Biology and Biotechnology of Environmental Stress Tolerance in Plants: Volume 2: Trace Elements in Environmental Stress Tolerance 1774912856, 9781774912850

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Biology and

Biotechnology of

Environmental Stress

Tolerance in Plants

Volume 2:

Trace Elements 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 2:

Trace Elements in Environmental

Stress Tolerance

Edited by

Aryadeep Roychoudhury, PhD

First edition published 2024 Apple Academic Press Inc. 1265 Goldenrod Circle, NE, Palm Bay, FL 32905 USA 760 Laurentian Drive, Unit 19, Burlington, ON L7N 0A4, CANADA

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© 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 2: Trace Elements in Environmental Stress Tolerance. Identifiers: Canadiana (print) 20230155588 | Canadiana (ebook) 20230155626 | ISBN 9781774912812 (set ; hardcover) | ISBN 9781774912829 (set ; softcover) | ISBN 9781774912850 (v. 2 ; hardcover) | ISBN 9781774912867 (v. 2 ; softcover) | ISBN 9781003346203 (v. 2 ; 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 Congress

ISBN: 978-1-77491-285-0 (hbk) ISBN: 978-1-77491-286-7 (pbk) ISBN: 978-1-00334-620-3 (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 at the Department of Biotechnology, 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: Trace Elements in Sustaining Plant Growth ........................................1

1.

Trace Elements in Mitigating Environmental Stress: An Overview ..........3

Somali Dhal and Harshata Pal

2.

Trace Elements and Their Role in Abiotic Stresses ...................................67

Simranjit Kaur, Anjali Joshi, Kriti Gupta, Anuj Kumar, Vajinder Kumar, Harsh Nayyar, and Avneesh Kumar

3.

Exogenous Application of Trace Elements and Their Uptake by

Plants to Mediate Abiotic Stress Tolerance...............................................147

Ankur Singh and Aryadeep Roychoudhury

PART II: Individual Trace Elements in Tolerance..........................................173

4.

Role of Iron and Manganese in Tolerance Against Different Environmental Stress..................................................................................175

Soumya Mukherjee

5.

Role of Zinc in Tolerance Against Different Environmental Stress........197

Subhashisa Praharaj, Sagar Maitra, Suprava Nath, Akbar Hossain, Lalichetti Sagar, Sudeepta Pattanayak, Mahua Banerjee, Biswajit Pramanick, Tanmoy Shankar, and Arunabha Pal

6.

Role of Silicon in Tolerance Against Different Environmental Stress ....215

Ashita Baishkhiyar, Anamika Paul, and Nilanjan Chakraborty

7.

Role of Selenium in Tolerance Against Different Environmental Stress..................................................................................257

Umair Riaz, Tayyaba Samreen, Muhammad Zulqernain Nazir,

Natasha Kanwal, Safdar Bashir, and Qamar-Uz-Zaman

8.

Role of Nickel as a Potent Environmental Stress Reliever in Plants......269

Disha Dasgupta, Krishnendu Acharya, and Nilanjan Chakraborty

Contents

viii

9.

Role of Cobalt in Plant Growth and Tolerance Against Different Environmental Stress..................................................................305 Debabrata Panda, Prafulla K. Behera, and Jayanta K. Nayak

10. Role of Molybdenum in Tolerance Against Different Environmental Stresses ..............................................................................325

Lekshmy Sathee, R. Suriyaprakash, Jyoti Priya, Sinto Antoo, and Shailendra K. Jha

11. Role of Copper in Tolerance Against Different Environmental Stress...351 Swarnali Dey, Ankita Biswas, Rita Kundu, and Subhabrata Paul

12. Role of Sulfur in Plant Tolerance to Environmental Stresses .................387

Lalichetti Sagar, Sultan Singh, Deepak Kumar, Subhashisa Praharaj,

Sudeepta Pattanayak, Ganesh Chandra Malik, Biswajit Pramanick,

Tanmoy Shankar, Akbar Hossain, and Sagar Maitra

13. Role of Chloride and Organic Acid Anions in Environmental Stress Tolerance ................................................................415 Titir Guha, Preeti Verma, and Rita Kundu

14. Role of Sulfur in Protection Against Major Environmental Stress in Plants ............................................................................................473 Snehalata Majumdar, Falguni Barman, Alivia Paul, and Rita Kundu

PART III: Nanoparticles in Stress Tolerance ..................................................531

15. Application of Nanomaterial-Based Technology in Stress Management of Plants ................................................................................533 Aditya Banerjee and Aryadeep Roychoudhury

16. Role of Nanoparticles in Tolerance Against Different Environmental Stress..................................................................................545

Ayushi Singh, Parul Tyagi, Pooja Saraswat, and Rajiv Ranjan

17. Nanotechnology and Use of Nanoparticles in Developing Environmental Stress-Tolerant Plants ......................................................571 Umair Riaz, Tayyaba Samreen, Muhammad Saqlain Shah, Humera Aziz, Laila Shahzad, Muhammad Zulqernain Nazir, Nimra Raiz,

Tariq Mehmood, and Ghulam Hussain Jatoi

Index .....................................................................................................................589

Contributors

Krishnendu Acharya

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

Sinto Antoo

Division of Plant Physiology, ICAR–Indian Agricultural Research Institute, New Delhi – 110012, India

Humera Aziz

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

Ashita Baishkhiyar

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

Aditya Banerjee

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

Mahua Banerjee

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

Falguni Barman

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

Safdar Bashir

Department of Soil and Environmental Sciences, Ghazi University (GU), D.G. Khan, Pakistan

Prafulla K. Behera

Department of Biodiversity and Conservation of Natural Resources, Central University of Odisha, Koraput – 764021, Odisha, India

Ankita Biswas

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

Nilanjan Chakraborty

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

Disha Dasgupta

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

Swarnali Dey

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

Somali Dhal

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

x

Contributors

Titir Guha

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

Kriti Gupta

Department of Botany, DAV College, Bathinda, Punjab – 151001, India

Akbar Hossain

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

Ghulam Hussain Jatoi

Department of Agriculture, Mir Chakar Khan Rind University, Sibi, Balochistan, Pakistan

Shailendra K. Jha

Division of Genetics, ICAR–Indian Agricultural Research Institute, New Delhi – 110012, India

Anjali Joshi

Center for Nanoscience and Nanotechnology (UIEAST), Panjab University, Chandigarh – 160014, India

Natasha Kanwal

Regional Agricultural Research Institute, Bahawalpur – 63100, Agriculture Department, Government of Punjab, Pakistan

Simranjit Kaur

Department of Botany, Akal University, Talwandi Sabo, Bathinda, Punjab – 151302, India

Anuj Kumar

Center for Agricultural Statistics, ICAR–Indian Agricultural Statistics Research Institute, New Delhi – 11012, India

Avneesh Kumar

Department of Botany, Akal University, Talwandi Sabo, Bathinda, Punjab – 151302, India, [email protected]

Deepak Kumar

Division of Agronomy, Sher-e-Kashmir University of Technology and Management, Jammu – 180009, Jammu and Kashmir, India

Vajinder Kumar

Department of Chemistry, Akal University, Talwandi Sabo, Bathinda, Punjab – 151302, India

Rita Kundu

Center of Advanced Study, Department of Botany, University of Calcutta, 35, Ballygunge Circular Road, Kolkata – 700019, West Bengal, India, E-mails: [email protected]; [email protected]

Sagar Maitra

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

Snehalata Majumdar

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

Ganesh Chandra Malik

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

Tariq Mehmood

College of Environment, Hohai University Nanjing, China

Contributors

xi

Soumya Mukherjee

Department of Botany, Jangipur College, West Bengal – 742213, India, E-mail: [email protected]

Suprava Nath

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

Jayanta K. Nayak

Department of Anthropology, Central University of Odisha, Koraput – 764020, Odisha, India

Harsh Nayyar

Department of Botany, Panjab University, Chandigarh – 160014, India

Muhammad Zulqernain Nazir

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

Arunabha Pal

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

Harshata Pal

Amity Institute of Biotechnology, Amity University Kolkata, Major Arterial Road (Southeast), Action Area II, Newtown, Kolkata – 700135, West Bengal, India, Tel.: 7003136942, E-mail: [email protected], ORCID: 0000-0002-4063-3836

Debabrata Panda

Department of Biodiversity and Conservation of Natural Resources, Central University of Odisha,

Koraput – 764021, Odisha, India, Tel.: 91-6852-251288, Fax: 91-6852-251244,

E-mail: [email protected], ORCID: orcid.org/0000-0002-8019-3062

Sudeepta Pattanayak

Division of Plant Pathology, ICAR–Indian Agricultural Research Institute, Pusa Campus, New Delhi – 110012, India

Alivia Paul

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

Anamika Paul

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

Subhabrata Paul

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

Subhashisa Praharaj

Department of Agronomy and Agroforestry, Centurion University of Technology and Management, Paralakhemundi – 761211, Odisha, India

Biswajit Pramanick

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

Jyoti Priya

Division of Plant Physiology, ICAR–Indian Agricultural Research Institute, New Delhi – 110012, India

Qamar-Uz-Zaman

Department of Environmental Sciences, University of Lahore, Lahore, Pakistan

Nimra Raiz

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

Rajiv Ranjan

Dayalbagh Educational Institute, Department of Botany, DayalBagh, Agra – 282005, Uttar Pradesh, India, E-mail: [email protected]

xii

Contributors

Umair Riaz

Soil and Water Testing Laboratory for Research, Bahawalpur – 63100, Agriculture Department, Government of Punjab, 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]

Lalichetti Sagar

Department of Agronomy and Agroforestry, Centurion University of Technology and Management, Paralakhemundi – 761211, Odisha, India

Tayyaba Samreen

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

Pooja Saraswat

Dayalbagh Educational Institute, Department of Botany, DayalBagh, Agra – 282005, Uttar Pradesh, India

Lekshmy Sathee

Division of Plant Physiology, ICAR–Indian Agricultural Research Institute, New Delhi – 110012, India, E-mail: [email protected]

Muhammad Saqlain Shah

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

Laila Shahzad

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

Tanmoy Shankar

Department of Agronomy and Agroforestry, Centurion University of Technology and Management, Paralakhemundi – 761211, Odisha, India

Ankur Singh

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

Ayushi Singh

Dayalbagh Educational Institute, Department of Botany, DayalBagh, Agra – 282005, Uttar Pradesh, India

Sultan Singh

Division of Agronomy, Sher-e-Kashmir University of Technology and Management, Jammu – 180009, Jammu and Kashmir, India

R. Suriyaprakash

Division of Plant Physiology, ICAR–Indian Agricultural Research Institute, New Delhi – 110012, India

Parul Tyagi

Dayalbagh Educational Institute, Department of Botany, DayalBagh, Agra – 282005, Uttar Pradesh, India

Preeti Verma

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

Abbreviations

AAO3 ABA ABC ABRE ACC ACO ACS Al ALDH2B7 ALMT AMP AO AO AOX APR APX AQP ARC ART1 As AsA ASH ASR ATP AuNPs B BICAT BNF bZIP C2H2 C2H2-ZFPs C3HC4 CaCA CalyA

abscisic aldehyde oxidase-3 abscisic acid ATP-binding cassette ABA-responsive elements aminocyclopropane-1-carboxylic acid aminocyclopropane-1-carboxylate oxidase 1-aminocyclopropane-1-carboxylate synthase aluminium acetaldehyde dehydrogenase 2B7 aluminum-activated malate transporters antimicrobial peptides aldehyde oxidase ascorbate oxidase alternative oxidase adenosine-5-phosphosulfate reductase ascorbate peroxidase aquaporins amidoxime reducing component aluminium resistance transcription factor 1 arsenic ascorbic acid salicyloyl hydrazone Asian soybean rust adenosine triphosphate gold nanoparticles boron bivalent cation transporter biological nitrogen fixation basic leucine zipper Cys2His2 Cys2His2-type zinc finger proteins Cys3HisCys4 Ca2+/cation antiporter calyculin A

xiv

CAM CAT CAX CBF3 CBL CCC CCC CCX Cd CDes CDF CDSP 32 CEM CH-Fe2O3 NPs CIPK Cl CLC CLE25 CMV CNR2 CNTs Co CO2 CODH COPT COR COX CPK/CDPK CRISPR CRISPR-Cas9 CRPs CSC CTR Cu Cu/Zn SOD CuChNp CuCl2 Cu-NPs Cys DHAP

Abbreviations

crassulacean acid metabolism catalase cation exchanger C-repeat binding factor 3 calcineurin-B like protein cation chloride cotransporter cation-coupled Cl– cation calcium exchanger cadmium cysteine desulfhydrases cation diffusion facilitator chloroplastic drought-induced stress protein 32 citrate exuding motif chitosan iron-oxide nanoparticles CBL-interacting protein kinase chlorine chloride channels CLAVAT3/embryo-surrounding region-related 25 cauliflower mosaic virus cell number regulator 2 carbon nanotubes cobalt carbon dioxide carbon monoxide dehydrogenase copper transporter protein cold regulated cytochrome-c oxidase calcium-dependent kinase clustered regularly interspaced short palindromic repeats CRISPR-associated proteins cysteine-rich peptides cysteine synthase complex copper transporter copper Cu/Zn–superoxide dismutase copper-chitosan nanoparticle copper chloride copper nanoparticles cysteine dihydroxy acetone phosphate

