroxychalcone) serves as an inhibitor of Phosphoenolpyruvate carboxylase (PEPC), which is needed for carbon fixation in C4 plants. Binding studies reveal that okanin has an IC50 value of 600 nM and a 45-fold selectivity towards C4 PEPC over C3 PEPC (Nguyen et al., 2016). In a recent study, it was found that 24 chalcone derivatives show inhibitory effects on PSII (Photosystem II) of spinach (Spinacia oleracea) leaves and among them, (E)-3-(4-bromophenyl)-1-(4fluorophenyl)prop-2-en-1-one and (E)-Chalcone) showed the best results (applied in a concentration of 100 µM) when evaluated via chlorophyll-a fluorescence measurement. They also reduced the amount of trapped energy

208

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

in PSII reaction centers by reducing the number of them. These two chalcone derivatives were also found to reduce the root biomass of Ipomoea grandifolia weed. At the same time, they did not have any negative effect on the dry biomass (of both root and aerial parts) of crop plants like Zea mays and Phaseolus vulgaris. Hence these two chalcones can be used as a potential natural herbicide (Pádua et al., 2021). Therefore, owing to the photosynthesis inhibition property of chalcones and their derivatives, they can be employed as selective and sustainable herbicides in place of harmful chemicals. 8.3 COUMARINS Coumarins were first isolated from the plant Coumarouna odorata (Dipteryx odorata) in the year 1820 but initially, it was misidentified as benzoic acid (Vogel, 1820), however, in the same year, Nicholas Jean Baptiste Gaston Guibourt independently isolated Coumarin. He depicted that as a new chemical entity. Later, following its source plant he named the new substance “Coumarin” (Guibourt, 1869). Coumarins are a wide family of secondary metabolites with a vast range of pharmacological property including antimicrobial, anti-coagulant, anti-inflammatory, neuroprotective, anti-diabetic, anti-convulsant, anti-proliferative (Srikrishna et al., 2018) and anti-aging (Nam & Kim, 2015). They are also greatly explored by food industries due to their antioxidant (Santra & Banerjee, 2020) and anti-fungicidal activities (Mark et al., 2019). Interestingly, benzocoumarins extracted from the rhizomes of Juncus acutus reportedly show an inhibitory effect on the growth of green alga Pseudokirchneriella subcapitata. However, among the seven isolated benzocoumarins, some shows bio-stimulatory effect on the algal growth at low concentration (2.5 mg/L) but manifest inhibitory activity at higher concentrations (40 mg/L) (DellaGreca et al., 2003). Due to its convenient chemical scaffold, coumarins are extensively used in the medicinal industry for new drug design (Guibourt, 2014). In plants, coumarin gives protection from both biotic and abiotic stress condition and provide the plant survivable benefits. 8.3.1 STRUCTURE AND PROPERTIES Coumarins belong to the huge class of aromatic molecules called benzopyrones. Bezopyrone is organic heterocycles and can be recognized as two

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

209

six-membered rings fused with one of them being a benzene ring, and the other containing an alkene and ester functional group inside the ring. In coumarin, the two adjacent hydrogen atom of the benzene ring is replaced by a lactone chain (Wu et al., 2009). According to systemic nomenclature, they are called benzopyrone (2H-1-benzopyran-2-one) which is established by IUPAC (International Union of Pure and Applied Chemistry). In most cases, coumarins are oxygenated at C-7 positions forming 7-hydroxy coumarin or commonly known as Umbelliferone (Venugopala et al., 2013). Due to its unique chemical structure, substitution can occur at many sites. As a result, there is an enormous amount of naturally occurring compounds with biological and pharmacological properties, all sharing the same coumarin nucleus. Based on the structural dynamics, the natural coumarins can be of diverse types (Table 8.3). TABLE 8.3  List of Different Classes of Coumarins and Their Respective Pharmacological Benefits Class

Example

Simple coumarins

Esculetin

Furanocoumarins

Pharmacological Benefits Antiadipogenic, Antioxidant

References Witaicenis et al. (2010)

Novobiocin Coumarin

Neuroprotective Antibacterial Chain (1992) Anti-inflammatory Piller (1975)

Psoralen

Anticancer Antifungal

Bourgaud et al. (2006)

Methoxsalen

Anti-TB Cytochrome P450

Kharasch et al. (2000)

Inhibitor Dihydrofuranocoumarins Anthogenol Antibacterial – – Pyranocoumarins Grandivittin Antibacterial •  Linear Agasyllin Antibacterial •  Angular Inophyllum A, B, Anti-viral C, E, P, G1, G Calanolide A, B, Anti-viral and F Bicoumarins Dicoumarol Anticoagulant Phenylcoumarins Isodispar B Anti-inflammatory Isocoumarin Thunberginols Antidiabetic

Chakthong et al. (2012) Basile et al. (2009) Basile et al. (2009) Istry et al. (1993) Gustafson et al. (1992) Poole & Poole (1994) Crombie et al. (1966) Pal et al. (2011)

210

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Coumarins are crystalline lactones. They are low molecular weight, soluble in most organic solvents, highly bio-available structure with a bitter taste. They have a sweet smell, resembling the smell of vanilla and hence are used as flavorings agents in the food industry (Annunziata et al., 2020). Some of the coumarin derivatives also have luminescent properties. It happens due to the intrinsic charge transfer properties of electron-rich conjugated pi-pi systems (Pereira et al., 2018). Therefore, they can be utilized as photo-cleavable protecting groups or fluorescent probes (Tasior et al., 2015). Rodents generally metabolize coumarins to 3,4-coumarin epoxide, a toxic and chemically unstable product, which after further downstream metabolism may give rise to liver cancer in rats (Vassallo et al., 2004) and lung cancer in mice (Born et al., 2003). However, humans metabolize coumarins to 7-hydroxycoumarins which have lower toxicity. So, it can be assumed that coumarins are less toxic to humans. For human beings, a tolerable daily intake of coumarin is 0.1 mg/kg body weight (German Federal Institute for Risk Assessment). The Occupational Safety and Health Administration (OSHA) of the United States do not classify coumarin as a carcinogen for humans. 8.3.2 SOURCE AND SYNTHESIS Coumarins are distributed among all life forms. It is found in different plants, animals, and also micro-organisms. In the plant kingdom, it has been reported in the members of several dicotyledonous families (Harborne, 1960; Bourgaud et al., 2006) with maximum occurrence in the members of Apiaceae (3041 different coumarins), followed by Rutaceae (1683) and Asteraceae (830) (Matos et al., 2015). Coumarins and their derivatives are also documented in different monocot families, such as Graminae and Orchidaceae. Linear furanocoumarins are primarily found in Rutaceae, Fabaceae, Apiaceae, and Moraceae (Wu et al., 2009). But certain coumarin derivatives can also be plant-specific (Table 8.4). Marine sponge (Axinella corrugate) was found to be the source for two coumarin derivates, namely esculetin-4-carboxylic acid methyl ester and esculetin-4-carboxylic acid ethyl ester. The ethyl ester derivative was found to be an in vitro inhibitor of SARS 3CL-protease and can inhibit DNA polymerization in-vivo (De Lira et al., 2007) Presence of Coumarin is also recorded in the aflatoxin of fungal micro-organisms named Aspergillus flavus (Sonie, 2010). Coumarins, like chalcones, are also produced through the phenylpropanoid pathway, downstream of the isoflavone metabolism (Bourgaud et al., 2006). Moreover, p-coumaroyl-CoA (intermediate of coumarin production), serves as the substrate for the CHS gene to produce chalcones and other flavonoids.

Name Dicotyledons Samidin, Anomalin, Calipteryxin I, soimperatorin, Deltoin Auraptene, trans-gleinadiene, 5,7-dimethoxy-8-(3-methyl2-oxo-butyl) coumarin, Toddalenone 5-methoxy-6,7-methylenedioxycoumarin, Ayapin, Prenyletin, Prenyletin-methyl-ether Umbelliferone, bruceol Eaculetin, scopoletin, soscopoletin (+)-(2’S,3’R)-3-Hydroxymarmesin, bergapten, psoralen, umbelliferone Glycoside of umbelliferone Monocotyledons Scoparone

Plant

Parts

References

Seseliresinosum (Umbelliferae) Murraya paniculata (Rutaceae)

Root Leaves

Tosun et al. (2006) Aziz et al. (2010)

Pterocaulon polystachyum (Asteraceae)

Aerial parts Stein et al. (2006)

Dipteryx odorata (Fabaceae) Olea africana (Oleaceae) Brosimum gaudicbaudi (Moraceae)

Seed Bark Root

Sarker & Nahar (2017) Nishibe et al. (1982) –

Stellera chamaejasme (Thymelaeaceae)

Root

Jiang et al. (2002)

Dendrobium sp. (Orchidaceae)

Powder of Caulis dendrobii Leaf

Xu et al. (2010)

Aesculin

Anthoxanthum puelii (Graminae)

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

TABLE 8.4  List of Different Coumarins Along with the Sources (Plant Parts from Where They can be Extracted)

Davies & Ashton (1964)

211

212

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

In Angelica decursiva, the biosynthesis of coumarin begins with the production of phenylalanine through the shikimate pathway followed by conversion into cinnamic acid catalyzed by PAL enzyme. Cinnamic acid is then hydroxylated by the enzyme C4H (cinnamate 4-hydroxylase) to form p-coumaric acid (Wu et al., 2009). The p-coumaric acid can also be directly generated from phenylalanine by the enzyme TAL (tyrosine ammonia-lyase) and converted to p-coumaryl CoA by the aid of enzyme 4CL (4-Coumarate: Coenzyme A Ligase). Thereafter, it is hydroxylated at 2’ and 4’ positions forming 2,4-dihydroxycinnamoyl-CoA by C2’H (P-Coumaroyl Coa 2’-Hydroxylase) followed by spontaneous cis/trans isomerization and lactonization that generates 7-hydroxy coumarin or Umbelliferone. Classically, it is considered as the parent molecule from which other coumarin derivatives like Osthenol, demethylsuberosin are produced by the enzyme prenyltransferase. These reaction steps are generally observed in the members of Apiaceae or other plants containing Umbelliferone (Zhao et al., 2019). In other plants like Arabidopsis, where scopoletin or esculentin is the main coumarin, some changes in steps are observed. Few steps, in the beginning, remain similar. But, in this case, p-coumaroyl CoA can act as a substrate for HCT (Hydroxycinnamol-coenzyme A shikimate/quinate hydroxycinnamoyltransferase) enzyme to p-coumaroyl shikimate. p-coumaroyl shikimate is converted to Caffeoyl shikimate by 4CL enzyme. This Caffeoyl shikimate also can act as a substrate for HCT to produce CaffeoylCoA. This specific product acts as a metabolic bifurcation for lignin biosynthesis and coumarin production. Caffeoyl CoA with the help of the enzyme CCoAOMT (caffeoyl CoA 3-O-methyltransferase) produces Feruloyl CoA. Feruloyl CoA provides another bifurcated route for lignin synthesis. Caffeoyl CoA (through some intermediate steps) and Feruloyl CoA, both are hydroxylated to produce 6-hydroxyl caffeoyl CoA and 6-hydroxyl Feruloyl CoA, respectively, by enzyme F6’H1 (Feruloyl-CoA 6’-hydroxylase-1) (Kai et al., 2008). Again, 6-hydroxyl Caffeoyl CoA and 6-hydroxyl Feruloyl CoA are transformed into Esculentin (Vanholme et al., 2019) and scopoletin (Kai et al., 2008) respectively through trans/cis isomerization of the sidechain and lactonization. This specific step is spontaneous in light but can be mediated in the dark by the enzyme COSY (coumarin synthase). Esculetin and scopoletin later can be inter-converted and act as a precursor molecule for the synthesis of other coumarins (Stassen et al., 2021). Hydroxylation of Scopoletin by SCOPOLETIN 8-HYDROXYLASE (S8H) (Siwinska et al., 2018; Tsai et al., 2018) gives rise to coumarin fraxetin and coumarin sideretin is generated through hydroxylation of fraxetin by the enzyme cytochrome P450 enzyme CYP82C4 (Rajniak et al., 2018).

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

213

8.3.3 POTENTIAL ROLES OF COUMARINS AGAINST ENVIRONMENTAL STRESS IN PLANTS Coumarins are generally produced in young leaves and are transported from one place to another via the phloem. The glycosylated form of the coumarin is loaded into the phloem through the AtSUC2 transporter. The aglycon form of the coumarin is very much toxic and highly reactive. Hence for easier storage and transport, Coumarins are converted into their non-toxic UDP-glycosylated form by the enzyme UDP-glycosyltransferases present in the cytoplasm. After their glycosylation coumarins are transported to the vacuole by ATP-binding cassette (ABC)-transporters or multidrug and toxic compound extrusion proteins. Upon stress conditions, coumarin glycosides can be de-glycosylated to biologically active aglycone and be released into the rhizosphere or apoplast. De-glycosylation is mediated by β-glucosidase enzymes (BGLUs). To maintain coumarin glycosides during the non-stress condition, BGLUs are present in cell walls, apoplasts, and endoplasmic reticulum bodies and glycosyltransferase are in vacuole and cytoplasm, respectively. In this way, they are spatially separated. Only upon receiving signals mediated tissue damage and stress coumarin glycosides come in contact with BGLUs (Figure 8.4) (Stassen et al., 2021). Coumarins are intricately related to the iron acquisition in plants. Recent developments reveal that plants when subjected to iron deficiency, not only induce expression of canonical iron-deficiency responsive genes but also upregulate expression of genes associated with phenylpropanoid pathway and coumarin biosynthesis (Stassen et al., 2021). Besides, Coumarins reportedly have diverse roles against various plant abiotic and biotic stress. 8.3.3.1 ROLES AGAINST ABIOTIC STRESS 8.3.3.1.1 Role Against Salinity Stress Salinity stress has become a major challenge in agricultural science negatively affecting the annual yield. Harmful effects of salinity stress mainly include hindrance in plant growth and osmotic disequilibrium due to increased uptake of sodium (Na+) and chloride (Cl–) ions in plants. Salinity also triggers the generation of ROS that results in oxidative stress and cellular damage (Isayenkov & Maathuis, 2019). Priming with coumarin could restore root and shoot length, dry weight, fresh weight and moisture content of wheat grains exposed to NaCl induced

214

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

FIGURE 8.4  Coumarins are produced in young leaves and are transported to other parts via the phloem in the glycosylated form through AtSUC2 transporter. The aglycon form of the coumarin being very toxic is converted into their non-toxic UDP-glycosylated form by the enzyme UDP-glycosyltransferases present in the cytoplasm and are transported to the vacuole through ATP-binding cassette (ABC)-transporters or multidrug and toxic compound extrusion proteins. Upon stress conditions, coumarin glycosides are de-glycosylated to biologically active aglycone and released into the rhizosphere or apoplast. De-glycosylation is mediated by β-glucosidase enzymes (BGLUs).

salinity stress. The sugar content, proline content, phenolic content, flavonoid content, activities of PAL, POD, and total antioxidant capacity [amount of non-enzymatic antioxidant] were also increased in the primed plant. An increment in the sugar and proline content contributed to the maintenance of cellular osmotic potential by allowing roots to absorb the required amount of water and maintain cell turgidity. Under optimal growth conditions, the most induced phenolic acids in COU primed plants are salicylic, syringic, gallic, and ferulic acids whereas, under salt stress, the most concentrated phenolics were chlorogenic (59%) and salicylic (54%) acids in shoots of COU primed

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

215

seedlings. Thus, coumarin may have a direct or indirect regulatory role in the shikimic acid pathway leading to the accumulation of phenolics and flavonoids, together resulting in better non-enzymatic antioxidant mechanism due to their free radical scavenging activity. However, the coumarin primed seedlings did not possess increased coumarin content within the shoot, implying that exogenous COU may serve as a precursor for COU derivatives (like esculetin and scopoletin or other related compounds) that in turn strengthen the antioxidant defense machinery of the plants (Saleh & Madany, 2015). It was already a known fact that germination rate, plant growth, chlorophyll synthesis gets greatly hampered under salinity stress. To check the efficiency of coumarin to alleviate such stress those stress markers were evaluated in the transgenic lines (plants over-expressing coumarin synthesis gene, GmF6’H1) as well as in the WT. Germination rates were found to be higher in the transgenic line than the wild type plants subjected to salinity. At the seedling stage, the transgenic plants showed improved growth and vigor and greater chlorophyll content. Higher accumulation of endogenous coumarin owing to greater expression of GmF6’H1 gene in transgenic plants validates the protective role of coumarins against salt-induced stress in plants (Duan et al., 2019). In another study, Solanum lycopersicum pre-treated with COU (20 and 30 Μm) when exposed to salinity stress (NaCl, 100 and 160 mM) resulted in better growth. Both root and shoot dry weight, as well as fresh weight, increased than the control plants (without coumarin). Stress tolerance markers like leaf RWC, proline content, chlorophyll, and carotenoids content were also uplifted. Besides, coumarin treatment increased levels of Ascorbate and DHA, GSH, and GSSG ratio and activity of antioxidant enzymes like APX, DHAR, GR, GPX, GST, SOD. At the same time activity of MDHAR and CAT significantly decreased. Under salinity stress, methylglyoxal content and activity of Gly I (glyoxalase I) and Gly II (glyoxalase II) increase. However, the seedlings pretreated with COU showed a reduction in methylglyoxal accumulation along with augmented Gly I and Gly II activities. It can thus be inferred that coumarin can shield plants from salinity stress by upregulating the antioxidant machinery and methylglyoxal detoxification (Parvin et al., 2020). 8.3.3.1.2 Role Against Drought Stress Rice seeds grown under drought conditions on treatment with either crude extract or the living hyphae of endophytic fungi collected from various

216

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

tissues of Myricaria laxiflora at pre-and post-flooding conditions revealed that living hyphae did not affect drought stress mitigation whereas the crude extract of some endophytic fungal hyphae augmented the survival rate of rice seedlings under drought stress. The latter seedlings also exhibited low proline and MDA content, decreased membrane permeability and higher water content. On investigation and analysis of the crude extract, a coumarin analog named (Z)-N-(4-hydroxystyryl) formamide or NFA gradually gets converted to an isomer called (E)-N-(4-hydroxystyryl) formamide or ENFA was identified. This compound supposedly possesses antioxidant properties that help to mitigate the effects of drought stress. Rice seedlings treated with purified NFA solution and exposed to drought stress showed better survival rates and also recorded the optimum activity of antioxidants enzymes (SOD, POD) and Hsp 70 (involved in the metabolism of ROS) (Qin et al., 2019). 8.3.3.1.3 Role Against Heat Stress Seeds of Bituminaria bituminosa were collected from 2 different plant populations. One was growing in Murcia, Spain, at Llano del Beal (LB) and were exposed to low winter temperature and heavy metal-contaminated soil and the other one is growing at Calnegre (exposed to mild winter and salinity stress). Seeds of both populations were sown in pots of vermiculite, with day/night temperature being 22/17°C. Around 10 days after sowing, they were transferred to hydroponic culture and grown for 23 days. Then they were given heat stress by increasing the temperature of the growth chamber from 22/17°C to 33/22°C over 9 days. In the hydroponic culture at HT furanocoumarin levels (mainly Angelicin and Psoralen) were increased more in the Calnegre population than the ‘LB’ population. Moreover, in the LB population after heat treatment angelicin content of root and psoralen content of leaf is dropped (Walker et al., 2012). 8.3.3.2 ROLES AGAINST BIOTIC STRESS A huge amount of annual yield loss in soybean is there due to Asian soybean rust (SBR), caused by the fungus Phakopsora pachyrhizi (Pp). Continual and excessive usage of synthetic fungicide can lead to fungicide resistance. Hence, researchers are always curious to find biotic or organic antifungal alternatives. Study shows that treatment of Pp uredospores with 500 µM scopoletin can significantly decrease the germination rates of the fungus. But its glycoside,

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

217

scopolin is unable to do so. It was also observed that another coumarin, esculetin together with antioxidant ascorbic acid can also inhibit Pp development significantly at 500 µM and 1,000 µM concentration. But both of them are less effective than scopoletin at both inhibiting Pp spore germination and development of pre-infection. Hence, coumarin can be used as a natural fungicide against Phakopsora pachyrhizi infection (Beyer et al., 2019). Priming of the sunflower seed with 0.3 mM COU can decrease the severity of Charcoal Rot Disease caused by Macrophomina phaseolina by 50%, thereby providing better protection and reducing the length of stem lesions. Coumarin at a low dose (0.3 mM) can increase the chitinase activity and at a higher dose (3.0 mM) can increase the β-1,3-glucanase activity. The amount of insoluble and soluble sugar content also increases in the infected plant after coumarin treatment (Al-Wakeel et al., 2013). Another approach of biological control is the application of exogenous compounds as priming agents to prevent pathogen attacks. Application of such compounds elevated the accumulation of endogenous coumarin. Coumarins have a ROS scavenging role during pathogen attacks (Stringlis et al., 2019). Exogenous application of priming agent acibenzolar-S-methyl (ASM) is used to protect the sunflower plants from the fungus Puccinia helianthi causing rust disease. The priming agent prevents the spore germination and appressorium formation of the fungus. Studies show after the application of ASM a huge amount of scopoletin and ayapin were accumulated inside the plant leaves and also on the leaf surface (Prats et al., 2002). External stimuli from beneficial bacteria induce the MYB72 transcription factor. This same transcription factor is also regulated by FIT (fer-like iron deficiency-induced transcription factor). FIT is a transcription factor that can monitor interior iron level and is stimulated during iron deficiency. After induction, MYB72 switches on one of its target genes called BGLU42 (Beta Glucosidase 42) in Arabidopsis (Van der Ent et al., 2008). It encodes for glycosidases that remove the sugar group from coumarin scopolin to convert it into its active form scopoletin. Scopoletin is released with root exudates in the rhizosphere where it performs a dual role. On the one hand, it helps in iron mobilization and uptake. On the other, due to its antimicrobial activity, it kills all the sensitive pathogens. This kind of sensitivity is only found in those organisms which harm plant growth. As a result, only the tolerant beneficial bacteria survive in the rhizosphere. They help to develop ISR in plants and protect the plant from future diseases. In this way, the MYB72 and BGLU42 take part in potential crosstalk between iron deficiency and the development of ISR (Lundberg & Teixeira, 2018; Stringlis et al., 2019).

218

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

8.4 CONCLUSION Due to the uprising population, loss in productivity and increasing demand of the consumers for chemical-free crops, it has become a major challenge for scientists to find naturally occurring compounds as potential alternatives to chemical fertilizers that are not only biohazard-free but can also increase the yield of economically important crop plants by combatting adverse stress situations. Chalcones and Coumarins are very strong and propitious contenders for this purpose as they are plant-derived and possess several beneficial properties to promote plant growth and provide protection against various environmental stress. Though being a secondary metabolite, both chalcone and coumarin can be externally applied to the plants for both biotic and abiotic stress management. It was also found that chalcones are more efficient than the commercially available fungicide, pesticides, etc. Owing to allelopathic properties, chalcones can also be used for weed management. Coumarins can promote nutrient uptake (nitrate, phosphate, iron) by the plant when resources are in a limited condition. Hence, coumarins can be used as natural fertilizers. Unfortunately, the investigation of their beneficial roles in agriculture has been focused on by the scientific community only for the past few years. More extensive study is required to understand the mechanism of action in detail, their advantageous role in alleviating environmental stress, their ability to increase plant productivity, the mode of application and safety limits. Only then use of chalcone and coumarin in agriculture can be expanded to increase the quality and quantity of the yield. KEYWORDS • • • • • •

chalcone synthase coumarins environmental stress fungicide malondialdehyde scopoletin

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

219

REFERENCES Al-Wakeel, S. M., Gabr, M. M. A., Abu-El-Soud, W. M., & Saleh, A. M., (2013). Coumarin and salicylic acid activate resistance to Macrophomina phaseolina in Helianthus annuus. Acta Agron. Hungarica, 61(1), 23–35. Annunziata, F., Pinna, C., Dallavalle, S., Tamborini, L., & Pinto, A., (2020). An overview of coumarin as a versatile and readily accessible scaffold with broad-ranging biological activities. Int. J. Mol. Sci., 21(13), 1–83. Aziz, S. S. S. A., Sukari, M. A., Rahmani, M., Kitajima, M., Aimi, N., & Ahpandi, N. J., (2010). Coumarins from Murraya paniculata (Rutaceae) (Koumarin daripada Murraya paniculata (Rutaceae)). Malaysian J. Anal. Sci., 14, 1–5. Baba, K., Nakata, K., Taniguchi, M., Kido, T., & Kozawa, M., (1990). Chalcones from Angelica keiskei. Phytochemistry, 29(12), 3907–3910. Bajgai, S. P., Prachyawarakorn, V., Mahidol, C., Ruchirawat, S., & Kittakoop, P., (2011). Hybrid flavan-chalcones, aromatase and lipoxygenase inhibitors, from Desmos cochinchinensis. Phytochemistry, 7(16), 2062–2067. Basile, A., Sorbo, S., Spadaro, V., Bruno, M., Maggio, A., Faraone, N., & Rosselli, S., (2009). Antimicrobial and antioxidant activities of coumarins from the roots of Ferulago campestris (Apiaceae). Molecules, 1(3), 939–952. Beyer, S. F., Beesley, A., Rohmann, P. F. W., Schultheiss, H., Conrath, U., & Langenbach, C. J. G., (2019). The Arabidopsis non-host defense-associated coumarin scopoletin protects soybean from Asian soybean rust. Plant J., 99(3), 397–413. Bita, C. E., & Gerats, T., (2013). Plant tolerance to high temperature in a changing environment: Scientific fundamentals and production of heat stress-tolerant crops. Front. Plant Sci., 4, 1–18. Born, S. L., Api, A. M., Ford, R. A., Lefever, F. R., & Hawkins, D. R., (2003). Comparative metabolism and kinetics of coumarin in mice and rats. Food Chem. Toxicol. an Int. J. Publ. Br. Ind. Biol. Res. Assoc., 41(2), 247–258. Bourgaud, F., Hehn, A., Larbat, R., Doerper, S., Gontier, E., Kellner, S., & Matern, U., (2006). Biosynthesis of coumarins in plants: A major pathway still to be unravelled for cytochrome P450 enzymes. Phytochem. Rev., 5(2, 3), 293–308. Bramati, L., Minoggio, M., Gardana, C., Simonetti, P., Mauri, P., & Pietta, P., (2002). Quantitative characterization of flavonoid compounds in rooibos tea (Aspalathus linearis) by LC-UV/DAD. Journal of Agricultural and Food Chemistry, 50(20), 5513–5519. Chain, E. B., (1992). Chemistry and biochemistry of antibiotics. Prog. Lipid Res., 31(1), 87–108. Chakthong, S., Weaaryee, P., Puangphet, P., Mahabusarakam, W., Plodpai, P., Voravuthikunchai, S. P., & Kanjana-Opas, A., (2012). Alkaloid and coumarins from the green fruits of Aegle marmelos. Phytochemistry, 75, 108–113. Chantrapromma, K., Rat-A-Pa, Y., Karalai, C., Lojanapiwatana, V., & Seechamnanturakit, V., (2000). A chalcone and a dihydrochalcone from Uvaria dulcis. Phytochemistry, 53(4), 511–513. Chappell, J., & Hahlbrock, K., (1984). Transcription of plant defense genes in response to UV light or fungal elicitor. Nature, 311(5981), 76–78. Chen, W. J., Yun, M. S., Deng, F., & Yogo, Y., (2004). Effects of root-applied naringenin and chalcone on the growth of annual plants. Weed Biol. Manag., 4(4), 235–238.

220

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Chen, W. J., Yun, M. S., Deng, F., & Yogo, Y., (2011). Chalcone suppresses lignin biosynthesis in illuminated soybean cells. Weed Biol. Manag., 11(1), 49–56. Chibber, S. S., Sharma, R. P., & Dutt, S. K., (1979). Rubone, a new chalcone from derris Robusta seed shells. Phytochemistry, 18(12), 2056. Choudhary, D. K., Prakash, A., & Johri, B. N., (2007). Induced systemic resistance (ISR) in plants: Mechanism of action. Indian J. Microbiol., 47(4), 289–297. Claisen, L., & Claparede, A., (1881). Condensations of ketones with aldehydes. Ber. Dtsch. Chem. Ges., 14, 2460–2468. Coberly, L., & Rausher, M. D., (2003). Analysis of a chalcone synthase mutant in ipomoea purpurea reveals a novel function for flavonoids: Amelioration of heat stress. Mol. Ecol., 12, 1113–1124. Crombie, L., & Games, D. E. M., (1966). Isolation and structure of mammea A/BA, A/AB and A/BB: A group of 4-arylcoumarin extractives of Mammea Americana L. tetrahedron. Tetrahedron Lett., 7, 145–149. Cuadra, P., Guajardo, J., Carrasco-Orellana, C., Stappung, Y., Fajardo, V., & Herrera, R., (2020). Differential expression after UV-B radiation and characterization of chalcone synthase from the Patagonian hair grass Deschampsia antarctica. Phytochemistry, 169, 112179. Dao, T. T. H., Linthorst, H. J. M., & Verpoorte, R., (2011). Chalcone synthase and its functions in plant resistance. Phytochem. Rev., 10(3), 397–412. Davies, E. G., & Ashton, W. M., (1964). Coumarin and related compounds of Anthoxanthum puelii and Melilotus alba and dicoumarol formation in spoilt sweet vernal and sweet clover hay. J. Sci. Food Agric., 15(11), 733–738. De Lira, S. P., Seleghim, M. H. R., Williams, D. E., Marion, F., Hamill, P., Jean, F., Andersen, R. J., et al., (2007). A SARS-coronavirus 3CL protease inhibitor isolated from the marine sponge Axinella Cf. Corrugata: Structure elucidation and synthesis. J. Braz. Chem. Soc., 18(2), 440–443. Del Rio, D., Rodriguez-Mateos, A., Spencer, J. P. E., Tognolini, M., Borges, G., & Crozier, A., (2013). Dietary (poly) phenolics in human health: Structures, bioavailability, and evidence of protective effects against chronic diseases. Antioxidants Redox Signal., 18(14), 1818–1892. DellaGreca, M., Fiorentino, A., Isidori, M., Previtera, L., Temussi, F., & Zarrelli, A., (2003). Benzocoumarins from the rhizomes of Juncus acutus. Tetrahedron, 59(26), 4821–4825. Díaz-Tielas, C., Graña, E., Reigosa, M. J., & Sánchez-Moreiras, A. M., (2017). Plasma membrane depolarization precedes photosynthesis damage and long-term leaf bleaching in (E)-chalcone-treated Arabidopsis shoots. J. Plant Physiol., 218, 56–65. Díaz-Tielas, C., Graña, E., Reigosa, M. J., & Sánchez-Moreiras, A. M., (2016). Biological activities and novel applications of chalcones. Planta Daninha, 34(3), 607–616. Díaz-tielas, C., Graña, E., Sotelo, T., Reigosa, M. J., & Sánchez-moreiras, A. M., (2012). The natural compound trans-chalcone induces programmed cell death in Arabidopsis thaliana roots. Plant Cell Environ., 35(8), 1500–1507. Dıaz-Tielas, C., Sotelo, T., Gran˜a, E., Sa´nchez-Moreira, M. A., & Reigosa, M. J., (2013). Phytotoxic potential of trans -chalcone on crop plants and model species. J. Plant Growth Regul., 33(2), 181–194. Dominguez, X. A., Tellez, O., & Ramirez, E. G., (1983). Mixtecacin, a prenylated flavanone and oaxacacin its chalcone from the roots of Tephrosia woodii. Phytochemistry, 22(9), 2047–2049.

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

221

Duan, C., Mao, T., Sun, S., Guo, X., Guo, L., Huang, L., Wang, Z., et al., (2019). Constitutive expression of GmF6′H1 from soybean improves salt tolerance in transgenic Arabidopsis. Plant Physiol. Biochem., 141, 446–455. Elkhalifa, D., Al-Hashimi, I., Al Moustafa, A. E., & Khalil, A., (2021). A comprehensive review on the antiviral activities of chalcones. J. Drug Target., 29(4), 403–419. Evranos, Aksöz, B., & Ertan, R., (2011). Chemical and structural properties of chalcones I. Fabad J Pharm Sci., 36, 223–242. Feinbaum, R. L., & Ausubel, F. M., (1988). Transcriptional regulation of the Arabidopsis thaliana chalcone synthase gene. Mol. Cell. Biol., 8(5), 1985–1992. Flickinger, B., Berghöfer, T., Hohenberger, P., Eing, C., & Frey, W., (2010). Transmembrane potential measurements on plant cells using the voltage-sensitive dye ANNINE-6. Protoplasma, 247(1, 2), 3–12. Gafner, S., Wolfender, J. L., Mavi, S., & Hostettmann, K., (1996). Antifungal and antibacterial chalcones from myrica serrata stefan. Planta Med., 62(1), 67–69. Guibourt, N. J. B. G., (1869). Dicotylèdones caliciflores. In: Histoire Naturelle des Drogues Simples (p 377). Cambridge Library Collection - History of Medicine; Cambridge University Press. Gustafson, K. R., Fuller, R. W., Cardellina, J. H., McMahon, J. B., Currens, M. J., Boyd, M. R., Kashman, Y., et al., (1992). The calanolides, a novel HIV-inhibitory class of coumarin derivatives from the tropical rainforest tree, Calophyllum lanigerum. J. Med. Chem., 35(15), 2735–2743. Harborne, J. B., (1960). Classes and functions of secondary products from plants. Ann. N. Y. Acad. Sci., 84(10), 333. Heck, R. F., & Nolley, J. P., (1972). Palladium-catalyzed vinylic hydrogen substitution reactions with aryl, benzyl, and styryl halides. J. Org. Chem., 37(14), 2320–2322. Hu, B., Yao, H., Gao, Y., Wang, R., Li, F., Guo, J., Li, K., et al., (2019). Overexpression of chalcone synthase gene improves flavonoid accumulation and drought tolerance in tobacco. Res. Sq., 1–11. Isayenkov, S. V., & Maathuis, F. J. M., (2019). Plant salinity stress: Many unanswered questions remain. Front. Plant Sci., 10, 80. Istry, M., Patil, A. D., Freyer, A. J., Eggleston, D. S., Haltiwanger, R. C., Bean, M. F., Taylor, P. B., et al., (1993). The inophyllums, novel inhibitors of HIV- 1 reverse transcriptase isolated from the Malaysian tree, Calophyllum Inophyllum Linn Ashok. J. Med. Chem., 36(26), 4130–4138. Iwashina, T., (2000). The structure and distribution of the flavonoids in plants. J. Plant Res., 113(3), 287–299. Jahns, P., & Holzwarth, A. R., (2012). The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim. Biophys. Acta - Bioenerg., 1817(1), 182–193. Jalil, S. U., & Ansari, M. I., (2019). Nanoparticles and Abiotic Stress Tolerance in Plants: Synthesis, Action, and Signaling Mechanisms. Elsevier Inc. Jayasinghe, L., Balasooriya, B. A. I. S., & Padmini, W. C., (2004). Geranyl chalcone derivatives with antifungal and radical scavenging properties from the leaves of Artocarpus nobilis. Phytochemistry, 65, 1287–1290. Jenkins, G. I., Long, J. C., Wade, H. K., Shenton, M. R., & Bibikova, T. N., (2001). UV and blue light signaling: Pathways regulating chalcone synthase gene expression in Arabidopsis. New Phytol., 151(1), 121–131.

222

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Jiang, Z. H., Tanaka, T., Sakamoto, T., Kouno, I., Duan, J. A., & Zhou, R. H., (2002). Biflavanones, diterpenes, and coumarins from the roots of Stellera chamaejasme L. Chem. Pharm. Bull., 50(1), 137–139. Jimenez, C. M., Sampietro, D. A., Sgariglia, M. A., & Vattuone, M. A., (2014). Isolation, identification and usefulness of antifungal compounds from Zuccagnia punctata for control of toxigenic ear rot pathogen. Nat. Prod. Commun., 9(10), 1461–1464. Kai, K., Mizutani, M., Kawamura, N., Yamamoto, R., Tamai, M., Yamaguchi, H., Sakata, K., & Shimizu, B., (2008). Scopoletin is biosynthesized via ortho-hydroxylation of feruloyl CoA by a 2-oxoglutarate-dependent dioxygenase in Arabidopsis Thaliana. Plant J., 55(6), 989–999. Kharasch, E. D., Hankins, D. C., & Taraday, J. K., (2000). Single-dose methoxsalen effects on human cytochrome P-450 2A6 activity. Drug Metab. Dispos., 28(1), 28–33. Leyva, A., Jarillo, J. A., Salinas, J., & Martinez-zapater, J. M., (2020). Low temperature induces the accumulation of phenylalanine ammonia-lyase and chalcone synthase MRNAs of Arabidopsis thaliana in a light-dependent manner. Plant Physiol., 108(1995), 39–46. Lijuan, C., Huiming, G., Yi, L., & Hongmei, C., (2015). Chalcone synthase EaCHS1 from eupatorium adenophorum functions in salt stress tolerance in tobacco. Plant Cell Rep., 34(5), 885–894. Lundberg, D. S., & Teixeira, P. J. P. L., (2018). Root-exuded coumarin shapes the root microbiome. Proc. Natl. Acad. Sci. U. S. A., 115(22), 5629–5631. Macías, F. A., Molinillo, J. M. G., Torres, A., Varela, R. M., & Castellano, D., (1997). Bioactive flavonoids from helianthus annuus cultivars. Phytochemistry, 45(4), 683–687. Mahapatra, D. K., & Bharti, S. K., (2016). Therapeutic potential of chalcones as cardiovascular agents. Life Sci., 148, 154–172. Malhotra, B., Onyilagha, J. C., Bohm, B. A., Towers, G. H. N., James, D., Harborne, J. B., & French, C. J., (1996). Inhibition of tomato ringspot virus by flavonoids. Phytochemistry, 43(6), 1271–1276. Mark, R., Lyu, X., Lee, J. J. L., Parra-Saldívar, R., & Chen, W. N., (2019). Sustainable production of natural phenolics for functional food applications. J. Funct. Foods, 57, 233–254. Miyaura, N., Yamada, K., & Suzuki, A., (1979). A new stereospecific cross-coupling by the palladium-catalyzed reaction of 1-alkenylboranes with 1-alkenyl or 1-alkynyl halides. Tetrahedron Lett., 20(36), 3437–3440. Nam, H., & Kim, M. M., (2015). Scopoletin has a potential activity for anti-aging via autophagy in human lung fibroblasts. Phytomedicine, 22(3), 362–368. Nguyen, G. T. T., Erlenkamp, G., Jäck, O., Küberl, A., Bott, M., Fiorani, F., & Gohlke, H., (2016). Chalcone-based selective inhibitors of a C 4 plant key enzyme as novel potential herbicides. Nat. Publ. Gr., 1–12. Ni, L., Meng, C. Q., & Sikorski, J. A., (2004). Recent advances in therapeutic chalcones. Expert Opin. Ther. Pat., 14(12), 1669–1691. Niron, H., & Türet, M., (2020). A putative common bean chalcone O-methyltransferase improves salt tolerance in transgenic Arabidopsis thaliana. J. Plant Growth Regul., 39(3), 957–969. Ono, E., Fukuchi-Mizutani, M., Nakamura, N., Fukui, Y., Yonekura-Sakakibara, K., Yamaguchi, M., & Tanaka, Y., (2006). Yellow flowers generated by expression of the aurone biosynthetic pathway. Proceedings of the National Academy of Sciences, 103(29), 11075–11080.

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

223

Onyilagha, J. C., Malhotra, B., Elder, M., French, C. J., & Towers, G. H. N., (1997). Comparative studies of inhibitory activities of chalcones on tomato ringspot virus (ToRSV). Can. J. Plant Pathol., 19(2), 133–137. Orlikova, B., Tasdemir, D., Golais, F., Dicato, M., & Diederich, M., (2011). Dietary chalcones with chemopreventive and chemotherapeutic potential. Genes Nutr., 6(2), 125–147. Pádua, G. M. S. De., Souza, J. M. De., Sales, M. C. M., Vasconcelosm, L. G. De., Dall’Oglio, E. L., Faraggi, T. M., Sampaio, O. M., & Vieira, L. C. C., (2021). Evaluation of chalcone derivatives as photosynthesis and plant growth inhibitors. Chem. Biodivers. Pal, S., Chatare, V., & Pal, M., (2011). Isocoumarin and its derivatives: An overview on their synthesis and applications. Curr. Org. Chem., 15(5), 782–800. Parmar, N., Singh, K. H., Sharma, D., Singh, L., Kumar, P., Nanjundan, J., Khan, Y. J., et al., (2017). Genetic engineering strategies for biotic and abiotic stress tolerance and quality enhancement in horticultural crops: A comprehensive review. 3 Biotech, 7(4), 1–35. Parvin, K., Hasanuzzaman, M., Mohsin, S. M., Nahar, K., & Fujita, M., (2020). Coumarin improves tomato plant tolerance to salinity by enhancing antioxidant defense, glyoxalase system and ion homeostasis. Plant Biol., 23, 181–192. Pereira, T. M., Franco, D. P., Vitorio, F., & Kummerle, A. E., (2018). Coumarin compounds in medicinal chemistry: Some important examples from the last years. Curr. Top. Med. Chem., 18(2), 124–148. Piller, N. B., (1975). A comparison of the effectiveness of some anti-inflammatory drugs on thermal oedema. Br. J. Exp. Pathol., 56(6), 554–560. Poole, S. K., & Poole, C. F., (1994). Thin-layer chromatographic method for the determination of the principal polar aromatic flavor compounds of the cinnamons of commerce. Analyst, 119(1), 113–120. Prats, E., Rubiales, D., & JorrÍn, J., (2002). Acibenzolar- S -methyl-induced resistance to sunflower rust (Puccinia helianthi) is associated with an enhancement of coumarins on foliar surface. Physiol. Mol. Plant Pathol., 60(3), 155–162. Qin, W., Liu, C., Jiang, W., Xue, Y., Wang, G., & Liu, S., (2019). A coumarin analogue NFA from endophytic Aspergillus fumigatus improves drought resistance in rice as an antioxidant. BMC Microbiol., 19(1), 1–11. Rajniak, J., Giehl, R. F. H., Chang, E., Murgia, I., Von, W. N., & Sattely, E. S., (2018). Biosynthesis of redox-active metabolites in response to iron deficiency in plants. Nat. Chem. Biol., 14(5), 442–450. Ramirez, F., & Dershowitz, S., (1957). Phosphinemethylenes.1 II. triphenylphosphineacylmethylenes. J. Org. Chem., 22(1), 41–45. Rao, G., Kumar, P., Singh, M., Singh, H., & Pandey, O., (1994). Efficacy of chalcone, hydrazide and oxadiazole derivatives against fungal pathogens of sugarcane. Sugar Cane, 5, 17–22. Sahu, N. K., Balbhadra, S. S., Choudhary, J., & Kohli, D. V., (2012). Exploring pharmacological significance of chalcone scaffold: A review. Curr. Med. Chem., 19(2), 209–225. Sako, K., Nguyen, H. M., & Seki, M., (2021). Advances in chemical priming to enhance abiotic stress tolerance in plants. Plant Cell Physiol., 61(12), 1995–2003. Saleh, A. M., & Madany, M. M. Y., (2015). Coumarin pretreatment alleviates salinity stress in wheat seedlings. Plant Physiol. Biochem., 88, 27–35. Santra, H. K., & Banerjee, D., (2020). Natural products as fungicide and their role in crop protection. In: Singh, J., & Yadav, A. N., (eds.), Natural Bioactive Products in Sustainable Agriculture (pp. 131–219). Springer Singapore: Singapore.

224

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Sarker, S. D., & Nahar, L., (2017). Progress in the Chemistry of Naturally Occurring Coumarins, 106, 241–304. Schröder, J., & Schäfer, E., (1980). Radioiodinated antibodies, a tool in studies on the presence and role of inactive enzyme forms: Regulation of chalcone synthase in parsley cell suspension cultures. Arch. Biochem. Biophys., 203(2), 800–808. Shang, Y. F., Oidovsambuu, S., Jeon, J. S., Nho, C. W., & Um, B. H., (2013). Chalcones from the flowers of coreopsis lanceolata and their in vitro antioxidative activity. Planta Med., 79(3, 4), 295–300. Shuai, C., Zhang, Y., Pan, X., Li, Y., Cui, L., Wu, F., Cao, M., et al., (2017). Gene from nicotiana tabacum. J. Integr. Agric., 16(7), 1443–1450. Singh, N., & Kumaria, S., (2020). Molecular cloning and characterization of chalcone synthase gene from Coelogyne Ovalis Lindl. and its stress-dependent expression. Gene, 762, 145104. Siwinska, J., Siatkowska, K., Olry, A., Grosjean, J., Hehn, A., Bourgaud, F., Meharg, A. A., et al., (2018). Scopoletin 8-hydroxylase: A novel enzyme involved in coumarin biosynthesis and iron-deficiency responses in Arabidopsis. J. Exp. Bot., 69(7), 1735–1748. Soine, T. O., (1964). Review article: Naturally occurring coumarins and related physiological activities by. J. Pharmacol. Sci., 53(3), 231–264. Srikrishna, D., Godugu, C., & Dubey, P. K., (2018). A review on pharmacological properties of coumarins. Mini Rev. Med. Chem., 18(2), 113–141. Stassen, M. J. J., Hsu, S. H., Pieterse, C. M. J., & Stringlis, I. A., (2021). Coumarin communication along the microbiome–root–shoot axis. Trends Plant Sci., 26(2), 169–183. Stein, A. C., Álvarez, S., Avancini, C., Zacchino, S., & Von, P. G., (2006). Antifungal activity of some coumarins obtained from species of Pterocaulon (Asteraceae). J. Ethnopharmacol., 107(1), 95–98. Stringlis, I. A., De Jonge, R., & Pieterse, C. M. J., (2019). The age of coumarins in plantmicrobe interactions. Plant Cell Physiol., 60(7), 1405–1419. Tanaka, H., Ichino, K., & Ito, K., (1984). Dihydrochalcones from Lindera umbellata. Phytochemistry, 23(5), 1198, 1199. Tasior, M., Kim, D., Singha, S., Krzeszewski, M., Ahn, K. H., & Gryko, D. T., (2015). π-expanded coumarins: Synthesis, optical properties and applications. J. Mater. Chem. C, 3(7), 1421–1446. Taylor, P., Esaki, S., Nishiyama, K., Sugiyama, N., Nakajima, R., Esaki, S., Nishiyama, K., et al., (2014). Preparation and taste of certain glycosides of flavanones and of dihydrochalcones preparation and taste of certain glycosides of flavanones and of dihydrochalcones. Biosci. Biotechnol. Biochem., 58(8), 1479–1485. Tosun, A., Baba, M., Bahadir, O., & Okuyama, T., (2006). Coumarins isolated from the roots of Seseli resinosum in Turkey. Pharm. Biol., 44(7), 528–533. Tropf, S., Kärcher, B., Schröder, G., & Schröder, J., (1995). Reaction mechanisms of homodimeric plant polyketide synthase (stilbenes and chalcone synthase). A single active site for the condensing reaction is sufficient for synthesis of stilbenes, chalcones, and 6’-deoxychalcones. J. Biol. Chem., 270(14), 7922–7928. Tsai, H. H., Rodríguez-Celma, J., Lan, P., Wu, Y. C., Vélez-Bermúdez, I. C., & Schmidt, W., (2018). Scopoletin 8-hydroxylase-mediated fraxetin production is crucial for iron mobilization. Plant Physiol., 177(1), 194–207.

Involvement of Chalcones and Coumarins in Environmental Stress Tolerance

225

Ullah, A., Ansari, F. L., Ihsan-Ul-Haq, Nazir, S., & Mirza, B., (2007). Combinatorial synthesis, lead identification, and antitumor study of a chalcone-based positional-scanning library. Chem. Biodivers., 4(2), 203–214. Uyar, T., Malterud, K. E., & Anthonsen, T., (1978). Two new dihydrochalcones from Myrica gale. Phytochemistry, 17(11), 2011–2013. Vanholme, R., Sundin, L., Seetso, K. C., Kim, H., Liu, X., Li, J., De Meester, B., et al., (2019). COSY Catalyses trans-Cis isomerization and lactonization in the biosynthesis of coumarins. Nat. Plants, 5(10), 1066–1075. Vassallo, J. D., Hicks, S. M., Daston, G. P., & Lehman-McKeeman, L. D., (2004). Metabolic detoxification determines species differences in coumarin-induced hepatotoxicity. Toxicol. Sci., 80(2), 249–257. Venugopala, K. N., Rashmi, V., & Odhav, B., (2013). Review on natural coumarin lead compounds for their pharmacological activity. Biomed Res. Int., 2013, 1–14. Verpoorte, T. T., (2011). Chalcone synthase and its functions in plant resistance. Phytochem. Rev., 10, 397–412. Vogel, A., (1820). Depiction of benzoic acid from the tonka bean and from the melilotes - or sweet clover - flowers. Ann. Phys., 64(2), 161–166. Walker, D. J., Martínez-Fernández, D., Correal, E., Romero-Espinar, P., & Antonio, D. R. J., (2012). Accumulation of furanocoumarins by Bituminaria bituminosa in relation to plant development and environmental stress. Plant Physiol. Biochem., 54, 133–139. Wang, F., Ren, G., Li, F., Qi, S., Xu, Y., Wang, B., Yang, Y., Ye, Y., Zhou, Q., & Chen, X., (2018). A Chalcone synthase gene AeCHS from Abelmoschus esculentus regulates flavonoid accumulation and abiotic stress tolerance in transgenic Arabidopsis. Acta Physiol. Plant., 40(5), 1–13. Witaicenis, A., Seito, L. N., & Di Stasi, L. C., (2010). Intestinal anti-inflammatory activity of esculetin and 4-methylesculetin in the trinitrobenzenesulphonic acid model of rat colitis. Chem. Biol. Interact., 186(2), 211–218. Wu, L., Wang, X., Xu, W., Farzaneh, F., & Xu, R., (2009). The structure and pharmacological functions of coumarins and their derivatives. Curr. Med. Chem., 16(32), 4236–4260. Wu, X., Zhang, S., Liu, X., Shang, J., Zhang, A., & Zhu, Z., (2020). Chalcone synthase (CHS) family members analysis from eggplant (Solanum melongena L.) in the flavonoid biosynthetic pathway and expression patterns in response to heat stress. PLoS One, 15(4), 1–18. Xu, J., Zhao, W. M., Qian, Z. M., Guan, J., & Li, S. P., (2010). Fast determination of five components of coumarin, alkaloids and bibenzyls in Dendrobium Spp. using pressurized liquid extraction and ultra-performance liquid chromatography. J. Sep. Sci., 33(11), 1580–1586. Yahyaa, M., Ali, S., Davidovich-Rikanati, R., Ibdah, M., Shachtier, A., Eyal, Y., Lewinsohn, E., & Ibdah, M., (2017). Characterization of three chalcone synthase-like genes from apple (Malus × domestica Borkh. Phytochemistry, 140, 125–133. Yao, X., Wang, T., Wang, H., Liu, H., Liu, S., Zhao, Q., Chen, K., & Zhang, P., (2019). Identification, characterization and expression analysis of the chalcone synthase family in the Antarctic moss Pohlia nutans. Antart. Sci., 31(1), 23–33. Yu, L., (2005). Chalcones from the seeds of Psoralea corylifolia. Pol. J. Chem., 79(7), 1173–1177.

226

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Yun, M. S., Chen, W., Deng, F., & Yogo, Y., (2009). Selective growth suppression of five annual plant species by chalcone and naringenin correlates with the total amount of 4-coumarate: Coenzyme A ligase. Weed Biol. Manag., 9(1), 27–37. Zhang, X. H., Zheng, X. T., Sun, B. Y., Peng, C. L., & Chow, W. S., (2018). Over-expression of the CHS gene enhances resistance of Arabidopsis leaves to high light. Environ. Exp. Bot., 154, 33–43. Zhang, X. S., Ni, R., Wang, P. Y., Zhu, T. T., Sun, C. J., Lou, H. X., & Cheng, A. X., (2019). Isolation and functional characterization of two caffeoyl coenzyme A 3-O-methyltransferases from the fern species Polypodiodes amoena. Plant Physiology and Biochemistry, 136, 169–177. Zhao, Y., Jian, X., Wu, J., Huang, W., Huang, C., Luo, J., & Kong, L., (2019). Elucidation of the biosynthesis pathway and heterologous construction of a sustainable route for producing umbelliferone. J. Biol. Eng., 13(1), 1–13. Zhao, Z. X., Jin, J., Lin, C. Z., Zhu, C. C., Liu, Y. M., Lin, A. H., Liu, Y. X., et al., (2011). Two new chalcone glycosides from the stems of Entada phaseoloides. Fitoterapia, 82(7), 1102–1105. Zhou, B., Li, Y., Xu, Z., Yan, H., Homma, S., & Kawabata, S., (2007). Ultraviolet A-specific induction of anthocyanin biosynthesis in the swollen hypocotyls of turnip (Brassica Rapa). J. Exp. Bot., 58(7), 1771–1781. Zhou, D., Xie, D., He, F., Song, B., & Hu, D., (2018). Bioorganic & medicinal chemistry letters antiviral properties and interaction of novel chalcone derivatives containing a purine and benzenesulfonamide moiety. Bioorg. Med. Chem. Lett., 28, 2091–2097. Zhou, Y., Huang, J. L., Zhang, X. L., Zhu, L. M., Wang, X. F., Guo, N., Zhao, J. M., & Xing, H., (2018). Overexpression of chalcone isomerase (CHI) increases resistance against phytophthora sojae in soybean. J. Plant Biol., 61(5), 309–319. Zhuang, C., Zhang, W., Sheng, C., Zhang, W., Xing, C., & Miao, Z., (2017). Chalcone: A privileged structure in medicinal chemistry. Chem. Rev., 117, 7762–7810.

CHAPTER 9

Role of Phenolic Acids and Flavonoids in the Mitigation of Environmental Stress in Plants ANKUR SINGH and ARYADEEP ROYCHOUDHURY

Post-Graduate Department of Biotechnology, St. Xavier’s College (Autonomous), 30, Mother Teresa Sarani, Kolkata – 700016, West Bengal, India *

Corresponding author. E-mail: [email protected]

ABSTRACT Phenolic compounds are an important class of secondary metabolites that are produced in plants in optimal and suboptimal conditions and play a pivotal role in their life cycle. This diverse group of metabolites contains various structures, from simple forms consisting of one aromatic ring to more complex ones consisting of a large number of polymerized molecules. Based on their structures, different polyphenolic compounds show different functions that range from protection against abiotic stress to plant growth and reproduction. To cope with abiotic stresses, plants enhance the production of secondary metabolites such as phenolic acid and flavonoids that detoxify the cytotoxic metabolites and help in improving the growth, development, and yield of plants. Polyphenolic compounds are synthesized in plants via. shikimate/phenylpropanoid pathway. The major enzymes of this pathway are phenylalanine ammonia-lyase (PAL), chalcone synthase (CHS), chalcone isomerase (CHI), cinnamate 4-hydroxylase (C4H), and 4-coumarate: CoA ligase (4CL). Phenylpropanoid pathway is activated under abiotic stress conditions (drought, heavy metal, salinity, high/low Biology and Biotechnology of Environmental Stress Tolerance in Plants: Secondary Metabolites in Environmental Stress Tolerance, Volume 1. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

228

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

temperature, and ultraviolet radiations) resulting in accumulation of various phenolic compounds which, among other roles, have the potential to scavenge harmful reactive oxygen species (ROS). Thus, the main focus of this chapter is to decipher the wide role of polyphenolic compounds in plants exposed to unfavorable environmental conditions. Through this chapter, an attempt has been made to provide updated information about the response of polyphenolic compounds under challenging environments. 9.1 INTRODUCTION In recent years, several scientific reports have shown a direct effect of climate and atmospheric changes on growth and development of plants around the world. Due to these undesirable changes in environment, plants are exposed to a plethora of abiotic stresses such as salinity, drought, temperature, heavy metal, and UV stress which negatively impact their growth and yield throughout their life cycle. Along with environmental factors, various anthropogenic activities have further aggravated the amplitude of these abiotic stresses. Various reports have shown that harsh environmental conditions reduce the productivity and overall yield of crops by 50% and 70%, respectively (Kaur et al., 2008; Mantri et al., 2012). Plants, being sessile in nature, are constantly exposed to unfavorable environmental conditions that ultimately lead to generating effective mechanisms to reduce the negative impact of abiotic stresses, thus enhancing the survival capacity of plants. To combat the negative effects of abiotic stresses, plants regulate the expression of various protective genes that in turn induces the activity of several proteins playing a pivotal role in ameliorating the toxic metabolites. Along with these proteins, plants also produce several beneficial metabolites, such as non-enzymatic antioxidants, phenolics, and flavonoids. Polyphenols are one of the most widely studied plant metabolites formed in response to abiotic stress conditions. They are known to be the largest groups of secondary metabolites that include more than 8,000 molecules varying from complex molecules to simpler aromatic rings (González-Sarrías et al., 2020). According to Sharma et al. (2019a), shikimate/phenylpropanoid pathway is the major pathway that mostly contributes toward the formation of these secondary metabolites. The most common structural feature of polyphenolic compounds is the presence of one or more aromatic rings containing one or more hydroxyl substituents. In plants, polyphenolic compounds are freely present or are conjugated with sugar moiety that can be mono-, di-,

Role of Phenolic Acids and Flavonoids in the Mitigation

229

or even polysaccharides (González-Sarrías et al., 2020). According to their structure, polyphenolic compounds can be further classified into four types, i.e., flavonoids, phenolic acids, lignans, and stilbenoids (Šamec et al., 2021). In this chapter, our main focus will be on the protective role of flavonoids and phenolic acids against unfavorable environmental conditions faced by plants. Phenolic acids are mostly found in conjugation with other smaller organic molecules (glucose, tartaric acid, quinic or malic acid), plant cell components like pectin, cellulose, and lignin, and other molecules such as flavonoids and terpenes via acetal, ester or ether bonds (Andreasen et al., 2000; Lam et al., 2001). The main feature of all the phenolic acids is the presence of a benzene ring linked with carboxyl group. Based on their structure, phenolics can be further classified into two groups, i.e., derivatives of cinnamic acid and derivatives of benzoic acid (Goleniowski et al., 2013). Phenolics play a pivotal role in abrogating the negative effects of abiotic stresses due to high antioxidative properties. They readily scavenge the ROS formed in plants under different abiotic stressors. On sensing unfavorable conditions, plants up regulate the expression of phenylalanine ammonia-lyase (PAL) and chalcone synthase (CHS) genes which in turn enhances the formation of phenolics via phenylpropanoid biosynthesis pathway that help in reducing the negative effects of abiotic stresses by scavenging the cytotoxic metabolite formed (Sharma et al., 2019b; Wang et al., 2019). According to Simic et al. (2007), the antioxidative property of phenolics is mostly controlled by the number of hydroxyl groups present. The beneficial role of phenolic acids has been shown in various abiotic stress conditions. Kısa et al. (2016) reported that on exposing maize plants to heavy metal stress such as cadmium (Cd), copper (Cu), and lead (Pb), the level of vanillic acid was enhanced; similar results were also observed by Liet al. (2018) in drought-stressed Cucumis sativus. Exogenous application of vanilic acid also proved to be beneficial in salt-stressed tomato plants by maintaining the homeostasis of calcium (Ca), potassium (K) and magnesium (Mg) along with up regulating the activity of other enzymatic and non-enzymatic antioxidants such as catalase (CAT), superoxide dismutase (SOD) and ascorbic acid (Parvin et al., 2020). Along with phenolic acids, other important group of polyphenols produced by plants to combat the harmful effects of abiotic stress are the flavonoids. Next to phenolics, flavonoids are the most widely found molecules in plants comprising of above 6,000 different structures (Panche et al., 2016). Flavonoids are mostly made up of two benzene rings which are connected by three carbon atoms and one oxygen atom. Based on their structure, flavonoids can

230

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

be classified into six different groups, i.e., flavones, flavanones, isoflavones, flavonols, flavanonols, and flavan-3-ols. According to Wen et al. (2017), flavonoids can be found in free form in plants or in conjugation via glycosidation, acetylation, prenylation, methylation, and polymerization which regulates their biological activity. Glycosidation enhances the metabolism, solubility, and transportation across various cell membranes, whereas methylation induces the entry of flavonoids into the cells that prevent cellular damages (Kytidou et al., 2020; Wen et al., 2017). The pivotal role played by the flavonoids in abrogating the negative effects of abiotic stress in plants has been reported earlier. Nakabayashi et al. (2014) reported that overexpression of MYB12/PFG1 (production of flavonol glycosides 1) or MYB75/PAP1 (production of anthocyanin pigment 1) in Arabidopsis reduced the damages caused due to drought and oxidative stress by regulating the formation of flavonoids and anthocyanins. Similarly, Abdel-Farid et al. (2020) showed that on being exposed to salt stress, the level of flavonoids was enhanced in cucumber and tomato seedlings which in turn detoxified the cytotoxic metabolites, thus improving the biomass of the seedlings along with root and shoot length. Additionally, the protective role of flavonoids has been reported in other abiotic stresses such as extreme temperature, heavy metal toxicity and UV stress in several crops. Based on such earlier works, the main focus of this chapter is to demonstrate the pivotal role played by phenolics and flavonoids in plants that eventually contribute towards their better survival under unfavorable conditions. This chapter comprises of a detailed overview of the phenylpropanoid pathway that mostly controls the synthesis of the above-mentioned metabolites followed by their classification, based on their structures. Lastly, we provide a detailed overview of the beneficial effects of flavonoids and phenolics in plants exposed to abiotic stresses. 9.2 BIOSYNTHESIS OF PHENOLICS AND FLAVONOIDS IN PLANTS According to Hattenschwiler & Vitousek (2000), shikimate and malonate pathways are the two major pathways involved in the biosynthesis of aromatic amino acids such as phenylalanine and tryptophan which are further utilized by the enzymes of phenylpropanoid pathway for biosynthesis of phenolics. Malonate pathway mostly operates in fungi and bacteria, whereas shikimate pathway mostly in higher plants. According to Tohge et al. (2013), under normal conditions, 20% of carbon fixed by the plants follows the shikimate pathway, which is further increased

Role of Phenolic Acids and Flavonoids in the Mitigation

231

in plants on being exposed to stressed conditions. Additionally, shikimate pathway also provides carbon backbone for other essential metabolites such as salicylic acid, indole-3-acetic acid, tetrahydrofolate, and plant pigments (Maeda & Dudareva, 2012). The shikimate pathway consists of seven enzymatic steps that eventually produce chorismate, the common precursor to aromatic amino acids (Singh & Christendat, 2007). The aromatic amino acids thus formed from chorismate via the shikimate pathway are further utilized for the synthesis of other important metabolites along with phenolics. Tyrosine gives rise to suberin, hydroxycinnamic acids (HCAs), tocopherols, and cyanogenic glycosides, whereas alkaloids, auxin, phytoalexins, and glucosinolates are formed from tryptophan. Phenylalanine is the major precursor of most of the simple phenolic compounds. Deamination, hydroxylation, and methylation are the three major steps involved in the biosynthesis of phenolics via phenylpropanoid pathway from L-tyrosine (L-Tyr) and/or L-phenylalanine. PAL initiates the phenylpropanoid pathway, which catalyzes the deamination of phenylalanine to form trans-cinnamic acid. PAL controls the major regulatory step in the formation of many phenolic compounds. Trans-cinammic acid is further hydroxylated at the C4 position via cinnamate 4-hydroxylase (C4H) to give p-coumaric acid. Additionally, tyrosine ammonia lyase (TAL) in grasses can also yield p-coumaric acid from tyrosine, bypassing the action of C4H (Barros et al., 2016). Trans-cinammic acid is further hydroxylated by removing the ethyl side chain to yield benzoic acid. Structurally, all phenolic acids are hydroxylated derivatives of cinnamic acid or benzoic acid. Phenylalanine also acts as a precursor of flavonoids which are again synthesized through the phenylpropanoid pathway. Initially, phenylalanine is converted to 4-coumaroyl CoA that marks the initiation of flavonoid biosynthesis. The first enzyme, specific to this pathway, is CHS which produces chalcone scaffolds that serves as the backbone for all the flavonoid derivatives. According to Martens et al. (2010), flavonoid biosynthesis pathway is conserved in plants; however, a group of enzymes like reductase, several Fe2+/2-oxoglutarate-dependent dioxygenases, isomerase, and hydroxylase modify the chalcone backbone that leads to the formation of various subclasses of flavonoids. Finally, the backbone of flavonoids is modified with methyl groups, acyl moieties or sugar molecules via the action of transferase that eventually modulates their physiological activities such as reactivity, solubility, and interaction with target molecules (Ferrer et al., 2008).