Abbreviations

DHAR DICs DMS DMT DNA DRE DS DTC DTX ESH ET ETRs FC Fe Fe-NPs FER1 FLC FT FTIR GA GABA GFP Gly I Gly II GO GOGAT GPS GPx GPX GR Grx GS GSH/Glu GSL GSNOR1 GST H2O2 H2S H4SiO4 HCys

xv

dehydroascorbate reductase dicarboxylate carriers dimethyl sulfide drug metabolite transporter deoxyribonucleic acid drought-responsive element drought stress dicarboxylate/tricarboxylate carriers detoxification efflux carrier ethyl methyl ketone salicyloyl hydrazone ethylene ethylene receptors field capacity iron iron nanoparticles ferritin 1 flowering locus C flowering locus T Fourier transform infrared spectroscopy gibberellic acid gamma amino-butyric acid green fluorescent protein glyoxalase I glyoxalase II glycolate oxidase glutamate synthase global position system glutathione peroxidase guaiacol peroxidase glutathione reductase glutaredoxins glutamine synthetase glutathione glucosinolates S-nitrosoglutathione reductase 1 glutathione transferase hydrogen peroxide hydrogen sulfide monosilicic acid homocysteine

Abbreviations

xvi

HDA6 Hg HMA HMWOAs HPCA1 HSF HSP IAA IAA-94 IAN ICS1 IDH IPCC IRT IRT/ZIP IRT1 ISR JA KCl LAI LDH LEA LHC LMWOA LPO LPR1 LRR-RLK MA MAMPs MAPK mARC MATE MCF MDA MDAR MeJA mETC MetSO MG

histone deacetylase 6 mercury heavy metal ATPase high molecular weight organic acids hydrogen-peroxide-induced Ca2+ increase heat shock factors heat shock protein indole-3 acetic acid indanyloxyacetic acid-94 indole-3-acetonitrile isochorismate synthase1 isocitrate dehydrogenase Intergovernmental Panel on Climate Change iron-regulated transporter ZRT-/IRT like proteins iron uptake transporter induced systemic resistance jasmonic acid potassium chloride leaf area index layered double hydroxide late embryogenesis abundant light-harvesting complex low molecular weight organic acids lipid peroxidation low phosphate root 1 leucine-rich repeat kinase mugineic acids microbe-associated molecular patterns mitogen-activated protein kinase mitochondrial amidoxime reductase multidrug and toxic compound extrusion mitochondrial carrier family malondialdehyde monodehydroascorbate reductase methyl jasmonate mitochondrial electron transport chain methionine sulfoxide methylglyoxal

Abbreviations

MIP MMS Mn MnNPs MnPhi MNPs Mo Moco MoS2-CuNPs MOT1 MRP MSI MSNs MT mTCA MTP MV MWCNTs N2 NA NaD1 NADPH NAXT NBS-LRRs NCED3 NG Ni Ni-AA NiCoT NIP NiR NiSOD NMs NO NPF NPPB NPs NR NRAMP

xvii

major intrinsic protein S-methyl methionine-salicylate manganese manganese (III) oxide nanoparticles manganese phosphite magnetic nanoparticles molybdenum Mo cofactors molybdenum disulfide loaded with copper nanoparticles molybdate transporter 1 multidrug resistance-associated protein membrane stability index mesoporous silica nanoparticles metallothioneins mitochondrial tricarboxylic acid metal tolerance protein methyl viologen multiwalled carbon nanotubes nitrogen nicotinamine Nicotiana alata defensin 1 nicotinamide adenine dinucleotide phosphate nitrate excretion transporter family nucleotide-binding sites-leucine rich repeats 9 cis-epoxycarotenoid dioxygenase 3 nanogel nickel Ni-amino acid nickel/cobalt transporters nodulin 26-like intrinsic proteins nitrite reductase Ni-containing superoxide dismutase nanomaterials nitric oxide nitrate transporter 1/peptide transporter 5-nitro-2-(3-phenylpropylamino)benzoic acid nanoparticles nitrate reductase natural resistance-associated macrophage protein

Abbreviations

xviii

NRAT1 NRT NSCC nSiO2 NUE OAS-TL OEC OKA OPT OST1 OXDC PAF PAL PAR Pb PC PCS PDC1 PEG PEP-case PEPCK PGAld PGPR PMSR POD PP ppm PPO ProDH PRs PS PSI PSII PtNPs PUFA PVA QDs QUAC1 RAE1

NRAMP aluminium transporter 1 nitrate transporters nonselective cation channels nano-silicon dioxide nitrogen use efficiency O-acetyl serine thiol lyase oxygen-evolving complex okadaic acid oligo peptide transporters open stomata-1 oxalate decarboxylase plants available form phenylalanine ammonia-lyase photosynthetically active radiation lead phytochelatins phytochelatin synthase pyruvate decarboxylase-1 polyethylene glycol phosphoenol pyruvate carboxylase phosphoenol pyruvate carboxy kinase phosphoglyceraldehyde plants growth promoting rhizobacteria peptide MetSO reductase peroxidase pathogenesis-related proteins parts per million polyphenol oxidase proline dehydrogenase pathogenesis-related phytosiderophores photosystem I photosystem II platinum nanoparticles polyunsaturated fatty acids potato virus A quantum dots quick anion channel-1 regulation of AtALMT1 expression 1

Abbreviations

RAM RBOH RLWC RNA RNS RONSS ROS RSS RT-PCR RuBisCO RUBP RWC SA SAH SAM SAP SAR SAT SATP Se SeCys SeMet SeMSC SERAT SFC SHST1 Si SiNPs SiR SLAC1 SLG SLIM1 SnRK SO SOD SPIO-NPs SSP STOP1 SULTR

xix

root apical meristem respiratory burst oxidase protein relative leaf water content ribonucleic acid reactive nitrogen species reactive oxygen, nitrogen, and sulfur species reactive oxygen species reactive sulfur species reverse transcription polymerase chain reaction ribulose-1,5-biphosphate carboxylase-oxygenase ribulose bisphosphate relative water content salicylic acid S-adenosyl-L-homocysteine S-adenosyl methionine salicylidine-o-aminopyridine systemic acquired resistance serine acetyltransferase salicylidine-o-amino-thiophenol selenium selenocysteine selenomethionine Se-methyloselenocysteine Ser acetyltransferase succinate/fumarate carrier Stylosanthes hamata sulfate transporter silicon silicon nanoparticles sulfite reductase slow anion channel-Associated 1 S-D lactoylglutathione sulfur limitation 1 transcription factor sucrose non-fermenting-related kinase sulfite oxidase superoxide dismutase superparamagnetic iron oxide single superphosphate sensitive to proton rhizotoxicity 1 sulfate/selenate cotransporter

Abbreviations

xx

SURE SWCNTs TAL TBARS TCA TEs TFs TIA TiO2 TMHs Trx TTL UV UV-B V VDAC VIT VOZ WHO WT WUE XDH XO XOD XOR XRD YSL ZFPs ZIP Zn ZnIP ZnO-NPs ZRT γ ECS

sulfur-responsive element single-walled carbon nanotubes tyrosine ammonia-lyase thiobarbituric acid reactive substance tricarboxylic acid trace elements transcription factors terpenoid indole alkaloids titanium dioxide transmembrane helices thioredoxin tetratricopeptide thioredoxin-like ultraviolet ultraviolet-B vanadium voltage-dependent anion channels vacuolar iron transporter vascular plant one zinc-finger World Health Organization wild type water use efficiency xanthine dehydrogenase xanthine oxidases oxygen dependent xanthine oxidoreductase X-ray diffraction yellow stripe 1-like zinc finger proteins zinc-regulated transporter proteins zinc zinc-iron permease zinc oxide nanoparticles zinc-regulated transporter gamma-EC synthase

Preface

Plants are frequently exposed to a wide diversity of unfavorable and adverse environmental conditions, which include drought, salinity, extreme temperature, anoxia, flooding, heavy metals, UV radiation, etc. Altogether, these stressors pose a major threat to the productivity of plant species and are responsible for 50% of crop yield reduction. Abiotic stress is an integral part of climate change, a complex phenomenon exerting a wide range of unpredictable impacts on the environment. Thus, understanding plant stress response is a fundamental requirement so as to develop tolerant plants and efficient management practices to withstand hostile situations. An overall understanding of the molecular and biochemical interactions of plants is important to implement the knowledge of resistance mechanisms. Prolonged exposure to environmental stresses incites oxidative damage to biomolecules and results in altered metabolism, triggering the defense mechanisms via upregulation of osmolytes, osmoprotectants, enzymatic and non-enzymatic antioxidants, etc. The role of mineral nutrients and trace elements (TEs) in mitigating diverse environmental stresses has been largely investigated by several research groups. Recently, beneficial trace elements like Fe, Cu, Zn, Mo, Si, Ni, etc., at very low concentrations or under an optimum range, induce essential biochemical reactions and confer protection against various environmental stresses. When applied exogenously to stressed plants, such elements can overcome the adverse effects of stress by reducing oxidative damage. Symplastic uptake of Si via plant roots is regulated by Nod26-like intrinsic proteins (NIPs) and influx transporters (OsLsi1), following which Si undergoes xylem loading to be released in the apoplast and finally translocated to the shoots. Si is a quasi-essential element ensuring tolerance against salinity, drought, heavy metal toxicity, UV, etc. Si application enables immobilization of toxic metals in the soil by lowering of soil pH or formation of metalsilicate complex. Silicon nanoparticles (SiNPs) have also shown efficacy in alleviating diverse environmental stress in plants. Exogenous application of Cu, Zn, and Fe can mitigate environmental stresses and improve crop yield by maintaining normal functioning of physiological processes like photosynthesis, sugar metabolism, stabilization of protein structure, synthesis of proteins and nucleic acids, and also regulating the optimum nutrient quotient

xxii

Preface

of the soil. Exogenous molybdenum (Mo) application has been shown to mitigate cadmium toxicity by immobilizing soil cadmium and reducing its uptake, along with improving physiological parameters like biomass and photosynthesis. Manganese is a component of different enzymes like malic dehydrogenase and oxalosuccinic decarboxylase. Cobalt also maintains proper growth and development by regulating plant water utilization and checking transpiration rates. Likewise, nickel is essential for the activation of enzymes like urease and glyoxalase I (Gly I), as well as controls nitrogen metabolism, photosynthesis, germination, and vegetative and reproductive development. Several sulfur‐containing compounds also directly act as antioxidants or modulate antioxidant defense systems during stress. Researchers all over the world have therefore focused their attention on exploring the mechanisms of trace element uptake, their effects on metabolism, balance of nutrients, and their significance in terms of stress tolerance. Taking all these observations into consideration, it is necessary to provide insight into the latest advancements in the field of trace element research with context to abiotic stress tolerance in crops. Volume 2, entitled “Trace elements in environmental stress tolerance,” of this three-volume book set therefore exhaustively throws light on the different inorganic trace elements, including nanoparticles, in coping with various environmental stresses. While these elements at high levels create considerable phytotoxicity and halt the metabolic and enzymatic activity, they promote growth and development in limited quantity, so that they have a lot of potential to revamp the plant morphology and physiology under stressed conditions. Hence, optimum concentration management of these elements can help to mitigate world hunger and contribute towards sustainable agriculture and food security under challenging environments.

PART I

Trace Elements in

Sustaining Plant Growth

CHAPTER 1

Trace Elements in Mitigating Environmental Stress: An Overview SOMALI DHAL and HARSHATA PAL

Amity Institute of Biotechnology, Amity University Kolkata, Major Arterial Road (Southeast), Action Area II, Newtown, Kolkata – 700135, West Bengal, India, Tel.: 7003136942 *

Corresponding author. E-mail: [email protected]

ABSTRACT Trace elements (TEs) are micronutrients being ubiquitous in the earth and are substantial to expedite a range of physiological functions and development in plants. Some of the beneficial TEs for plant growth and development include zinc, manganese, iron, molybdenum, silicon, etc. As these elements are persistent and non-biodegradable, they get accumulated in a place and hence taken up by the plant through root or foliar penetration. The TEs can have a dual role in plant development. Some of the documented TEs show positive effects in growth and stress mitigation, however, they can have negative effects if their concentration rises above the optimal levels. These elements can be used exogenously to establish a stress mitigating technique to withstand unfavorable natural environments since they promote antioxidant protection systems. Few elements like copper, iron, manganese, etc., have a significant role in alleviating biotic stress and protect the plants against diseases such as stalk rot, rust, powdery mildew, and other pathogen infections. It becomes necessary to understand the uptake process of the TEs as it differs for different types of abiotic and biotic stress and also for different plant species. This chapter reflects on the overall purposes of Biology and Biotechnology of Environmental Stress Tolerance in Plants: Trace Elements in Environmental Stress Tolerance, Volume 2. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