232

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

9.3 SUBCLASSES OF PHENOLICS AND FLAVONOIDS Depending on their structure, phenolic acids can be further classified into two groups: derivatives of cinnamic acid (hydroxycinnamic acid) and derivatives of benzoic acid (hydroxybenzoic acid) (Goleniowski et al., 2013). HCAs include ferulic acid, p-coumaric acid, caffeic, and sinapic acid. Additionally, the esterified or etherified conjugates of the above-mentioned metabolites such as chlorogenic acid are also derivatives of HCAs. Hydroxylation and methylation of p-coumaric acid led to the formation of ferulic, sinapic, caffeic, and 5-hydroxyferulic acid, catalyzed by monophenol monooxygenase (Strack, 1997). Ferulic acid along with p-coumaric acid acts as a precursor of lignin that is an important natural polymer playing a pivotal role in abiotic stress tolerance in plants (Goleniowski et al., 2013). Along with hydroxycinnamic acid, hydroxybenzoic acid also acts as a backbone for major phenolic acids in plants. Salicylic acid, gallic acid, vanillic acid, and other derivatives of dihydroxybenzoic acid (DHBA) mostly belong to the hydroxybenzoic acid group (Macheix et al., 1990). Few simple hydroxybenzoic acids (HBAs), such as gallic acid are formed early as an intermediate of the shikimate pathway. In spite of playing a pivotal role in inducing the tolerance capacity of plants against abiotic stress, very few works have been done on the biosynthetic pathway of hydroxybenzoic acid and thus the mechanism of the enzymes controlling the biosynthesis of hydroxybenzoic acid, and their derivatives is not completely known. In contrast to that of phenolics, flavonoids are classified based on their structural dissimilarities: flavan-3-ols, flavanones, isoflavones, flavonols, flavones, and anthocyanins. Flavan-3-ols are mostly derived from flavanones by the catalytic activity of dihydroflavonol-4-reductase that reduces the C4 atom in the pyrene ring. The general structure of flavan-3-ols contains a hydroxyl group at the C3 position of the core flavan structure. Epicatechin, catechin, and their glycoside derivatives are widely reported members of this group. The role of flavan-3-ols is reported in case of biotic stress, whereas its beneficial role in abiotic stress is less investigated (Bais et al., 2003). Shi et al. (2020) reported that the level of flavan-3-ols was lowered in Juvenal tea plants, whereas contrasting results were demonstrated by Hernandez et al. (2004) where they showed that drought stress enhances the level of flavan-3-ols in plants. Similarly, the protective role of flavan-3-ols was also reported by Cuong et al. (2020) in salt-stressed plants. Flavanones are produced by the action of flavanone-4-reductase and CHI on flavan-4-ol and chalcone-like compounds, respectively. According to Khan

Role of Phenolic Acids and Flavonoids in the Mitigation

233

et al. (2014), flavanones serve as a precursor for all other flavonoid groups and can easily undergo glycosylation, hydroxylation, and O-methylation due to their high reactivity. Unlike flavan-3-ols, the role of flavanones in abiotic stress is widely investigated. Silybin, hesperetin, eridictyol, naringenin, and isosakuratenin are few major flavanones identified till date. According to Martinez et al. (2016), the level of naringenin was enhanced in tomato plants on being exposed to heat stress, whereas the level of the same was reduced in salt stressed plants in the presence of heat stress. Isoflavones are mostly found in legumes (Saviranta et al., 2009). Formononetin, daidzein, and genistein are synthesized from naringenin and liquirtigenin by the catalytic activity of 2-hydroxyisoflavone dehydrate and 2-hydroxyisoflavanone synthase which are further modified by methyltransferases and glycosyltransferases to yield diverse groups of isoflavonoids (He et al., 2019). According to Ahmad et al. (2017), malonylation, and glycosylation enhance the stability, solubility, and transport of isoflavonoids. Liu et al. (2017) reported that UV-B stress induces the glycosylation of isoflavonoids in Astragalus plants. The role of isoflavones in plants on being exposed to abiotic stress is still unambiguous. Swigonska et al. (2014) reported that the level of isoflavones was enhanced during long and short cold stress and osmotic stress in soybean plants, whereas contrasting results were obtained by the study conducted by Gutierrez-Gonzalez et al. (2010) where they showed that the level of all the isoflavones was lowered in the developmental stage of drought-stressed soybean. Catalytic oxidation of flavanonols at C3 and C2 atoms by flavonol synthase (FLS) yield flavonols. Kaempferol, quercetin, and myricetin are the few widely studied flavonols. Flavonols are most emphasized flavonoid type against abiotic stress response. The importance of flavonols was diversely reported in various plants against UV stress (Harborne & Williams, 2000; Huyskens-Keil et al., 2012; Nascimento et al., 2015). Along with this, the protective role of flavonols, i.e., quercetin was also reported by Kidd et al. (2001) against aluminum toxicity in maize plants. Flavones are the other major groups of flavonoids that are synthesized by the catalytic oxidation of flavanones at C2 and C3 atoms by flavone synthase. The major flavones identified in plants are chrysin, luteolin, tangeritin, apigenin, orientin, diosmetin, scoparin, and baicalein. The catalytic activity of flavones depends on the presence of hydroxyl groups, such as the radical scavenging activity of dihydroxy flavones like luteolin is higher than that of monohydroxy-bearing group like apigenin. A similar report was published by Hodaei et al. (2018) where they showed that the level of luteolin was

234

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

enhanced in drought-stressed Chrysanthemum cultivars, whereas the level of apigenin remained unchanged or was reduced. Anthocyanins are glycosylated polyphenolic compounds that belong to the largest group of water-soluble pigments in plants (Dini et al., 2019). According to Pervaiz et al. (2017), the main structure of anthocyanins mostly consists of three parts, i.e., two benzyl rings and one heterocyclic benzopyran along with three side groups, i.e., –H, –OH and –OCH3. The protective role of anthocyanins in plants against abiotic and biotic stress is widely reported. Under stressed environment, anthocyanins serve as stress signaling molecules, ROS scavengers and photoprotectants. Kovinich et al. (2014) reported the accumulation of 20 anthocyanin derivatives in Arabidopsis plants under stressed environment. 9.4 BENEFICIAL ROLE OF PHENOLICS AND FLAVONOIDS AGAINST ABIOTIC STRESSES On being exposed to abiotic stresses, plant enhances the production of secondary metabolites, including phenolics and flavonoids. Polyphenolic metabolites confer higher tolerance to plants against unfavorable environments like drought, temperature, salinity, UV radiation and heavy metal stress. Phenolics and flavonoids have high antioxidative properties and thus can easily scavenge the free radicals formed in plants, eventually protecting the cell membrane and cell organelles. Biosynthesis of phenolics under stressed environment is up regulated by the enhanced expression of the key enzymes such as PAL and CHS. The protective role of phenolics and flavonoids under various abiotic stresses has been discussed in the underlying sections. 9.4.1 DROUGHT The shortage of water is currently one of the crucial problems that negatively affects plant development, growth, and yield. Drought stress occurs when the atmospheric condition enhances the water loss from the plant tissues due to high temperature (HT) or solar radiation, which further aggravates due to shortage of water in soil. Drought stress induces the formation of ROS in plants which eventually leads to degradation of photosynthetic pigments of plants, such as carotenoids and chlorophyll (Massacci et al., 2008). Additionally, drought stress also hampers the activity of enzymes controlling

Role of Phenolic Acids and Flavonoids in the Mitigation

235

the metabolic cycle in plants that in turn lowers the energy production. The negative effects of drought stress are seen in all plants, but its extent varies from species to species. According to the study conducted by Daryanto et al. (2016), around 21% and 40% yield reduction were noted (between 1980 to 2015) in wheat and maize plants, respectively due to shortage of water. To provide proper food, shelter, and clothing to ever increasing population of the world, the production of crops must be improved under water shortage condition. To reverse the negative effect of drought stress, the importance of phenolics and flavonoids is widely reported in plants. Various metabolomics and transcriptomics studies have demonstrated the beneficial role of phenolics and flavonoids in drought-stressed Arabidopsis plants. According to Sanchez-Rodriguez et al. (2011), the level of quercetin and kaempferol were enhanced in drought-stressed tomato plants that confers tolerance to plants by scavenging the cytotoxic metabolites. A similar report was also published by Hernandez et al. (2009) where they showed that accumulation of flavonoids can efficiently detoxify H2O2 molecules formed in the cytoplasm of drought stressed plants. In another study, Gharibiet al. (2019) reported that the content of total phenolics and flavonoids (chlorogrnic acid, rutin, caffeic acid, kaempferol, luteolin, and luteolin-7-O-glycoside) was enhanced in Achillea pachycephala along with up-regulated expression of PAL, CHS, CHI, FLS, and flavanone 3-hydroxylase (F3H). Similar results were also reported by Rezayian et al. (2018), where they showed that enhanced expression and activity of PAL in drought-stressed Brassica napus plants eventually led to higher content of phenolics and flavonoids. Higher content of rutin and caftaric acid was reported by Galieni et al. (2015) in Lactuca sativa gown under limited water supply. Griesser et al. (2015) and Castellarin et al. (2007) reported higher formation of polyphenolic compounds (4-coumaric acid, caffeic acid, ferulic acid, cis-resveratrol-3-O-glucoside, trans-resveratrol-3-O-glucoside, catechin, epicatechin, caftaric acid, epicatechin gallate, kaempferol-3-O-glucoside, cyanidin-3-O-glucoside, quercetin-3-O-glucoside and quercetin-3-O glucuronide) and anthocyanins along with higher expression of genes (UDP flavonoid glycosyltransferase, chalcone synthase and flavanone 3-hydroxylase) in drought-stressed Vitis vinifera. Additionally, the protective role of polyphenolic compounds in abrogating the negative effects of drought stress in various other plants like Nicotiana tabacum, Cucumis sativus, Chrysanthemum morifolium, Triticum aestivum, etc., has also been reported earlier (Silva et al., 2018; Li et al., 2018; Hodaei et al., 2018; Kaur & Zhawar, 2015). An interesting work was

236

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

demonstrated by Silva et al. (2018) where they showed that drought stress enhanced the activity of PAL in Nicotiana tabacum plants followed by higher formation of lignin that detoxified cytotoxic metabolites generated in plants thus enhancing tolerance capacity. Based on such earlier studies, we can conclude that polyphenolic compounds play a critical role in ameliorating the negative effects of drought stress in a variety of plants by scavenging the toxic compounds formed that in turn enhanced the survival capability of plants and also maintained the quality and quantity of grain yield. 9.4.2 SALINITY Salinity is a major problem all over the earth, affecting nearly 1 billion ha of land, which is more or less, about 20% worldwide land and also about half of the total arable land irrigated globally (Velmurugan et al., 2020). Poor irrigation approach, industrial pollution, and inappropriate application of fertilizers have drastically enhanced the amount of salt in the environment. High salt level in soil leads to excess accumulation of Na+ and Cl– ions in soil which results in hyperosmotic and hypertonic conditions that impede the absorption of nutrients and water from the soil (Ismail et al., 2014). Additionally, salinity also hampers germination, photosynthesis, growth, stomatal conductance, leaf water potential, and turgor pressure and enhances the ROS content in plant tissues. Thus, the presence of high salt levels in plants induces secondary stresses such as ionic stress and osmotic stress. To survive under high salt level, plants have to modify their biological and physiological processes like regulation of ions, homeostatic balance of cells and repair and control of cellular damages (Zhu, 2002). Polyphenolic compounds due to their higher antioxidative potential plays a pivotal role in conferring salt stress tolerance in plants. In response to salt stress, plants enhance the activity of enzymes controlling the phenylpropanoid pathway that stimulate the production of various phenolics and flavonoids having strong antioxidative potential. According to Wang et al. (2016), the expression of VvbHLH1 gene was up regulated in sunflower plants that resulted in higher synthesis of flavonoids by regulating the concerned genes of the biosynthetic pathway. Similarly, in another work, Chen et al. (2019a) showed that in response to salt stress, the expression of chalcone synthase 1 was up regulated in tobacco plants that resulted in higher formation of flavonoids directly favoring the detoxification of ROS in plant tissues. The level flavone biosynthesis was also reported to be enhanced in soybean

Role of Phenolic Acids and Flavonoids in the Mitigation

237

plants on being exposed to salt stress due to up regulated expressions of flavone synthase genes, i.e., GmFNSII-1 and GmFNSII-2 (Yan et al., 2014). Up regulated expression of genes also contributed towards higher formation of phenolics and flavonoids in plants. The level of total phenolics, i.e., HBAs (gallic acid, vanillic acid, syringic acid, p-hydroxybenzoic acid, ellagic acid) and HCAs (caffeic acid, chlorogenic acid, p-coumaric acid, m-coumaric acid, ferulic acid, sinapic acid, trans-cinnamic acid) and flavonoids (isoquercetin, hyperoside, rutin) were found to be enhanced in Amaranthus tricolor in response to salt stress (Sarker & Oba, 2018). Similarly, the level of total phenolics, quercetin, and kaempferol were found to be increased in salt stressed Olea europaea due to up regulated expression of PAL, CHI, C4H, 4-coumarate: CoA ligase (4CL) and CHS (Rossi et al., 2016). On being exposed to salt stress, the expression of PAL and FLS was found to be up regulated in Solanum villosum that eventually lowered the level of toxic metabolites by increasing the content of caffeic acid, total phenolics, quercetin, and 3-β-D-glucoside (Ben-Abdallah et al., 2019). The beneficial role of the above-mentioned metabolites was also observed in other plants such as Fragaria ananassa, Hordeum vulgare, Cynara cardunculus, Salvia mirzayanii and Salvia acrosiphon, etc. (Perin et al., 2019; Ma et al., 2019; Lucini et al., 2016; Valifard et al., 2015). 9.4.3 TEMPERATURE With the rise in industrial activities of the human population, the level of greenhouse gases (GHGs) has also increased in the atmosphere which constantly enhances the atmospheric temperature. Global temperature has appreciably increased in the last decade, and under present conditions, it is predicted by several groups that global temperature can further shoot up in an uncontrolled manner (Hansen et al., 2012). This abrupt rise in temperature poses an imminent challenge to growth, development, and yield of the plants. According to Larkindale et al. (2005), heat stress occurs when plants are exposed to higher temperature above the optimal temperature, which in turn hampers the fluidity and integrity of the membrane along with extensive aggregation of proteins. Additionally, HT also affects enzyme activity by altering their structure which may cause an imbalance of metabolic processes. In order to survive under heat stress, plants produce a variety of secondary protective metabolites along with phenolics and flavonoids. On being exposed to heat stress (35°C), the level of phenolics was increased in tomato

238

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

plants that conferred tolerance in plants (Rivero et al., 2001). It was further reported that higher levels of phenolics in stressed plants might be due to higher activity of PAL and lower activity of polyphenol oxidase. However, contrasting result was obtained in the case of watermelon where heat stress reduced the level of total phenolics in plants (Rivero et al., 2001). Recently, Ren et al. (2021) reported that exogenous application of γ-aminobutyric acid (GABA) enhanced the level of total phenolics in heat stressed (42°C/40°C) tea plants due to up regulated enzyme activity of PAL, C4H and 4-coumaroyl: CoA ligase along with higher transcript level of other enzymes (PAL, C4H, CHS, CHI, anthocyanin synthase, FLS, flavan-3-ol gallate synthase 1 and 4-coumaroyl: CoA ligase) involved in phenylpropanoid pathway. In contrast to these reports, Alhaithloul et al. (2019) reported that heat stress (35°C) lowered the level of total phenolics and total flavonoids in medicinal plants like Mentha piperita and Catharanthus roseus. Thus, there lies some ambiguity in the role of the above-mentioned metabolites in plants on being exposed to heat stress, and in coming years, more work needs to be done to further decipher the role of these important secondary metabolites. 9.4.4 HEAVY METAL Heavy metals generally occur in the crust of the earth and are extensively mined in several parts of the world. Such uncontrolled mining has extensively contributed toward anthropogenic input of heavy metals in the environment. Due to their non-degradable nature, they can persist in the environment for a long time which exerts toxic effects on microorganisms, plants, and human health. Heavy metals have turned out to be a major environmental issue for human population and in near future, condition is further going to deteriorate. Of all the heavy metals, arsenic, cadmium, lead, mercury, and chromium are ranked most toxic with significant effects on plant and human health (Keyster et al., 2020). Excess uptake and accumulation of metal in plants lead to the formation of ROS that in turn cause peroxidation of lipid membrane, higher electrolyte leakage, chlorophyll loss, retarded growth and development. Additionally, deposition of heavy metal in grains lead to bioaccumulation of these metals, thus causing severe health hazards to human. Enhanced biosynthesis of polyphenols in plants under metal stress scavenges toxic radicals protecting plants from oxidative damage. According to Williams et al. (2004), flavonoids can further induce the metal chelation property in plants which lowers the formation of hydroxyl radicals. The

Role of Phenolic Acids and Flavonoids in the Mitigation

239

level of anthocyanins and flavonols significantly shoot up along with the level of other flavonoids in stressed plants (Handa et al., 2019). Zafari et al. (2016) and Chen et al. (2019b) stated that the level of phenolic acid was also enhanced in stressed plants due to higher activity of enzymes involved in phenylpropanoid pathways such PAL, CHS, shikimate dehydrogenase, cinnamyl alcohol dehydrogenase (CAD), and polyphenol oxidase which were further regulated by the transcript levels of genes encoding such enzymes. Flavonoids also play a pivotal role in scavenging H2O2 formed and are considered to play a major part in the ascorbate-peroxidase cycle (Keilig et al., 2009). The protective role of polyphenols against metal toxicity has been widely reported in various crops. Poonam et al. (2015) and Handa et al. (2019) demonstrated that the level of total phenolics, flavonoids, caffeic acid, coumaric acid, kaempferol, and anthocyanins was enhanced in copper and cadmium stressed Brassica juncea, respectively. Further, Handa et al. (2019) stated that higher level of the above-mentioned secondary metabolites could be explained by up regulated expression of PAL and CHS. Increased level of phenolic acids along with other polyphenols like vanillic acid and chlorogenic acid was also noted to be enhanced in Zea mays on being exposed to copper, lead or cadmium toxicity (Kisa et al., 2016). In a similar study, Chen et al. (2019b) reported that the level of phenolic acids along with activity of phenol metabolizing enzymes like polyphenol oxidase, CAD and shikimate dehydrogenase were found to be enhanced in cadmium and zinc stressed Kandelia obovata. Lead-induced accumulation of H2O2 in Prosopis farcta was scavenged by enhanced formation of polyphenolic compounds such as ferulic acid, caffeic acid, cinnamic acid, daidzein, vitexin, resveratrol, myricetin, quercetin, kaempferol, naringenin, luteolin, and diosmin that was accompanied by enhanced activity of PAL (Zafari et al., 2016). Thus, based on these earlier studies, it can be inferred that the above-mentioned metabolites play a significant role in abrogating the negative effects of metal stress (whether single-applied or combined) in plants. 9.4.5 UV RADIATION Since the advent of human civilization, UV radiation has reached the earth’s surface, but due to human activities, the ozone layer has been depleted in recent decades, which has subsequently increased the amount of UV radiation (Rowland et al., 2006). Plants being sessile organisms are inevitably exposed to UV radiation. Higher doses of radiation can cause metabolic disorders

240

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

in plants. Altered morphological traits, biochemical changes, physiological characters, and genetic changes are a few adaptive modifications that occur in plants on being exposed to mild UV radiation (Yang et al., 2005; Kumari et al., 2010). In order to combat the negative effects of radiation, plants develop certain protective structures (waxes, hairs, and other cellular modifications that provide protection against optical damages) and higher formation of protective metabolites (phenolics, flavonoids, and osmolytes) (Kakani et al., 2003; Hamid et al., 2018). Polyphenols can absorb wavelength ranging in between 280 nm and 350 nm and thus they directly provide protection to the plants by absorbing UV radiation. Additionally, their high antioxidative potential also protects plants tissues from oxidative damage. Such enhanced synthesis of polyphenolic compounds is mainly due to higher activity of enzymes controlling flavonoid biosynthesis pathways and their corresponding gene transcripts levels (Kolb et al., 2001). The key enzymes up regulated in plants in response to UV radiation are PAL, CHS, flavanone 3β-hydroxylase, dihydroflavonol 4-reductase (DFR), FLS, CHI and flavonoid glycosyltransferases (FGT) (Xu et al., 2017). Liu et al. (2012) reported that the level of flavonoids and anthocyanins was induced in Caryopteris mongolica in response to UV radiation due to higher activity of PAL and CHI. Similar reports were also published by Xu et al. (2017) where they reported that UV radiation up regulated the expression of the enzymes controlling the flavonoid pathway that eventually enhanced the level of secondary metabolites such as kaempferol, ellagic acid, glucoside derivative of cyanidin, pelargonidin, and quercetin in Fragaria × ananassa. Enhanced levels of free, bound, and total phenolics in wheat plants along with higher activity of PAL enzyme ameliorated the negative effects of UV radiation (Chen et al., 2019c). The beneficial effects of polyphenolic compounds against UV radiation have also been established in other crops like Vigna radiata, Vitis vinifera, Lactuca sativa, Solanum lycopersicum and Brassica oleracea (Goyal et al., 2014; Berli et al., 2011; Sytar et al., 2018; Mariz-Ponte et al., 2018; Moreira-Rodriguez et al., 2017). 9.5 CONCLUSION Polyphenols play a pivotal in plant-environment interactions. In this chapter, we tried to summarize recent data from the available literature on the beneficial role of phenolic acid and flavonoids in stressed plants. Their high antioxidative property and bioactivity contributes towards detoxification of

Role of Phenolic Acids and Flavonoids in the Mitigation

241

cytotoxic metabolites that confers abiotic stress tolerance in plants. Numerous studies have demonstrated the ameliorating role of polyphenolic compounds in plants against abiotic stresses such as drought, salinity, heat, UV radiation and heavy metals. Abiotic stresses activate the signaling processes that eventually up regulate the transcript levels of enzymes controlling the phenylpropanoid pathway that results in higher tolerance capability of plants. The increase in plant resistance is correlated with the multiple functions of polyphenols in plants, principally consisting in their ROS scavenging ability and/or the capacity of some polyphenol classes to protect the plant from excessive light such as UV (flavonoids) and visible light (anthocyanins). Thus, the role of polyphenols in stressed plants is widely known, and a huge number of articles have been published in the past. In spite of such wide knowledge, the role of specialized polyphenols in response to certain abiotic stresses and the mechanisms which cause a shift from primary metabolism to the up regulation of phenylpropanoid pathway is yet unexplored. Therefore, in the coming years, such areas need to be addressed that can further enhance the beneficial role of these widely available secondary metabolites. ACKNOWLEDGMENTS Financial assistance from the Science and Engineering Research Board, Government of India, through the grant [EMR/2016/004799] and Department of Higher Education, Science and Technology and Biotechnology, Government of West Bengal, through the grant [264(Sanc.)/ST/P/S&T/1G-80/2017] to Dr. Aryadeep Roychoudhury is gratefully acknowledged. KEYWORDS • • • • • •

abiotic stresses Cucumis sativus flavonoids phenolic acids phenylalanine ammonia-lyase shikimate/phenylpropanoid pathway

242

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

REFERENCES Abdel-Farid, I. B., Marghany, M. R., Rowezek, M. M., & Sheded, M. G., (2020). Effect of salinity stress on growth and metabolomic profiling of Cucumis sativus and Solanum lycopersicum. Plants, 9, 1626. Ahmad, M. Z., Li, P., Wang, J., Rehman, N. U., & Zhao, J., (2017). Isoflavone malonyl transferases GmIMaT1 and GmIMaT3 differently modify isoflavone glucosides in soybean (Glycine max) under various stresses. Front Plant Sci., 8, 735. Alhaithloul, H. A., Soliman, M. H., Ameta, K. L., El-Esawi, M. A., & Elkelish, A., (2019). Changes in ecophysiology, osmolytes, and secondary metabolites of the medicinal plants of Mentha piperita and Catharanthus roseus subjected to drought and heat stress. Biomolecules, 10, 43. Andreasen, M. F., Christensen, L. P., Meyer, A. S., & Hansen, A., (2000). Content of phenolic acids and ferulic acid dehydrodimers in 17 rye (Secale cereale L.) varieties. J. Agric. Food Chem., 48, 2837–2842. Bais, H. P., Vepachedu, R., Gilroy, S., Callaway, R. M., & Vivanco, J. M., (2003). Allelopathy and exotic plant invasion: From molecules and genes to species interactions. Science, 301, 1377–1380. Barros, J., Serrani-Yarce, J. C., Chen, F., Baxter, D., Venables, B. J., & Dixon, R. A., (2016). Role of bifunctional ammonia-lyase in grass cell wall biosynthesis. Nat. Plants, 2, 16050. Ben-Abdallah, S., Zorrig, W., Amyot, L., Renaud, J., Hannoufa, A., Lachâal, M., & KarrayBouraoui, N., (2019). Potential production of polyphenols, carotenoids and glycoalkaloids in Solanum villosum mill. under salt stress. Biologia, 74, 309–324. Berli, F. J., Fanzone, M., Piccoli, P., & Bottini, R., (2011). Solar UV-B and ABA are involved in phenol metabolism of Vitis vinifera L. increasing biosynthesis of berry skin polyphenols. J. Agric. Food Chem., 59, 4874–4884. Castellarin, S. D., Pfeiffer, A., Sivilotti, P., Degan, M., Peterlunger, E., & Di Gaspero, G., (2007). Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant Cell Environ., 30, 1381–1399. Chen, S., Wang, Q., Lu, H., Li, J., Yang, D., Liu, J., & Yan, C., (2019b). Phenolic metabolism and related heavy metal tolerance mechanism in Kandelia obovata under Cd and Zn stress. Ecotoxicol. Environ. Saf., 169, 134–143. Chen, S., Wu, F., Li, Y., Qian, Y., Pan, X., Li, F., Wang, Y., et al., (2019a). NtMYB4 and NtCHS1 are critical factors in the regulation of flavonoid biosynthesis and are involved in salinity responsiveness. Front Plant Sci., 10, 178. Chen, Z., Ma, Y., Weng, Y., Yang, R., Gu, Z., & Wang, P., (2019c). Effects of UV-B radiation on phenolic accumulation, antioxidant activity and physiological changes in wheat (Triticum aestivum L.) seedlings. Food Biosci., 30, 100409. Cuong, D. M., Kwon, S. J., Van, N. B., Chun, S. W., Kim, J. K., & Park, S. U., (2020). Effect of salinity stress on phenylpropanoid genes expression and related gene expression in wheat sprout. Agronomy, 10, 390. Daryanto, S., Wang, L., & Jacinthe, P. A., (2016). Global synthesis of drought effects on maize and wheat production. PLoS One, 11, e0156362. Dini, C., Zaro, M. J., & Viña, S. Z., (2019). Bioactivity and functionality of anthocyanins: A review. Curr. Bioact. Compd., 15, 507–523. Ferrer, J., Austin, M., Stewart, C. J., & Noel, J., (2008). Structure and function of enzymes involved in the biosynthesis of phenylpropanoids. Plant. Physiol. Biochem., 46, 356–370.

Role of Phenolic Acids and Flavonoids in the Mitigation

243

Galieni, A., Di Mattia, C., De Gregorio, M., Speca, S., Mastrocola, D., Pisante, M., & Stagnari, F., (2015). Effects of nutrient deficiency and abiotic environmental stresses on yield, phenolic compounds and antiradical activity in lettuce (Lactuca sativa L.). Sci. Hortic., 187, 93–101. Gharibi, S., Sayed, T. B. E., Saeidi, G., Talebi, M., & Matkowski, A., (2019). The effect of drought stress on polyphenolic compounds and expression of flavonoid biosynthesisrelated genes in Achillea pachycephala rech. f. Phytochemistry, 162, 90–98. Goleniowski, M. E., Bonfill, M., Cusido, R., & Palazon, J., (2013). Phenolic acids. In: Ramawat, K., & Mérillon, J. M., (eds.), Natural Products (pp. 1951–1973). Springer Science and Business Media: Berlin/Heidelberg, Germany. González-Sarrías, A., Tomás-Barberán, F. A., & García-Villalba, R., (2020). Structural diversity of polyphenols and distribution in foods. In: Tomás-Barberán, F. A., GonzálezSarrías, A., & Gar-cía-Villalba, R. R., (eds.) Dietary Polyphenols: Their Metabolism and Health Effects (pp. 1–29). Wiley, Chichester, UK. Goyal, A., Siddiqui, S., Upadhyay, N., & Soni, J., (2014). Effects of ultraviolet irradiation, pulsed electric field, hot water and ethanol vapors treatment on functional properties of mung bean sprouts. J. Food Sci. Technol., 51, 708–714. Griesser, M., Weingart, G., Schoedl-Hummel, K., Neumann, N., Becker, M., Varmuza, K., Liebner, F., et al., (2015). Severe drought stress is affecting selected primary metabolites, polyphenols, and volatile metabolites in grapevine leaves (Vitis vinifera cv. Pinot noir). Plant Physiol. Biochem., 88, 17–26. Gutierrez-Gonzalez, J. J., Guttikonda, S. K., Tran, L. S. P., Aldrich, D. L., Zhong, R., Yu, O., Nguyen, H. T., & Sleper, D. A., (2010). Differential expression of isoflavone biosynthetic genes in soybean during water deficits. Plant Cell Physiol., 51, 936–948. Hamid, A., Singh, S., Agrawal, M., & Agrawal, S. B., (2018). Heteropogon contortus BL-1 (Pilli grass) and elevated UV-B radiation: The role of growth, physiological and biochemical traits in determining forage productivity and quality. Photochem. Photobiol. doi: 10.1111/ php.12990. Handa, N., Kohli, S. K., Sharma, A., Thukral, A. K., Bhardwaj, R., Abd_Allah, E. F., Alqarawi, A. A., & Ahmad, P., (2019). Selenium modulates dynamics of antioxidative defense expression, photosynthetic attributes and secondary metabolites to mitigate chromium toxicity in Brassica juncea L. plants. Environ. Exp. Bot., 161, 180–192. Hansen, J., Sato, M., & Ruedy, R., (2012). Perception of climate change. Proc. Natl. Acad. Sci. USA, 109, 2415–2423. Harborne, J. B., & Williams, C. A., (2000). Advances in flavonoid research since 1992. Phytochemistry, 55, 481–504. Hattenschwiler, S., & Vitousek, P. M., (2000). The role of polyphenols in terrestrial ecosystem nutrient cycling. Tree, 15, 238–243. He, M., Yao, Y., Li, Y., Yang, M., Li, Y., Wu, B., & Yu, D., (2019). Comprehensive transcriptome analysis reveals genes potentially involved in isoflavone biosynthesis in Pueraria thomsonii benth. PLoS One, 14, e0217593. Hernandez, I., Alegre, L., & Munne-Bosch, S., (2004). Drought-induced changes in flavonoids and other low molecular weight antioxidants in Cistus clusii grown under Mediterranean field conditions. Tree Physiol., 24, 1303–1311. Hernandez, I., Alegre, L., Van, B. F., & Munne-Bosch, S., (2009). How relevant are flavonoids as antioxidants in plants? Trends Plant Sci., 14, 125–132.