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different TEs in plants, highlighting, in particular, the recent developments in the resistance of environmental stress to the behavior of several TEs. 1.1 INTRODUCTION Trace elements (TEs) have varied meanings depending upon the scientific domain and are special due to the importance of their quantity ratio (KabataPendias & Szteke, 2015). A TE is defined by an analytical chemist as an element in a given sample with an average concentration of less than 100 ppm on an atomic counting basis or less than 100 μg/g on a mass basis. In comparison, biochemists characterize “trace elements” as “elements that, while being present in trace quantities, are needed to preserve an organism’s physiological equilibrium, often serving as cofactors in enzymatic reactions; this biochemical classification includes various heavy metals, certain nonmetals, and some metalloids” (Koller & Saleh, 2018). Because of their lower abundance in biological tissues and identification in minute levels by older techniques, the minor components were given many titles in the literature, including “minor elements,” “oligo-elements,” “oligo-metals,” “micronutrients,” “trace metals,” and “trace elements.” Some of the TEs including boron (B), copper (Cu), iron (Fe), manganese (Mn), molybdenum (Mo), zinc (Zn), etc., are important for the plants in their morphological as well physiological aspects (Shive, 1941). The combination of TEs and major elements is necessary to achieve continued growth and healthy growing plants (Robson & Pitman, 1983). In essence, these elements are required by the plants throughout their life cycle. TEs are beneficial in lower concentrations but can cause deleterious effects (phytotoxic) if present at high concentrations (Robinson et al., 2009). TE typically penetrates plants through the roots and accumulates in either the roots or the shoots of the plants (Zhao et al., 2000). Water absorption in the plant causes TE translocation from the roots to the shoots via the xylem (Salt et al., 1995). Phloem transport is responsible for the redistribution of some TEs (Mn, Zn, Co, Ni, Fe, etc.) within the plant system (Pate et al., 1975; Riesen & Feller, 2005; Salt et al., 1995). TEs are involved in a variety of complex cellular processes. Examples include, but are not limited to, enzyme synthesis, development of chlorophyll, secondary metabolite formation, cell wall lignification, ribosomal fraction stabilization, primary and secondary metabolism, gene regulation, hormonal balance, nitrogen assimilation, cell signaling, ionic homeostasis, and protection against biotic and abiotic stresses (Khan et al., 2018; Stiles, 2013). Furthermore, numerous essential physiological activities in plants are all TE-dependent systems. For example, stomata opening and shutting control,

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transport through xylem and phloem, and membrane permeability utilize different TEs (Hänsch & Mendel, 2009). Plants are sessile organisms whose physiology, metabolism, as well as productivity, depend on/are affected by environmental conditions. In general, plants are exposed to two types of environmental stress: abiotic and biotic stress. Biotic stress is triggered by living organisms such as fungi, viruses, bacteria, nematodes, harmful insects, and parasites (Lata et al., 2018). Abiotic stressors include extreme temperatures, drought, flood, salt, light, and heavy metals. These stress factors mainly influence plant development and crop productivity (Gong et al., 2020). The environmental stresses influence different processes in the plants, and to cope with such situations, plants try to utilize the minerals/ nutrients available in their surroundings to bring out various responses against those stress factors. During stress conditions, the level of reactive oxygen species (ROS) increases in the plants and can be harmful for the plants. The plants respond to such high levels of ROS by the help of different enzymes which finally maintains the redox homeostasis in the plants (Miller et al., 2010). The exact mechanism by which these TEs mediate stress tolerance is not clear, however, several advantageous responses have been seen to mitigate the stress conditions with the help of different mechanisms (Habibi, 2014). In this chapter, we will have an overview of how different TEs are involved in the mitigation of stress and what changes they bring out in plant physiology by sensing and activating signaling cascades that help the plants to survive different environmental conditions. At the end we will also try to explore the possible external application of TEs that are beneficial for plants. 1.2 HOW DO PLANTS RETORT TO THE ABIOTIC AND BIOTIC STRESSES? During the abiotic and biotic stress conditions, the plant produces ROS, reactive nitrogen species (RNS), and reactive sulfur species (RSS). ROS includes hydrogen peroxide (H2O2), hydroxyl radical (OH▪), hypochlorous acid (HOCl), ozone (O3), superoxide (O2▪−), and singlet oxygen (1O2) like molecules (Saminathan et al., 2016). As a result, plants have evolved stress tolerance mechanisms that contribute to the expression of certain genes engaged in various respiratory and metabolic processes. Such mechanisms include genes involved in encoding enzymes for scavenging ROS, genes involved in osmolyte synthesis, genes for molecular chaperons (heat shock proteins (HSPs)), genes encoding the late embryogenesis abundant (LEA), genes encoding heterologous enzymes with different temperature optima, genes encoding transcription factors (TFs) and proteins involved in ion homeostasis

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(Fraire-Velázquez et al., 2011). ROS has intricated downstream effects on both primary and secondary metabolisms (Forrester et al., 2018; Huang et al., 2019). To employ ROS as a signaling molecule, a careful balance between ROS generation using ROS-complete enzymes and the inevitability of ROS creation during basic cell activities, as well as biochemical contra-processes involving ROS spray channels, must be maintained (Baxter et al., 2014). In addition, the processing of superoxide plasma membranes is one of the key ways higher plants relay information about changing environments (Shao et al., 2008). The RNS is the result of the interaction of nitric oxide (NO) with O2 and O2▪− (Molassiotis & Fotopoulos, 2011) and the RSS originated from the one-electron oxidation of hydrogen sulfide (H2S) (Olson & Straub, 2015). The strong interaction of RNS with ROS and RSS is a critical component of the natural line of defense against stress situations (Ijaz et al., 2019; Savvides et al., 2016). Hence, RONSS (reactive oxygen, nitrogen, and sulfur species) can act as chemicals for priming schemes to develop cross-tolerance against abiotic stress such as heat, drought, salt, and chilling stress (Terrile et al., 2020). The changes made in the major primary metabolic pathways such as in glycolysis, the mitochondrial tricarboxylic acid (mTCA), and the mitochondrial electron transport chain (mETC), are an important survival strategy for the plants to overcome the environmental fluctuations. This can affect the activity of enzymes of the TCA cycle as well as glycolysis and might induce complex variations in metabolite pools in carbon metabolism (Dumont & Rivoal, 2019). The photosynthetic fixation of CO2 in chloroplasts can control ROS production. Limited CO2 fixation reduces adenosine triphosphate (ATP) and NADPH consumption and lowers nicotinamide adenine dinucleotide phosphate (NADP1) levels in the presence of strong light (Miller et al., 2010). When NADP1 is reduced, electrons are transported from photosystem I (PSI) to molecular oxygen, resulting in the formation of ROS. During times of stress, the over-reduction of complex I and complex III in the mETC is also a key source of ROS production (Miller et al., 2010). Glycolate oxidase (GO) generates glycolate in plant peroxisomes and utilizes O2 as an electron acceptor to make H2O2 (Mhamdi et al., 2012). Along with the generation of ROS, plants also respond to stress by activating enzymes related to oxidative stress such as ascorbate peroxidase (APX), chitinase, β-1,3-glucanase, guaiacol peroxidase (GPX), glutathione reductase (GR), and superoxide dismutase (SOD) (GarcíaCristobal et al., 2015). Secondary metabolites such as phenolics, terpenes, and nitrogen (N) and sulfur (S) containing substances, in addition to primary metabolites, protect plants from herbivores and pathogenic microbes, as well as abiotic stressors (Edreva et al., 2008; Gershenzon, 1984; Mazid et al., 2011). Secondary metabolites are either produced to protect against bacteria

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and insects (phytoalexins) or they are preserved in inactive forms (phytoanticipins) (Zaynab et al., 2018). Phytochemicals, such as alkaloids, flavonoids, and phenolics, possess antiviral/antifungal characteristics that are functional during various biotic stress (Crozier et al., 2008; Koga et al., 1995). Likewise, TEs also have critical roles during stress conditions and are essential for the proper functioning of many enzymes. They are used to enhance the resistive power of the plants against abiotic and biotic stress. 1.3 HOW DO TRACE ELEMENTS (TES) INTERACT WITH THE PLANTS? TEs are required by the plants in lower concentrations, however, they are substantial in plant functioning. Furthermore, element deficits or toxicities have a significant impact on the plant life cycle by generating a variety of symptoms, including plant mortality (Marschner, 2011). Figure 1.1 and Table 1.1 summarize the importance and interaction of TEs in the plants. Zinc (Zn) is one of the crucial TE that has a catalytic function in many enzymes such as tryptophan synthetase, aldolases, isomerases, transphosphorylases, SOD, etc. (Broadley et al., 2007) and is responsible for maintaining the structural integrity of many proteins including Zn finger, Zn cluster, and RING finger domains/motifs (Fox & Guerinot, 1998). The uptake and homeostasis of Zn are maintained by the zinc-regulated, iron-regulated transporter-like proteins (ZIP) transporters (Guerinot, 2000). Seven ZIP families of genes including iron-regulated transporter (IRT1-3) and ZIP1-4 have been characterized in Arabidopsis thaliana (Grotz et al., 1998). These genes have different affinities toward the uptake of Zn. Deficiency of Zn causes chlorosis, necrotic spots and also reduces plant growth (Sadeghzadeh & Rengel, 2011). A recent study showed the application of zinc oxide nanoparticles (ZnO-NPs) to reduce the cadmium (Cd) toxicity in tomato plants (Faizan et al., 2021). ZnO-NPs enhanced plant growth by supplying the Zn2+ ions, improving the photosynthesis process, reducing oxidative stress, and increasing the ROS scavenging activity (Faizan et al., 2021). Iron has a unique role in the behavior of numerous TEs and occupies a middle ground between macro and micronutrients in plants (Kabata-Pendias & Szteke, 2015). Chlorophyll formation is strongly influenced by Fe as it is concentrated in the chloroplasts and occurs in the heme and non-heme proteins. Fe containing proteins (siderophores, ferritins) are involved in the transport/storage/binder systems and have a catalytic role in metabolic/enzymatic processes. Fe insufficiency induces abnormalities such as interveinal chlorosis in plant leaves and lowers agricultural yield (LópezMillán et al., 2013). Fe deficiency inevitably results in chlorophyll loss and

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chloroplast degeneration (Mondal & Bose, 2019). Fe also interacts with other elements such as TEs such as Zn/S/Se which can affect its deficiency (Loneragan & Webb, 1993). Cobalt (Co) and nickel (Ni) are TEs with properties similar to Fe. Manganese, copper, and nickel are usually absorbed by the plants in a +2-oxidation state, i.e., Mg2+, Cu2+, and Ni2+. These three TEs play an important structural role in many enzymes and are involved in physiological functions as listed in Table 1.1. Mn deficiency in plants causes chlorosis, tissue necrosis and hinders the growth of plants (Socha & Guerinot, 2014; Yin et al., 2014) whereas Cu deficiency affects the younger leaves and reproductive organs (Marschner, 2011). Necrotic lesions in leaves and accumulation of urea are caused due to Ni deficiency (Polacco et al., 2013). Interaction of Cu with other TEs (Cu–Zn, Cu–Mn, Cu–Fe) can have serious consequences in plants (Yruela, 2009). Ni toxicity is mainly due to its interaction with Fe (KabataPendias & Szteke, 2015) and reduces plant growth by inducing oxidative stress and inhibiting certain metabolism/enzymatic activities (Gajewska et al., 2009; Molas, 2002). Co is not a necessary element, although as heavy metal and a micronutrient, it has been reported to be beneficial and harmful to plants (Akeel & Jahan, 2020; Minz et al., 2018). Lower Co concentrations promote greater nodulation and growth in legumes, whereas higher Co concentrations cause leaf chlorosis, root nodule suppression, and ultimately reduce plant yield (Moreno‐Caselles et al., 1997). Like other TEs, Co also interacts with metals such as calcium, Fe, Cu, Zn, and cadmium (Lison & Lauwerys, 1995; Lwalaba et al., 2019). Boron (B) can induce the movement of sugars and other compounds, particularly those involved in bio complexing membrane bindings. Thus, an adequate supply of B to is required for sugar synthesis in plants such as sugar beets (Kabata-Pendias & Szteke, 2015). Most mycorrhizal plants require adequate B supply for nodule formation and activity of nitrogenase enzyme, hence, the deficiency of B affects major crops such as legumes, sunflower, sugar beets, etc. (Archana & Pandey, 2021; Granado-Rodríguez et al., 2020). B also can interact with other elements (Ca, P, Zn, K) to bring out some antagonistic/synergistic effects in plants. Molybdenum is an important TE in the aspect that it is required for nitrogen fixation and assimilation of metabolites in nodulated legumes (Bambara & Ndakidemi, 2010). Mo functions as a redox carrier and is also involved in the enzymatic activities of RNA and DNA (Zimmer & Mendel, 1999). Mo deficiency symptoms are similar to nitrogen deficiency in that older leaves become chlorotic (Das et al., 2017). Broyer and co-authors established the fundamental role of chlorine as a micronutrient in plants in 1954 (Broyer et al., 1954). Cl deprivation is uncommon under normal environmental conditions since soil chlorine concentrations are

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often high and plants only require minimal quantities (White & Broadley, 2001). Rather the plants such as cereals, vegetables, and fruit crops can be vulnerable to Cl– toxicity due to its higher concentration in the soil. Cl promotes growth in plants, such as celery, cabbage, spinach, and fodder beet, as it is involved in photosynthesis and transpiration. Cl deficiency can result in a decrease in photosynthetic efficiency (Terry, 1977), wilting of plants, stunted roots, and reduced fruit size (Vatansever et al., 2017). Silicon (Si) and Selenium (Se) are the non-metals that belongs to group 14 and 16 of the periodic table, respectively (Kabata-Pendias & Szteke, 2015). Accumulation of Si in gramineous and cyperaceous plants can exert beneficial effects (Epstein, 1999; Liang et al., 2005) under stressful conditions (Li et al., 2009). A recent study has shown the potential of Si in increasing the biomass production in bast fiberproducing plants (Luyckx et al., 2017). They further hypothesized that Si has an influence on bast fiber development by acting on endogenous phytohormone levels and playing a mechanical function in resistance to turgor pressure during elongation. On the other hand, excess of Si can compete with the uptake of other required nutrients, and its deficiency can affect the leaves, roots, and stems along with the increase in disease susceptibility (Wiese et al., 2007). Se can boost the activity of antioxidant enzymes and metabolites (Schiavon et al., 2017) and is incorporated into the plant structure through various metabolites (Fordyce, 2013). Selenomethionine (SeMeth), which predominates in cereal grains and legume seeds, and Se-methyloselenocysteine (SeMSC), which predominates in vegetables, are the most common Se forms in plants. SeMSC, the most potent anticarcinogenic Se molecule, is found mostly in garlic, broccoli, and brussels sprouts (Meharg, 2011). Excess of selenite and selenite can be toxic to the plants as they interfere with cellular biochemical reactions. At low pH levels, trivalent aluminum (Al3+) is the most prevalent and has the largest influence on plant development (Bojórquez-Quintal et al., 2017). Al promotes the development and biomass accumulation of phytoplankton, primarily diatoms in marine environments (Zhou et al., 2016). Apart from the beneficial roles, Al toxicity has a major impact on plant growth. For example, in Solanaceae plants, Al can severely affect cell division, damage cell structure, impair nutrition and water absorption, and impede root elongation development (He et al., 2019). Plants from industrialized areas may have high levels of Vanadium (V) (Kabata-Pendias & Szteke, 2015). V at low levels is essential in many physiological processes (sucrose synthesis) in plants such as pepper, sugar beet, and sunflower (Table 1.1) (Aihemaiti et al., 2020). However, high levels of V can disrupt the energy metabolism by inhibiting the key enzymes and lead to V toxicity in plants (Cantley et al., 1977; Rehder, 1999). This can

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cause growth retardation, abnormalities of roots and shoots, chlorosis, dwarfing, and eventually death of the plants. Vanadium is a well-known inhibitor of Na+/K+ ATPase, which hydrolyzes effectively at the ATP site. It also significantly reduces the activity of the plasma membrane hydrogentranslocation ATPase, which aids in nutrient absorption by cells in plants (Vara & Serrano, 1982). It also reduces the activity of different transporters such as divalent cation transporter, zinc-iron permease (ZnIP), and drug metabolite transporter (DMT) (Lin et al., 2013). These interactions of TEs with plants suggest that TEs are important towards plant lifecycle. Further, these interactions are finally going to help the plants to respond during the stressful environments. The effect of TEs in increasing plant tolerance to abiotic/biotic stressors is complex. In this chapter, we have focused mainly on the elements such as zinc, iron, copper, aluminum, manganese, molybdenum, chloride, boron, nickel, vanadium, silicon, and cobalt, with an emphasis on the role of those elements in the stress (abiotic and biotic) conditions.

FIGURE 1.1 Application of trace elements (TEs) to mitigate the environmental (abiotic and biotic) stress in plant systems. Abbreviations: Al: Aluminum; APX: Ascorbate peroxidase; As: Arsenic; B: Boron; CAT: Catalase; Cd: Cadmium; Cl: Chlorine; Co: Cobalt; Cu: Copper; Fe: Iron; GPX: Glutathione peroxidase; GR: Glutathione reductase; Hg: Mercury; Mn: Manganese; Mo: Molybdenum; Ni: Nickel; NUE: Nitrogen use efficiency; Pb: Lead; RNS: Reactive nitrogen species; ROS: Reactive oxygen species; RSS: Reactive sulfur species; SAR: Systemic acquired resistance; Se: Selenium; Si: Silicon; TE: Trace elements; UV: Ultraviolet; V: Vanadium; WUE: Water use efficiency; Zn: Zinc. Source: Arif et al. (2016); Kul et al. (2020); Mishra et al. (2018); Paramo et al. (2020).

List of Trace Elements (TEs) and Their Functions in Plants

Trace Elements State of (TEs) Availability Zinc (Zn)

TE Uptake Mechanisms

Involvement and Interaction with Proteins/Enzymes

IRT, ZIP, Hydrogenase, carbonic Zn2+, Hydrated Zn HMA2/HMA4 anhydrase, Cu/Zn SOD, alcohol dehydrogenases, proteinases, peptidases, phosphohydrolases, stromal processing peptidase, peptide deformylase, a-mannosidase, matrix metalloproteinase, Zn cluster, Zn finger, RING finger domains/ motifs, and others 2+ Manganese (Mn) Mn NRAMP, ZIP, Mn-SOD, arginase, allantoate YSL, CAX, phosphotransferase, malic CCX, P-type enzyme, PEP-carboxykinase, ATPases, VIT, amidohydrolase, isocitrate lyase, CDF/MTP PEP carboxylase, hexokinase, glucokinase, dehydrogenases, transferases, hydroxylases, and others Iron (Fe) Fe2+, Fe3+, Fe ZIP, ZRT, CAT, non-specific peroxidases, chelates NRAMP, OPTs APX, Fe-SOD, aconitase, succinate dehydrogenase, NADH-Q oxidoreductase, thioredoxin reductase, nitrite reductase, cytochrome P450, Leg hemoglobin, lipoxygenase, alternative oxidase, ferritin

Important Physiological Functions

Literatures

Stabilization of ribosomal fractions, proteosynthesis, synthesis of cytochrome, seed development, integrity of biomembranes, proliferation, and differentiation of cells

Antoniadis et al. (2017); Chakmak (2000); Hussain et al. (2004); Kabata-Pendias & Szteke (2015); Maidment et al. (1999); Palmer & Guerinot (2009); Richter & Lamppa (2003); Serero et al. (2001); Tisdale & Nelson (1966)

Formation of multi-protein pigment complex embedded in the thylakoid membranes, reconstructs oxygen evolution rates in photo-activation, NO2˗ reduction process

Bowler et al. (1994); Graham & Habibi (2014); Kabata-Pendias & Szteke (2015); Marschner (2011); Socha & Guerinot (2014); Werner et al. (2008)

Root cell wall lignification, maintenance of period length of circadian rhythm, enhancement of photosynthetic pigment accumulation

Chen et al. (2013); Dai et al. (2007); Habibi (2014); Hänsch & Mendel (2009); Harrison & Arosio (1996); Kabata-Pendias & Szteke (2015); Lee et al. (2007); Marschner (2011)

Trace Elements in Mitigating Environmental Stress: An Overview

TABLE 1.1

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(Continued)

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TABLE 1.1

TE Uptake Mechanisms

Involvement and Interaction with Proteins/Enzymes

Copper (Cu)

Cu2+

COPT, CTR

Cu/Zn–SOD, plastocyanin, phenol oxidase, Cumetallothionein, ascorbate oxidase

Boron (B)

H3BO3

Molybdenum (Mo)

MoO42˗

Chlorine (Cl)

Cl–, NaCl

Important Physiological Functions

Lignin synthesis, accumulation of free amino acids and proline, stimulates ethylene biosynthesis, water permeability, protein metabolism MIP proteins, Rhamnogalacturonan II Photosynthesis, carbohydrate, BOR and nitrogen metabolism, transporters, ascorbate/glutathione system, passive auxin transit, cellular signaling, diffusion structural integrity of the plasma membrane MOT1/2, Nitrogenase, xanthine NO3 reduction, chlorophyll SHST1 dehydrogenase/oxidase, aldehyde biosynthesis, conversion oxidase, sulfite oxidase, nitrate of inorganic phosphorus reductase, mitochondrial into organic forms, ureide amidoxime reductase component biosynthesis Cytochrome oxidase, Stomatal regulation, SLAC1, photosynthetic O2 evolution, ALMT, anion/ phosphorylase, asparagine H+ antiporters, synthetase, vacuolar protonseismonastic movement, proton pumping ATPase ABC pump and enzyme activity transporter, regulation, cell elongation, CLC anion regulates photosynthetic channels, CCC, electron transport VDAC,

Literatures Al-Hakimi & Hamada (2011); Antoniadis et al. (2017); Arteca & Arteca (2007); Jansson et al. (2003); Kabata-Pendias & Szteke (2015) González-Fontes et al. (2008); Habibi (2014); Kabata-Pendias & Szteke (2015); Kohorn (2000); Ruuhola et al. (2011a); Ryden et al. (2003) Fitzpatrick et al. (2008); Habibi (2014); Kannan & Ramani (1978); Mendel (2009); Mendel & Hänsch (2002); Sun et al. (2006) Churchill & Sze (1984); Franco-Navarro et al. (2016); Herdean et al. (2016); Marschner (2011); Meharg & Kabata-Pendias (2011); Moran (2007); Rognes (1980); Teakle & Tyerman (2010); Wege et al. (2017)

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Trace Elements State of (TEs) Availability

(Continued)

Trace Elements State of (TEs) Availability

TE Uptake Mechanisms

Involvement and Interaction with Proteins/Enzymes

Important Physiological Functions

Literatures

Nickel (Ni)

Ni2+

ZIP, nonselective transporters, permeases, YSLs

Urease, Ni-chaperone, glyoxalases (family I), methylCoM reductase, SOD, peptide deformylases

Lipid composition, ureolysis, methane biogenesis, acitogenesis, maintenance of optimum nitrogen use efficiency, H-ATPase activity

Silicon (Si)

Si(OH)4

Lsi1/2 (NIPs)

Improvement of canopy photosynthesis, reduction of transpiration loss, strengthening of plant tissues

Selenium (Se)

SeO42−, SeO3− SULTR1;1, SULTR1;2, amino acid permeases

Chitinase, peroxidases, polyphenoloxidases, β-1,3glucanase, phenylalanine ammonia-lyase, superoxide dismutase, APX, glutathione reductase, CAT, lipoxygenase, glucanase Glutathione peroxidase/ reductase, dismutase, SOD, MDHAR, DHAR, CAT

Bai et al. (2006); Fabiano et al. (2015); Freyermuth et al. (2000); Habibi (2014); Maier et al. (1993); Nagajyoti et al. (2010); Nishida et al. (2011, 2015); Yusuf et al. (2011) Habibi (2014); Kabata-Pendias & Szteke (2015); Ma et al. (2006); Mitani et al. (2008); Wang et al. (2017a)

Cobalt (Co)

Co2+

IRT1, NiCoT

Methionyl aminopeptidase

De Kok et al. (1993); Guignardi & Schiavon (2017); Habibi (2014); Hasanuzzaman et al. (2012); Hawkesford et al. (1993); Kabata-Pendias & Szteke (2015); Lass & UllrichEberius (1984); Pilon-Smits (2015) DalCorso et al. (2014); Howden & Preston (2009); Komeda et al. (1997); Minz et al. (2018); Morrissey et al. (2009); Talukder & Sharma (2016); Watanabe et al. (1994)

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Prolidase, nitrile hydratase, glucose isomerase, aldehyde decarbonylase, urease, bromoperoxidase, cobalt– porphyrin-containing proteins, CAT, ATPase, ACC oxidase, calmodulin

Antioxidant and ROS regulation, heavy metal uptake and transport inhibition, sulfur metabolism, construction of chloroplast components and cell membrane, generation of SeCys SeMet, synthesis of glucosinolates Regulation of plant water utilization, Reduction of transpiration rate, enhancement of growth, yield, and nutrient levels, enhances photosynthesis, nitrogen fixation, formation of leghemoglobin

Trace Elements in Mitigating Environmental Stress: An Overview

TABLE 1.1

(Continued)

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TABLE 1.1

TE Uptake Mechanisms

Involvement and Interaction with Proteins/Enzymes

Aluminum (Al)

Al3+

NRAT1, NIP1;2 Actin filaments, microtubules

Vanadium (V)

VO2+, V3–, V5+, HV42˗

NRAMP

Important Physiological Functions

Promotes plant growth in acidic soil, increases P and B uptake efficiency, alleviates H+ toxicity, stimulates the PGPRs, increased antioxidant enzyme activity in tea plants Elevation of plant height, Nitrogenase, phosphorylases, root length, and biomass mutases, phosphatases, ribonucleases, nitrate reductase, production, enhanced glutamic–pyruvic transaminases, chlorophyll biosynthesis, seed germination, essential element invertase, sucrose invertase, uptake, nitrogen assimilation haloperoxidase and utilization, stimulation of flowering in pepper plant

Literatures Ghanati et al. (2005); Hajiboland (2012); Muhammad et al. (2019); Poschenrieder et al. (2019); Wang et al. (2017c); Xia et al. (2011); Zhang et al. (2007) García-Jiménez et al. (2018); Kabata-Pendias & Szteke (2015); Singh & Wort (1969); Ueki et al. (2011)

Abbreviations: ABC: ATP-binding cassette; ACC: 1-aminocyclopropane-1-carboxylic acid; ALMT: Aluminum activated malate channels; APX: Ascorbate peroxidase; CAX: Cation exchanger; CCC: Cation-coupled Cl−; CCX: Cation calcium exchanger; CDF: Cation diffusion facilitator; COPT: Copper transporter protein; CTR: Copper transporter; DHAR: Dehydroascorbate reductase; IRT: Iron-regulated transporter; HMA: Heavy metal ATPase; MDHAR: Monodehydroascorbate reductase; MIP: Major intrinsic protein; MOT1: Molybdate transporter 1; MTP: Metal tolerance protein; NiCoT: Nickel/cobalt transporters; NIP: Nodulin 26-like intrinsic proteins; NRAMP: Natural resistance-associated macrophage protein; NRAT1: NRAMP aluminum transporter 1; OPTs: Oligo peptide transporters; PGPRs: Plants growth promoting rhizobacteria; SeCys: Selenocysteine; SeMet: Selenomethionine; SHST1: Stylosanthes hamata sulfate transporter; SLAC1: Slow anion channel associated protein 1; SOD: Superoxide dismutase; SULTR: Sulfate/selenate cotransporter; VDAC: Voltage-dependent anion channels; VIT: Vacuolar iron transporter; YSL: Yellow stripe 1-like; ZIP: Zinc-regulated, iron-regulated transporter-like proteins.