244

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Hodaei, M., Rahimmalek, M., Arzani, A., & Talebi, M., (2018). The effect of water stress on phytochemical accumulation, bioactive compounds and expression of key genes involved in flavonoid biosynthesis in Chrysanthemum morifolium L. Ind. Crop Prod., 120, 295–304. Huyskens-Keil, S., Eichholz, I., Kroh, L., & Rohn, S., (2012). UV-B induced changes of phenol composition and antioxidant activity in blackcurrant fruit (Ribes nigrum L.). J. Appl. Bot. Food Qual., 81, 140–144. Ismail, A., Takeda, S., & Nick, P., (2014). Life and death under salt stress: Same players, different timing? J. Exp. Bot., 65, 2963–2979. Kakani, V. G., Reddy, K. R., Zhao, D., & Sailaja, K., (2003). Field crop responses to ultraviolet-B radiation: A review. Agric. Forest Meteor., 120, 191–218. Kaur, G., Kumar, S., Nayyar, H., & Upadhyaya, H., (2008). Cold stress injury during the pod-filling phase in chickpea (Cicer arietinum L.): Effects on quantitative and qualitative components of seeds. J. Agron. Crop Sci., 194, 457–464. Kaur, L., & Zhawar, V. K., (2015). Phenolic parameters under exogenous ABA, water stress, and salt stress in two wheat cultivars varying in drought tolerance. Indian J. Plant Physiol., 20, 151–156. Keilig, K., & Ludwig-Mueller, J., (2009). Effect of flavonoids on heavy metal tolerance in Arabidopsis thaliana seedlings. Bot. Stud., 50, 311–318. Keyster, M., Niekerk, L. A., Basson, G., Carelse, M., Bakare, O., Ludidi, N., Klein, A., et al., (2020). Decoding heavy metal stress signaling in plants: Towards improved food security and safety. Plants, 9, 1781. Khan, M. K., Huma, Z. E., & Dangles, O., (2014). A comprehensive review on flavanones, the major citrus polyphenols. J. Food Compos. Anal., 33, 85–104. Kidd, P. S., Llugany, M., Poschenrieder, C., Gunse, B., & Barcelo, J., (2001). The role of root exudates in aluminium resistance and silicon induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.). J. Exp. Bot., 52, 1339–1352. Kısa, D., Elmastas, M., Öztürk, L., & Kayır, Ö., (2016). Responses of the phenolic compounds of Zea mays under heavy metal stress. Appl. Biol. Chem., 59, 813–820. Kolb, C. A., Kaser, M. A., Kopecky, J., Zotz, G., Riederer, M., & Pfundel, E. E., (2001). Effects of natural intensities of visible and ultraviolet radiation on epidermal ultraviolet screening and photosynthesis in grape leaves. Plant Physiol., 127, 863–875. Kovinich, N., Kayanja, G., Chanoca, A., Riedl, K., Otegui, M. S., & Grotewold, E., (2014). Not all anthocyanins are born equal: Distinct patterns induced by stress in Arabidopsis. Planta, 240, 931–940. Kumari, R., Singh, S., & Agrawal, S. B., (2010). Response of ultraviolet-B induced antioxidant defense system in a medicinal plant Acorus calamus. J. Environ. Bot., 31, 907–911. Kytidou, K., Artola, M., Overkleeft, H. S., & Aerts J. M. F. G., (2020). Plant glycosides and glycosidases: A treasure-trove for therapeutics. Front Plant Sci., 11, 357. Lam, T. B. T., Kadoya, K., & Liyama, K., (2001). Bonding of hydroxycinnamic acids to lignin: Ferulic and p-coumaric acids are predominantly linked at the benzyl position of lignin, not the β-position, in grass cell walls. Phytochemistry, 57, 987–992. Larkindale, J., Hall, J. D., Knight, M. R., & Vierling, E., (2005). Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol., 138, 882–897. Li, M., Li, Y., Zhang, W., Li, S., Gao, Y., Ai, X., Zhang, D., Liu, B., & Li, Q., (2018). Metabolomics analysis reveals that elevated atmospheric CO2 alleviates drought stress in cucumber seedling leaves. Anal. Biochem., 559, 71–85.

Role of Phenolic Acids and Flavonoids in the Mitigation

245

Liu, M., Cao, B., Zhou, S., & Liu, Y., (2012). Responses of the flavonoid pathway to UV-B radiation stress and the correlation with the lipid antioxidant characteristics in the desert plant Caryopteris mongolica. Acta Ecol. Sin., 32, 150–155. Liu, Y., Liu, J., Wang, Y., Abozeid, A., Tian, D. M., Zhang, X. N., & Tang, Z. H., (2017). The different resistance of two Astragalus plants to UV-B stress is tightly associated with the organ-specific isoflavone metabolism. Photochem. Photobiol., 94, 115–125. Lucini, L., Borgognone, D., Rouphael, Y., Cardarelli, M., Bernardi, J., & Colla, G., (2016). Mild potassium chloride stress alters the mineral composition, hormone network, and phenolic profile in artichoke leaves. Front Plant Sci., 7, 948. Ma, Y., Wang, P., Gu, Z., Tao, Y., Shen, C., Zhou, Y., Han, Y., & Yang, R., (2019). Ca2+ involved in GABA signal transduction for phenolics accumulation in germinated hulless barley under NaCl stress. Food Chem. X, 2, 100023. Macheix, J. J., Fleuriet, A., & Billot, J., (1990). Fruit Phenolics. CPC Press: Boca Raton, FL, USA. Maeda, H., & Dudareva, N., (2012). The shikimate pathway and aromatic amino acid biosynthesis in plants. Annu. Rev. Plant Biol., 63, 73–105. Mantri, N., Patade, V., Penna, S., Ford, R., & Pang, E., (2012). Abiotic stress responses in plants: Present and future. In: Ahmad, P., & Prasad, M. N. V., (eds.), Abiotic Stress Responses in Plants (pp. 1–19). Springer, New York. Mariz-Ponte, N., Mendes, R. J., Sario, S., De Oliveira, J. F., Melo, P., & Santos, C., (2018). Tomato plants use non-enzymatic antioxidant pathways to cope with moderate UV-A/B irradiation: A contribution to the use of UV-A/B in horticulture. J. Plant Physiol., 221, 32–42. Martens, S., Preuss, A., & Matern, U., (2010). Multifunctional flavonoid dioxygenases: Flavonols and anthocyanin biosynthesis in Arabidopsis thaliana L. Phytochemistry, 71, 1040–1049. Martinez, V., Mestre, T. C., Rubio, F., Girones-Vilaplana, A., Moreno, D. A., Mittler, R., & Rivero, R. M., (2016). Accumulation of flavonols over hydroxycinnamic acids favors oxidative damage protection under abiotic stress. Front Plant Sci., 7, 838. Massacci, A. S. M., Nabiev, L., Pietrosanti, S. K., Nematov, T. N., Chernikova, K. T., & Leipner, J., (2008). Response of the photosynthetic apparatus of cotton (Gossypium hirsutum) to the onset of drought stress under field conditions studied by gas-exchange analysis and chlorophyll fluorescence imaging. Plant Physiol. Biochem., 46, 189–195. Moreira-Rodriguez, M., Nair, V., Benavides, J., Cisneros-Zevallos, L., & Jacobo-Velazquez, D. A., (2017). UVA, UVB light, and methyl jasmonate, alone or combined, redirect the biosynthesis of glucosinolates, phenolics, carotenoids, and chlorophylls in broccoli sprouts. Int. J. Mol. Sci., 18, 2330. Nakabayashi, R., Yonekura-Sakakibara, K., Urano, K., Suzuki, M., Yamada, Y., Nishizawa, T., Matsuda, F., et al., (2014). Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J., 77, 367–379. Nascimento, L. B. D. S., Leal-Costa, M. V., Menezes, E. A., Lopes, V. R., Muzitano, M., Costa, S. S., & Tavares, E. S., (2015). Ultraviolet-B radiation effects on phenolic profile and flavonoid content of Kalanchoe pinnata. J. Photochem. Photobiol. B Biol., 148, 73–81. Panche, A. N., Diwan, A. D., & Chandra, S. R., (2016). Flavonoids: An overview. J. Nutr. Sci., 5, e47.

246

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Parvin, K., Nahar, K., Hasanuzzaman, M., Bhuyan, M. B., Mohsin, S. M., & Fujita, M., (2020). Exogenous vanillic acid enhances salt tolerance of tomato: Insight into plant antioxidant defense and glyoxalase systems. J. Plant Physiol. Biochem., 150, 109–120. Perin, E. C., Da Silva, M. R., Borowski, J. M., Crizel, R. L., Schott, I. B., Carvalho, I. R., Rombaldi, C. V., & Galli, V., (2019). ABA-dependent salt and drought stress improve strawberry fruit quality. Food Chem., 271, 516–526. Pervaiz, T., Songtao, J., Faghihi, F., Haider, M. S., & Fang, J., (2017). Naturally occurring anthocyanin, structure, functions and biosynthetic pathway in fruit plants. J. Plant Biochem. Physiol., 5, 1–9. Poonam, R. K., Bhardwaj, R., & Sirhindi, G., (2015). Castasterone regulated polyphenolic metabolism and photosynthetic system in Brassica juncea plants under copper stress. J. Pharmacogn. Phytochem., 4, 282–289. Ren, T., Zheng, P., Zhang, K., Liao, J., Xiong, F., Shen, Q., MA, Y., et al., (2021). Effects of GABA on the polyphenol accumulation and antioxidant activities in tea plants (Camellia sinensis L.) under heat-stress conditions. Plant Physiol. Biochem., 159, 363–371. Rezayian, M., Niknam, V., & Ebrahimzadeh, H., (2018). Differential responses of phenolic compounds of Brassica napus under drought stress. Iran J. Plant Physiol., 8, 2417–2425. Rivero, R. M., Ruiz, J. M., Garcı́a, P. C., López-Lefebre, L. R., Sánchez, E., & Romero, L., (2001). Resistance to cold and heat stress: Accumulation of phenolic compounds in tomato and watermelon plants. Plant Sci., 160, 315–321. Rossi, L., Borghi, M., Francini, A., Lin, X., Xie, D. Y., & Sebastiani, L., (2016). Salt stress induces differential regulation of the phenylpropanoid pathway in Olea europaea cultivars Frantoio (salt-tolerant) and Leccino (salt-sensitive). J. Plant Physiol., 204, 8–15. Rowland, F. S., (2006). Stratospheric ozone depletion. Phi. Trans. R Soc. B, 361, 769–790. Šamec, D., Karalija, E., Šola, I., Vujcic, B. V., & Salopek-Sondi, B., (2021). The role of polyphenols in abiotic stress response: The influence of molecular structure. Plants, 10, 118. Sanchez-Rodriguez, E., Moreno, D. A., Ferreres, F., Rubio-WilhelmiMdel, M., & Ruiz, J. M., (2011). Differential responses of five cherry tomato varieties to water stress: Changes on phenolic metabolites and related enzymes. Phytochemistry, 72, 723–729. Sarker, U., & Oba, S., (2018). Augmentation of leaf color parameters, pigments, vitamins, phenolic acids, flavonoids and antioxidant activity in selected Amaranthus tricolor under salinity stress. Sci. Rep., 8, 12349. Saviranta, N. M., Julkunen-Tiitto, R., Oksanen, E., & Karjalainen, R. O., (2009). Red clover (Trifolium pratense L.) isoflavones: Root phenolic compounds affected by biotic and abiotic stress factors. J. Sci. Food Agric., 90, 418–423. Sharma, A., Shahzad, B., Rehman, A., Bhardwaj, R., Landi, M., & Zheng, B., (2019a). Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules, 24, 2452. Sharma, A., Yuan, H., Kumar, V., Ramakrishnan, M., Kohli, S. K., Kaur, R., Thukral, A. K., et al., (2019b). Castasterone attenuates insecticide induced phytotoxicity in mustard. Ecotoxicol. Environ. Saf., 179, 50–61. Shi, J., Zhang, X., Zhang, Y., Lin, X., Li, B., & Chen, Z., (2020). Integrated metabolomic and transcriptomic strategies to understand the effects of dark stress on tea callus flavonoid biosynthesis. Plant Physiol. Biochem., 155, 549–559.

Role of Phenolic Acids and Flavonoids in the Mitigation

247

Silva, F. L. B., Vieira, L. G. E., Ribas, A. F., Moro, A. L., Neris, D. M., & Pacheco, A. C., (2018). Proline accumulation induces the production of total phenolics in transgenic tobacco plants under water deficit without increasing the G6PDH activity. Theor. Exp. Plant Physiol., 30, 251–260. Simic, A., Manojlovic, D. D., Segan, D., & Todorovic, M., (2007). Electrochemical behavior and antioxidant and prooxidant activity of natural phenolics. Molecules, 12, 2327–2340. Singh, S. A., & Christendat, D., (2007). The DHQ-dehydroshikimate-SDH-shikimateNADP(H) complex: Insights into metabolite transfer in the shikimate pathway. Cryst. Growth Des., 7, 2153–2160. Strack, D., (1997). Phenolic metabolism. In: Dey, P. M., & Harborne, J. B., (eds.), Plant Biochemistry (p. 387). Academic Press, London, UK. Swigonska, S., Amarowicz, R., Król, A., Mostek, A., Badowiec, A., & Weidner, S., (2014). Influence of abiotic stress during soybean germination followed by recovery on the phenolic compounds of radicles and their antioxidant capacity. Acta Soc. Bot. Pol., 83, 209–218. Sytar, O., Zivcak, M., Bruckova, K., Brestic, M., Hemmerich, I., Rauh, C., & Simko, I., (2018). Shift in accumulation of flavonoids and phenolic acids in lettuce attributable to changes in ultraviolet radiation and temperature. Sci. Hortic., 239, 193–204. Tohge, T., Watanabe, M., Hoefgen, R., & Fernie, A. R., (2013). Shikimate and phenylalanine biosynthesis in the green lineage. Front Plant Sci., 4, 62. Valifard, M., Mohsenzadeh, S., Niazi, A., & Moghadam, A., (2015). Phenylalanine ammonialyase isolation and functional analysis of phenylpropanoid pathway under salinity stress in ‘salvia’ species. Aust. J. Crop Sci., 9, 656–665. Velmurugan, A., Swarnam, P., Subramani, T., Meena, B., & Kaledhonkar, M. J., (2020). Water demand and salinity. Desalination - Challenges and Opportunities. Intech Open. Wang, F., Zhu, H., Chen, D., Li, Z., Peng, R., & Yao, Q., (2016). A grape bHLH transcription factor gene, VvbHLH1, increases the accumulation of flavonoids and enhances salt and drought tolerance in transgenic Arabidopsis thaliana. Plant Cell Tiss. Org. Cult., 125, 387–398. Wang, L., Shan, T., Xie, B., Ling, C., Shao, S., Jin, P., & Zheng, Y., (2019). Glycine betaine reduces chilling injury in peach fruit by enhancing phenolic and sugar metabolisms. Food Chem., 272, 530–538. Wen, L., Jiang, Y., Yang, J., Zhao, Y., Tian, M., & Yang, B., (2017). Structure, bioactivity, and synthesis of methylated flavonoids. Ann. NY Acad. Sci., 1398, 120–129. Williams, R. J., Spencer, J. P., & Rice-Evans, C., (2004). Flavonoids: Antioxidants or signaling molecules? Free Radic. Biol. Med., 36, 838–849. Xu, Y., Charles, M. T., Luo, Z., Mimee, B., Veronneau, P. Y., Rolland, D., & Roussel, D., (2017). Preharvest ultraviolet C irradiation increased the level of polyphenol accumulation and flavonoid pathway gene expression in strawberry fruit. J. Agric. Food Chem., 65, 9970–9979. Yan, J., Wang, B., Jiang, Y., Cheng, L., & Wu, T., (2014). GmFNSII-controlled soybean flavone metabolism responds to abiotic stresses and regulates plant salt tolerance. Plant Cell Physiol., 55, 74–86. Yang, Y., Yao, Y., Xu, G., & Li, C., (2005). Growth and physiological responses to drought and elevated ultraviolet-B in two contrasting populations of Hippophaer hamnoides. Physiol. Plant, 124, 431–440.

248

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Zafari, S., Sharifi, M., AhmadianChashmi, N., & Mur, L. A., (2016). Modulation of Pb-induced stress in Prosopis shoots through an interconnected network of signaling molecules, phenolic compounds and amino acids. Plant Physiol. Biochem., 99, 11–20. Zhu, J. K., (2002). Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol., 53, 247–273.

PART III Application and Analysis of Secondary Metabolites

CHAPTER 10

Seedling and Seed Priming in Regulating Secondary Metabolite Level for Stress Tolerance ROBAB SALAMI,1 MASOUMEH KORDI,1 NASSER DELANGIZ,2 BEHNAM ASGARI LAJAYER,3 and TESS ASTATKIE4*

Department of Plant Sciences and Biotechnology, Faculty of Life Sciences and Biotechnology, Shahid Beheshti University, Tehran, Iran 1

Department of Plant Biotechnology and Breeding, Faculty of Agriculture, University of Tabriz, Tabriz, Iran

2

Health and Environment Research Center, Tabriz University of Medical Science, Tabriz, Iran, E-mail: [email protected]

3

4 *

Faculty of Agriculture, Dalhousie University, Truro, NS B2N 5E3, Canada

Corresponding author. E-mail: [email protected]

ABSTRACT Priming is used to increase the germination rate of seeds or to increase their tolerance to stressful conditions. Priming affects plant metabolites, among which secondary metabolites have special importance and are activated as soon as the seed uptakes water. Secondary metabolites initiate seed-repairing mechanisms. DNA repairing and antioxidative systems of plants are repairing mechanisms that facilitate seed germination and seedling establishment. As a seed uptakes water, reactive oxygen species (ROS) released inside of it cause damage to proteins and lipids. However, plants have enzymatic and non-enzymatic defense systems to fight these invasive oxidants. Seed and seedling priming cause the production of secondary metabolites in plants. Biology and Biotechnology of Environmental Stress Tolerance in Plants: Secondary Metabolites in Environmental Stress Tolerance, Volume 1. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

252

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

This chapter examines the effects of seedling and seed priming on increasing their tolerance and resistance under environmental stresses. 10.1 INTRODUCTION Production of healthy seeds and seedlings can be the basis of efficient and healthy agricultural production. Proper and strong seed growth is especially important for the production of healthy plants in agriculture because weak seeds will be susceptible to diseases and stresses (Mwando, 2021). Seed and seedling priming is a good way to increase seed germination rate and increase seedling tolerance and resistance to adverse environmental conditions (Johnson & Puthur, 2021; Abbasi et al., 2021). Priming improves the seed vigor, which is a multi-gene trait and is of special importance in agriculture (Jisha et al., 2013). Plants make changes at different levels to adapt to adverse environmental conditions. These changes include morphological, physiological, biochemical, and molecular changes (Heshmat et al., 2021; Ghassemi et al., 2018, 2021; Asgari et al., 2017, 2019a, Saghafi et al., 2019a, b; Khadem Moghadam et al., 2019). Seed and seedling priming can have many beneficial effects on these changes. It can trigger or accelerate the changes. For example, priming can break seed or bud dormancy and exposes the plant to a wider temperature range (Rao et al., 2019). Also, seed and seedling priming can strengthen the plant in dealing with diseases and weeds. However, the response to stressful conditions in different plants is different and depending on the type of stress, environmental conditions, plant species, etc. Various methods have been adopted to reduce the negative effects of the environment on plants, including the use of different cultivation patterns, the use of genetic engineering, the use of plant breeding and the optimization of plant nutrition. Because the optimal use of these methods often requires accurate identification of genes involved in stress resistance, and because many genes are involved, simpler methods need to be developed. In recent years, various biotechnological approaches such as QTL mapping, characterization of drought-responsive genes, genome-wide association studies (GWAS), and genetic engineering are being followed to mitigate the effects of drought stress, but the risk assessors still face challenges in assessing the food and environmental safety of genetically modified crops (GM crops) (Liang, 2016).

Seedling and Seed Priming in Regulating Secondary Metabolite Level

253

Secondary metabolites are considered as organic compounds that play an indirect role in plant processes (Asgari Lajayer et al., 2017, 2019b). Lack of secondary metabolites in the plant may not lead to immediate death, but it can cause effects such as weakening and deformity in the plant. These substances can protect the plant against invaders or non-living stresses. In addition, they act as a medicine or flavoring for humans. Over the last 20–30 years, analyzes of secondary production in plants have greatly improved using new techniques. Secondary metabolites may often be created by synthetic modification of the primary metabolites by sharing the primary material of the primary metabolites (Ping & Yee, 2021). Seed and seedling priming has attracted a lot of attention, but in the study of the effects of priming, more in-depth studies with modern approaches need to be done to identify the mechanisms involved in this area as soon as possible and to increase the efficiency of agricultural production. Holistic approaches such as omics in recent years have deciphered priming-influenced processes with power and success. However, a better understanding of the metabolic events during the priming treatment is needed to use this technology in a more efficient way. In this chapter, we investigate the function of secondary metabolites under the influence of seed and seedling priming under stress conditions. 10.2 DROUGHT TOLERANCE Drought stress is the most destructive environmental stress that can severely reduce seedling growth and development or prevent seed germination and seedling emergence (Kaya et al., 2006; Khoshmanzar et al., 2020). Global warming has caused a lot of damage to crops and horticulture every year, and this trend could get worse every year. Under this condition, the soil water potential is reduced and consequently, the plant or the seed will not be able to absorb water (Farooq et al., 2009). The destructive effects of drought stress are manifested through the production of reactive oxygen species (ROS) in cells, and it is necessary for plants to mitigate these effects as much as possible (Ashraf & Rauf, 2001; Gill & Tuteja, 2010). There are several ways to increase plant adaptation to drought stress, but seed and seedling priming is one of the inexpensive methods that can be easily done (Ashraf & Foolad, 2005). Seed and seedling priming is a simple and inexpensive way to increase plant tolerance to drought stress. Drought stress is a determining factor in seed germination rate and seedling growth vigor. The species of the

254

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

plant is also important in this case. However, seed and seedling priming can reduce the detrimental effect of drought stress. There are different priming methods. Among them is wheat seed priming with ascorbic acid, which has increased drought tolerance in this plant (Farooq et al., 2013). Also, water and KNO3 priming of sunflower seeds increased seed germination and seedling growth and development under drought and salinity stress (Kaya et al., 2006). Moreover, PEG and hydro-priming of rice seeds improved the drought stress tolerance in germination stage (Yuan-Yuan et al., 2010). Seed and seedling priming by applying changes in plant physiology and metabolites can show its positive effects and improve plant adaptation under stress conditions (Shehab et al., 2010). Enzymes play an important role in plant adaptation to stressful conditions. These enzymes include catalase (CAT), peroxidase (POX), superoxide dismutase (SOD), etc. (Farhad et al., 2011). In addition, soluble proteins and sugars and proline as osmoprotectants play an important role in this issue (Farhad et al., 2011). The activity of antioxidant enzymes neutralizes ROS and mitigates its destructive effects (Figure 10.1). Moreover, osmoprotectants keep the cell water level at an optimal level and prevent cell disruption.

FIGURE 10.1  ROS is produced when the plant is stressed. Under this condition, antioxidant enzymes are produced in order for the plant to survive. Seed and seedling priming can be used to enhance the action of antioxidative enzymes.

Seedling and Seed Priming in Regulating Secondary Metabolite Level

255

10.3 TEMPERATURE STRESS TOLERANCE Temperature stress could be stress caused by high temperature (HT) or low temperature. Seed and seedling priming can produce phenotypes resistant to high and low temperatures. For instance, priming of potato seedlings with hydrogen peroxide (H2O2) has caused resistance to transient low temperature in this plant (Işeri et al., 2013). Anthocyanin content of treated plants was much higher than control plants. Resistant plants also showed higher RWC (relative water content) levels and lower MDA (malondialdehyde) levels. Moreover, the amount of APX (ascorbate peroxidase) and CAT in acclimated plants were more than the ones in the control plants (Işeri et al., 2013). Wang et al. (2014) reported that priming of Festuca arundinacea and Lolium perenne seedlings by H2O2 increased its resistance to HTs. In their study, the higher activity of CAT, GR (glutathione reductase), APX, POD (Peroxidase) and GPX (glutathione peroxidase) was observed in treated plants under heat stress compared with control plants. Compared to other abiotic stresses, cold stress is one of the most limiting factors for plant growth and development (Hussain et al., 2018; Ghassemi et al., 2021). In the early stages of germination and seedling growth, cold stress can severely affect plant growth and development, so seed and seedling priming can greatly reduce the negative effects of cold. These include hormonal priming, nutritional priming, hydropriming, and chemical priming (Hussain et al., 2018; Jisha et al., 2013; Paparella et al., 2015). One of the reasons that seed and seedling priming cause stress resistance in the plant is the activation of antioxidant enzymes. Salicylic acid (SA) and H2O2 priming of seeds and seedling can enhance the seed germination rate and growth of plant as it suppresses the ROS accumulation, and regulates hormonal metabolism, metabolites, and energy supply (Li et al., 2017). Xu et al. (2011) stated that priming the seeds of the tobacco plant increases the germination and the growth rate of the subsequent plant. They mentioned that the activation of antioxidant enzymes is the major cause of those results. This provides more available energy for seeds and seedlings so that they can more easily withstand low temperatures (Wang et al., 2016). Seedlings obtained from primed seeds showed higher levels of proline, soluble carbohydrates and soluble protein in their tissues than that in control plants (Turk et al., 2014). 10.4 BIOTIC STRESSES Agricultural production is strongly influenced by biological stressors, and every year a large amount of these products is damaged by diseases

256

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

and pests. As climate change accelerates, so does the negative impact of biological stress. Therefore, it is necessary to find ways to develop resistance to these stresses. The commonly known diseases are rust, root diseases, canker, wilt, blast, and blight (Medda et al., 2015). Improper use of synthetic pesticides to prevent diseases and pests has caused irreversible destructive effects on various organisms, including humans. The recent approach to prevent the destructive effects of biotic stresses is to create resistance in plants in order to reduce the destructive effects of diseases and pests by strengthening the plant’s own defense system. Every plant is susceptible to some parasites, tolerates some, and is resistant to others (Horns & Hood, 2012). Some methods have been developed by researchers to increase plant’s resistance and tolerance to parasites. One of the modern methods is the expression of resistance induction genes in plants. For example, expression of alfAFP (alfalfa anti-fungal peptide) gene in potato plant has caused resistance to Verticillium in greenhouse condition (Gao et al., 2000). These methods are often costly and timeconsuming and, in some cases, pose safety problems. So, it is important to develop some inexpensive and safe methods that can be conducted easily. Seed and seedling priming are used to induce plants’ resistance and tolerance to diseases and pests. Some biochemical reactions in plants can be enhanced or even started by priming. Beckers & Conrath (2007) stated that if priming makes the defense response in the plant faster or stronger, then it is considered effective. Hydropriming of maize seeds with plant extracts is effective against toxigenic fungi and improves seed quality parameters (Ayaz et al., 2014). Redox state of plants is important and plays a crucial role in their growth and development. The redox state is changed in plants exposed to environmental stimuli. The extent of this reaction depends on the nature, dose, and duration of the stimulus. In addition, the potential of the plant to respond to the stimuli indicates the redox state (Jisha et al., 2013). Gama ray, UV ray, and X-ray priming improves seedling strength and seed germination rate. Priming seeds with microorganisms that is known as biopriming can be beneficial in seed germination and seedling strength (Waqas et al., 2019). Seed priming helps to reduce seed response time to disease. Also, seedling priming improves the seedling disease tolerance and enhances the yield of crops (Jisha et al., 2013). The characteristics that are created in seeds and seedlings through priming can be transferred to the next generation (Lal et al., 2018). To increase the efficiency of seed and seedling priming, the method used, the time, and the cost should be considered.

Seedling and Seed Priming in Regulating Secondary Metabolite Level

257

10.5 OMICS APPROACH IN PRIMING Identification of primed seed and seedling biomarkers is important for plant physiologists. For example, when a seed absorbs water and a series of biochemical reactions begin in it, it is possible to study very carefully what happens at each molecular level inside the seed by studying its biomarkers. This gives a clear understanding of the processes involved in germination and can help researchers develop appropriate priming techniques for each seed. In most cases, there is no direct relationship between translation and transcription. This means that we cannot study the functions of proteins in the next step by studying mRNA, and therefore these two steps should be studied separately. However, this approach has its drawbacks, the most important of which is that it is expensive. 10.5.1 TRANSCRIPTOMICS Transcriptomics is the study of transcriptomes, a collection of RNAs that are transcribed under certain conditions through high-throughput approaches (Motie-Noparvar et al., 2020). Drought stress increases transcripts in Brassica oleracea seeds, which decreases through the osmopriming and germination process (Ali et al., 2019). Transcriptomic data revealed that the molecular study related to such feature might be comparable to those included in the usual seed dehydration procedure in the maturation. In Medicago truncatula, in germination, the expression of the same genes is increased, which manifests scarcity stresses. When priming occurs, these genes are expressed after water uptake, while genes involved in cell wall generation, metabolic energy, and cell cycle are suppressed (Buitink et al., 2006). Transcripts that accumulate after seed priming include those encoded by seed-load late embryogenesis abundant (LEA) proteins. Although genes incorporated in cell wall alterations and photosynthesis process are normally suppressed (Maia et al., 2011). Transcriptomics can also be used to treat epigenetic changes caused by priming. 10.5.2 METABOLOMICS Metabolome means the metabolic content of plant tissue at a given time under certain conditions. Metabolomics has developed a new approach to the study of cell biochemistry. This approach is done quantitatively and

258

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

qualitatively and is a powerful tool in the field of biological systems. In order for plants to survive in an environment that is constantly changing and has different stressors, they must use different levels of the immune system. This system can include primary and secondary metabolites and various epigenetic changes in plants (Tugizimana et al., 2018). Plant metabolism plays an important role in plant functional genomics. It is very difficult to study complete metabolites through analytical methods alone. Therefore, the use of other methods, along with analytical methods, has helped with this issue. HPLC, gas chromatography (GC), chemical ionization, and mass spectrometry (MS) are some of these techniques (Ali et al., 2019). Comprehensive elucidation of the molecular and biochemical processes associated with the phenotypic defense state is vital for a better understanding of the molecular mechanisms that define the metabolism of plant-pathogen interactions. Such insights are essential for translational research and applications. However, the metabolomics approach has its own drawbacks. For instance, superfluous soluble sugar can prevent the separation of small but involved compounds in the germination process in response to priming from the plant sample. Similarly, some compounds are present in certain tissues of the plant that may undergo chemical alterations and change their nature as a result of extraction operations (Williams et al., 2021). Gibberellins, for example, are among the facilitators of seed germination that combine with sugars and phenols and are, therefore, an obstacle to the accurate identification of many metabolites (Wu et al., 2014). 10.6 CONCLUSION Seed and seedling priming have important effects on secondary metabolites. These metabolites play a vital role in seed germination and seedling resistance to biotic and abiotic environmental stresses. The study of secondary metabolites helps to induce plant resistance to stress in order to increase their efficiency. Increasing plants’ crop production efficiency means increasing crop yields in agriculture. These studies can also diversify seed and seedling priming methods and thus reduce the sensitivity of plants to changing environmental conditions at a time when the planet’s population is growing rapidly. A population that is dependent on agricultural products and various methods, such as priming, can save the health and life of many people in different parts of the world, including sensitive areas such as Africa. New

Seedling and Seed Priming in Regulating Secondary Metabolite Level

259

study methods can lead to the production of new materials that ultimately increase the quality of seeds and enhance plant resistance. KEYWORDS • • • • • •

genetically modified genome-wide association studies peroxidase secondary metabolites seeds germination stressful conditions

REFERENCES Abbasi, K. M., Moameri, M., Asgari, L. B., & Astatkie, T., (2021). Influence of nano-priming on seed germination and plant growth of forage and medicine species. Plant Growth Regul., 93, 13–28, doi.org/10.1007/s10725-020-00670-9. Ali, Q., Ashraf, S., Kamran, M., Rehman, A., & Ahmad, S., (2019). Alterations in plant secondary metabolism by seed priming. In: Hasanuzzaman, M., & Fotopoulos, V., (eds.), Priming and Pretreatment of Seeds and Seedlings: Implication in Plant Stress Tolerance and Enhancing Productivity in Crop Plants (pp. 147–161). Springer Singapore: Singapore. Asgari, L. B., Ghorbanpour, M., & Nikabadi, S., (2017). Heavy metals in contaminated environment: Destiny of secondary metabolite biosynthesis, oxidative status and phytoextraction in medicinal plants. Ecotox. Environ. Safe., 145, 377–390. doi. org/10.1016/j.ecoenv.2017.07.035. Asgari, L. B., Khadem, M. N., Maghsoodi, M. R., Ghorbanpour, M., & Kariman, K., (2019a) Phytoextraction of heavy metals from contaminated soil, water and atmosphere using ornamental plants: Mechanisms and efficiency improvement strategies. Environ. Sci. Pollut. Res., 26(9), 8468–8484. doi.org/10.1007/s11356-019-04241-y. Asgari, L. B., Najafi, N., Moghiseh, E., Mosaferi, M., & Hadian, J., (2019b). Effects of gamma-irradiated and non-irradiated sewage sludge on essential oil content and constituents of Ocimum basilicum L. J. Med. Plant., 18(71), 99–117. Ashraf, M., & Foolad, M. R., (2005). Pre-sowing seed treatment—A shotgun approach to improve germination, plant growth, and crop yield under saline and non-saline conditions. Adv. Agron., 88, 223–271. Ashraf, M., & Rauf, H., (2001). Inducing salt tolerance in maize (Zea mays L.) through seed priming with chloride salts: Growth and ion transport at early growth stages. Acta Physiol. Plant., 23, 407–414.