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1.4 IMPORTANCE OF TRACE ELEMENTS (TES) IN MITIGATING ENVIRONMENTAL STRESS TE’s importance in higher plants has traditionally been determined by physiological and metabolic roles, as well as deficient symptoms. They are involved in a variety of complex cellular processes. Extreme climatic conditions, such as heat, cold, salinity, heavy metal toxicity, drought, and floods may have a disastrous effect on plant growth and production, potentially leading to the collapse of entire ecosystems (Zandalinas et al., 2020) (Figure 1.1). TEs have been seen to effectively reduce the biotic stress caused by pathogens (bacteria, fungi) and herbivores (insects, pests, aphids). The TEs respond differently to enhance the resistance of the plants to different biotic stressors. Plants respond to these stresses through a variety of multifaceted biochemical and molecular mechanisms (Pardo-Hernández et al., 2020). TEs not only boost plant physiological processes and development but also help plants cope with stress (Hasanuzzaman et al., 2017). 1.4.1 ZINC 1.4.1.1 ABIOTIC STRESS Zn appears to be important in the maintenance of the gene expression necessary for plant stress tolerance (Habibi, 2014). The Cu/Zn-SOD is an important enzyme that catalyzes ROS scavenging in plants. Several studies have documented the importance of Cu/Zn-SOD in increasing resistance to oxidative stress in plants such as tobacco (Gupta et al., 1993) and Arabidopsis (Li et al., 2017). Zn increases plant tolerance to dry and hot conditions by influencing protein, chlorophyll, and abscisic acid (ABA) levels (Zengin, 2006). Due to the important functioning in plant physiology (Table 1.2), scientists have developed ZnO-NPs that can alter RNS homeostasis, protein carbonylation, nitration, and modulate different enzymes and non-enzymatic antioxidants (Molnár et al., 2020). Application of ZnO-NPs at a low level promotes seed germination and overall plant growth (Sabir et al., 2014). According to a recent study, ZnO-NPs is an ideal eco-friendly and low-cost application for plant development under salinity, with the capacity to mitigate the salt stress impact of plants (Alabdallah & Alzahrani, 2020). The vascular plant one zinc-finger (VOZ) has been shown to have a role in abiotic stress signaling pathways Arabidopsis (Mitsuda et al., 2004) and rice (Ganie et al., 2019). Cys2His2-type

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Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 2

zinc finger proteins (C2H2-ZFPs) are well-known ZFPs that have a role in plant development, growth, and stress responses (Kiełbowicz-Matuk, 2012) in plants such as cucumber (Chen et al., 2020; Yin et al., 2020) and tomato (Ming et al., 2020). TaZnF is a C3HC4 (Cys3HisCys4) type RING ZFP that has been demonstrated to serve as a positive regulator of stress response and can be utilized as a candidate gene to improve and enhance dehydration and salinity stress tolerance in wheat and other agricultural plants (Agarwal & Khurana, 2020). 1.4.1.2 BIOTIC STRESS Zn has a key role in the response of plants to pests and diseases. Zn is closely linked to two broad-spectrum reactions involved in plant-pest/ pathogen interactions: oxidant stress and Zn finger protein modulation. It influences plant-pathogen interactions through its critical involvement in the activation/stabilization of metalloenzymes (like SOD) involved in oxidative stress mitigation (Fones & Preston, 2012). NBS-LRRs (nucleotide-binding sites-leucine rich) proteins, which are involved in the effector-triggered immune response, contain zinc finger binding domains (Gupta et al., 2012). Recently, eight C2H2-ZFP genes were discovered in response to pathogen stressors in the tomato plants. With the help of KEGG analysis, the authors concluded that genes in the C2H2-ZFP family mostly regulate stress via sphingolipid metabolism, glycosphingolipid biosynthesis, galactose metabolism, glycosaminoglycan degradation, and endocytosis pathways (Zhao et al., 2020). The high Zn accumulation in plant tissues is more harmful to the pest/pathogen than to the plant, implying that direct elemental defense by Zn is more hazardous to the pest/pathogen than to the plant. High Zn leaf concentrations may assist in protection through stimulating defensive signaling pathways and enhancing structural defenses, in addition to their possible direct toxic effect in defense (Balafrej et al., 2020; Gallego et al., 2017; Poschenrieder et al., 2006). The plant response to hazardous Zn concentrations is thought to be aided by NO. NO has recently been discovered in Solanum nigrum to have a role in the production of numerous Zn-mediated miRNA, with the anticipated target genes showing that too much Zn affects pathogen resistance and the transcriptional process via miRNA pathways (Xie et al., 2017). Table 1.2 provides evidence of some of the functions of Zn in mitigating plant defenses.

Importance of Trace Elements (TEs) in Mitigating Environmental Stresses

Trace Elements (TEs)

Role in Abiotic Stress

Zn

Maintain the balance of ROS production and scavenging in plants

References

Marschner (2011); Millaleo et al. (2013) Modulates the protection of DNA from CdWong & Cobbett induced damage (2009) Elevates tolerance to heavy metal toxicity like Badawi et al. cadmium, salt stress, and water stress (2004); Gill & Tuteja (2010); Rizwan et al. (2019b) Suppresses the bioaccumulation of Cd by reducing Han et al. (2010) its uptake Increases yields under water stress in droughtWaraich et al. resistant genotypes (2011b) Stomata regulation and ion balance to reduce the Babaeian et al. tensions of drought (2010) Enhances auxin levels and improves drought Bennett & Skoog tolerance (1938); Waraich et al. (2011b) Maintains integrity of membranes by interacting Claus et al. (2013); with sulfhydryl groups of membrane proteins and Habibi (2014) with membrane-bound NADPH oxidase activity

Role in Biotic Stress

References

Decreases attack by root pathogens of tomato, including Fusarium solani, Rhizoctonia solani, and Macrophoma phaseoli Decreases Rhizoctonia root rots of wheat, cowpea, and Medicago Increase activity of Cu/Zn-SOD in herbivore/ pathogen-challenged plants

Duffy (2007)

Genes with the Zn-finger domain confers durable resistance against the fungus Magnaporthe oryzae. Zn hyperaccumulation is essential for Noccaea caerulescens resistance to A. brassicicola infection Enhances the JA-ET-dependent defense signaling pathway Enhances the toxicity to insects of other metals (Cd, Ni, or Pb)

Gupta et al. (2012)

RAR1, a zinc-binding protein of wheat, confers resistance against the stripe rust pathogen through SA-mediated oxidative burst and hypersensitive response

Wang et al. (2017b)

Kalim et al. (2003) Deepak et al. (2006); Fodor et al. (1997)

Gallego et al. (2017) Thomma et al. (1999) Jhee et al. (2006)

Trace Elements in Mitigating Environmental Stress: An Overview

TABLE 1.2

17

Trace Elements (TEs)

Role in Abiotic Stress

References

Role in Biotic Stress

References

Prevents the photo-inhibitory damage to photosynthetic apparatus during exposure of plants to high light conditions Modifies the capacity for water uptake and transport that enhances tolerance to salt stress Increases the activity of MnSOD isozyme during salt stress in Lycopersicon esculentum and Cicer arietinum Overexpression of MnSOD in plants have less oxidative damage under photooxidative stress

Munekage et al. (2002); Takahashi et al. (2009) Disante et al. (2011) Gapińska et al. (2008)

–

–

–

–

The foliar application increases the resistance to orange rot caused by Puccinia kuehnii in sugarcane plants Controls pathogenic diseases such as downy mildew, take-all, and tan spot

Mesquitaa et al. (2019)

Mn fertilization reduces Cd uptake and leads to amelioration of Cd-induced root growth inhibition in maize seedlings Protects photosynthetic apparatus under drought stress Reduces generation of ROS by increasing the antioxidant capacity of the plant

Paľove-Balang et al. (2006)

Reduces the adverse effects of temperature stress indirectly by enhancing the photosynthetic rate and nitrogen metabolism in plants.

Melchiorre et al. (2009)

Inhibits the action of fungal enzymes, aminopeptidase, and pectin methylesterase, essential for fungal growth Wang et al. (2004) High leaf Mn concentration induces protective mechanisms against powdery mildew in grapevines Peng et al. (2008) Strengthens the defensive structures of the plant and help to prevent the disease caused by Podosphaera fuliginea and Colletotrichum lagenarium in cucumber Aktas et al. (2005); Ameliorates Alfalfa mosaic virus infection by Aloni et al. (2008) improving the antioxidant system and phenol content of pepper

Heckman et al. (2003); Simoglou & Dordas (2006) Habibi (2014)

Yao et al. (2012) Eskandari et al. (2018, 2020)

Hosseini et al. (2021)

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 2

Mn

(Continued)

18

TABLE 1.2

(Continued)

Trace Elements (TEs)

Role in Abiotic Stress

References

Role in Biotic Stress

References

Fe

Alleviates the negative effects of Cd by retaining both quantity and quality of chloroplast An increase in FeSOD and GPX activities enhances Nicotiana tabacum tolerance to drought, high temperature, and high light intensity stresses

Ameliorates salinity stress by producing antioxidative enzymes Fe plaque has an important role in regulating Cd, Cu, and Pb toxicities in rice plants

Nada et al. (2007)

Helps during diseases such as apple canker, blank shank, and wilt in different crops Fe3O4 NPs increase Medicago falcata L. resistance to fungal diseases, such as powdery mildew

Gupta et al. (2017)

Cu

Demirevska et al. (2010)

Scandalios (1990) Siderophores have antifungal effects due to strong Fe-chelating capacity Huang et al. (2009) Fe-shortage alters plant defense responses and confers resistance to Dickeya dadantii and Botrytis

cinerea Foliar application on sunflower under drought Ebrahimian et al. FER1 protects plant cells against the high amounts stress plays an important role in seed and oil (2011) of iron that are released from the cell walls upon

production pathogen infection

Fe + Zn foliar application diminishes oxidative Baghizadeh & Fe2O3/Fe3O4-NPs inhibit the growth of stress by reducing H2O2 content and lessening Shahbazi (2013) fungal pathogens like Trichothecium roseum, lipid peroxidation by enhancing antioxidant Cladosporium herbarum, Penicillium chrysogenum,

enzymes under drought stress Alternaria alternata, and Aspergillus niger

Over-expression of Fe-SOD helps in the reduction McKersie et al. – of secondary injury symptoms and leads to (2000)

enhancement in drought tolerance

Intracellular Cu helps to escape the toxicity caused Brewer (2010) Enhances the activation of peroxidase and laccase by O2▪− and H2O2 for higher levels of lignification in pepper

Kokina et al.

(2020)

Seong & Shin

(1996)

Kieu et al. (2012)

Aznar et al. (2015)

Parveen et al.

(2018)

Trace Elements in Mitigating Environmental Stress: An Overview

TABLE 1.2

–

Dıaz ́ et al. (2001); Passardi et al. (2005) 19

Trace Elements (TEs)

Role in Abiotic Stress

References

Role in Biotic Stress

References

Overproduction of three isoforms of Cu/Zn-SOD enhances tolerance to oxidative stress during drought Improve nitrogen metabolism and increase the build-up of soluble phenolic compounds and lignin to mitigate the negative effects of water stress Upregulation of Cu-Zn SOD improves transgenic tobacco’s tolerance to low temperature and water deficiency Cytosolic Cu-Zn SOD from Oryza sativa enhances tolerance of rice to MV and salt stresses Overexpression of cytosolic Cu-Zn SOD enhances cold-tolerance in Eucalyptus grandis × E. ophylla Cu-microRNAs mediate responses to an array of abiotic stresses Reduces Al toxicity via stimulating GSH accumulation

Faize et al. (2011)

Because excess Cu is harmful to pathogens, its accumulation in plants may inhibit pathogen infection Because excess Cu increases ethylene production, plant defense reactions generated by copper may also be controlled by ethylene.

Maksymiec (2007)

Increases Zea mays’s ability to produce volatile chemical compounds in the presence of insect attacks. Cytosolic Cu/Zn-SOD enhances resistance against P. syringae pv. tabaci. Reduces the growth of saprotrophic fungi and the production of extracellular enzymes –

Winter et al. (2012)

High B supply increases antioxidative enzyme (SOD) activities in tomato, citrus, and chickpea

Waraich et al. (2011a, b)

Faize et al. (2011)

Prashanth et al. (2008) Zhao et al. (2018) Pilon (2017) Ruiz et al. (2006)

Controls or reduces the severity of tobacco mosaic virus in bean, and tomato yellow leaf curl virus in tomato Ardıc et al. (2009); Reduces biotic stress-induced by Fusarium solani Han et al. (2009); in soybeans, Verticillium alboatrum in tomato and Kaya et al. (2009); cotton, and Blumeria graminis in wheat Tombuloglu et al. (2012)

Arteca & Arteca (2007)

Faize et al. (2012) Hartikainen et al. (2012) – Graham & Webb (1991) Marschner (1995)

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 2

B

(Continued)

20

TABLE 1.2

Trace Elements (TEs)

Mo

(Continued) Role in Abiotic Stress

References

Role in Biotic Stress

Deficiency of B activates an antioxidant system in Camellia sinensis plants to alleviate stress induced by high light B lessens the stress markers such as proline and H2O2 and improves the plant pigment content through foliar application under water-deficit conditions Reduces the production of ROS species and enhances the photosynthetic rate under low temperatures Increases the tolerance of plants to droughtinduced oxidative damage by enhancing the activities of CAT and POD The combined effect of both Ca and B can mitigate the harmful effects caused by salinity Enhances wheatgrass adaptation to salinity stress due to enhanced activities of xanthine dehydrogenase, nitrate reductase, and aldehyde oxidase Improves the drought tolerance of wheat by enhancing water utilization capability and the abilities of antioxidative defense and osmotic adjustment

B in combination with Ca, has a positive role in establishing rhizobial symbiosis in Pisum sativum under saline conditions Abdel-Motagally & B and Fe have multifunctional roles in reducing the severity of diseases by affecting the growth of F. El-Zohri (2018) oxysporum and the responses between plants and pathogens. Pennycooke et al. Boric acid can control the Eutypa dieback of (2005); Waraich et grapevines al. (2012) Karim et al. (2012) Plays a role in defense against herbivorous animals as B modulates the phenolic metabolism of plants

El‐Hamdaoui et al. (2003)

Yermiyahu et al. (2008) Babenko et al. (2015)

–

–

Mo-requiring enzyme AO is essential for the production of the ABA, which is involved in biotic stress responses

Mendel (2009)

Wu et al. (2014)

XDH is very likely to produce superoxide radicals and is involved in host‐pathogen relationships between phytopathogenic fungi like Uromyces or Puccinia

Montalbini (1992b)

Hajiboland et al. (2013, 2015)

References

Dong et al. (2016)

Rolshausen & Gubler (2005) Ruuhola et al. (2011b)

Trace Elements in Mitigating Environmental Stress: An Overview

TABLE 1.2

21

Trace Elements (TEs)

Ni

Role in Abiotic Stress

References

Role in Biotic Stress

Improves the cold resistance of winter wheat due to an increase in the activities of Mocontaining enzymes, antioxidative enzymes, nitrogen-containing compounds, and chlorophyll biosynthesis Improves water uptake via extensive root morphology, increased ionic concentrations, and aquaporin expressions under drought stress Role in enhancing soybean heat stress tolerance when applied on seeds as a biostimulant Involved in stomatal regulation of coconut plant during the dry season and help plants in counteracting the negative effects of drought stress by maintaining a relatively high level of leaf gas exchanges Chlorinated phenols such as caffeoylquinic/ chlorogenic acids, having an antioxidant role, are accumulates in postharvest stress conditions Alleviate salinity stress by suppression of nitrification and increase the availability of Mn leading to host resistance to diseases in grain crops Activator of Glyoxalase I and may play an important role in antioxidant metabolism

Imran et al. (2020); Multifunctional MoS2-CuNPs enhances the Sun et al. (2009); antibacterial activity, promotes rice growth, and Wang et al. (1999) induces rice resistance

Li et al. (2020)

Wu et al. (2019)

–

–

Campobenedetto et – al. (2020) Hajiboland (2012) Alleviate biotic stresses and is involved in the protection of corn plants from stalk rot, wheat from stripe rust, take-all, and septoria

References

– Graham & Webb (1991); Mann et al. (2004)

Jacobo-Velázquez et al. (2011)

Sesquiterpenoids are Cl-containing compounds that Weissenborn et al. have the role of disease resistance in plants (1995)

Huber & Huber (1996)

Higher concentrations of Cl in plant tissues can also – enhance water retention and turgor when roots are attacked by pathogens Have potential to increase the basal level of Einhardt et al. soybean resistance to ASR, caused by the fungus (2020) Phakopsora pachyrhizi

Fabiano et al. (2015)

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 2

Cl

(Continued)

22

TABLE 1.2

Trace Elements (TEs)

Si

(Continued) Role in Abiotic Stress

References

Mediates the formation of precursors for the biosynthesis of polyamines that are ROS scavengers Beneficial for wheat plant growth by alleviating salinity stress by modulating the concentration of Na+ and K+ Role in osmotic adjustment and protection of Stackhousia tryoni plants against drought Maintains the cellular redox state, stress tolerance/ defense, and optimum NUE Improves the water use efficiency and stimulates the antioxidative defense system during drought stress Effectively protects O. sativa, T. aestivum, Z. mays, and B. napus from salt-induced oxidative stress by enhancing Na+1 exclusion and inhibiting the peroxidation of membrane lipids through stimulation of antioxidants Reduces stress induced by UV radiation in soybeans and wheat

Alcázar et al. Hyper-accumulation defends the Streptanthus (2010); Polacco et polygaloides against plant bacterial pathogens al. (2013) Ain et al. (2016) –

–

Bhatia et al. (2005) –

–

Fabiano et al. (2015) Cooke & Leishman (2011); Liang et al. (2007) Hasanuzzaman & Fujita (2011); Lekklar & Chaidee (2011); Tahir et al. (2012) Shen et al. (2010); Yao et al. (2011)

–

–

Triggers natural defense responses by stimulating the activity of chitinases, peroxidases, and polyphenol oxidases Increases the accumulation of fungi-toxic phenolic compounds and silica depositions at the site of infection and the formation of papillae and deposition of callose and H2O2 against powdery mildew of roses Enhances resistance against biotic stresses in rice, wheat, and banana

Dallagnol et al. (2011)

Roy et al. (1988)

Polymerized Si might induce disease resistance by delaying infections via inhibiting fungal germ tube penetration of the epidermis

References

Boyd et al. (1994)

Shetty et al. (2012); Van Bockhaven et al. (2013) Graham & Webb (1991); Kamenidou et al. (2009) Robert-Seilaniantz et al. (2011)

23

Counteracts the negative effects of Al toxicity in most strongly acid soils by decreasing the toxic Al3+ concentration via forming Al-Si complexes

Role in Biotic Stress

Trace Elements in Mitigating Environmental Stress: An Overview

TABLE 1.2

Trace Elements (TEs)

Co

Role in Abiotic Stress

References

Role in Biotic Stress

Reduces the toxicity of high Mn. This decline may be related to an apoplastic activity of PODs and phenols in cowpea, pumpkin, and cucumber Se-pretreated rapeseed seedlings exhibit elevated ascorbate and GSH levels and significantly enhanced APX, CAT, DHAR, GR, GPX, and MDAR activity under drought stress Affects the antioxidant enzyme activities and proline content in plants protects the cell membrane against lipid peroxidation and leads to enhanced tolerance to salt stress Protect plants against damage caused by As, Pb, Cd, Zn, Cu, and Cr

Führs et al. (2009); – Shi et al. (2005)

–

Hasanuzzaman & Fujita (2011)

Tamaoki et al. (2008)

Alleviate pathogen stress by up-regulation of JA and ethylene, sulfate/selenate assimilation, and the production of defense-related proteins

Djanaguiraman et Protects the plants against spider mite feeding due al. (2005); Kong et to toxic effects on spider mites by reducing growth al. (2005) and interfering with reproduction

References

Xu et al. (2021)

Adrees et al. Low concentrations alleviate oxidative stress caused Łukaszewicz et al. (2015); Bhat et al. by aphid feeding on pea leaves (2021b) (2019) Valadabadi et al. – – (2013)

Protect plants from high and low-temperature stresses because of its structural role in the synthesis of GPX enzyme Improves growth and increases the nodulation Habibi (2014) and leghemoglobin concentration along with CAT activity in legume plants that results in stress tolerance Excess Co causes oxidative stress in Phaseolus Tewari et al. (2002) aureus; however, H2O2 generation and lipid peroxidation can be reduced due to enhanced activities of SOD and APX

Improves biotic stress resistance indirectly in medicinal plants by the accumulation of alkaloids

Palit et al. (1994)

Acts as a chelator of SATP and SAP and exerts biocidal activity against the molds Aspergillus nidulans Winter, A. niger Tiegh, and the yeast Candida albicans

Parashar et al. (1987)

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 2

Se

(Continued)

24

TABLE 1.2

Trace Elements (TEs)

Al

V

(Continued) Role in Abiotic Stress

References

Pre-treatment of seeds with cobalt nitrate improves drought tolerance in Aesculus hippocastanum L. Curbs salt stress in wheat, maize, cucumber, and tomato plants through different mechanisms Al-supplementation results in a high CO2 assimilation rate, greater B root-shoot transport, and less oxidative damage under B deficiency stress Increases tolerance to ion toxicity and nutrient deficiency

–

Role in Biotic Stress

High tissue Co2+ levels protect the plant from herbivory or pathogens Akeel & Jahan Antifungal activities with acetone ASH and ESH (2020) against A. niger and A. flavus Hajiboland (2012) Role in resistance to black root rot pathogen (Thielaviopsis basicola) and mycelial growth and sporangial germination of potato late blight pathogen (Phytophthora infestans) Kaur et al. (2016) Reduces herbivory in Lychnophora ericoides by inducing leaf lignification and strengthening sclerophylly Thornton et al. Prevents the effects of H+ toxicity and that of Increases activity of CAT and GPX against different elements when found in excess in wheat, (1986, 1989) Fusarium incarnatum-equiseti in pigeon pea Japanese radish, and pea plants Prevents bronzing of the leaves due to the toxic Hajiboland et al. – effect of Fe and also reduces the Fe content in (2013); Watanabe leaves and roots et al. (2006) Prevents the Mn toxicity in rice by decreasing its Wang et al. (2015); – uptake and also help to detoxify fluoride (F) in tea Yang et al. (2016) plants by forming Al-F compounds V-salts manipulate plant secondary metabolism Grzanka et al. Complexes of oxo-vanadium (III, IV, V) exhibits (2020); Smoleń et bactericidal, antidermatophytic, insect sterilant, and al. (2020) ovicidal properties

References

Pilon-Smits et al.

(2009)

Johari et al. (1987)

Habibi (2014)

Amauri et al.

(2017)

Satapathy et al.

(2012)

–

Trace Elements in Mitigating Environmental Stress: An Overview

TABLE 1.2

–

Datta et al. (1982); Shahzadi et al. (2007) 25

Trace Elements (TEs)

(Continued)

26

TABLE 1.2

References

Role in Biotic Stress

References

V-compounds reduces the effects of stress and to improves the growth of plants under unfavorable conditions Reduces the detrimental effects or prevent accumulation of toxic trace metals (Cu, Hg, and Pb)

Hanus-Fajerska et – al. (2021)

–

Akoumianaki– Ioannidou et al. (2016); Wang et al. (2013)

–

Abbreviations: AO: Aldehyde oxidase; ABA: abscisic acid; ASR: Asian soybean rust; APX: ascorbate peroxidase; ASH: salicyloyl hydrazone; CAT: catalase; DHAR: dehydroascorbate reductase; DNA: deoxyribonucleic acid; ESH: ethyl methyl ketone salicyloyl hydrazone; ET: ethylene; FER1: Ferritin 1; GPX: glutathione peroxidase; GR: glutathione reductase; JA: jasmonic acid; MDAR: monodehydroascorbate reductase; MoS2CuNPs: molybdenum disulfide loaded with copper nanoparticles, MV: methyl viologen; NADPH: nicotinamide adenine dinucleotide phosphate; NUE: nitrogen use efficiency; POD: peroxidase; ROS: reactive oxygen species; SA: salicylic acid; SAP: salicylidine-o-aminopyridine; SATP: salicylidine-o-amino-thiophenol; SOD: superoxide dismutase; XDH: xanthine dehydrogenase/oxidase.

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 2

Role in Abiotic Stress

Trace Elements in Mitigating Environmental Stress: An Overview

27

1.4.2 MANGANESE

1.4.2.1 ABIOTIC STRESS Manganese aids plant abiotic stress tolerance in many ways (Table 1.2). Manganese is a cofactor for several enzymes involved in redox processes which detoxify oxygen free radicals in plants (Wang et al., 2004). The main function of Mn in some enzymes, such as MnSOD, phosphoenol pyruvate carboxy kinase (PEPCK), allantoate amidohydrolase, phosphoenol pyruvate carboxylase (PEP-case), isocitrate dehydrogenase (IDH), NAD+-malic enzyme, enolase, is to neutralize the harmful effects of abiotic stress (Pandey, 2018). These enzymes aid in the accelerated growth of particularly C4 plants when cultivated under drought-stressed circumstances (Chen et al., 2002). MnSOD is an important Mn-containing enzyme that is located in the mitochondrial matrix, peroxisomes, and cell wall (del Río et al., 2003; Kukavica et al., 2009). The use of Mn altered the nutritional status and contributed to ROS detoxification, which helped to ameliorate the detrimental impacts of drought in wheat (Karim et al., 2012), soybean (Vadez et al., 2000), mustard (Khan et al., 2016), and perennial ryegrass (Wang et al., 2010b). Further, Mn has very important roles during temperature (Gao et al., 2009; Waraich et al., 2012) and salt stress (Nadeem et al., 2020; Rahman et al., 2016). Like ZnO-NPs, the manganese (III) oxide nanoparticles (MnNPs) might be thought of as nano modulators for plants exposed to abiotic stressors (Ye et al., 2019). A recent study demonstrated that the MnNPs can be used as a priming agent for C. annuum L. seedlings at low doses which was found to enhance root elongation and reduce salt stress during germination (Ye et al., 2020). 1.4.2.2 BIOTIC STRESS Mn aids in the treatment of a variety of plant root and foliar diseases (Huber & Graham, 1999). The application of Mn is effective during powdery mildew pumpkin, rust of wheat, leaf spot of the areca palm, bacterial blight leaf lesions on rice, wilt of pigeon pea, lentils, and tomato (Huber & Wilhelm, 1988). Lignin and suberin are key biochemical barriers to the entry of fungal pathogens (Agrios, 2005; Vidhyasekaran, 2004). Mn plays an essential role in the production of lignin and suberin by activating numerous enzymes in the shikimic acid and phenylpropanoid pathways (Marschner, 1995). Coffee is a valuable agricultural product; unfortunately, coffee rust disease caused