260

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Ayaz, M., Junaid, M., Ahmed, J., Ullah, F., Sadiq, A., Ahmad, S., & Imran, M., (2014). Phenolic contents, antioxidant and anticholinesterase potentials of crude extract, subsequent fractions and crude saponins from Polygonum hydropiper L. BMC Complement Altern. Med., 14, 145–145. doi: 10.1186/1472-6882-14-145. Beckers, G. J. M., & Conrath, U., (2007). Priming for stress resistance: From the lab to the field. Cur. Opin. Plant. Biol., 10, 425–431. doi: https://doi.org/10.1016/j.pbi.2007.06.002. Buitink, J., Leger, J. J., Guisle, I., Vu, B. L., Wuillème, S., Lamirault, G., Le Bars, A., Le Meur, N., Becker, A., Küster, H., et al., (2006). Transcriptome profiling uncovers metabolic and regulatory processes occurring during the transition from desiccation-sensitive to desiccation-tolerant stages in Medicago truncatula seeds. The Plant J: For Cell and Molecular Biology, 47, 735–750. doi: 10.1111/j.1365-313X.2006.02822.x. Farhad, W., Cheema, M. A., Saleem, M. F., & Saqib, M., (2011). Evaluation of drought tolerance in maize hybrids. International Journal of Agriculture & Biology, 13. Farooq, M., Irfan, M., Aziz, T., Ahmad, I., & Cheema, S., (2013). Seed priming with ascorbic acid improves drought resistance of wheat. J. Agron. Crop Sci., 199, 12–22. Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., & Basra, S., (2009). Plant drought stress: Effects, mechanisms and management. Sustain. Agr., 153–188. Gao, A. G., Hakimi, S. M., Mittanck, C. A., Wu, Y., Woerner, B. M., Stark, D. M., Shah, D. M., et al., (2000). Fungal pathogen protection in potato by expression of a plant defensin peptide. Nat. Biotechnol., 18, 1307–1310. doi: 10.1038/82436. Ghassemi, S., Delangiz, N., Asgari, L. B., Saghafi, D., & Magi, F., (2021). Review and future prospects on the mechanisms related to cold stress resistance and tolerance in medicinal plants. Acta Ecol. Sinica., 41, 120–129. doi.org/10.1016/j.chnaes.2020.09.006. Ghassemi, S., Farhangi-Abriz, S., Faegi-Analou, R., Ghorbanpour, M., & Asgari, L. B., (2018). Monitoring cell energy, physiological functions and grain yield in field-grown mung bean exposed to exogenously applied polyamines under drought stress. J. Soil Sci. Plant Nutr., 18(4), 1108–1125. doi.org/10.4067/S0718-95162018005003102. Gill, S. S., & Tuteja, N., (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem., 48, 909–930. Heshmat, K., Asgari, L. B., Shakiba, M. R., & Astatkie, T., (2021). Assessment of physiological traits of common bean cultivars in response to water stress and molybdenum levels. J. Plant Nutr., 44(3), 366–372. doi.org/10.1080/01904167.2020.1822395. Horns, F., & Hood, M. E., (2012). The evolution of disease resistance and tolerance in spatially structured populations. Ecol. Evol., 2, 1705–1711. doi: 10.1002/ece3.290. Hussain, H. A., Hussain, S., Khaliq, A., Ashraf, U., Anjum, S. A., Men, S., & Wang, L., (2018). Chilling and drought stresses in crop plants: Implications, cross talk, and potential management opportunities. Front. Plant Sci., 9. doi: 10.3389/fpls.2018.00393. Işeri, O., Körpe, D., Sahin, F., & Haberal, M., (2013). Hydrogen peroxide pretreatment of roots enhanced oxidative stress response of tomato under cold stress. Acta Physiol. Plant., 35, doi:10.1007/s11738-013-1228-7. Jisha, K. C., Vijayakumari, K., & Puthur, J. T., (2013). Seed priming for abiotic stress tolerance: An overview. Acta Physiol. Plant., 35, 1381–1396. doi: 10.1007/s11738-012-1186-5. Johnson, R., & Puthur, J. T., (2021). Seed priming as a cost-effective technique for developing plants with cross-tolerance to salinity stress. Plant Physiol. Biochem., 162, 247–257. Kaya, M. D., Okçu, G., Atak, M., Cıkılı, Y., & Kolsarıcı, Ö., (2006). Seed treatments to overcome salt and drought stress during germination in sunflower (Helianthus annuus L.). Eur. J. Agron., 24, 291–295.

Seedling and Seed Priming in Regulating Secondary Metabolite Level

261

Khadem, M. N., Hatami, M., Rezaei, S., Bayat, M., & Asgari, L. B., (2019). Induction of plant defense machinery against nanomaterials exposure. In: Ghorbanpour, M., & Wani, S. H., (eds.), Advances in Phytonanotechnology: From Synthesis to Application (pp. 241–263). Elsevier Inc doi.org/10.1016/B978-0-12-815322-2.00010-9. Khoshmanzar, E., Aliasgharzad, N., Neyshabouri, M. R., Khoshru, B., Arzanlou, M., & Asgari, L. B., (2020). Effects of Trichoderma isolates on tomato growth and inducing its tolerance to water‑deficit stress. Int. J. Environ. Sci. Technol., 17, 869–878. doi.org/10.1007/ s13762-019-02405-4. Lal, S. K., Kumar, S., Sheri, V., Mehta, S., Varakumar, P., Ram, B., Borphukan, B., et al., (2018). Seed priming: An emerging technology to impart abiotic stress tolerance in crop plants. In: Rakshit, A., & Singh, H. B., (eds.), Advances in Seed Priming (pp. 41–50). Springer Singapore: Singapore. Li, Z., Xu, J., Gao, Y., Wang, C., Guo, G., Luo, Y., Huang, Y., et al., (2017). The synergistic priming effect of exogenous salicylic acid and H2O2 on chilling tolerance enhancement during maize (Zea mays L.) seed germination. Front. Plant Sci., 8, 1153. Liang, C., (2016). Genetically modified crops with drought tolerance: Achievements, challenges, and perspectives. In: Hossain, M. A., Wani, S. H., Bhattacharjee, S., Burritt, D. J., & Tran, L. S. P., (eds.), Drought Stress Tolerance in Plants (Vol 2, pp. 531–547). Molecular and Genetic Perspectives, Springer International Publishing: Cham. Maia, J., Dekkers, B. J. W., Provart, N. J., Ligterink, W., & Hilhorst, H. W. M., (2011). The re-establishment of desiccation tolerance in germinated Arabidopsis thaliana seeds and its associated transcriptome. PLOS One, 6, e29123. doi: 10.1371/journal.pone.0029123. Medda, S., Hajra, A., Dey, U., Bose, P., & Mondal, N. K., (2015). Biosynthesis of silver nanoparticles from Aloe vera leaf extract and antifungal activity against Rhizopus sp. and Aspergillus sp. Appl. Nanosci., 5, 875–880. Motie-Noparvar, P., Behrouzi, V. M., Asgari, L. B., & Ghorbanpour, M., (2020). Engineering transcription factors: An emerging strategy for developing abiotic stress-tolerant crops. In: Wani, S. H., (ed.). Transcription Factors for Abiotic Stress Tolerance in Plants (pp. 241– 267). Elsevier Inc. doi.org/10.1016/B978-0-12-819334-1.00013-7. Mwando, E., (2021). The Genetics of Barley (Hordeum vulgare) Salinity Tolerance During Germination and the Instantaneous Seedling Endurance. Murdoch University. Paparella, S., Araújo, S., Rossi, G., Wijayasinghe, M., Carbonera, D., & Balestrazzi, A., (2015). Seed priming: State of the art and new perspectives. Plant Cell Rep., 34, 1281–1293. Ping, W. Y. S., & Yee, M. K. Y., (2021). Not one for all: The interwoven relationship between morphophysiology and secondary metabolite production in plant cell cultures. Exploring Plant Cells for the Production of Compounds of Interest, 77. Rao, M. J., Hussain, S., Anjum, M. A., Saqib, M., Ahmad, R., Khalid, M. F., Sohail, M., Nafees, M., Ali, M. A., Ahmad, N., et al., (2019). Effect of seed priming on seed dormancy and vigor. In: Hasanuzzaman, M., & Fotopoulos, V., (eds.), Priming and Pretreatment of Seeds and Seedlings: Implication in Plant Stress Tolerance and Enhancing Productivity in Crop Plants (pp. 135–145). Springer Singapore: Singapore. Saghafi, D., Delangiz, N., Asgari, L. B., & Ghorbanpour, M., (2019a). An overview on improvement of crop productivity in saline soils by halotolerant and halophilic PGPRs. 3Biotech, 9, 261. doi.org/10.1007/s13205-019-1799-0. Saghafi, D., Ghorbanpour, M., Shirafkan, A. H., & Asgari, L. B., (2019b). Enhancement of growth and salt tolerance of canola (Brassica napus L.) seedlings by halotolerant

262

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Rhizobium strains containing ACC-deaminase activity. Plant Physiol Rep., 24, 225–235. doi.org/10.1007/s40502-019-00444-0. Shehab, G. G., AHMED, O. K., & El-Beltagi, H. S., (2010). Effects of various chemical agents for alleviation of drought stress in rice plants (Oryza sativa L.). Notulae Botanicae Horti. Agrobotanici Cluj-Napoca, 38, 139–148. Tugizimana, F., Mhlongo, M. I., Piater, L. A., & Dubery, I. A., (2018). Metabolomics in plant priming research: The way forward? Int. J. Mol. Sci., 19, 1759. Turk, H., Erdal, S., Genisel, M., Atici, O., Demir, Y., & Yanmis, D., (2014). The regulatory effect of melatonin on physiological, biochemical and molecular parameters in coldstressed wheat seedlings. Plant Growth Regul., 74, 139–152. Wang, W., Chen, Q., Hussain, S., Mei, J., Dong, H., Peng, S., Huang, J., et al., (2016). Presowing seed treatments in direct-seeded early rice: Consequences for emergence, seedling growth and associated metabolic events under chilling stress. Sci. Rep., 6, 1–10. Wang, Y., Zhang, J., Li, J. L., & Ma, X. R., (2014). Exogenous hydrogen peroxide enhanced the thermotolerance of Festuca arundinacea and Lolium perenne by increasing the antioxidative capacity. Acta Physiol. Plant., 36, 2915–2924. Waqas, M., Korres, N. E., Khan, M. D., Nizami, A. S., Deeba, F., Ali, I., & Hussain, H., (2019). Advances in the concept and methods of seed priming. In: Priming and Pretreatment of Seeds and Seedlings (pp. 11–41). Springer. Williams, A., Gamir, J., Gravot, A., & Pétriacq, P., (2021). Untangling plant immune responses through metabolomics. In: Plant Metabolomics in Full Swing: Advances in Botanical Research (Vol. 98, pp. 73–105). Elsevier. Wu, X., Li, N., Li, H., & Tang, H., (2014). An optimized method for NMR-based plant seed metabolomic analysis with maximized polar metabolite extraction efficiency, signal-tonoise ratio, and chemical shift consistency. The Analyst, 139, 1769–1778. doi: 10.1039/ c3an02100a. Xu, S., Hu, J., Li, Y., Ma, W., Zheng, Y., & Zhu, S., (2011). Chilling tolerance in Nicotiana tabacum induced by seed priming with putrescine. Plant Growth Regul., 63, 279–290. Yuan-Yuan, S., Yong-Jian, S., Ming-Tian, W., Xu-Yi, L., Xiang, G., Rong, H., & Jun, M., (2010). Effects of seed priming on germination and seedling growth under water stress in rice. Acta Agron. Sinica., 36, 1931–1940.

CHAPTER 11

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism for Stress Tolerance

SUBIR GHOSH,1 KUNTAL BERA,1,2 PUSPENDU DUTTA,2 and SANJOY SADHUKHAN1

Plant Molecular Biology Laboratory, Department of Botany, Raiganj University, Raiganj – 733134, Uttar Dinajpur, West Bengal, India, E-mails: [email protected] (S. Ghosh), [email protected] (S. Sadhukhan)

1

Department of Seed Science and Technology, Uttar Banga Krishi Viswavidyalaya, Pundibari – 736165, Cooch Behar, West Bengal, India, E-mails: [email protected] (K. Bera), [email protected] (P. Dutta)

2

ABSTRACT Plants, while grown under natural conditions, are regularly exposed to a multitude of environmental stresses caused by hazardous chemicals, UV rays, submergence, extreme temperature, salinity, and drought. These stress factors adversely affect seed germination and seedling emergence, either alone or in combination, and thereby are unfavorable for the growth and survival of plants. Crop productivity is negatively controlled by environmental stresses. The seed priming technique has long been explored as an effective value-added tool that results in improved germination, reduced seedling emergence time, shortened crop duration, high level of tolerance to stresses, and ultimately higher crop yield. Various physiological responses, including the alterations in the growth, enhancement in photosynthetic Biology and Biotechnology of Environmental Stress Tolerance in Plants: Secondary Metabolites in Environmental Stress Tolerance, Volume 1. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

264

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

pigments, taste or quality composition of fruits, increasing level of photoprotection, upregulating the plant defense systems to strengthen crop production, and enhanced production of secondary metabolites have also been observed as a consequence of seed priming. Primed seeds exhibit resistance to biotic and abiotic stresses. There are two perspectives on the improved germination, seedling vigor, and/ or cross-tolerance mechanism of primed seeds against stress. Firstly, seed priming treatments usually activate the pre-germinative metabolism, which includes energy metabolism, loosening of endosperm, better utilization of reserved food materials and elongation of embryo cells, resulting in a seed with improved germination and vigor. Secondly, the application of abiotic stresses before re-drying also reserves the benefits of priming by stimulating cross-tolerance in response to stress and reduces the apprehension on post-priming seed longevity. A “priming memory” is initiated in the seeds, resulting in a robust tolerance response towards stress. With the onset of imbibition of seeds, initiation of secondary metabolism takes place along with the seed-repairing processes, which in turn induces both the antioxidant system and initiation of DNA repair mechanisms. Seed priming significantly modifies the production and storage of different secondary metabolites and antioxidants viz. ascorbate, glutathione, α-tocopherol, etc. The amount of secondary metabolites, such as total phenolics, flavonoids, and glycine-betaine are enhanced by priming treatment. This antioxidant machinery helps to avert the effect of abiotic stress by restraining the oxidative stresses imposed on plants. Thus, these mechanisms lead the seed germination and consequently seedling establishment to be a successful event. Keeping these in the background, this chapter aims to depict the recent progress in underlying the mechanism involved in seed priming induced improvement in seed germination and uniform plant establishment. Further, attempts have been taken to illustrate how seed priming speeds up cross-tolerance involving secondary metabolism in plants to environmental stresses. 11.1 INTRODUCTION The exposure of plants to diverse abiotic stimuli is quite inescapable, particularly in the context of global climate change (Zhao et al., 2007). Thus, the agricultural production system is severely impeded due to the frequent and unpredictable occurrence of environmental extremities. But such exposure of plants to the environmental stresses has been recognized to activate various

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

265

defense mechanisms that result in changes in metabolites profile, stimulation of hormonal signaling pathways regulated by abscisic acid (ABA), salicylic acid, jasmonic acid (JA) or ethylene, and activation of signaling pathways as induced by reactive oxygen species (ROS) (Fujita et al., 2006). As such, plants have evolved a variety of mechanisms that allow them to operate more freely under fluctuating environments without disrupting their cellular and physiological processes (Arnold et al., 2019; Yang et al., 2018). Secondary metabolites (SMs) are naturally formed by plants in response to their exposure to fluctuating environments and such generation of a variety of secondary metabolites is one of the strategies that help the plant to adapt to changing environmental conditions (Berini et al., 2018; Kroymann, 2011). Secondary metabolites are classified into three major groups viz.: (i) isoprenoids; (ii) nitrogen-containing secondary metabolites like alkaloids; and (iii) phenolic compounds like flavonoids. Flavonoids mostly function as antioxidants that reduce oxidative damage by scavenging ROS. Increased phenylalanine ammonia-lyase (PAL) activity during environmental stresses enhances flavonoid and anthocyanin synthesis (Ravindran et al., 2010; Wang et al., 2018). As a result, PAL has been identified as a key biomarker for environmental stress in several plant species (Shaki et al., 2018). Thus, the increased synthesis of various metabolites in plants under stressful conditions is thought to be an adaptive mechanism to defend cellular organizations from damage caused by oxidative stress (Chalker-Scott & Fuchigami, 2018; Close & McArthur, 2002; Wahid & Ghazanfar, 2006; Winkel-Shirley, 2002). Primary metabolites, which are formed from the first carbon reactions, play a direct role in osmotic regulation and the formation of cellular structures (Taiz & Zeiger, 2002). Among the primary metabolites, the buildup of free proline, glycine betaine, and soluble sugars are crucial for controlling osmotic adjustments and defending the structural components of cells from various osmotic stress factors (Bohnert et al., 2006). The most studied metabolites in the plant kingdom are carotenoids (carotenes and xanthophylls) and they are produced through the terpenoid or isoprenoid pathway while the phenolics are formed through the shikimic acid pathway (Buchanan et al., 2000). Carotenoids have antioxidant properties in addition to being accessory or antenna pigments. Furthermore, the carotenoids also protect photosystems by terminating chain reaction associated with lipid peroxidation as achieved through scavenging of singlet oxygens and releasing the energy in the form of heat, preventing singlet oxygen production by reacting with triplet-excited chlorophyll molecules or using the xanthophyll cycle to dissipate excess excitation energy (Rmiki et al., 1999).

266

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Phenolics also act as strong antioxidants in stressed plant tissue. These metabolites serve several functions, including protection against biotic stress factors, providing mechanical strength, attracting pollinating insects, absorbing high-energy radiation, and inhibiting the growth of weeds present in proximity (Harborne & Williams, 2000; Taiz & Zeiger, 2002). Likewise, anthocyanins, highly water-soluble pigments, are formed in response to environmental stresses (Balakumar et al., 1993; Krol et al., 1995; Rajendran et al., 1992). The ultimate aim of modern agriculture is to augment productivity by reducing abiotic stress-related losses either at pre-harvest or after harvest (Gust et al., 2010). This means that one of the most pressing challenges to humanity is not only to improve agriculture’s productivity rather reduce the adverse impact of environmental stresses towards ensuring the food demands of the ever-growing global population (Edmondson et al., 2014). Thus, the entire world is in search of potential but cost-effective agroecological technologies to combat various abiotic stresses. Seed or seedling priming is one of such promising technologies that can instigate tolerance in crop plants against abiotic stresses, and thereby allowing them to increase productivity even in harsh conditions (Jisha et al., 2013). Seed priming, a useful method, has been effectively applied to create proper stands in both natural and stressful conditions (Cao et al., 2016; Hussain et al., 2016; Jafar et al., 2012). It is the process where the seeds are exposed to various natural chemical compounds preceding actual germination. Pre-sowing seed treatments like hydration, halo-priming, osmo-priming, and magneto-priming are being extensively used in the present day’s agricultural production system. Both seed and crop priming technologies result in improved, quick, and synchronized emergence of seedlings with high vigor and finally higher crop yields (García-Cristobal et al., 2015; Ibrahim, 2016). Thus, plants grown from primed seeds attain several advantages over non-primed seeds. In many agricultural and horticultural crops, seed enhancement techniques have been shown to minimize the time required for seedling appearance, achieve even emergence, and provide improved plant population (Ashraf & Foolad, 2005). Further, the occurrence of stresses can interrupt the beginning of germination and decrease the rate and homogeneity of germination, resulting in poor yield (Demir et al., 2006). As a result, the benefits of priming can be noticeable more in adverse rather than favorable circumstances. Thereby, concerned stakeholders of the seed industry are very interested in finding proper priming techniques that would be utilized to improve plant resistance in adverse field conditions (Job, 2000; Parera & Cantliffe, 1994).

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

267

Under this perspective, this chapter has been conceived to illustrate the scientific background of utilizing seed priming to improve abiotic stress tolerance in crop species with a focus on their effects on growth, physiological parameters, and yield. Moreover, it aims to describe the cross-tolerance with special emphasis on the regulation of secondary metabolism as induced by seed priming. 11.2 A BRIEF HISTORY OF SEED PRIMING Seed priming is an ancient Greek process that dates back thousands of years. In Heydecker et al. coined the term “Seed Priming” for the first time and they successfully used it to increase seed germination and seedling emergence under environmental stress conditions (Heydecker et al., 1973). Theophrastus (372–287 BC) worked on physiological aspects of seed germination and suggested that the germination procedure be temporarily disrupted as well (Evenari, 1984). He observed that pre-sowing imbibition of cucumber seeds in milk or water helped them to germinate faster and more effectively (Evenari, 1984). According to the Roman naturalist Gaius Plinius Secundus, Roman farmers used to pre-hydrate legume seeds before sowing to boost germination rate and synchronize germination. Many botanists began to characterize morphological processes related to seed germination during the 18th century (Amici, 1830; Sachs, 1859). Later on, during the 1970s, the possibility of influencing ultimate germination as a result of priming had led to the development of a varied range of practical procedures for a variety of crop species (Khan et al., 1980). 11.3 SEED PRIMING INDUCES ABIOTIC STRESS TOLERANCE Crop plants are very frequently exposed to abiotic stresses at various growth stages, and this results in impairment in their physiological aspects and ultimately results in reduced productivity (Hussain et al., 2018). Several studies have recently been published that indicate the benefits of priming in various field crops under various abiotic stresses (Hussain et al., 2018). Plants grown from primed seeds show quick growth and are more resistant to stress, owing to improved energy metabolism, rapid activation of cellular defense mechanisms, a larger embryo, or increased enzyme activities. Seed priming also improves the buildup of various osmolytes like proline, glycine-betaine, polyamines, etc., by altering metabolic pathways (Delavari et al., 2010).

268

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Several seed priming techniques have also been established for energizing seeds and reducing the impacts of environmental stresses. The performance of seed priming varies with the priming technique and plant species. Apart from the several physical and chemical factors like osmotica or water potential, exposure time, temperature, O2 concentration, and physiological status of seeds, the efficacy of different priming agents also varies depending on the presence of stress factors and crop species (Iqbal & Ashraf, 2005). 11.3.1 HYDROPRIMING Hydro-priming is a cost-effective and eco-friendly seed treatment method that involves soaking seeds in regular water and followed by seed drying to their original moisture content prior to sowing (Singh et al., 2015). The benefit of hydro-priming is that it enhances physiological and biochemical activities in seeds even when seedling emergence is halted due to more negative osmotic potential and insignificant matric potential in the absorbing media (Basra et al., 2003). Such pre-soaking of seeds in water before sowing has been demonstrated to promote germination, improved crop stand, and higher yields in diverse environments (Rashid et al., 2006). Hydro-priming has been reported to enhance seedling vigor, germination percentage, and seedling dry weight in basil (Ocimum basilicum L.) grown in salty circumstances (Farahani & Maroufi, 2011). Among the different priming methods tested, hydro-priming has been observed to be the most successful in the case of mustard (Srivastava et al., 2010). Further, hydropriming and hydro priming with proline have been reported to be a useful priming strategy for enhancing seed germination and early growth of mung bean (Vigna radiate) at low temperatures as well as for quick repair of stressinduced damage (Posmyk & Janas, 2007). 11.3.2 OSMOPRIMING The most popular priming approach is osmo-priming, which includes aerobically hydration of seeds in osmotic solution with different water potentials and exposure duration (Lutts et al., 2016). Various chemicals like KNO3, CaCl2, MgSO4, NaCl, KCl, mannitol, and PEG (polyethylene glycol) are some of the most frequently utilized osmotic solutions, and among these PEG is the most often utilized in osmo-priming (Singh et al., 2014). Osmopriming has greater advantages than hydro-priming since it leads to quicker seedling emergence and better responsiveness to additional stimuli like salt and cold (Moradi & Younesi, 2009).

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

269

Under salt and drought stress, seed priming with PEG has been identified as a good strategy for enhancing germination of Bromus seeds (Tavili et al., 2011). Apart from enhancing seed germination capacity, osmo-priming with PEG also strengthens the antioxidant system that results in greater stress tolerance in spinach seedlings (Chen & Arora, 2011). When compared to hydropriming, seed germination and seedling growth under drought stress have been found to be improved by priming with PEG at the proper concentration (Yuan-Yuan et al., 2010). Further, pre-germination salt priming with NaCl has been reported to be an efficient way to combat the adverse effects of salinity and drought in sugarcane (Patade et al., 2009). Further, priming with NaCl has been reported to be easy, inexpensive and appropriate to prescribe to farmers for improving crop establishment and synchronized growth of medicinal plants under extreme environments (Sedghi et al., 2010). Pre-treatment of mung bean seeds with a sub-lethal dosage of NaCl reduces the detrimental effects of NaCl stress and causes enhancement in growth, photosynthetic pigments, antioxidant enzyme activities, and osmolytes accumulation for osmotic adjustments (Saha et al., 2010). 11.3.3 NUTRIENT PRIMING Nutrient priming is a new approach that delivers the benefits of seed priming along with increased nutrient availability. Plant mineral nutrient status appears to play a key role in enhancing plant resilience to environmental stress factors. Potassium is one of the basic elements that help crop plants to survive when they are exposed to harsh weather conditions (Cakmak, 2005). Similarly, Zn-priming of chickpea seed shows improvement in crop canopy, drought tolerance index, and yield parameters (Shivay et al., 2014). It has also been reported that seed priming with calcium is a very effective and practicable way to enhancing stress tolerance in diverse crops (Bagheri et al., 2019; Jafar et al., 2012). Under stressful conditions, calcium acts as a secondary messenger, causing the build-up of osmolytes and antioxidants (Farooq et al., 2017). 11.3.4 CHEMICAL PRIMING Plants can also develop resistance against abiotic stresses after being exposed to a variety of natural and synthetic substances, including butenolide, selenium, putrescine, paclobutrazol, choline, chitosan, etc. (Demir et al., 2012; Foti et al., 2008; Mirza et al., 2010). Exogenous choline administration to

270

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

seeds results in salt tolerance in plants via glycine betaine buildup (Cha‐um et al., 2006; Su et al., 2006). Likewise, seed treatment with chitosan has been found to speed up seed germination and improve the resilience of hybrid rice seedlings to stress factors (Songlin & Qingzhong, 2002). Further, at low quantities, selenium has been proven to improve crop development and stress tolerance (Mirza et al., 2010). Seed priming with putrescine can also improve cold tolerance through activation of the antioxidant system in tobacco during germination and early stage of growth (Xu et al., 2011). Drought resistance has been found to be improved by seed priming with mannose and such resistance is attributed to the accumulation of more reducing sugars for osmotic regulation in plants and reducing oxidative damage or increasing antioxidant activities (Hameed & Iqbal, 2014). 11.3.5 BIOLOGICAL PRIMING/BIOPRIMING Imbibing the seeds in the priming solution containing biologically active bacterial inoculants is known as biopriming (Mahmood et al., 2016). The addition of plant growth promoting rhizobacteria (PGPRs), biological control agents, and fungicides to the priming solution results in enhanced germination and seedling vigor, synchronized plant establishment, yield characteristics, as well as tolerance to biotic and abiotic challenges (Rakshit et al., 2015; Timmusk et al., 2014). Trichoderma, Pseudomonas, Azotobactor, Azospirillum, and Agrobacterium are the most frequently used PGPRs for improving drought tolerance (Reddy, 2012). Stimulation in the biosynthesis of plant growth hormones has been ascribed for improved drought resistance in biopriming of seed with Trichoderma (Harman, 2006). Further, biopriming with Trichoderma has been reported to improve stress tolerance by triggering physiological defense mechanisms against oxidative injury by generating ROS scavengers as well as to increase disease resistance via coat films over the seed (Shukla et al., 2015). Biopriming of seeds with various saline tolerant isolates of Trichoderma has also been found to improve the germination percentage of wheat under salt stress (Rawat et al., 2011). 11.3.6 HORMONAL PRIMING The use of plant growth regulators or phytohormones as priming agents can improve seed performance in a variety of crops. Hormonal priming induces better crop establishment in temperature and drought stress conditions

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

271

(Bakhtavar et al., 2015; Wei et al., 2017). It has been reported that presowing treatment of rice seeds with polyamines like spermidine is very effective in inducing drought tolerance (Zheng et al., 2016). Further, seed priming with gibberellic acid (GA) enhances germination and increases antioxidant production in rye seedlings under water-deficient stress (Ansari et al., 2013). ABA is a phytohormone that plays a key role in plant responses to various abiotic stresses such as drought, low temperature, and osmotic stress. Exogenous ABA treatment has been found to improve salt tolerance of treated plants or tissues (Xiong & Zhu, 2002). In fennel, seed priming with salicylic acid (SA) results in greater germination under osmotic stress conditions. Seed priming of Agropyron elongatum with gibberellin (GA) and ABA has been reported to show higher CAT and SOD activities under water deficits conditions than non-primed seeds (Eisvand et al., 2010). Pre-sowing seed priming with benzyl adenine (BA) has been found to increase growth, root biomass, and conversion efficiency of soybean and such results indicate that BA can induce drought tolerance in this crop too (Khan et al., 2018). 11.4 PLANT RESPONSES TO ABIOTIC STRESS FACTORS Plants are regularly exposed to a varied range of environmental extremities like high temperature (HT), cold, drought, salinity, waterlogging, UV, pathogens, insects or herbivorous animals, etc. But as a stress-responsive strategy, various secondary metabolites are bio-synthesized constantly in plants, and these secondary metabolites help the plant to tolerate or prevent the adverse effects of these stresses. Many plant species synthesize various secondary metabolites like phenolics to protect themselves from biotic or abiotic stress growth conditions, and the accumulation of these SMs has been found to be correlated with plant antioxidant potential in several species (Abideen et al., 2015; Gan et al., 2010). The account of different secondary metabolites as synthesized within plants to counter the adversities of several environmental stresses has been discussed in subsections, and it has also been summarized in Table 11.1. 11.4.1 DROUGHT Drought escape, drought avoidance, and drought tolerance are the three main types of plant responses to drought stress (Fang et al., 2017; Kooyers, 2015). Plants have evolved drought escape mechanisms by managing their

272

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

development period and thereby minimizing osmotic stress in drought-prone locations. Whereas drought avoidance is accomplished by the control of morphological and physiological processes, that help plants to avoid osmotic stress by increasing root growth, reducing the area of leaves, leaf thickness, production of cuticular wax on plant parts, and folding leaves to limit evapotranspiration (Lee & Suh, 2013; Liu et al., 2017). But drought-tolerant plants synthesize various osmolytes to adjust their osmotic pressure through cellular, metabolic, and osmotic changes (Blum, 2017; Khan et al., 2015). These osmolytes help to maintain the structural integrity of biomolecules and cell membranes (Liu et al., 2007; Sharma et al., 2019). Apart from the osmolytes synthesis in tolerant plants, activities of antioxidants are also increased to minimize drought-induced oxidative stress (Chen et al., 2016; Cao et al., 2016). ABA is a naturally occurring stress-responsive phytohormone that regulates the expression of many transcription factors associated with the production of osmoprotectants (Daszkowska-Golec & Szarejko, 2013). JA, for example, is thought to be involved in continuous ABA deposition in the root systems under water shortages (de Ollas et al., 2015). Similarly, proline and glycine betaine accumulation in drought-stressed cells has been reported to be a key tolerance mechanism for maintaining the structure and integrity of the cell wall by regulating the osmotic stress (Hayat et al., 2012; Szabados & Savouré, 2010). Proline is also involved in a variety of physiological processes, including the macromolecular stability, the structural integrity of cell membranes, and the scavenging of ROS (Kaur & Asthir, 2015). Drought tolerance is also influenced by metabolomic components (Guo et al., 2020). The typical features of the crop response to stress involve a sophisticated signaling network that includes frequent crosstalk between the primary and secondary metabolic pathways (Jacobo-Velázquez et al., 2015). It has been reported that plants reorganize their metabolic pathways in response to drought stress, which enhances upstream metabolite production but downstream use of metabolite (Isah, 2019). The buildup of available substrates for protein synthesis and rapid recovery of plant metabolic activities during the post-stress period is linked to the increase of amino acids such as valine, glutamine, ornithine, tryptophan, and tyrosine (Suguiyama et al., 2014). Drought stress has been reported to increase flavonoids and phenolic acids, and also to cause alterations in chlorophyll “a” and “b” ratios, as well as carotenoids (Anjum et al., 2003). Flavonoids are often implicated to protect plants growing in soils containing metals such as aluminum at toxicity levels (Winkel-Shirley, 2001).