28

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 2

by Hemileia vastatrix reduces coffee yield. However, with the application of Mn, there was a 52.3% reduction in the severity of coffee rust due to the increase in the lignin concentration (Pérez et al., 2020). Manganese phosphite (MnPhi) also has fungicidal/fungistatic action against fungi such as Fusarium virguliforme, F. tucumaniae, Sclerotinia sclerotiorum, and Macrophomina phaseolina which are causal agents of soil-borne diseases (Carmona et al., 2017). 1.4.3 IRON 1.4.3.1 ABIOTIC STRESS Fe plays critical functions in plant growth, development, and adaptation to significant abiotic stressors such as drought, salt, and heavy metals (Tripathi et al., 2018). Fe is a co-factor or constituent of a large number of antioxidant enzymes, including FeSOD, catalase (CAT), non-specific peroxidase, and APX. FeSOD is found predominantly in chloroplasts (Alscher et al., 2002), with A. thaliana having three FeSOD genes (FSD1, FSD2, and FSD3). During the early stages of chloroplast formation, heteromeric FSD2 and FSD3 act as H2O2 scavengers by shielding chloroplast nucleoids from H2O2 (Myouga et al., 2008). FeSOD is beneficial for plants during Mn deficiency, high temperature, osmotic stress, chilling stress, and oxidative stress (Mishra & Sharma, 2019). The application of Fe facilitates the production of assimilates that enhance the tolerance of plants under drought conditions (Pourgholam et al., 2013) and salinity stress (Ghasemi et al., 2014). 1.4.3.2 BIOTIC STRESS Fe has lately been recognized as a key regulator of plant-pathogen resistance (Brissot et al., 2011). The potential of Fe-NPs in mitigating stress is being experimented on plants and has positive effects. The organometallic chitosan iron-oxide nanoparticles (CH-Fe2O3 NPs) has antifungal activity against Rhizopus oryzae and hence can be used against additional phytopathological diseases (Saqib et al., 2019). The CH-Fe2O3 NPs inhibited microbial (Rhizopus stolonifera) development on the fruit surface, which causes postharvest soft rot disease in peach fruit, resulting in fruit damage and weight loss (Saqib et al., 2020). Several studies have shown that high concentrations

Trace Elements in Mitigating Environmental Stress: An Overview

29

of Fe help in mitigating rust infections in wheat leaf, Colletotrichum musae on banana, and smut on wheat. Foliar applications of Fe have been effective in increasing resistance to Sphaeropsis malorum in apple and pear, and tolerance against Olpidium brassicae in cabbage (Graham & Webb, 1991). Because of the potential of Fe-binding rhizobacteria and fungi as biological control agents, the function of Fe in systems including soil-borne diseases and rhizosphere bacteria has been the focus of significant investigation in recent years. Some of the important mechanisms through which Fe helps in abiotic as well as biotic stress include lignin synthesis (Barber & Ride, 1988), phytoalexin synthesis, enzyme activation, synthesis of antioxidants, and synthesis of siderophores (Graham & Webb, 1991; Swinburne, 1986). According to a recent study, the molecular overlap between Fe deficiency and induced systemic resistance (ISR) is crucial for dicot plants to cope with biotic stressors caused by biological agents such as diseases and insects (Romera et al., 2019). 1.4.4 COPPER 1.4.4.1 ABIOTIC STRESS More than 30 enzymes involved in diverse metabolic processes use Cu as a redox catalyst. In the plant cells, the main Cu proteins are plastocyanin, cytochrome c oxidase, and Cu/Zn SODs (Khan et al., 2018). The Cu/Zn SODs have 3 isoforms, namely cytosolic (CSD1), chloroplastic (CSD2), and peroxisomal (CSD3), in Arabidopsis (Chu et al., 2005). The alleviation of stress by Cu is because Cu (in high concentrations) helps in the activation of some important enzymes such as glucose-6-phosphate dehydrogenase, CAT, shikimate dehydrogenase, laccase, phenylalanine ammonia-lyase, caffeic acid-peroxidase, polyphenol oxidase (PPO), and β-glucosidase (Akgül et al., 2007). The various roles of Cu during abiotic stress are listed in Table 1.2. Like other metal-NPs, CuNPs are in experimentation for their role in abiotic stress tolerance. A recent experiment on wheat plants demonstrated that CuNPs alleviate oxidative stress damage by reducing the bioavailability of toxic element chromium and increasing plant growth (Noman et al., 2020). Cu enhanced the transcriptional expression of biosynthetic genes and antioxidant enzyme-related genes in Haematococcus pluvialis (unicellular alga) under high-light and nitrogen-deficiency conditions but decreased ROS levels (Guo et al., 2021).

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1.4.4.2 BIOTIC STRESS Cu can activate plant defense systems (Maksymiec, 2007). During fungal pathogen stress, Verticillium dahliae Kleb., Cu increases the activity of enzymes such as proline oxidase and genes including a sesquiterpene cyclase gene (CASC1), a β-1,3-glucanase (CABGLU), phenolic compound peroxidase gene (CAPO1), and a pathogenesis-related-1 gene (CABPR1) (Chmielowska et al., 2010). The application of CuNPs along with K₂SiO₃ in tomato plants was found to be effective in decreasing the severity of infection by a plant fungal pathogen C. michiganensis. This was due to the modulation of levels of enzymatic and non-enzymatic compounds that are crucial in the defense of tomato plants (Noman et al., 2020). Many Cu-based antimicrobial compounds are used in foliar disease management caused by plant pathogenic fungi, bacteria, and oomycetes (Lamichhane et al., 2018). Those compounds include copper chloride (CuCl2), copper hydroxide (Cu(OH)2), copper oxide (Cu2O), copper oxychloride sulfate (Cu4(OH)6(SO4)), basic copper sulfate (CuSO43Cu(OH)2), and many more (Lamichhane et al., 2018). These compounds are effective in managing diseases such as citrus canker (Behlau et al., 2017), mango apical necrosis (Cazorla et al., 2002), fire blight of pome fruits (Elkins et al., 2015), walnut blight (Ninot et al., 2002), and olive knot (Teviotdale & Krueger, 2004). 1.4.5 BORON 1.4.5.1 ABIOTIC STRESS The diverse role of B in the structural, biochemical, and physiological functions of plants, makes it an important element that enhances plant growth and development (Ozturk et al., 2010; Ruuhola et al., 2011b). B deficiency causes photooxidative damage in leaf cells, leading to decreased plant chilling tolerance (Lehto et al., 2010). Recent studies comply with the fact that B is required for mitigating the effects of temperature stress, salinity, drought, and heat stress in plants. The addition of B can improve plant drought tolerance by activating early stress response systems (Aydin et al., 2019). When high daytime stress periods are predicted in rice areas, the usage of B compounds like boric acid or sodium borate might be considered as an agronomic approach to minimize the detrimental impact of heat stress (Calderón-Páez et al., 2021). B performs critical roles in promoting plant development under such sodic and salt environments because B controls

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ion fluxes via cell membranes by preserving cell wall integrity. El-Aidy and colleagues found that B, coupled with Mn and Zn, may effectively buffer the negative effects of salinity on pea plant development (El-Aidy et al., 2021). 1.4.5.2 BIOTIC STRESS The role of B in mitigating biotic stress has been accessed in recent years. B increases the concentration of certain chemicals like terpenes and volatile norisoprenoids in olives, which improves olive plant resilience to insects and diseases (Pasković et al., 2019). Boron compounds such as boric acid, disodium octaborate tetrahydrate, disodium tetraborate, and disodium tetraborate decahydrate are effective against Rhizoctonia root and crown rot in winter squash caused by Rhizoctonia solani anastomosis. Such compounds at low concentrations can serve as an alternative to synthetic fungicides to alleviate the impacts of the disease (Erper et al., 2019). As a foliar application, B was shown to be effective in suppressing the plant-fungal disease stem rot caused by Sclerotinia sclerotiorum (Ni & Punja, 2020). Boron had a positive impact on table grapes at room temperature or 0°C in potassium tetraborate to prevent the postharvest gray mold produced by the Botrytis cinerea. The processes by which boron help in the reduction of gray mold decline of table grapes has been hypothesized to be connected to the disruption activity of boron in the fungal pathogens cell membrane that has resulted in cell membrane disintegration and the loss of hyphae cytoplasmic material (Qin et al., 2010). 1.4.6 MOLYBDENUM 1.4.6.1 ABIOTIC STRESS The crucial function of Mo in plant cell metabolism and biology is owing to the essential redox processes in which molybdoenzymes engage (Manuel et al., 2018). The molybdoenzymes such as nitrogenase, xanthine dehydrogenase/oxidase (XDH), aldehyde oxidase, sulfite oxidase (SO), nitrate reductase (NR), and mitochondrial amidoxime reductase (mARC) components are involved in mitigating the abiotic stress conditions. Through the antioxidative enzymes, escalating activities of Mo in plants improve the scavenging ability of species of active oxygen and provide tolerance to chilling stress in the grass, drought stress (DS) in wheat (Rana et al., 2020). The AO enzyme

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participates in the conversion of abscisic aldehyde to ABA. Improved AO activity results in ABA buildup and increased drought tolerance in maize plants (Rana et al., 2020). The molybdenum cofactor sulfurase gene (LOS5) in Arabidopsis encodes the sulfurylated form of a molybdenum cofactor involved in the control of AO activity (Bittner et al., 2001). 1.4.6.2 BIOTIC STRESS The reports stating the role of Mo in biotic stress is limited, however, the mechanism is mainly related to the activity of the molybdoenzymes. XDH appears to have a physiological function in ROS metabolism, and its signaling emerges in plant-pathogen interactions (Montalbini, 1992a). Recently, it has been hypothesized that Arabidopsis XDH1 serves two opposing functions in the metabolism of ROS linked with plant-pathogen interactions. XDH1 acts as an oxidase in leaf epidermal cells, where it, along with other plant NADPH oxidases, produces superoxide, which can be dismutated to H2O2, contributing to disease resistance. Furthermore, XDH1 activity in leaf mesophyll cells generates uric acid in local and systemic tissues, which scavenges H2O2 and hence protects plants from stress-induced oxidative damage (Ma et al., 2016). 1.4.7 CHLORINE 1.4.7.1 ABIOTIC STRESS Cl is an essential anion in several organic molecules found in plants. Cl keeps the charge balance in cells stable. K influx from subsidiary cells and the osmoregulating capability of Cl– keep guard cells in stomata turgid (Khan et al., 2018). It suggests that Cl might have critical roles during the water stress conditions through stomatal regulation. Studies also suggest that Cl interacts with other nutrient ions such as K+, nitrate (NO3−), and phosphoric acid (H2PO4−) (Chen et al., 2010). It had a synergistic effect with K and combine to form KCl (potassium chloride) which is quite effective in reducing the severity of plant diseases and DS (Singh, 2015). The application of chlorocholine chloride to the leaves increases leaf mineral nutrition, antioxidant enzyme activity, and potato tuber production (Wang et al., 2010a).

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1.4.7.2 BIOTIC STRESS Cl has been reported to reduce a variety of diseases in several crops. Such diseases include corn stalk rot, stripe rust on wheat, glume blotch, tan spots, and downy mildew of millet. Cl– can also directly or indirectly inhibit septoral organisms in wheat through its actions in take-all (Christensen et al., 1982). It also aids in the reduction of the severity of illnesses such as stalk rot caused by Gibberella zeae, leaf blight caused by Helminthosporium species in corn, sudden death syndrome in soya bean, and the physiological and physiological disorders of potato (hollow heart and brown center) (Dordas, 2008; Singh, 2015). With increased chloride supply, the quantity of organic acids in plant tissues and released from roots reduces; this action deprives pathogens of an organic substrate (Goos et al., 1987; Heckman, 2016). During storage, compounds such as chlorine oxide ClO2 reduced hydrogen peroxide (H2O2) concentration and the fruit senescence index, including browning and disease signs in the pericarp (Chumyam et al., 2017). 1.4.8 NICKEL 1.4.8.1 ABIOTIC STRESS Ni is an essential ultra-micronutrient that is crucial for urea metabolism because it is part of the active site of the enzyme urease, which catalyzes the hydrolysis of urea to ammonia and bicarbonate (Polacco et al., 2013). Ni easily binds, complexes, and chelates a variety of biologically important chemicals and is found in all biological systems (Brown, 2016). Ni is also an activator of glyoxalase (OsGLY11.2) (Mustafiz et al., 2014), which is activated by a variety of stress factors in rice plants, indicating that Ni may be crucial for the redox equilibrium of cells during oxidative stress (Fabiano et al., 2015). The glyoxylases such as OsGLYII-1 and OsGLYII-2 have important roles during the tolerance of abiotic stress such as salt stress, heavy metal stress, and methylglyoxal (MG) accumulation (Singla-Pareek et al., 2008; Yadav et al., 2007). Ni reduces the amount of MG in plants, protecting them from stressful situations via the action of glyoxalase, as well as participating in the control of the reduced glutathione (GSH) pool. Thus, the significance of Ni may be characterized not only by urease activation but also by stress tolerance modulation (Fabiano et al., 2015).