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

273

Transcriptomic and metabolomic studies have demonstrated that flavonoid accumulation is critical for improving drought tolerance in wild-type and Arabidopsis thaliana mutants (Nakabayashi et al., 2014). Flavonol levels have been found to be higher in other species, including Crataegus laevigata and Crataegus monogyna, under drought conditions (Kirakosyan et al., 2003). Hypericum brasiliense has been found to accumulate 10% higher phenolic compounds under water deficit stress as compared to control plants (de Abreu & Mazzafera, 2005). 11.4.2 SALT STRESS In the context of global climate change, salt stress tolerance is thought to be extremely promising, as salinity is expected to harm more than half of the earth’s cultivable land by 2050 (Diem & Dommergues, 1990; Nations, 2009; Zhong et al., 2013). Tolerance to salinity-induced stress refers to a plant’s ability to maintain metabolic activities by adjusting physiological processes at the systemic level (Parihar et al., 2015). Salinity stress is thought to prompt the synthesis of higher levels of various aromatic compounds as well as phenylpropanoid-derived compounds in plants (Selmar, 2008; Sytar et al., 2018). Anthocyanin levels have been found to rise in response to salt stress, but salt stress causes a reduction in anthocyanin levels in salt-sensitive species (Mbarki et al., 2018; Oyiga et al., 2016; Parida & Das, 2005). Endogenous JA has been observed to accumulate in tomato cultivars under salt stress (Pedranzani et al., 2003). Polyphenol production and accumulation are often triggered by biotic or abiotic stressors (Dixon & Paiva, 1995; Muthukumarasamy et al., 2000). Likewise, a variety of plants have shown an increase in polyphenol content in various tissues when salinity increases (Parida & Das, 2005). Further, salinity stress can act as an elicitor for the production of SMs that protect cells from oxidative damage caused by ion buildup at the cellular and subcellular organizations, and thus help to reduce the toxic consequence of salinity (Hossain et al., 2017). Apart from several polyols like sorbitol and mannitol, other compounds like glycine betaine, fructans, trehalose sugars, as well as proline also help in increasing the development and generation of higher or “oversupply” of reducing equivalents besides osmotic adjustment (Shulaev et al., 2008). Further, exposure to salinity stress levels in Solanum nigrum Calli has been reported to increase solasodine and proline output for tolerance (Šutković et al., 2011). Differential levels of salinity stress have been reported to result

274

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

in a stimulatory effect on oleuropein and phenol biosynthesis in leaves than in other tissues of four Olea europaea cultivars particularly at higher levels (Petridis et al., 2012). In several plant species, tissue-dependent increases in polyphenol development in response to salinity stress have also been recorded (Parida & Das, 2005; Slama et al., 2017). 11.4.3 TEMPERATURE STRESS Due to the ever-increasing global temperature, plants are often being exposed and got influenced by temperature variations. The changes in the optimum temperature for different plant species cause alterations in different metabolic processes. Exposure to HT generally leads to premature senescence and dysfunctionality in water transport, transpiration, and reduces photosynthetic activity. On the other hand, exposure to cold stress results in various morphological changes like stunted growth, chlorosis of the leaves, dormancy of seed or lower germination, wilting of leaves, etc. The temperature variations have not only been found to induce the production of various secondary metabolites rather the synergistic actions have been reported when temperature stress is combined with light and heavy metals (Joshi, 2015; Thomsen et al., 2011). In Panax quinquefolius, an increase in temperature by 5°C has been reported to accumulate higher levels of quinosenoside but a negative impact on the photosynthetic activity and biomass production has also been observed (Jochum et al., 2007). A significant increase in alkaloids accumulation has been recorded in Lupinus angustifolius with HTs (Jansen et al., 2009). Further, a positive correlation has been found between the accumulation of phenolic compounds viz., myrtillin, tulipanin, and myricetin-3-O-glycoside and temperature in the cultivars of Ribes nigrum (Zheng et al., 2012). Incubation at 40°C for 2 hours has also been reported to accumulate 6 times more 10-hydroxycamptothecin in the leaves of Camptotheca acuminata (Zu et al., 2003). In the latest study, it has also been observed that short term high-temperature stress (at 40°C for 8 hours) in Brassica rapa results in a significant enhancement in the production and accumulation of aliphatic and indolic glucosinolates and 4-Methoxyglucobrassicin (Jochum et al., 2007; Rao et al., 2021). On the contrary, cold stress or the reduction in temperature also makes alterations in the production of secondary metabolites. A significant reduction in the level of catharanthine and vindoline content has been observed

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

275

when Catharanthus roseus plants are exposed to low temperatures (Dutta et al., 2007). It has also been reported that stress due to certain low temperatures can increase the accumulation of phenolic compounds like suberin and lignin and that results in the successful integration of these compounds to the cell wall (Griffith & Yaish, 2004). The production of various secondary metabolites with low temperatures has also been observed in cell cultures. Incubation of cell culture at low temperature can induce the production of anthocyanins with higher biomass in Melastoma malabathricum (Chan et al., 2010). Similar observations have also been found in strawberries when the cell culture incubated at 15°C has recorded the maximum yield of anthocyanins, and the quantity has been found to be 18 times more than the incubation temperature of 35°C (Zhang et al., 1997). Further, low-temperature treatment of soybean seedlings at 10°C for 24 hours has been found to increase the level of two isoflavonoids viz., daidzein or genistein as well as the total phenolics significantly higher as compared to control (Janas et al., 2002). 11.4.4 LIGHT STRESS The metabolites production is also influenced by the different wavelengths (colors) of the spectrum of light. In the callus culture of Ocimum basilicum L. var purpurascens, red light enhances the production of cichoric acid, while exposure to the blue spectrum has also been proved to significantly enhance the overall production of phenolics and flavonoids. This study has also described that the incubation of callus in the dark would enhance the biosynthesis of rosmarinic acid, cyanidin, and peonidin (Nazir et al., 2020). In Fagopyrum tataricum, monochromatic exposure of blue spectrum with an intensity of 50 μmol/m2/s has resulted in the enhancement in the production of zeaxanthin but the reduction in the level of total carotenoids (Tuan et al., 2013). On the contrary, 300 μmol/m2/s of monochromatic blue light exposure of Oryza sativa L. has been reported to accumulate higher levels of carotenoids than the white light exposure (Hamdani et al., 2019). Similar types of effects have also been recorded when the exposure to blue spectrum of 350 μmol/m2/s causes to produce higher carotenoids as compared to red light exposure (Shiga et al., 2009). But, in Ocimum basilicum L., the accumulation of rosmarinic acid has been found to be improved at 100 μmol/m2/s of the red spectrum (Shiga et al., 2009). However, the red-light exposure has also recorded negative impacts on the secondary metabolites production. In the shoot culture of

276

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Aronia prunifolia, 60 μmol/m2/s of monochromatic red spectrum causes to reduce the accumulation and yield of chlorogenic acid, protocatechuic acid and quercitrin but it enhances the level of total flavonoids and polyphenols content (Szopa et al., 2018). The green spectrum of light also has some positive and some negative effects on secondary metabolites production. In Prunella vulgaris L., green light increases the level of total phenolic compounds but reduces the level of total flavonoids (Fazal et al., 2016). In Hyptis marrubioides Epling, 50 μmol/m2/s of the green spectrum has been found to enhance the accumulation of rutin in respect to blue light but decreases in respect to white light exposure (Pedroso et al., 2017). 11.4.5 HEAVY METAL STRESS Heavy metal toxicity to plants is one of the most important abiotic stresses that impedes the natural growth of a plant. Heavy metal contaminations in the soil are a serious threat to recent agriculture practices. Recent studies indicate that seed priming with heavy metals can help the plants to tolerate their toxicity. Heavy metals can either induce or reduces the biosynthesis of various secondary metabolites. The application of copper and zinc has been reported to improve the accumulation of pulegone, thymal, 1,8-cineol and some other essential oils (Lajayer et al., 2017). In Artemisia annua L., the application of arsenic enhances the biosynthesis of artemisinin (Rai et al., 2011). Further, when Trigonella foenum-graceum L is treated with cadmium and cobalt, the level of diosgenin has been reported to increase significantly (De & De, 2011). According to (Ibrahim et al., 2017), the application of cadmium in Gynura procumbens maximizes the accumulation of total phenolics and total flavonoids content, but contrasting results have been found when a combination of cadmium and calcium is applied. The positive role of cadmium application in plants to tolerate metal toxicity has recently been reported by (Kazemi et al., 2020) as they have observed that seedlings treatment with 250 μg/g perlite cadmium causes total phenolics to increase. 11.4.6 UV STRESS The phenolic compounds are found to accumulate at higher levels under UV irradiation and they play a strong protective role in the defense mechanisms against UV stress. It is also noteworthy that other groups of SMs like

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

277

terpenes, alkaloids, glucosinolates, etc., also play important roles in the tolerant mechanisms under solar stress (Yavaş et al., 2020). The implication of UV-B as priming agent at seed and seedling stage in Oryza sativa var. Kanchan & Aiswarya have been reported to increase the tolerance to UV-B stress by increasing the buildup of SMs like flavonoids and anthocyanins that can absorb UV-B (Thomas & Puthur, 2020). In Capsicum annuum var. Stayer, UV-A (at 4–5 W/m2/3hrs/day) and UV-B (at 10–14 W/m2/3hrs/day) irradiation along with salt stress have been described to enhance the production of two SMs viz., cynaroside and Graveobioside A. The first one accumulates at a high level of UV stress while the latter accumulates during salt stress. But the combination of these two treatments has been found to increase the accumulation of SMs at its highest level (Ellenberger et al., 2020). Further, UV-C radiation also enhances the accumulation of phenolic compounds through upregulation of the genes responsible for the biosynthesis of SMs such as PAL, CHS, STS, and ANS in different plant species. UV-C irradiation for 5 min at a distance of 20 cm has been reported to increase the level of total flavonoids content in the callus culture of Okuzgozu verity of grape (Mishra et al., 2020). Another secondary metabolite of phytoalexin group viz., stilbenes are also enhanced by UV-C irradiation in grapes (Hasan & Bae, 2017). UV-C irradiation has also been reported to enhance the accumulation of different terpenes like saponins (Mishra et al., 2020), carotenoids (Rahimzadeh et al., 2011). 11.5 GENERAL BIOSYNTHETIC PATHWAY OF DIFFERENT SECONDARY METABOLITES The biosynthesis of secondary metabolites generally follows three distinct pathways for the production of three main types of secondary metabolites such as phenolic compounds, terpenoids, and N-containing secondary metabolites (Abdallah & Quax, 2017; Darragh et al., 2021; Jan et al., 2021). These pathways are: i.

Shikimate pathway in which shikimate-3-phosphate is converted into chorismate by a series of alterations in the fundamental structures of the intermediate biomolecules. Chorismate act as the first stable precursor for the formation of other intermediates, which in turn

Stress Condition

Name of Secondary Metabolites

Plant Species

References

Phenol

Fe and Pi deficiency Salt stress

Umbelliferone/esculetin/scopoletin

Arabidopsis thaliana

Oleuropein Caffeic acid, salicylic acid, vanillic acid, trans-cinnamic acid, gallic acid, chlorogenic acid, rutin, isoquercetin, and m-coumaric acid Chlorogenic acid, rutin, hyperoside, isoquercetine, quercitrine, and quercetine Hydroxycinnamic acids Catechin, epicatechin, epicatechin benzyl thioether, hydroxycinnamic acid Polyphenol

Olea europaea Amaranthus tricolor

Chutia et al. (2019); Stringlis et al. (2019) Petridis et al. (2012) Sarker & Oba (2018)

Hypericum pruinatum

Caliskan et al. (2017)

Solanum lycopersicon cv. Boludo Mesembryanthemum edule

Martinez et al. (2016) Falleh et al. (2012)

Cakile maritima, Bruguiera parviflora Dimorphandra mollis Grevillea ilicifolia and Triticum aestivum L. cv. Guizi 1

Ksouri et al. (2007); Parida et al. (2002) Lucci & Mazzafera (2009) Kennedy & De Filippis (1999); Li et al. (2018); Parida & Das (2005) Wang et al. (2015) Izhaki (2002)

Rutin Anthocyanins

Light stress

Tannin, gossypol, and flavone Emodin Chlorogenic acid, flavonoids Gingerol Anthocyanin

Gossypium hirsutum L. Rheum undulatum, Rhamnus frangula, Rhamnus purshiana Centella asiatica Zingiber officinale Rosc. Perilla frutescens

Alqahtani et al. (2015) Anasori & Asghari (2009) Miki et al. (2015); Zhong et al. (1991)

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Class of Metabolite

278

TABLE 11.1  List of Some Important Secondary Metabolites, Their Class of Origin and Associated Stress Condition

Class of Metabolite

Stress Condition

Name of Secondary Metabolites

Plant Species

References

Drought stress

Ferulic acids, chlorogenic acid, quercetin, rutin, luteolin, and apigenin Chlorogenic acid, apigenin, and luteolin

Chrysanthemum morifolium

Flavonoids, isoflavonoids Tanshinone, cryptotanshinone Chlorogenic acid, catechins, and (–)-epicatechins

Arabidopsis thaliana Salvia miltiorrhiza Bunge Crataegus laevigata, Crataegus monogyna Prisms sativum Hypericum brasiliense, Dimorphandra mollis

Hodaei et al. (2018); Xie et al. (2012) Rodríguez-Calzada et al. (2019) Nakabayashi et al. (2014) Liu et al. (2011) Kirakosyan et al. (2004)

Flavonoids, anthocyanins Quercetin, 1,5 dihydroxyxanthone, isouliginosin B and rutin

Temperature stress Cold stress

Capsicum annuum L

de Abreu & Mazzafera (2005) Pérez-Ilzarbe et al. (1997) Christie et al. (1994) Kovács et al. (2010) Hawrylak et al. (2007) Michalak (2006) Pande et al. (2000) Ngadze et al. (2014)

279

Salicylic acid, vanilic acid, gallic acid, chlorogenic acid, Amaranthus tricolor Trans-cinnamic acid, rutin, isoquercetin, m-coumaric acid and p-hydroxybenzoic acid Quercetin, 1,5 dihydroxyxanthone, isouliginosin B and Hypericum brasiliense rutin Catechin, epicatechin, procyanidins, chlorogenic acid Malus domestica Borkh L., cv. Granny Smith Anthocyanin Zea mays Spermidine, putrescine Triticum aestivum Anthocyanin Lactuca sativa Catechin and quercetin Zea mays L Lepidine Lepidium sativum Chlorogenic acid, caffeic acid Solanum tuberosum

Nogués et al. (1998) de Abreu & Mazzafera (2005); Lucci & Mazzafera (2009) Sarker & Oba (2018)

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

TABLE 11.1  (Continued)

Class of Metabolite

Stress Condition

Water stress

Biotic stress

Plant Species

References

Rutin Ellagic acid, vanillic acid, cinnamic acid derivate, m-coumaric acid, caffeic acid, caffeic acid derivatives, p-coumaric acid derivatives Spermidine, spermine Coniferyl alcohol, ferulic acid and coumaric acid

Brassica juncea Erica andevalensis

Kapoor (2016) Márquez-García et al. (2009)

Helianthus annuus L Oryza sativa, Cucumis sativus

Quercetin, rutin, and catechin Chlorogenic acid, rutin

Fagopyrum esculentum and Fagopyrum tataricum Vaccinium corymbosum

Groppa et al. (2001) Ahanger et al. (2020); Dragišić Maksimović et al. (2007); Goto et al. (2003) Regvar et al. (2012)

Flavonoids, anthocyanins Chlorogenic acid, apigenin, and luteolin

Prisms sativum Capsicum annuum L

Anthocyanin Caffeoylquinic acid, chlorogenic acid, cryptochlorogenic acid, caffeoyl-hexoside, p coumaroylhexoside, feruloyl-hexoside, caffeoylhexoside isomer and sinapoyl-hexoside Shikimic acid, gallic acid, chlorogenic acid, syringic acid, p-coumaric acid, cinnamic acid, salicylic acid, myricetin, quercetin, and kaempferol Urushiol Ferulic acid, tannic acid, cinnamic acid, gallic acid

Malus pumila Mill. cv. Jonathan Lycopersicon esculentum

Inostroza-Blancheteau et al. (2014) Nogués et al. (1998) Rodríguez-Calzada et al. (2019) Arakawa et al. (1985) Sánchez-Rodríguez et al. (2012)

Pisum sativum

Jain et al. (2015)

Toxicodendron radicans Oryza sativa

Aziz et al. (2017) Mishra et al. (2006)

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Nutrient deficiency stress UV-B stress

Name of Secondary Metabolites

280

TABLE 11.1  (Continued)

Class of Metabolite

Stress Condition

Name of Secondary Metabolites

Plant Species

Scopoletin

Solanum lycopersicum; Nicotiana Santhanam et al. (2019); attenuata and Nicotiana tabacum Stringlis et al. (2019); Sun et al. (2014) Olea europaea Ortega‐García & Peragón (2010); Petridis et al. (2012) Ahmed & Baig (2014) Psoralea corylifolia L Izhaki (2002) Rhamnus alnifolia, Rhamnus cathartica, Muhaimin et al. (2016) Eusideroxylon zwagery Several plants of Selaginellaceae, Yu et al. (2017) Cupressaceae, Euphorbiaceae, etc. Llorens-Molina & Vacas Thymus vulgaris L. (2017) Turtola et al. (2003) Pinus sylvestris Munné-Bosch et al. (2001) Salvia officinalis L. Brown (2010) Artemisia annua L Anasori & Asghari (2009) Zingiber officinale Rosc. Fournier et al. (2003) Panax quinquefolius Spicher et al. (2017) Solanum lycopersicum

Oleuropein, hydroxytyrosol Psoralen Emodin Eusiderin Amentoflavone

Terpenes

Drought stress

Light stress

Cineole Dehydroabietic acid Carnosic acid Artemisinin Zingiberene Ginsenosides Phytol, tocopherol, and plastoquinone

Arabidopsis thaliana

Ahmed et al. (2017)

281

Combination of high temperature and high light stress Water stress Abscisic acid

References

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

TABLE 11.1  (Continued)

Class of Metabolite

Name of Secondary Metabolites

Plant Species

References

UV-B stress

Abscisic acid, quercetin, kaempferol, flavonols, 2-hydroxy-cinnamic acids, ferulic, and caeffic acids Gossypol; capsidiol and zealexin

–

Ahmed et al. (2017)

Gossypium sp., Nicotiana tabacum and Zea maize Arabidopsis thaliana (L) Heynh. Pinus sp. Scopolia parviflora Asclepias syriaca Citrus fruits of family Rutaceae; Azadirachta indica Plantago lanceolata Chrysanthemum sp. and plants of Cupressaceae Papaver somniferum Citrullus lanatus L. Sorghum bicolor L. Citrullus lanatus L. Solanum lycopersicum Catharanthus roseus Crotalaria spectabilis Senecio jacobaea Plants of Asteraceae, Boraginaceae, Heliotropiaceae, Apocynaceae, and some particular genera of Orchidaceae and the Fabaceae

Tian et al. (2019)

Biotic stress

Menthol Abietic acid Scopolamine Sterols Limonoids, azadirectin Catalpol Pyrethroids, α-pinene and β-pinene Nitrogencontaining secondary metabolites

Drought stress

Salt stress UV stress Biotic stress

Narkotine/codeine/morphine Citrulline Dhurrin Citrulline Tomatidine, solasodine Vincristine/vinblastine Monocrotaline Senecionine Pyrrolizidine alkaloids

Lin et al. (2017) Ahmed et al. (2017) Jung et al. (2003) Ahmed et al. (2017) Ahmed et al. (2017) Schweiger et al. (2014) Ahmed et al. (2017) Szabó et al. (2003) Yokota et al. (2002) Emendack et al. (2018) Yokota et al. (2002) Rivero et al. (2018) Binder et al. (2009) Irmer et al. (2015) Hill et al. (2018) Hartmann & Ober (2000); Schramm et al. (2019)

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Stress Condition

282

TABLE 11.1  (Continued)

Class of Metabolite

Stress Condition

Name of Secondary Metabolites

Plant Species

References

Mimosine Canavanine/azetidine-2-carboxylic acid

Leucaena leucocephala Canavalia ensiformis, Convallaria majalis Prunus dulcis/Prunus armeniaca/ Prunus avium/Prunus persica Lotus japonicus Sorghum bicolor L. Brassica napus Brassica oleracea

Xuan et al. (2006) Mazid et al. (2011); Yamane et al. (2010) Mazid et al. (2011)

Amygdalin

Sulfurcontaining secondary metabolites

Water stress Osmotic stress Salt stress

UV-B stress

Biotic stress

Linamarin Dhurrin Pipecolic acid Sinigrin Wasalexins Glucoraphanin, 4-methoxy-glucobrassicin, neoglucobrassicin Wasalexins, 1-methoxybrassenin B and rapalexin A Camalexin, 6-methoxycamalexin Brassinin, 1-methoxybrassinin, cyclobrassinin/Brassitin, 1-methoxyspirobrassinol Glucobrassicin

Wasabia japonica Brassica oleracea var. italica Thellungiella halophila Camelina sativa Brassica campestris L. ssp. Pekinensis/Raphanus sativus var. hortensis Brassica rapa

Lai et al. (2015) Emendack et al. (2018) Moulin et al. (2006) Kim et al. (2018); Martínez‐ Ballesta et al. (2014) Pedras et al. (2007) Moreira-Rodríguez et al. (2017) Pedras et al. (2009) Abdalla & Mühling (2019) Abdalla & Mühling (2019)

Villarreal-García et al. (2016)

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

TABLE 11.1  (Continued)

283

284

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

are responsible for the synthesis of different secondary metabolites including phenolic compounds, alkaloids, etc. ii. Different terpenoids are synthesized in the mevalonate pathway, in which mevalonate is the first stable precursor of other precursors responsible for the production of different terpenoids. iii. The N-containing secondary metabolites are produced from the extension of the TCA cycle and alkaloids by the shikimate pathway. Stepwise schematic representations of these pathways with respective enzymes involved are configured under Figures 11.11 and 11.2.

FIGURE 11.1  Shikimate pathway along with pathway for N-containing SMs.

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

285

FIGURE 11.2  The mevalonate pathway.

11.6 MECHANISM BEHIND THE REGULATION OF SMS IN PLANTS Generally, a healthy plant produces some secondary metabolites in a very less quantity for maintaining its normal physio-biochemical activity under favorable environmental conditions. But when they are exposed to different abiotic or biotic stresses or the elicitors, there is an overproduction or reduction in the secondary metabolites. However, the production of such

286

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

elicitor specific secondary metabolites depends on the type of elicitors, their concentration, strength, duration, etc. These elicitors act as signals which are recognized by specific signal receptors located in the membrane of the plant cells. After the correct perception of the properties of the specific elicitor, the signal transduction cascade with activation of various signaling molecules initiated within the cell. Thereafter, the signaling cascade switches on the changes in the expression strategies of various specific transcriptional factors or genes and such changes or modifications in genetic expression are reflected in the production of specific secondary metabolites or several alterations in the morphological traits like changes in the leaf area, root volume, height of the plants, etc., to avoid the damage prompted by the elicitors or to combat with the stress condition (Halder et al., 2019; Jan et al., 2021). 11.7 CONCLUSION It is now well established that environmental extremities can adversely affect the growth and yield of plants. In fact, changing climate is severely influencing water availability, salinity, and other adverse growth conditions which is having a direct impact on crop productivity. However, plants are sessile in nature and therefore they adapt several indigenous defense systems to combat stress factors. But various means like artificial external stimuli or using different possible priming techniques have been found to improve the tolerance of plants towards stress factors by enhancing the production of secondary metabolites. Albeit plants naturally produce some secondary metabolites in very low concentrations as the by-product of different pathways, but it is now well-established that the biosynthesis of SMs is induced with environmental stimuli, and the buildup of SMs is very crucial for the natural defense mechanisms of the plant. Plants utilize SMs as natural tools to develop tolerance against biotic and abiotic stress factors. Various artificial or external stimuli generally act as a signal to activate different transcriptional factors involved in different subcellular pathways and then help in accumulating various kinds of secondary metabolites. However, the comprehensive study on transcription factors and the signaling mechanisms along with high-throughput profiling of SMs in primed seeds across species, genotypes, and cultivars would be worthy.

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

287

KEYWORDS • alkaloids • phenolics • • • • •

secondary metabolism seed priming seedling pre-treatment stress tolerance terpenoids

REFERENCES Abdallah, I. I., & Quax, W. J., (2017). A glimpse into the biosynthesis of terpenoids. KnE Life Sci., 81–98. Abideen, Z., Qasim, M., Rasheed, A., Adnan, M. Y., Gul, B., & Khan, M. A., (2015). Antioxidant activity and polyphenolic content of Phragmites karka under saline conditions. Pak. J. Bot., 47(3), 813–818. Ahanger, M. A., Bhat, J. A., Siddiqui, M. H., Rinklebe, J., & Ahmad, P., (2020). Integration of silicon and secondary metabolites in plants: A significant association in stress tolerance. J. Exp. Bot., 71, 6758–6774. Ahmed, E., Arshad, M., Khan, M. Z., Amjad, H. S., Sadaf, H. M., Riaz, I., Sabir, S., & Ahmad, N., (2017). Secondary metabolites and their multidimensional prospective in plant life. J. Pharmacogn. Phytochem., 6, 205–214. Ahmed, S. A., & Baig, M. M. V., (2014). Biotic elicitor enhanced production of psoralen in suspension cultures of Psoralea corylifolia L. Saudi J. Biol. Sci., 21, 499–504. Almansouri, M., Kinet, J. M., & Lutts, S., (2001). Effect of salt and osmotic stresses on germination in durum wheat (Triticum durum Desf.). Plant. Soil., 231(2), 243–254. Al‐Mudaris, M., & Jutzi, S., (1999). The influence of fertilizer‐based seed priming treatments on emergence and seedling growth of Sorghum bicolor and Pennisetum glaucum in pot trials under greenhouse conditions. J. Agron. Crop. Sci., 182(2), 135–142. Alqahtani, A., Tongkao-on, W., Li, K. M., Razmovski-Naumovski, V., Chan, K., & Li, G. Q., (2015). Seasonal variation of triterpenes and phenolic compounds in Australian Centella asiatica (L.) urb. Phytochem. Anal., 26, 436–443. Amici, G., (1830). Note on pollen action mode on stigmata. Ann. Sci. Nat. Bot., 21, 329–332. Anasori, P., & Asghari, G., (2008). Effects of light and differentiation on gingerol and zingiberene production in callus culture of Zingiber officinale rosc. Res. Pharm. Sci., 3, 59–63. Anjum, F., Yaseen, M., Rasul, E., Wahid, A., & Anjum, S., (2003). Water stress in barley (Hordeum vulgare L.). II. effect on chemical composition and chlorophyll contents. Pak. J. Agric. Sci., 40, 45–49.

288

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Ansari, O., Azadi, M., Sharif-Zadeh, F., & Younesi, E., (2013). Effect of hormone priming on germination characteristics and enzyme activity of mountain rye (Secale montanum) seeds under drought stress conditions. J. Stress Physiol. Biochem., 9(3), 61–71. Arakawa, O., Hori, Y., & Ogata, R., (1985). Relative effectiveness and interaction of ultraviolet-B, red and blue light in anthocyanin synthesis of apple fruit. Physiol. Plant., 64(3), 323–327. Arnold, P. A., Kruuk, L. E., & Nicotra, A. B., (2019). How to analyze plant phenotypic plasticity in response to a changing climate. New Phytol., 222(3), 1235–1241. Ashraf, M., & Foolad, M. R., (2005). Pre‐sowing seed treatment - a shotgun approach to improve germination, plant growth, and crop yield under saline and non‐saline conditions. Adv. Agron., 88, 223–271. Aziz, M., Sturtevant, D., Winston, J., Collakova, E., Jelesko, J. G., & Chapman, K. D., (2017). MALDI-MS imaging of urushiols in poison ivy stem. Molecules, 22(5), 711. Bagheri, N., Alizadeh, O., Zadeh, S. S., Aref, F., & Ordookhani, K., (2019). Evaluation of auxin priming and plant growth promoting rhizobacteria on yield and yield components of wheat under drought stress. Eur. Asian J. Biosci., 13(2), 711–716. Bakhtavar, M. A., Afzal, I., Basra, S. M. A., & Noor, M. A., (2015). Physiological strategies to improve the performance of spring maize (Zea mays L.) planted under early and optimum sowing conditions. PloS One, 10(4), e0124441. Balakumar, T., Vincent, V. H. B., & Paliwal, K., (1993). On the interaction of UV‐B radiation (280–315 nm) with water stress in crop plants. Physiol. Planta., 87(2), 217–222. Basra, S. M. A., Farooq, M., Tabassam, R., & Ahmad, N., (2005). Physiological and biochemical aspects of pre-sowing seed treatments in fine rice (Oryza sativa L.). Seed Sci. Tech., 33(3), 623–628. Basra, S. M. A., Pannu, I. A., & Afzal, I., (2003). Evaluation of seedling vigor of hydro and matriprimed wheat (Triticum aestivum L.) seeds. Int. J. Agric. Biol., 5(2), 121–123. Berini, J. L., Brockman, S. A., Hegeman, A. D., Reich, P. B., Muthukrishnan, R., Montgomery, R. A., & Forester, J. D., (2018). Combinations of abiotic factors differentially alter production of plant secondary metabolites in five woody plant species in the borealtemperate transition zone. Front. Plant Sci., 9, 1257. Binder, B. Y., Peebles, C. A., Shanks, J. V., & San, K. Y., (2009). The effects of UV-B stress on the production of terpenoidindole alkaloids in Catharanthus roseus hairy roots. Biotechnol. Prog., 25(3), 861–865. Bisht, C., Badoni, A., Vashishtha, R., & Nautiyal, M., (2009). Photoperiodic effect on seed germination in pyrethrum (Chrysanthemum cinerariaefolium vis.) under the influence of some growth regulators. J. Am. Sci., 5(4), 147–150. Blum, A., (2017). Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant Cell Environ., 40(1), 4–10. Bohnert, H. J., Gong, Q., Li, P., & Ma, S., (2006). Unraveling abiotic stress tolerance mechanisms–getting genomics going. Curr. Opin. Plant Biol., 9(2), 180–188. Brown, G. D., (2010). The biosynthesis of artemisinin (Qinghaosu) and the phytochemistry of Artemisia annua L. (Qinghao). Molecules, 15(11), 7603–7698. Bruggink, G. T., Ooms, J. J., & Van, D. T. P., (1999). Induction of longevity in primed seeds. Seed Sci. Res., 9(1), 49–53. Buchanan, B. B., Gruissem, W., & Jones, R. L., (2000). Biochemistry and molecular biology of plants. Am. Soci. Plant Physiol., 1158–1202.

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

289

Cakmak, I., (2005). The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J. Plant Nutri. Soil Sci., 168(4), 521–530. Caliskan, O., Radusiene, J., Temizel, K. E., Staunis, Z., Cirak, C., Kurt, D., & Odabas, M. S., (2017). The effects of salt and drought stress on phenolic accumulation in greenhouse grown Hypericum pruinatum. Ital. J. Agron., 12(3), 271–275. Chalker-Scott, L., & Fuchigami, L., (2018). The role of phenolic compounds in plant stress responses. In: Low Temperature Stress Physiology in Crops (pp. 67–80). CRC Press: United States. Chan, L., Koay, S., Boey, P., & Bhatt, A., (2010). Effects of abiotic stress on biomass and anthocyanin production in cell cultures of Melastoma malabathricum. Biol. Res., 43(1), 127–135. Cha‐Um, S., Supaibulwatana, K., & Kirdmanee, C., (2006). Water relation, photosynthetic ability and growth of Thai jasmine rice (Oryza sativa L. ssp. indica Cv. KDML 105) to salt stress by application of exogenous glycinebetaine and choline. J. Agron. Crop Sci., 192(1), 25–36. Chen, J., Yang, L., Yan, X., Liu, Y., Wang, R., Fan, T., Ren, Y., Tang, X., Xiao, F., & Liu, Y., (2016). Zinc-finger transcription factor ZAT6 positively regulates cadmium tolerance through the glutathione-dependent pathway in Arabidopsis. Plant Physiol., 171(1), 707–719. Chen, K., & Arora, R., (2011). Dynamics of the antioxidant system during seed osmopriming, post-priming germination, and seedling establishment in Spinach (Spinacia oleracea). Plant Sci., 180(2), 212–220. Choudhury, F. K., Rivero, R. M., Blumwald, E., & Mittler, R., (2017). Reactive oxygen species, abiotic stress and stress combination. Plant J., 90(5), 856–867. Christie, P. J., Alfenito, M. R., & Walbot, V., (1994). Impact of low temperature stress on general phenylpropanoid and anthocyanin pathways: Enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta, 194(4), 541–549. Chutia, R., Abel, S., & Ziegler, J., (2019). Iron and phosphate deficiency regulators concertedly control coumarin profiles in Arabidopsis thaliana roots during iron, phosphate and combined deficiencies. Front. Plant Sci., 10, 113. Close, D. C., & McArthur, C., (2002). Rethinking the role of many plant phenolics–protection from photodamage not herbivores? Oikos., 99(1), 166–172. Cuartero, J., & Fernández-Muñoz, R., (1998). Tomato and salinity. Sci. Hortic., 78(1–4), 83–125. D’andrea, R. M., Andreo, C. S., & Lara, M. V., (2014). Deciphering the mechanisms involved in Portulaca oleracea (C4) response to drought: Metabolic changes including crassulacean acid‐like metabolism induction and reversal upon re‐watering. Physiol. Planta., 152(3), 414–430. Daneshmand, F., Arvin, M. J., & Kalantari, K. M., (2010). Physiological responses to nacl stress in three wild species of potato in vitro. Acta Physiol. Planta., 32(1), 91–101. Darragh, K., Orteu, A., Black, D., Byers, K. J., Szczerbowski, D., Warren, I. A., Rastas, P., et al., (2021). A novel terpene synthase controls differences in anti-aphrodisiac pheromone production between closely related Heliconius butterflies. PLoS Biol., 19(1), e3001022. Daszkowska-Golec, A., & Szarejko, I., (2013). Open or close the gate–stomata action under the control of phytohormones in drought stress conditions. Front. Plant Sci., 4, 138.

290

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

De Abreu, I. N., & Mazzafera, P., (2005). Effect of water and temperature stress on the content of active constituents of Hypericum brasiliense choisy. Plant. Physiol. Biochem., 43(3), 241–248. De Ollas, C., Arbona, V., & GóMez‐Cadenas, A., (2015). Jasmonoyl isoleucine accumulation is needed for abscisic acid build‐up in roots of Arabidopsis under water stress conditions. Plant. Cell. Environ., 38(10), 2157–2170. De, D., & De, B., (2011). Elicitation of diosgenin production in Trigonella foenum-graecum L. seedlings by heavy metals and signaling molecules. Acta Physiol. Planta., 33(5), 1585–1590. Delavari, P., Baghizadeh, A., Enteshari, S., Kalantari, K. M., Yazdanpanah, A., & Mousavi, E., (2010). The effects of salicylic acid on some of biochemical and morphological characteristic of Ocimum basilicucm under salinity stress. Aust. J. Basic Appl. Sci., 4(10), 4832–4845. Demir, A. O., Göksoy, A. T., Büyükcangaz, H., Turan, Z. M., & Köksal, E. S., (2006). Deficit irrigation of sunflower (Helianthus annuus L.) in a sub-humid climate. Irrig. Sci., 24(4), 279–289. Demir, I., Ozuaydın, I., Yasar, F., & Van, S. J., (2012). Effect of smoke-derived butenolide priming treatment on pepper and salvia seeds in relation to transplant quality and catalase activity. S. Afr. J. Bot., 78, 83–87. Diem, H., & Dommergues, Y., (1990). Current and potential uses and management of Casuarinaceae in the tropics and subtropics. Biol. Frankia Actinorhizal Plants, 317–342. Dixon, R. A., & Paiva, N. L., (1995). Stress-induced phenylpropanoid metabolism. Plant Cell, 7(7), 1085. DragišićMaksimović, J., Bogdanović, J., Maksimović, V., & Nikolic, M., (2007). Silicon modulates the metabolism and utilization of phenolic compounds in cucumber (Cucumis sativus L.) Grown at excess manganese. J. Plant Nutri. Soil Sci., 170, 739–744. Dutta, A., Sen, J., & Deswal, R., (2007). Downregulation of terpenoid indole alkaloid biosynthetic pathway by low temperature and cloning of a AP2 type C-repeat binding factor (CBF) from Catharanthus roseus (L). G. don. Plant Cell Rep., 26(10), 1869–1878. Edmondson, J. L., Davies, Z. G., Gaston, K. J., & Leake, J. R., (2014). Urban cultivation in allotments maintains soil qualities adversely affected by conventional agriculture. J. Appl. Ecol., 51(4), 880–889. Edreva, A., Velikova, V., Tsonev, T., Dagnon, S., Gürel, A., Aktaş, L., & Gesheva, E., (2008). Stress-protective role of secondary metabolites: Diversity of functions and mechanisms. Gen. Appl. Plant Physiol., 34(1, 2), 67–78. Eisvand, H., Tavakkol-Afshari, R., Sharifzadeh, F., Maddah, A. H., & Hesamzadeh, H. S., (2010). Effects of hormonal priming and drought stress on activity and isozyme profiles of antioxidant enzymes in deteriorated seed of tall wheatgrass (Agropyron elongatum host). Seed Sci. Technol., 38(2), 280–297. Ellenberger, J., Siefen, N., Krefting, P., Schulze, L. J. B., Pfarr, D., Remmel, M., Schröder, L., & Röhlen-Schmittgen, S., (2020). Effect of UV radiation and salt stress on the accumulation of economically relevant secondary metabolites in bell pepper plants. Agron., 10(1), 142. Emendack, Y., Burke, J., Laza, H., Sanchez, J., & Hayes, C., (2018). Abiotic stress effects on sorghum leaf dhurrin and soluble sugar contents throughout plant development. Crop Sci., 58(4), 1706–1716. Evelyn, J., (1664). A Discourse of Forest Trees and the Propagation of Timber. John Martin (Royal Society). London.

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

291

Evenari, M., (1984). Seed physiology: Its history from antiquity to the beginning of the 20th century. Bot. Rev., 50(2), 119–142. Falleh, H., Jalleli, I., Ksouri, R., Boulaaba, M., Guyot, S., Magne, C., & Abdelly, C., (2012). Effect of salt treatment on phenolic compounds and antioxidant activity of two Mesembryanthemum edule provenances. Plant Physiol. Biochem., 52, 1–8. Fang, Y., Du, Y., Wang, J., Wu, A., Qiao, S., Xu, B., Zhang, S., et al., (2017). Moderate drought stress affected root growth and grain yield in old, modern and newly released cultivars of winter wheat. Front. Plant Sci., 8, 672. Farahani, H. A., & Maroufi, K., (2011). Effect of hydropriming on seedling vigor in basil (Ocimum basilicum L.) under salinity conditions. Adv. Environ. Biol., 5(5), 828–833. Farahbakhsh, H., (2012). Germination and seedling growth in unprimed and primed seeds of fennel as affected by reduced water potential induced by NaCl. Int. Res. J. Appl. Basic Sci., 3(4), 737–744. Farooq, M., Gogoi, N., Barthakur, S., Baroowa, B., Bharadwaj, N., Alghamdi, S. S., & Siddique, K., (2017). Drought stress in grain legumes during reproduction and grain filling. J. Agron. Crop Sci., 203(2), 81–102. Fazal, H., Abbasi, B. H., Ahmad, N., Ali, S. S., Akbar, F., & Kanwal, F., (2016). Correlation of different spectral lights with biomass accumulation and production of antioxidant secondary metabolites in callus cultures of medicinally important Prunella vulgaris L. J. Photochem. Photobiol. B: Biol., 159, 1–7. Foot, J., Caporn, S., Lee, J., & Ashenden, T., (1996). The effect of long‐term ozone fumigation on the growth, physiology and frost sensitivity of Calluna vulgaris. New Phytol., 133(3), 503–511. Foti, R., Abureni, K., Tigere, A., Gotosa, J., & Gere, J., (2008). The efficacy of different seed priming osmotica on the establishment of maize (Zea mays L.) caryopses. J. Arid Environ., 72(6), 1127–1130. Fournier, A. R., Proctor, J. T., Gauthier, L., Khanizadeh, S., Belanger, A., Gosselin, A., & Dorais, M., (2003). Understory light and root ginsenosides in forest grown Panax quinquefolius. Phytochem., 63(7), 777–782. Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Yamaguchi-Shinozaki, K., & Shinozaki, K., (2006). Crosstalk between abiotic and biotic stress responses: A current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol., 9(4), 436–442. Gan, Y., Zhou, L., Shen, Z. J., Shen, Z. X., Zhang, Y. Q., & Wang, G. X., (2010). Stomatal clustering, a new marker for environmental perception and adaptation in terrestrial plants. Bot. Stud., 51(3), 325–336. García-Cristobal, J., García-Villaraco, A., Ramos, B., Gutierrez-Mañero, J., & Lucas, J., (2015). Priming of pathogenesis related proteins and enzymes related to oxidative stress by plant growth promoting rhizobacteria on rice plants upon abiotic and biotic stress challenge. J. Plant Physiol., 188, 72–79. Goto, M., Ehara, H., Karita, S., Takabe, K., Ogawa, N., Yamada, Y., Ogawa, S., Yahaya, M. S., & Morita, O., (2003). Protective effect of silicon on phenolic biosynthesis and ultraviolet spectral stress in rice crop. Plant Sci., 164(3), 349–356. Griffith, M., & Yaish, M. W., (2004). Antifreeze proteins in overwintering plants: A tale of two activities. Trends Plant Sci., 9(8), 399–405.

292

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Groppa, M. D., Tomaro, M. L., & Benavides, M. P., (2001). Polyamines as protectors against cadmium or copper-induced oxidative damage in sunflower leaf discs. Plant Sci., 161(3), 481–488. Guo, X., Xin, Z., Yang, T., Ma, X., Zhang, Y., Wang, Z., Ren, Y., & Lin, T., (2020). Metabolomics response for drought stress tolerance in Chinese wheat genotypes (Triticum aestivum). Plants, 9(4), 520. Gupta, B., & Huang, B., (2014). Mechanism of salinity tolerance in plants: Physiological, biochemical, and molecular characterization. Int. J. Genomics, 2014. Gust, A. A., Brunner, F., & Nürnberger, T., (2010). Biotechnological concepts for improving plant innate immunity. Curr. Opin. Biotechnol., 21(2), 204–210. Halder, M., Sarkar, S., & Jha, S., (2019). Elicitation: A biotechnological tool for enhanced production of secondary metabolites in hairy root cultures. Eng. Life Sci., 19(12), 880–895. Hamdani, S., Khan, N., Perveen, S., Qu, M., Jiang, J., & Zhu, X. G., (2019). Changes in the photosynthesis properties and photoprotection capacity in rice (Oryza sativa) grown under red, blue, or white light. Photosyn. Res., 139(1), 107–121. Hameed, A., & Iqbal, N., (2014). Chemo-priming with mannose, mannitol and H2O2 mitigate drought stress in wheat. Cereal Res. Commun., 42(3), 450–462. Harborne, J. B., & Williams, C. A., (2000). Advances in flavonoid research since 1992. Phytochem., 55(6), 481–504. Harman, G. E., (2006). Overview of mechanisms and uses of Trichoderma spp. Phytopathology, 96(2), 190–194. Hartmann, T., & Ober, D., (2000). Biosynthesis and metabolism of pyrrolizidine alkaloids in plants and specialized insect herbivores. In: Biosynthesis (Vol. 209, pp. 207–243). Springer: Heidelberg, Berlin. Hasan, M., & Bae, H., (2017). An overview of stress-induced resveratrol synthesis in grapes: Perspectives for resveratrol-enriched grape products. Molecules, 22(2), 294. Havaux, M., (1998). Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci., 3(4), 147–151. Hawrylak, B., Matraszek, R., & Szymanska, M., (2007). Response of lettuce (Lactuca sativa L.) to selenium in nutrient solution contaminated with nickel. Veg. Crop. Res. Bull., 67, 63–70. Hayat, S., Hayat, Q., Alyemeni, M. N., Wani, A. S., Pichtel, J., & Ahmad, A., (2012). Role of proline under changing environments: A review. Plant Signal. Behav., 7(11), 1456–1466. He, J., Qin, L., Chong, E. L., Choong, T. W., & Lee, S. K., (2017). Plant growth and photosynthetic characteristics of Mesembryanthemum crystallinum grown aeroponically under different blue-and red-LEDs. Front. Plant Sci., 8, 361. Heydecker, W., Higgins, J., & Gulliver, R., (1973). Accelerated germination by osmotic seed treatment. Nature, 246(5427), 42–44. Hill, E. M., Robinson, L. A., Abdul-Sada, A., Vanbergen, A. J., Hodge, A., & Hartley, S. E., (2018). Arbuscular mycorrhizal fungi and plant chemical defense: Effects of colonization on aboveground and belowground metabolomes. J. Chem. Ecol., 44(2), 198–208. Hodaei, M., Rahimmalek, M., Arzani, A., & Talebi, M., (2018). The effect of water stress on phytochemical accumulation, bioactive compounds and expression of key genes involved in flavonoid biosynthesis in Chrysanthemum morifolium L. Ind. Crop. Prod., 120, 295–304. Hossain, M. S., Persicke, M., ElSayed, A. I., Kalinowski, J., & Dietz, K. J., (2017). Metabolite profiling at the cellular and subcellular level reveals metabolites associated with salinity tolerance in sugar beet. J. Exp. Bot., 68(21, 22), 5961–5976.

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

293

Hussain, H. A., Hussain, S., Khaliq, A., Ashraf, U., Anjum, S. A., Men, S., & Wang, L., (2018). Chilling and drought stresses in crop plants: Implications, cross talk, and potential management opportunities. Front. Plant Sci., 9, 393. Hussain, M., Farooq, M., Basra, S. M., & Ahmad, N., (2006). Influence of seed priming techniques on the seedling establishment, yield and quality of hybrid sunflower. Int. J. Agri. Biol., 8(1), 14–18. Hussain, S., Khan, F., Cao, W., Wu, L., & Geng, M., (2016). Seed priming alters the production and detoxification of reactive oxygen intermediates in rice seedlings grown under suboptimal temperature and nutrient supply. Front. Plant Sci., 7, 439. Hussain, S., Khan, F., Hussain, H. A., & Nie, L., (2016). Physiological and biochemical mechanisms of seed priming-induced chilling tolerance in rice cultivars. Front. Plant Sci., 7, 116. Ibrahim, E. A., (2016). Seed priming to alleviate salinity stress in germinating seeds. J. Plant Physiol., 192, 38–46. Ibrahim, M. H., Chee, K. Y., & Mohd, Z. N. A., (2017). Effect of cadmium and copper exposure on growth, secondary metabolites and antioxidant activity in the medicinal plant Sambung nyawa (Gynura procumbens (Lour.) Merr). Molecules, 22(10), 1623. Inostroza-Blancheteau, C., Reyes-Díaz, M., Arellano, A., Latsague, M., Acevedo, P., Loyola, R., Arce-Johnson, P., & Alberdi, M., (2014). Effects of UV-B radiation on anatomical characteristics, phenolic compounds and gene expression of the phenylpropanoid pathway in highbush blueberry leaves. Plant Physiol. Biochem., 85, 85–95. Iqbal, M., & Ashraf, M., (2005). Changes in growth, photosynthetic capacity and ionic relations in spring wheat (Triticum aestivum L.) due to pre-sowing seed treatment with polyamines. Plant Growth Regul., 46(1), 19–30. Irmer, S., Podzun, N., Langel, D., Heidemann, F., Kaltenegger, E., Schemmerling, B., Geilfus, C. M., et al., (2015). New aspect of plant–rhizobia interaction: Alkaloid biosynthesis in crotalaria depends on nodulation. Proc. Natl. Acad. Sci., 112, 4164–4169. Isah, T., (2019). Stress and defense responses in plant secondary metabolites production. Biol. Res., 52. Izhaki, I., (2002). Emodin–A secondary metabolite with multiple ecological functions in higher plants. New Phytol., 155, 205–217. Jacobo-Velázquez, D. A., González-Agüero, M., & Cisneros-Zevallos, L., (2015). Crosstalk between signaling pathways: The link between plant secondary metabolite production and wounding stress response. Sci. Rep., 5(1), 1–10. Jafar, M., Farooq, M., Cheema, M., Afzal, I., Basra, S., Wahid, M., Aziz, T., & Shahid, M., (2012). Improving the performance of wheat by seed priming under saline conditions. J. Agron. Crop Sci., 198(1), 38–45. Jain, A., Singh, A., Singh, S., & Singh, H. B., (2015). Phenols enhancement effect of microbial consortium in pea plants restrains Sclerotinia sclerotiorum. Biol. Control., 89, 23–32. Jan, R., Asaf, S., Numan, M., & Kim, K. M., (2021). Plant secondary metabolite biosynthesis and transcriptional regulation in response to biotic and abiotic stress conditions. Agronomy, 11(5), 968. Janas, K. M., Cvikrová, M., Pałagiewicz, A., Szafranska, K., & Posmyk, M. M., (2002). Constitutive elevated accumulation of phenylpropanoids in soybean roots at low temperature. Plant Sci., 163(2), 369–373.

294

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Janmohammadi, M., Dezfuli, P. M., & Sharifzadeh, F., (2008). Seed invigoration techniques to improve germination and early growth of inbred line of maize under salinity and drought stress. Gen. Appl. Plant Physiol., 34(3, 4), 215–226. Jansen, G., Jürgens, H. U., & Ordon, F., (2009). Effects of temperature on the alkaloid content of seeds of Lupinus angustifolius cultivars. J. Agron. Crop Sci., 195(3), 172–177. Jisha, K., Vijayakumari, K., & Puthur, J. T., (2013). Seed priming for abiotic stress tolerance: An overview. Acta Physiol. Planta., 35(5), 1381–1396. Job, D. C. I., Job, C., Dacher, F., Corbineau, F., & Come, D., (2000). Identification of germination-specific protein markers and their use in seed priming technology. In: Black M. B. K., & Vazguez-Ramos, J., (eds.), Seed Biology: Advances and Applications (pp 449– 459). CAB International: Wallingford. Jochum, G. M., Mudge, K. W., & Thomas, R. B., (2007). Elevated temperatures increase leaf senescence and root secondary metabolite concentrations in the understory herb Panax quinquefolius (Araliaceae). Am. J Bot., 94(5), 819–826. Joshi, N., (2015). Influence of light and temperature on secondary metabolite accumulation in callus cultures of Helicteres isora L. IOSR J. Environ. Sci. Toxicol. Food Technol., 1(1), 2319–2399. Jung, H. Y., Kang, S. M., Kang, Y. M., Kang, M. J., Yun, D. J., Bahk, J. D., Yang, J. K., & Choi, M. S., (2003). Enhanced production of scopolamine by bacterial elicitors in adventitious hairy root cultures of Scopolia parviflora. Enzym. Microb. Technol., 33, 987–990. Kapoor, D., (2016). Antioxidative defense responses and activation of phenolic compounds in Brassica juncea plants exposed to cadmium stress. Int. J. Green Pharm., 10, 228–234. Kaur, G., & Asthir, B., (2015). Proline: A key player in plant abiotic stress tolerance. Biol. Planta., 59(4), 609–619. Kaur, G., Kumar, S., Nayyar, H., & Upadhyaya, H., (2008). Cold stress injury during the pod‐filling phase in chickpea (Cicer arietinum L.): Effects on quantitative and qualitative components of seeds. J. Agron. Crop Sci., 194(6), 457–464. Kaur, S., Gupta, A. K., & Kaur, N., (2002). Effect of osmo-and hydropriming of chickpea seeds on seedling growth and carbohydrate metabolism under water deficit stress. Plant Growth Regul., 37(1), 17–22. Kaur, S., Gupta, A., & Kaur, N., (2005). Seed priming increases crop yield possibly by modulating enzymes of sucrose metabolism in chickpea. J. Agron. Crop Sci., 191(2), 81–87. Kazemi, E. M., Kolahi, M., Yazdi, M., & Goldson-Barnaby, A., (2020). Anatomic features, tolerance index, secondary metabolites and protein content of chickpea (Cicer arietinum) seedlings under cadmium induction and identification of PCS and FC genes. Physiol. Mol. Biol. Plant., 26(8), 1551–1568. Kennedy, B. F., & De Fillippis, L. F., (1999). Physiological and oxidative response to NaCl of the salt tolerant Grevillea ilicifolia and the salt sensitive Grevillea ilicifolia. J. Plant Physiol., 155, 746–754. Khajeh-Hosseini, M., Powell, A., & Bingham, I., (2003). The interaction between salinity stress and seed vigor during germination of soybean seeds. Seed Sci. Technol., 31(3), 715–725. Khan, A. A., Peck, N. H., & Samimy, C., (1980). Seed osmoconditioning: Physiological and biochemical changes. Isr. J. Bot., 29(1–4), 133–144. Khan, A., Pan, X., Najeeb, U., Tan, D. K. Y., Fahad, S., Zahoor, R., & Luo, H., (2018). Coping with drought: Stress and adaptive mechanisms, and management through cultural and

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

295

molecular alternatives in cotton as vital constituents for plant stress resilience and fitness. Biol. Res., 51. Khan, M. I. R., & Khan, N. A., (2017). Reactive Oxygen Species and Antioxidant Systems in Plants: Role and Regulation Under Abiotic Stress (1st edn.). Springer: Singapore. Khan, M. S., Kanwal, B., & Nazir, S., (2015). Metabolic engineering of the chloroplast genome reveals that the yeast ArDH gene confers enhanced tolerance to salinity and drought in plants. Front. Plant Sci., 6, 725. Kim, S. Y., Park, J. E., Kim, E. O., Lim, S. J., Nam, E. J., Yun, J. H., Yoo, G., et al., (2018). Exposure of kale root to NaCl and Na2SeO3 increases isothiocyanate levels and Nrf2 signaling without reducing plant root growth. Sci. Rep., 8(1), 1–11. Kirakosyan, A., Kaufman, P., Warber, S., Zick, S., Aaronson, K., Bolling, S., & Chul, C. S., (2004). Applied environmental stresses to enhance the levels of polyphenolics in leaves of hawthorn plants. Physiol. Plant., 121, 182–186. Kirakosyan, A., Seymour, E., Kaufman, P. B., Warber, S., Bolling, S., & Chang, S. C., (2003). Antioxidant capacity of polyphenolic extracts from leaves of Crataegus laevigata and Crataegus monogyna (Hawthorn) subjected to drought and cold stress. J. Agri. Food Chem., 51(14), 3973–3976. Kooyers, N. J., (2015). The evolution of drought escape and avoidance in natural herbaceous populations. Plant Sci., 234, 155–162. Kovacs, Z., Simon-Sarkadi, L., Szucs, A., & Kocsy, G., (2011). Differential effects of cold, osmotic stress and abscisic acid on polyamine accumulation in wheat. Amino Acids., 38, 623–631. Król, A., Amarowicz, R., & Weidner, S., (2014). Changes in the composition of phenolic compounds and antioxidant properties of grapevine roots and leaves (Vitis vinifera L.) under continuous of long-term drought stress. Acta Physiol.Plant., 36, 1491–1499. Krol, M., Gray, G., Huner, N., Hurry, V., Öquist, G., & Malek, L., (1995). Low-temperature stress and photoperiod affect an increased tolerance to photo inhibition in Pinus banksiana seedlings. Can. J. Bot., 73(8), 1119–1127. Kroymann, J., (2011). Natural diversity and adaptation in plant secondary metabolism. Curr. Opin. Plant Biol., 14(3), 246–251. Ksouri, R., Megdiche, W., Debez, A., Falleh, H., Grignon, C., & Abdelly, C., (2007). Salinity effects on polyphenol content and antioxidant activities in leaves of the halophyte Cakile maritima. Plant Physiol. Biochem., 45, 244–249. Lai, D., Picmanová, M., Abou, H. M., Motawia, M. S., Olsen, C. E., Møller, B. L., Rook, F., & Takos, A. M., (2015). Lotus japonicus flowers are defended by a cyanogenic β-glucosidase with highly restricted expression to essential reproductive organs. Plant Mol. Biol., 89, 21–34. Lajayer, B. A., Ghorbanpour, M., & Nikabadi, S., (2017). Heavy metals in contaminated environment: Destiny of secondary metabolite biosynthesis, oxidative status and phytoextraction in medicinal plants. Ecotoxicol. Environ. Safety., 145, 377–390. Larson, R. A., (1988). The antioxidants of higher plants. Phytochem., 27(4), 969–978. Lea, P. J., Sodek, L., Parry, M. A., Shewry, P. R., & Halford, N. G., (2007). Asparagine in plants. Ann. Appl. Biol., 150(1), 1–26. Lee, S. B., & Suh, M. C., (2013). Recent advances in cuticular wax biosynthesis and its regulation in Arabidopsis. Mol. Plant., 6(2), 246–249.

296

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Lee, S. S., Kim, J. H., Hong, S. B., Yun, S. H., & Park, E. H., (1998). Priming effect of rice seeds on seedling establishment under adverse soil conditions. Korean J. Crop Sci., 43(3), 194–198. Li, X., Lv, X., Wang, X., Wang, L., Zhang, M., & Ren, M., (2018). Effects of abiotic stress on anthocyanin accumulation and grain weight in purple wheat. Crop Pasture Sci., 69, 1208–1214. Liu, H. Y., Yu, X., Cui, D. Y., Sun, M. H., Sun, W. N., Tang, Z. C., Kwak, S. S., & Su, W. A., (2007). The role of water channel proteins and nitric oxide signaling in rice seed germination. Cell Res., 17(7), 638–649. Liu, H., Wang, X., Wang, D., Zou, Z., & Liang, Z., (2011). Effect of drought stress on growth and accumulation of active constituents in Salvia miltiorrhiza bunge. Ind. Crops Prod., 33, 84–88. Liu, Y., Li, P., Xu, G. C., Xiao, L., Ren, Z. P., & Li, Z. B., (2017). Growth, morphological, and physiological responses to drought stress in Bothriochloa ischaemum. Front. Plant Sci., 8, 230. Llorens-Molina, J. A., & Vacas, S., (2017). Effect of drought stress on essential oil composition of Thymus vulgari L (chemotype 1, 8-cineole) from wild populations of eastern Iberian Peninsula. J. Essent. Oil Res., 29, 145–155. Lucci, N., & Mazzafera, P., (2009). Distribution of rutin in fava d’anta (Dimorphandra mollis) seedlings under stress. J Plant Interact., 4(3), 203–208. Lutts, S., Benincasa, P., Wojtyla, L., Kubala, S., Pace, R., Lechowska, K., Quinet, M., & Garnczarska, M., (2016). Seed priming: New comprehensive approaches for an old empirical technique. In: Araujo, S., & Balestrazzi, A., (eds.), New Challenges in Seed Biology-Basic and Translational Research Driving Seed Technology (pp. 1–46). InTech: Croatia. Ma, D., Sun, D., Wang, C., Li, Y., & Guo, T., (2014). Expression of flavonoid biosynthesis genes and accumulation of flavonoid in wheat leaves in response to drought stress. Plant Physiol. Biochem., 80, 60–66. Mahmood, A., Turgay, O. C., Farooq, M., & Hayat, R., (2016). Seed biopriming with plant growth promoting rhizobacteria: A review. FEMS Microbiol. Ecol., 92(8), fiw112. Majumdar, S., Ghosh, S., Glick, B. R., & Dumbroff, E. B., (1991). Activities of chlorophyllase, phosphoenolpyruvate carboxylase and ribulose‐1, 5‐bisphosphate carboxylase in the primary leaves of soybean during senescence and drought. Physiol. Planta., 81(4), 473–480. Manavalan, L. P., Guttikonda, S. K., Phan, T. L. S., & Nguyen, H. T., (2009). Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol., 50(7), 1260–1276. Mantri, N., Patade, V., Penna, S., Ford, R., & Pang, E., (2012). Abiotic stress responses in plants: Present and future. In: Ahmad, P., & Prasad, M., (eds.), Abiotic Stress Responses in Plants (pp 1–19). Springer: New York. Márquez-García, B., Fernández, M. A., & Córdoba, F., (2009). Phenolics composition in Erica sp. differentially exposed to metal pollution in the Iberian southwestern pyritic belt. Bioresour. Tech., 100, 446–451. Marschner, H., (1995). Mineral Nutrition of Higher Plants (2nd edn.). Academic Press: United Kingdom. Martinez, V., Mestre, T. C., Rubio, F., Girones-Vilaplana, A., Moreno, D. A., Mittler, R., & Rivero, R. M., (2016). Accumulation of flavonols over hydroxycinnamic acids favors oxidative damage protection under abiotic stress. Front. Plant Sci., 7, 838.

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

297

Martínez-Ballesta, M. D. C., Muries, B., Moreno, D. Á., Dominguez-Perles, R., GarcíaViguera, C., & Carvajal, M., (2014). Involvement of a glucosinolate (sinigrin) in the regulation of water transport in Brassica oleracea grown under salt stress. Physiol. Plant, 150, 145–160. Matysik, J., Alia, Bhalu, B., & Mohanty, P., (2002). Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr. Sci., 525–532. Mazid, M., Khan, T., & Mohammad, F., (2011). Role of secondary metabolites in defense mechanisms of plants. Biol. Med., 3, 232–249. Mbarki, S., Sytar, O., Zivcak, M., Abdelly, C., Cerda, A., & Brestic, M., (2018). Anthocyanins of colored wheat genotypes in specific response to salt stress. Molecules, 23(7), 1518. McDonald, M. B., (2000). Seed priming. In: Black, M., & Bewley, J. D., (eds.), Seed Technology and its Biological Basis (pp. 287–325). Sheffield Academic Press: Sheffield. Mendez, M., Jones, D. G., & Manetas, Y., (1999). Enhanced UV‐B radiation under field conditions increases anthocyanin and reduces the risk of photoinhibition but does not affect growth in the carnivorous plant Pinguicula vulgaris. New Phytol., 144(2), 275–282. Michalak, A., (2006). Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol. J. Environ. Stud., 15, 523–530. Miki, S., Wada, K. C., & Takeno, K., (2015). A possible role of an anthocyanin filter in lowintensity light stress-induced flowering in Perilla frutescens var. crispa. J. Plant Physiol., 175, 157–162. Miller, G., Suzuki, N., Ciftci‐Yilmaz, S., & Mittler, R., (2010). Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant. Cell Environ., 33(4), 453–467. Mirza, H., Hossain, M. A., & Fujita, M., (2010). Selenium in higher plants: Physiological role, antioxidant metabolism and abiotic stress tolerance. J. Plant Sci., 5(4), 354–375. Mishra, A. K., Choi, S. J., & Baek, K. H., (2020). Application of ultraviolet C irradiation for the increased production of secondary metabolites in plants. J. Anim. Plant Sci., 30, 1082–1091. Mishra, R. P., Singh, R. K., Jaiswal, H. K., Kumar, V., & Maurya, S., (2006). Rhizobiummediated induction of phenolics and plant growth promotion in rice (Oryza sativa L.). Curr. Microbiol., 52, 383–389. Moradi, A., & Younesi, O., (2009). Effects of osmo-and hydro-priming on seed parameters of grain sorghum (Sorghum bicolor L.). Aust. J. Basic Appl. Sci., 3(3), 1696–1700. Moreira-Rodríguez, M., Nair, V., Benavides, J., Cisneros-Zevallos, L., & Jacobo-Velázquez, D. A., (2017). UVA, UVB light, and methyl jasmonate, alone or combined, redirect the biosynthesis of glucosinolates, phenolics, carotenoids, and chlorophylls in broccoli sprouts. Int. J. Mol. Sci., 18, 2330. Moulin, M., Deleu, C., Larher, F., & Bouchereau, A., (2006). The lysine-ketoglutarate reductase-saccharopine dehydrogenase is involved in the osmo-induced synthesis of pipecolic acid in rapeseed leaf tissues. Plant Physiol. Biochem., 44, 474–482. Muhaimin, S., Chaerunisaa, A. Y., & Sinaga, M. S., (2016). Eusiderin I from eusideroxylon zwagery as antifungal agent against plant pathogenic fungus. Int. J. Chemtech Res., 9, 418–424. Munné-Bosch, S., Mueller, M., Schwarz, K., & Alegre, L., (2001). Diterpenes and antioxidative protection in drought-stressed Salvia officinalis plants. J. Plant Physiol., 158, 1431–1437. Munns, R., & Tester, M., (2008). Mechanisms of salinity tolerance. Annu. Rev. Plant Biol., 59, 651–681.

298

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Muthukumarasamy, M., Gupta, S. D., & Panneerselvam, R., (2000). Enhancement of peroxidase, polyphenol oxidase and superoxide dismutase activities by triadimefon in NaCl stressed Raphanus sativus L. Biol. Planta., 43(2), 317–320. Nakabayashi, R., Yonekura, S. K., Urano, K., Suzuki, M., Yamada, Y., Nishizawa, T., Matsuda, F., et al., (2014). Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. The Plant J., 77, 367–379. Nazir, M., Ullah, M. A., Younas, M., Siddiquah, A., Shah, M., Giglioli-Guivarc’h, N., Hano, C., & Abbasi, B. H., (2020). Light-mediated biosynthesis of phenylpropanoid metabolites and antioxidant potential in callus cultures of purple basil (Ocimum basilicum L. var purpurascens). Plant Cell Tissue Organ Cult., 142(1), 107–120. Ngadze, E., Coutinho, T. A., Icishahayo, D., & Van, D. W. J., (2014). Effect of calcium soil amendments on phenolic compounds and soft rot resistance in potato tubers. Crop Prot., 62, 40–45. Nogues, S., Allen, D. J., Morison, J. I. L., & Baker, N. R., (1998). Ultraviolet-B radiation effects on water relations, leaf development and photosynthesis in droughted pea plants. Plant Physiol., 117, 173–181. Ortega-García, F., & Peragón, J., (2010). HPLC analysis of oleuropein, hydroxytyrosol and tyrosol in stems and roots of Olea europaea L. cv. picual during ripening. J. Sci. Food Agric., 90, 2295–2300. Oyiga, B. C., Sharma, R., Shen, J., Baum, M., Ogbonnaya, F., Léon, J., & Ballvora, A., (2016). Identification and characterization of salt tolerance of wheat germplasm using a multivariable screening approach. J. Agron. Crop Sci., 202(6), 472–485. Pande, D., Iqbal, M., & Srivastava, P., (2000). Effect of ZnSO4 and CuSO4 on regeneration and lepidine content in Lepidium sativum L. Biol. Planta., 43(2), 253–256. Parera, C. A., & Cantliffe, D. J., (1994). Presowing seed priming. Hortic. Rev., 16(16), 109–141. Parida, A. K., & Das, A. B., (2005). Salt tolerance and salinity effects on plants: A review. Ecotoxicol. Environ. Saf., 60, 324–349. Parida, A., Das, A. B., & Das, P., (2002). NaCl stress causes changes in photosynthetic pigments, proteins and other metabolic components in the leaves of a true mangrove, Bruguiera parviflora, in hydroponic cultures. J. Plant Biol., 45, 28–36. Parihar, P., Singh, S., Singh, R., Singh, V. P., & Prasad, S. M., (2015). Effect of salinity stress on plants and its tolerance strategies: A review. Environ. Sci. Pollu. Res., 22(6), 4056–4075. Pascale, S. D., Maggio, A., Fogliano, V., Ambrosino, P., & Ritieni, A., (2001). Irrigation with saline water improves carotenoids content and antioxidant activity of tomato. J. Hortic. Sci. Biotechnol., 76(4), 447–453. Patade, V. Y., Bhargava, S., & Suprasanna, P., (2009). Halopriming imparts tolerance to salt and PEG induced drought stress in sugarcane. Agric. Ecosys. Environ., 134(1, 2), 24–28. Pedranzani, H., Racagni, G., Alemano, S., Miersch, O., Ramírez, I., Peña-Cortés, H., Taleisnik, E., et al., (2003). Salt tolerant tomato plants show increased levels of jasmonic acid. Plant Growth Regul., 41(2), 149–158. Pedras, M. S. C., Zheng, Q. A., & Sarma-Mamillapalle, V. K., (2007). The phytoalexins from Brassicaceae: Structure, biological activity, synthesis and biosynthesis. Nat. Prod. Commun., 2, 319–330. Pedras, M. S. C., Zheng, Q. A., Schatte, G., & Adio, A. M., (2009). Photochemical dimerization of wasalexins in UV-irradiated Thellungiella halophila and in vitro generates unique cruciferous phytoalexins. Phytochem., 70, 2010–2016.

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

299

Pedroso, R. C. N., Branquinho, N. A. A., Hara, A. C., Costa, A. C., Silva, F. G., Pimenta, L. P., Silva, M. L. A., et al., (2017). Impact of light quality on flavonoid production and growth of Hyptis marrubioides seedlings cultivated in vitro. Revista Brasileira de Farmacognosia., 27, 466–470. Perez-Ilzarbe, J., Hernandez, T., Estrella, I., & Vendrell, M., (1997). Cold storage of apples (cv. Granny Smith) and changes in phenolic compounds. Z. Lebensm. Unters. Forsch., 204, 52–55. Petridis, A., Therios, I., Samouris, G., & Tananaki, C., (2012). Salinity-induced changes in phenolic compounds in leaves and roots of four olive cultivars (Olea europaea L.) and their relationship to antioxidant activity. Environ. Exp. Bot., 79, 37–43. Posmyk, M., & Janas, K., (2007). Effects of seed hydropriming in presence of exogenous proline on chilling injury limitation in Vigna radiata L. seedlings. Acta Physiol. Planta, 29(6), 509–517. Rahimzadeh, P., Hosseini, S., & Dilmaghani, K., (2011). Effects of UV-A and UV-C radiation on some morphological and physiological parameters in savory (Satureja hortensis L.). Ann. Biol. Res., 2(5), 164–171. Rai, R., Pandey, S., & Rai, S. P., (2011). Arsenic-induced changes in morphological, physiological, and biochemical attributes and artemisinin biosynthesis in Artemisia annua, an antimalarial plant. Ecotoxicol., 20(8), 1900–1913. Rajendran, L., Ravishankar, G., Venkataraman, L., & Prathiba, K., (1992). Anthocyanin production in callus cultures of Daucus carota as influenced by nutrient stress and osmoticum. Biotechnol. Letter., 14(8), 707–712. Rakshit, A., Sunita, K., Pal, S., Singh, A., & Singh, H. B., (2015). Bio-priming mediated nutrient use efficiency of crop species. Nutri. Efficien. Basics Adv., 181–191. Rao, S. Q., Chen, X. Q., Wang, K. H., Zhu, Z. J., Yang, J., & Zhu, B., (2021). Effect of short-term high temperature on the accumulation of glucosinolates in Brassica rapa. Plant Physiol. Biochem., 161, 222–233. Rashid, A., Hollington, P., Harris, D., & Khan, P., (2006). On-farm seed priming for barley on normal, saline and saline–sodic soils in Northwest frontier province, Pakistan. Eur. J. Agron., 24(3), 276–281. Ravindran, K., Indrajith, A., Pratheesh, P., Sanjiviraja, K., & Balakrishnan, V., (2010). Effect of ultraviolet-B radiation on biochemical and antioxidant defense system in Indigofera tinctoria L. seedlings. Int. J. Eng. Sci. Technol., 2(5), 226–232. Rawat, L., Singh, Y., Shukla, N., & Kumar, J., (2011). Alleviation of the adverse effects of salinity stress in wheat (Triticum aestivum L.) by seed biopriming with salinity tolerant isolates of Trichoderma harzianum. Plant Soil., 347(1), 387–400. Reddy, P. P., (2012). Bio-priming of seeds. In: Recent Advances in Crop Protection (pp 83–90). Springer: New Delhi. Regvar, M., Bukovnik, U., Likar, M., & Kreft, I., (2012). UV-B radiation affects flavonoids and fungal colonization in Fagopyrum esculentum and F. tataricum. Open Life Sci., 7, 275–283. Rivero, J., Álvarez, D., Flors, V., Azcón-Aguilar, C., & Pozo, M. J., (2018). Root metabolic plasticity underlies functional diversity in mycorrhiza-enhanced stress tolerance in tomato. New Phytol., 220, 1322–1336. Rmiki, N. E., Lemoine, Y., & Schoeff, B., (1999). Carotenoids and stress in higher plants and algae. In: Pessarakl, M., (ed.), Handbook of Plant and Crop Stress (pp. 465–482). Marcel Dekker: New York.

300

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Rodríguez-Calzada, T., Qian, M., Strid, Å., Neugart, S., Schreiner, M., Torres-Pacheco, I., & Guevara-González, R. G., (2019). Effect of UV-B radiation on morphology, phenolic compound production, gene expression, and subsequent drought stress responses in chili pepper (Capsicum annuum L.). Plant Physiol. Biochem., 134, 94–102. Saba, P. D., Iqbal, M., & Srivastava, P. S., (2000). Effect of ZnSO4 and CuSO4 on regeneration and lepidine content in Lepidium sativum. Biol Plant., 43, 253–256. Sachs, J., (1859). About treatments modifying germination strength in seeds. Bot. Zeitung., 17, 177–188. Sachs, J., (1887). Lectures on the Physiology of Plants. Clarendon Press: Oxford. Saha, P., Chatterjee, P., & Biswas, A. K., (2010). NaCl pretreatment alleviates salt stress by enhancement of antioxidant defense system and osmolyte accumulation in mungbean (Vigna radiata L. Wilczek). Indian J. Exp. Biol., 48(6), 593–600. Sánchez-Rodríguez, E., Ruiz, J. M., Ferreres, F., & Moreno, D. A., (2012). Phenolic profiles of cherry tomatoes as influenced by hydric stress and rootstock technique. Food Chem., 134, 775–782. Santhanam, R., Menezes, R. C., Grabe, V., Li, D., Baldwin, I. T., & Groten, K. A., (2019). Suite of complementary biocontrol traits allows a native consortium of root-associated bacteria to protect their host plant from a fungal sudden-wilt disease. Mol. Ecol., 28, 1154–1169. Schramm, S., Köhler, N., & Rozhon, W., (2019). Pyrrolizidine alkaloids: Biosynthesis, biological activities and occurrence in crop plants. Molecules, 24(3), 498. Sedghi, M., Nemati, A., Amanpour-Balaneji, B., & Gholipouri, A., (2010). Influence of different priming materials on germination and seedling establishment of milk thistle (Silybum marianum) under salinity stress. World Appl. Sci. J., 11(5), 604–609. Selmar, D., (2008). Potential of salt and drought stress to increase pharmaceutical significant secondary compounds in plants. Landbauforsch. Volkenrode., 58(1, 2), 139. Sgherri, C., Stevanovic, B., & Navari‐Izzo, F., (2004). Role of phenolics in the antioxidative status of the resurrection plant Ramonda serbica during dehydration and rehydration. Physiol. Planta., 122(4), 478–485. Shaki, F., Maboud, H. E., & Niknam, V., (2018). Growth enhancement and salt tolerance of safflower (Carthamus tinctorius L.) by salicylic acid. Curr. Plant Biol., 13, 16–22. Shao, C., Hu, J., Song, W., & Hu, W., (2005). Effects of seed priming with chitosan solutions of different acidity on seed germination and physiological characteristics of maize seedling. J. Zhejiang Uni. (Agric. Life Sci.), 31(6), 705–708. Sharma, A., Shahzad, B., Kumar, V., Kohli, S. K., Sidhu, G. P. S., Bali, A. S., Handa, N., et al., (2019). Phytohormones regulate accumulation of osmolytes under abiotic stress. Biomolecule, 9(7), 285. Shiga, T., Shoji, K., Shimada, H., Hashida, S. N., Goto, F., & Yoshihara, T., (2009). Effect of light quality on rosmarinic acid content and antioxidant activity of sweet basil, Ocimum basilicum L. Plant Biotechnol., 26(2), 255–259. Shivay, Y. S., Prasad, R., & Pal, M., (2014). Genetic variability for zinc use efficiency in chickpea as influenced by zinc fertilization. Int. J. Bio-resour. Stress Manag., 5(1), 031–036. Shukla, N., Awasthi, R., Rawat, L., & Kumar, J., (2015). Seed biopriming with drought tolerant isolates of Trichoderma harzianum promote growth and drought tolerance in Triticum aestivum. Ann. Appli. Biol., 166(2), 171–182. Shulaev, V., Cortes, D., Miller, G., & Mittler, R., (2008). Metabolomics for plant stress response. Physiol. Planta., 132(2), 199–208.

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

301

Singh, A., Dahiru, R., Musa, M., & Sani, H. B., (2014). Effect of osmopriming duration on germination, emergence, and early growth of cowpea (Vigna unguiculata (L.) walp.) in the Sudan savanna of Nigeria. Int. J. Agron. Singh, H., Jassal, R. K., Kang, J., Sandhu, S., Kang, H., & Grewal, K., (2015). Seed priming techniques in field crops: A review. Agric. Rev., 36(4), 251–264. Singh, M., Singh, A., Prasad, S. M., & Singh, R. K., (2017). Regulation of plants metabolism in response to salt stress: An omics approach. Acta Physiol. Planta., 39(2), 48. Slama, I., M’Rabet, R., Ksouri, R., Talbi, O., Debez, A., & Abdelly, C., (2017). Effects of salt treatment on growth, lipid membrane peroxidation, polyphenol content, and antioxidant activities in leaves of Sesuvium portulacastrum L. Arid Land Res. Manag., 31(4), 404–417. Songlin, R., & Qingzhong, X., (2002). Effects of chitosan coating on seed germination and salt-tolerance of seedling in hybrid rice (Oryza sativa L.). Zuo Wu Xue Bao., 28(6), 803–808. Spicher, L., Almeida, J., Gutbrod, K., Pipitone, R., Dörmann, P., Glauser, G., Rossi, M., & Kessler, F., (2017). Essential role for phytol kinase and tocopherol in tolerance to combined light and temperature stress in tomato. J. Exp. Bot., 68, 5845–5856. Srivastava, A. K., Lokhande, V. H., Patade, V. Y., Suprasanna, P., Sjahril, R., D’Souza, S. F., (2010). Comparative evaluation of hydro-, chemo-, and hormonal-priming methods for imparting salt and PEG stress tolerance in Indian mustard (Brassica juncea L.). Acta Physiol. Planta., 32(6), 1135–1144. Stringlis, I. A., De Jonge, R., & Pieterse, C. M., (2019). The age of coumarins in plant-microbe interactions. Plant Cell Physiol., 60, 1405–1419. Su, J., Hirji, R., Zhang, L., He, C., Selvaraj, G., & Wu, R., (2006). Evaluation of the stressinducible production of choline oxidase in transgenic rice as a strategy for producing the stress-protectant glycine betaine. J. Exp. Bot., 57(5), 1129–1135. Suguiyama, V. F., Da Silva, E. A., Meirelles, S. T., Centeno, D. D. C., & Braga, M. R., (2014). Leaf metabolite profile of the Brazilian resurrection plant Barbacenia purpurea hook. (Velloziaceae) shows two time-dependent responses during desiccation and recovering. Front. Plant Sci., 5, 96. Sun, H., Wang, L., Zhang, B., Ma, J., Hettenhausen, C., Cao, G., et al., (2014). Scopoletin is a phytoalexin against Alternaria alternata in wild tobacco dependent on jasmonate signaling. J. Exp. Bot., 65, 4305–4315. Šutković, J., Ler, D., & Gawwad, M. R. A., (2011). In vitro production of solasodine alkaloid in Solanum nigrum under salinity stress. J. Phytol., 3(1), 43–49. Sytar, O., Mbarki, S., Zivcak, M., & Brestic, M., (2018). The involvement of different secondary metabolites in salinity tolerance of crops. In: Kumar, V., Wani, S., Suprasanna, P., & Tran, L. S., (eds.), Salinity Responses and Tolerance in Plants (Vol. 2, pp. 21–48). Springer: Cham. Szabados, L., & Savouré, A., (2010). Proline: A multifunctional amino acid. Trend. Plant Sci., 15(2), 89–97. Szabó, B., Tyihák, E., Szabó, G., & Botz, L., (2003). Mycotoxin and drought stress induced change of alkaloid content of Papaver somniferum plantlets. Acta Bot. Hung., 45, 409–417. Szopa, A., Kubica, P., & Ekiert, H., (2018). Agitated shoot cultures of Aronia arbutifolia and Aronia× prunifolia: Biotechnological studies on the accumulation of phenolic compounds and biotransformation capability. Plant Cell Tissue Organ Cult., 134(3), 467–479. Taiz, L., & Zeiger, E., (2002). Plant Physiology (3rd edn., p. 690). Sinauer Associates: Sunderland.

302

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Tavili, A., Zare, S., Moosavi, S. A., & Enayati, A., (2011). Effects of seed priming on germination characteristics of Bromus species under salt and drought conditions. Am. Eurasian. J. Agric. Environ. Sci., 10(2), 163–168. Thomas, T. T. D., & Puthur, J. T., (2020). UV-B priming enhances specific secondary metabolites in Oryza sativa (L.) empowering to encounter diverse abiotic stresses. Plant Growth Regul., 92(2), 169–180. Thomsen, M., Galambosi, B., Galambosi, Z., Uusitalo, M., Mordal, R., & Heinonen, A., (2011). Harvest time and drying temperature effect on secondary metabolites in Rhodiola rosea. In: Carlen, C., Baroffio, C. A., & Vouillamoz, J. F., (eds.), International Symposium on Medicinal, Aromatic and Nutraceutical Plants from Mountainous Areas (MAP-Mountain 2011) (Vol. 1, pp. 243–252). International Society for Horticultural Science: Leuven. Timmusk, S., Abd El-Daim, I. A., Copolovici, L., Tanilas, T., Kännaste, A., Behers, L., Nevo, E., et al., (2014). Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: Enhanced biomass production and reduced emissions of stress volatiles. PloS One, 9(5), e96086. Tuan, P. A., Thwe, A. A., Kim, Y. B., Kim, J. K., Kim, S. J., Lee, S., Chung, S. O., & Park, S. U., (2013). Effects of white, blue, and red light-emitting diodes on carotenoid biosynthetic gene expression levels and carotenoid accumulation in sprouts of Tartary buckwheat (Fagopyrum tataricum Gaertn.). J. Agric. Food Chem., 61(50), 12356–12361. Turtola, S., Manninen, A. M., Rikala, R., & Kainulainen, P., (2003). Drought stress alters the concentration of wood terpenoids in Scots pine and Norway spruce seedlings. J. Chem. Ecol., 29, 1981–1995. Varier, A., Vari, A. K., & Dadlani, M., (2010). The subcellular basis of seed priming. Curr. Sci., 99(4), 450–456. Villarreal-García, D., Nair, V., Cisneros-Zevallos, L., & Jacobo-Velázquez, D. A., (2016). Plants as biofactories: Postharvest stress-induced accumulation of phenolic compounds and glucosinolates in broccoli subjected to wounding stress and exogenous phytohormones. Front. Plant Sci., 7, 45. Wahid, A., & Ghazanfar, A., (2006). Possible involvement of some secondary metabolites in salt tolerance of sugarcane. J. Plant Physiol., 163(7), 723–730. Wang, Q., Eneji, A. E., Kong, X., Wang, K., & Dong, H., (2015). Salt stress effects on secondary metabolites of cotton in relation to gene expression responsible for aphid development. PLoS One, 10(6), e0129541. Wang, W., Vinocur, B., & Altman, A., (2003). Plant responses to drought, salinity and extreme temperatures: Towards genetic engineering for stress tolerance. Planta, 218(1), 1–14. Wang, Y., Wen, T., Huang, Y., Guan, Y., & Hu, J., (2018). Salicylic acid biosynthesis inhibitors increase chilling injury to maize (Zea mays L.) seedlings. Plant Growth Regul., 86(1), 11–21. Wargent, J. J., & Jordan, B. R., (2013). From ozone depletion to agriculture: Understanding the role of UV radiation in sustainable crop production. New Phytol., 197(4), 1058–1076. Wei, L. X., Lv, B. S., Li, X. W., Wang, M. M., Ma, H. Y., Yang, H. Y., Yang, R. F., et al., (2017). Priming of rice (Oryza sativa L.) seedlings with abscisic acid enhances seedling survival, plant growth, and grain yield in saline-alkaline paddy fields. Field Crop. Res., 203, 86–93. Winkel-Shirley, B., (2001). Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol., 126(2), 485–493.

Seed Priming and Seedling Pre-Treatment in Regulating Secondary Metabolism

303

Winkel-Shirley, B., (2002). Biosynthesis of flavonoids and effects of stress. Curr. Opin. Plant Biol., 5(3), 218–223. Xie, Y. Y., Qu, J. L., Wang, Q. L., Wang, Y., Yoshikawa, M., & Yuan, D., (2012). Comparative evaluation of cultivars of Chrysanthemum morifolium flowers by HPLC-DAD-ESI/MS analysis and antiallergic assay. J. Agric. Food Chem., 60, 12574–12583. Xiong, L., & Zhu, J. K., (2002). Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ., 25(2), 131–139. Xu, S., Hu, J., Li, Y., Ma, W., Zheng, Y., & Zhu, S., (2011). Chilling tolerance in Nicotiana tabacum induced by seed priming with putrescine. Plant Growth Regul., 63(3), 279–290. Xuan, T., Elzaawely, A., Deba, F., Fukuta, M., & Tawata, S., (2006). Mimosine in Leucaena as a potent bio-herbicide. Agron. Sustain. Dev., 26, 89–97. Yamane, H., Konno, K., Sabelis, M., Takabayashi, J., Sassa, T., & Oikawa, H., (2010). Chemical Defense and toxins of plants. In: Mander, L., & Liu, H. W., (eds.), Comprehensive Natural Products II: Chemistry and Biology (Vol. 4. pp. 339–385). Elsevier: Amsterdam. Yang, L., Wen, K. S., Ruan, X., Zhao, Y. X., Wei, F., & Wang, Q., (2018). Response of plant secondary metabolites to environmental factors. Molecule., 23(4), 762. Yang, Y., & Guo, Y., (2018). Elucidating the molecular mechanisms mediating plant salt‐ stress responses. New Phytol., 217(2), 523–539. Yavaş, I., Ünay, A., Ali, S., & Abbas, Z., (2020). UV-B radiations and secondary metabolites. Turk. J. Agric. Food Sci. Technol., 8(1), 147–157. Yokota, A., Kawasaki, S., Iwano, M., Nakamura, C., Miyake, C., & Akashi, K., (2002). Citrulline and DRIP-1 protein (ArgE homologue) in drought tolerance of wild watermelon. Ann. Bot., 89, 825–832. Yu, S., Yan, H., Zhang, L., Shan, M., Chen, P., Ding, A., & Li, S. F., (2017). A review on the phytochemistry, pharmacology, and pharmacokinetics of amentoflavone, a naturally occurring biflavonoid. Molecule, 22(2), 299. Yuan-Yuan, S., Yong-Jian, S., Ming-Tian, W., Xu-Yi, L., Xiang, G., Rong, H., & Jun, M., (2010). Effects of seed priming on germination and seedling growth under water stress in rice. Acta Agron. Sinica. 36(11), 1931–1940. Zhang, W., Seki, M., & Furusaki, S., (1997). Effect of temperature and its shift on growth and anthocyanin production in suspension cultures of strawberry cells. Plant Sci., 127(2), 207–214. Zhao, T. J., Liu, Y., Yan, Y. B., Feng, F., Liu, W. Q., & Zhou, H. M., (2007). Identification of the amino acids crucial for the activities of drought responsive element binding factors (DREBs) of Brassica napus. FEBS Letters., 581(16), 3044–3050. Zheng, J., Yang, B., Ruusunen, V., Laaksonen, O., Tahvonen, R., Hellsten, J., & Kallio, H., (2012). Compositional differences of phenolic compounds between black currant (Ribes nigrum L.) cultivars and their response to latitude and weather conditions. J. Agric. Food Chem., 60(26), 6581–6593. Zheng, M., Tao, Y., Hussain, S., Jiang, Q., Peng, S., Huang, J., Cui, K., & Nie, L., (2016). Seed priming in dry direct-seeded rice: Consequences for emergence, seedling growth and associated metabolic events under drought stress. Plant Growth Regul., 78(2), 167–178. Zhong, C., Mansour, S., Nambiar-Veetil, M., Bogusz, D., & Franche, C., (2013). Casuarina glauca: A model tree for basic research in actinorhizal symbiosis. J. Biosci., 38(4), 815–823. Zhong, J., Seki, T., Kinoshita, S., & Yoshida, T., (1991). Effect of light irradiation on anthocyanin production by suspended culture of Perilla frutescens. Biotechnol. Bioeng., 38.

304

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

Zu, Y. G., Tang, Z. H., Yu, J. H., Liu, S. G., Wang, W., & Guo, X. R., (2003). Different responses of camptothecin and 10-hydroxycamptothecin to heat shock in Camptotheca acuminata seedlings. Acta Bot. Sinica., 45(7), 809–814.

CHAPTER 12

Tools and Approaches for Assessing Stress-Responsive Secondary Metabolites to Design Climate-Smart Crops DEBAPRIYA RAJLAKSHMI DAS,1 MONOLINA SARKAR,2 and ANINDITA PAUL3*

Department of Botany, Taki Government College, Taki – 743429, West Bengal, India

1

Department of Botany, Sammilani Mahavidyalaya, Eastern Metropolitan Bypass, Kolkata – 700094, West Bengal, India

2

Molecular Biophysics Unit, Indian Institute of Science, Bangalore – 560012, Karnataka, India

3

*

Corresponding author. E-mail: [email protected]

ABSTRACT Agricultural environments are constantly jeopardized by abiotic stresses, including periodical droughts, temperature extremes, water deficit, flooding, salinity, and changes in atmospheric CO2 levels. These agro-climatic factors severely affect crop quality, productivity, and yield. Crop plants’ responses to such drastic climatic stresses involve alterations in gene expression and extensive metabolic reprogramming, impacting their proteome and metabolome. Thereby, the plants ensure metabolic homeostasis and improved stress tolerance. Among multiple adaptive responses, the production and accumulation of low molecular weight, chemically diverse, bioactive, Biology and Biotechnology of Environmental Stress Tolerance in Plants: Secondary Metabolites in Environmental Stress Tolerance, Volume 1. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

306

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 1

exogenous, and endogenous secondary metabolites (SMs) are noteworthy. Metabolites are spatio-temporal chemical footprints of the cellular state under particular physiological or developmental conditions that reflect the complex crosstalk between genotype and the environment. Consequently, it is imperative to conduct a qualitative and quantitative assessment of the multi-parametric metabolic responses, analyze reconfigured metabolic networks under diverse stress conditions, and identify the underlying candidate genes in various metabolic biosynthetic pathways. Herein, we discuss the advances in analytical methods and sequencing technologies which offer high-throughput, cutting-edge, and cost-effective techniques for systematic identification of SMs and genetic dissection of commercially important agronomic traits. Integration of metabolomics with transcriptomics allows large-scale metabolite profiling with desirable accuracy and coverage, and mapping of trait-specific markers with high confidence levels, respectively. Inferring from large volumes of multi-omics data facilitates the identification of metabolic biomarkers and enables informed decision-making for crop breeding programs, which aim to develop climate-smart future crops with enhanced fitness, improved productivity, and increased stress tolerance. 12.1 INTRODUCTION Over the decades, the human population has been growing at an alarming speed. To provide food and shelter to this booming population, the world’s natural resources have been exploited at an unprecedented rate. This in combination with global climate change has direly affected the earth’s environment. A rapid shrinkage in food supplies has also been observed as a result. To ward off the developing food crisis, researchers aim at developing climate-smart plants which can tolerate or acclimatize to the changing climate. Plants as sessile organisms are usually exposed to a variety of environmental stresses such as water stress, temperature stress, salinity, radiation, nutritional, and chemical stress (Figure 12.1(A)). These fluctuations in the environment affect different developmental processes of plants, causing osmotic imbalances photosynthetic malfunctioning, and perturbed biosynthetic pathways which ultimately result in decreased plant biomass production and reduced plant health (Isah, 2019; Razzaq et al., 2019). Plants that are capable of coping with these environmental stresses can do so via bringing about changes in their metabolome, resulting from the interaction

Tools and Approaches for Assessing Stress-Responsive Secondary Metabolites

307

of the plant genotype with its surroundings. This causes morphological as well as physiological changes via alteration in metabolites synthesized. Biosynthesis of these metabolites further involves alteration in the transcriptome and proteome of the organism. These alterations, if favorable, lead to better adaptability of the plant and are fixed into plant genotype, either via natural selection or through selective breeding (Akula & Ravishankar, 2011; Delgoda & Murray, 2017; Kumar et al., 2017). A huge array of metabolites is synthesized by most plants’ cells, to perform various structural and physiological functions throughout their life span. Metabolites represent small organic compounds or biomolecules (