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1.4.8.2 BIOTIC STRESS A direct phytosanitary impact of Ni on pathogenic agents or a function of nickel on mechanisms to resist plants is linked to Ni involvement in plant disease resistance (Mishra & Kar, 1974). An earlier study has demonstrated that Ni supply to cowpea roots can effectively reduce the leaf fungal infection, however, the exact mechanism remains unknown (Graham & Webb, 1991). Nickel is also a necessary component of hydrogenases, which are involved in nitrogen fixation and other associative bacterial activities, and nickel impacts plant disease response (Brown, 2016). 1.4.9 SILICON 1.4.9.1 ABIOTIC STRESS Si is a common mineral component of plants that is essential for plant growth and development (Kabata-Pendias & Szteke, 2015). Studies have shown that Si mitigates several stress factors and helps in increasing the tolerance of the plants. Silicon improves treated plants’ ability to detoxify ROS via regulating antioxidant defense systems and the expression of critical genes involved in oxidative stress mitigation and hormone metabolism. When combined with other environmental stimuli, silicon also has an additive function in the elimination of ROS (Mostofa et al., 2021). Under salt stress conditions, Si improves and maintains the plant water status, K+ concentrations in shoots, chlorophyll content, and membrane permeability in wheat plants (Tahir et al., 2012). A recent study demonstrated the role of Si during salt, drought, and heavy metal (Cd) stress conditions in wheat. The authors supplemented Si which resulted in higher growth, gas exchange, tissue water, and antioxidant defense against the abiotic stress. Further, the enzymatic activity of SOD, CAT, and peroxidase led to the elevated activities of osmoprotectants and antioxidants such as soluble sugars, free proline, GSH, and ascorbic acid (AsA) (Alzahrani et al., 2018). Si has been found to bind to hazardous metal ions (Al, Cd), producing metal silicates and therefore promoting metal sequestration in vacuoles (Pilon-Smits et al., 2009; Shi et al., 2005). Silica depositions decrease the UV penetration through the sclerenchyma and the mesophyll, thus, protecting against harmful radiations (Schaller et al., 2013).

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1.4.9.2 BIOTIC STRESS Since Si has relative atmospheric abundance, it plays a significant metabolic role in living organisms. Plants having a greater Si content in the shoot or root are less susceptible to pest attack and have higher stress resistance. The more notable benefit of Si, however, is the reduction in the number of seed intensities/soil-borne and foliar diseases of important plant types affected by biotrophic, hemibiotrophic, necrotrophic pathogens, fungi, and bacteria (Cai et al., 2008; Chérif et al., 1994; Liang et al., 2015; Rodrigues et al., 2015). The influence of Si on several parameters involved in providing host resistance, including time of incubation, size, shape, and many lesions, is responsible for the improvement in disease symptoms (Song et al., 2021). The development of a mechanical barrier beneath the cuticle and in the cell walls by Si polymerization was initially postulated as a mechanism by which this element reduces plant disease severity. Si deposition may also wear away the eating mouthparts/mandibles, of insects (Jeer et al., 2017), and reduce plant digestibility for both insect and mammalian herbivores (Frew et al., 2016, 2018). Notably, plant tissue silicification may be triggered more in plants that are heavily attacked by different species. The interaction of Si with Fe can lead to the formation of silicates and as Fe is a central factor regulating plant pathogen defense (Brissot et al., 2011; Fleck et al., 2011), it can lead to good resistive power of the plant against the biotic stress. 1.4.10 SELENIUM 1.4.10.1 ABIOTIC STRESS Because of its ability to promote the production of S- and N-compounds, as well as increasing the activity of antioxidant enzymes and metabolites, Se can help plant development and minimize the negative effects of abiotic stress. Se has been documented to mitigate stress factors such as drought, temperature, salinity, and heavy metals (Habibi, 2014). During DS, Se enhanced the amounts and activity of osmoprotectants and antioxidant defense system components, resulting in decreased electrolyte leakage and oxidative stress indicators (malondialdehyde (MDA), H2O2, and O2–) as well as improved growth characteristics (Rady et al., 2020). These improvements were also seen in the case of using Se-NPs to alleviate the negative effects of drought on strawberry plants. It resulted in an increase in water use efficiency (WUE), relative water content (RWC), membrane stability index (MSI), and

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antioxidants enzymes (SOD, CAT, APX, GPX) (Zahedi et al., 2020). Similar results were found during the investigation of the involvement of ethylene (ET) in the Se-modulation of the antioxidative defense system in response to Cd-stress (Alves et al., 2019) as well as salt stress (Shah et al., 2020). Application of Nano-Se on cucumber plants as anti-stress compounds improved the growth parameters and helped the plants in controlling osmotic balance during heat stress and soil salinity (Shalaby et al., 2021). 1.4.10.2 BIOTIC STRESS Se alleviates a range of biotic stressors and hence plays a role in protecting plants against herbivores and fungal/pest diseases (Quinn et al., 2007). Accumulation of Se helps to protect the plants against aphids, herbivores, flies, caterpillars, weevils, crickets, and cabbage loopers by repelling them and reducing their growth while having a positive impact on the developmental process of plants (Mechora, 2019; Pilon-Smits, 2019). Se treatment has been demonstrated to protect Brassica juncea from fungal pathogens such as a leaf fungus (Alternaria brassicicola) and a stem/root fungus (Fusarium sp.) (Hanson et al., 2003). The reduction in the activity of aphids by Se has been associated with reduction of female fertility or the reproductive potential of the insects with a simultaneous decrease in the ROS levels and increase in the activity of antioxidant, synthesis of flavonols and carotenoids, detoxifying, and redox enzymes in the plant tissues (Łukaszewicz et al., 2021a). 1.4.11 COBALT 1.4.11.1 ABIOTIC STRESS Co is a component of cobalamine and cobamide coenzyme involved in N2 fixing in the leguminous root nodules. It may operate as an important metal that controls the symbiotic rhizobia that live in leguminous nodules. Nodules are important generators of ROS in leguminous plants due to the intensive usage of O2 and have enzymatic/non-enzymatic antioxidant defense mechanisms that minimize the harm caused by ROS (Marschner, 1995; Palit et al., 1994). Co has been shown to enhance the activity of antioxidant enzymes like peroxidase (POX) and PPO, which aids in the resistance to oxidative damage caused by high/low temperatures, water scarcity, salinity, and other factors (Jaleel et al., 2008). Several studies have demonstrated the role of

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Co during salinity stress (Gad and El-Metwally, 2015; Gad & Kandil, 2011). Co enhances the levels of macro-/micro-nutrients along with endogenous levels of phytohormones such as auxin, cytokinin, and gibberellins in plants (cucumber, onion) irrigated under saline conditions (Gad et al., 2018a, 2020). Co supplementation can enhance the resistance to DS along with an increase in growth, nutritional status, WUE, and yield (Gad et al., 2018b, 2019). Co also helps in mitigating heavy metal stress and osmotic stress (Akeel & Jahan, 2020). 1.4.11.2 BIOTIC STRESS It has recently been proposed that plants absorb large quantities of metals from their surroundings as a form of self-defense against pathogen stressors and herbivores (Poschenrieder et al., 2006). Micronutrients are also necessary for the production of secondary metabolites with antibiotic action, and antibiotics must be bonded to a divalent metal ion to be bactericidal. Some of the Metallo-antibiotics can bind to ions such as Co2+, Zn2+, Mn2+, and Cd2+ (Ming, 2003). Table 1.2 enlists some of the roles of Co in mitigating biotic stresses. 1.4.12 ALUMINIUM (AL) 1.4.12.1 ABIOTIC STRESS Although Al is the most common metal in the earth’s crust, it is not considered a necessary element, despite having some positive effects as a TE on plant development and stress situations (Bojórquez-Quintal et al., 2017). Al enhanced the activity of antioxidant enzymes including SOD, CAT, and APX, contributing to improved membrane integrity, delayed lignification, and aging of tea (Camelia sinensis L.) plants. Al3+ is also required for root development in tea plants via maintaining DNA integrity in meristematic cells (Sun et al., 2020). Minimal quantities of Al have aided plants by stimulating growth, providing tolerance to acidic soils (Osaki et al., 1997; Watanabe et al., 1997), and alleviating H+ ion toxicity (Kinraide et al., 1992). Al seems to enhance root activity in Melastoma malabathricum and induce root cell elongation, perhaps leading to the formation of many fine roots (Watanabe et al., 2005). Al is also able to prevent the toxic effects caused by elements such as P, Zn, and Cu (Asher, 1991).

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1.4.12.2 BIOTIC STRESS The toxicity of Al towards the pathogenic microorganisms can be used to control various diseases. Al inhibits the germination of spores or fungus (Meyer et al., 1994) and Al-salt compounds can be used to control/resist the diseases caused by fungi in crops such as carrot and potato (Kolaei et al., 2013). Al is also effective against Phytophthora infestans, which is due to the accumulation of H2O2 in the roots and the initiation of the acquired systemic response based on salicylic acid (SA) and nitric oxide (NO) (ArasimowiczJelonek et al., 2014). Some plants (particularly, Festuca arundinacea) can hyper accumulate Al and thus, allowing the tissues to discourage the herbivory (Pilon-Smits et al., 2009; Potter & Yong, 1999). 1.4.13 VANADIUM 1.4.13.1 ABIOTIC STRESS V is a transition element that may play two roles in plants depending on the concentration, degree of oxidation, and duration of exposure (HanusFajerska et al., 2021). A lower V content in soils is favorable for plant development, increased chlorophyll synthesis, and nitrogen fixation, as well as facilitating plant use of potassium from the soil (Pilbeam, 2016). V can be a potent elicitor, a stimulator of secondary metabolite synthesis, and a stress-protective molecule that may be utilized to prime plants for abiotic stress tolerance (Hanus-Fajerska et al., 2021). Compounds of V (NH4VO3 and NaVO3·2H2O) have been shown to enhance the antioxidant system in Oryza sativa, Cicer arietinum, and Nicotiana tabacum by increasing the activity of SOD, CAT, POD, and APX (Altaf et al., 2020; Imtiaz et al., 2018; Wu et al., 2021). 1.4.13.2 BIOTIC STRESS V is important for life, especially in aquatic settings where ocean algae use it as an active center of the haloperoxidase enzymes (Roychoudhury, 2020). Limited studies are available on the role of V in biotic stress. Datta and colleagues demonstrated the pathogenic properties of V-compounds and had inhibitory effects on Agrobacterium tumefaciens, Helminthosporium oryzae (a rice plant pathogen), and Dysdercus koenigi (red cotton bug) (Datta et al., 1982). Some of the functions of V is listed in Table 1.2.

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1.5 IMPLICABILITY OF TRACE ELEMENTS (TES) BY EXTERNAL APPLICATIONS TO EXECUTE POSITIVE RESPONSES DURING STRESS Chemical elements in the soil are considered TEs since they occur at minor concentrations of less than 100 mg kg–1 (Robinson et al., 2009). Generally, plants remove the TEs that are present in the surrounding or soil. Among those TEs, some are toxic, whereas others are important for plant functioning. TEs in plant tissue serve an enzyme-activation function rather than a structural function (Salisbury & Ross, 1992). Essential TEs can occur at inadequate, optimum, or phytotoxic quantities in plant tissue, depending on their concentration. As we have already discussed regarding the beneficial use of TEs in the plants, it seems supplementation of TEs through certain ways can help the plants to increase their tolerance and response towards the various kinds of stress factors (Figure 1.1). Depending on the requirement and diagnosis, the TEs can be supplied to the plants through soil application or foliar treatments (Na, 2007). Plant development and yield are significantly affected by various TEs and their application techniques (soil fertilizers, foliar spray, grain coating, grain soaking, etc.) (Nadim et al., 2012; Salem & El-Gizawy, 2012). Foliar spraying is becoming more prevalent in most crops where environmental conditions prevent farmers from applying nutrients through soil medium. The foliar spray is inexpensive and provides quick corrective actions to rectify a deficit at a specific growth stage (Noreen et al., 2018). Studies have shown that nutrients such as Zn, Cu, B, Mn, Cl, Ni, Mo, Fe, Si, and Co can be supplied to the plants through the foliar applications for stress tolerance, growth, and high yield (de Queiroz Barcelos et al., 2017; Duan et al., 2018; Rios et al., 2020; Rizwan et al., 2019a; Stewart et al., 2021; Sutradhar et al., 2017). For example, Se and Si foliar spray reduced Cd-induced oxidative stress by enhancing antioxidative mechanisms (Zhou et al., 2021). Foliar treatments of ZnO NPs can be utilized to increase fruit set and quality in coffee plants, particularly in locations with a significant Zn deficit (Rossi et al., 2019). Fe and Zn-chelate nano fertilizers, when applied as foliar sprays, were seen to improve the yield in cucumber plants by influencing the number of fruits, chlorophyll content, and SOD (Javadimoghadam et al., 2015). Recent foliar applications have been focusing on various metal-based NPs. When compared to traditional soil–root treatment, foliar spraying of NPs improves the efficiency of plant protection technologies. Foliar-sprayed NPs enter the leaves primarily through the stomata and are distributed to other plant sections via apoplastic and symplastic routes.

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Foliar NPs boost crop production and quality by increasing defenses and resilience to pests and diseases (Bocchini et al., 2018; Hong et al., 2021; Ikram et al., 2020; López-Vargas et al., 2018). Therefore, it becomes necessary to explore the different compounds of TEs/micronutrients that can give us the best results under stress conditions while having minimum toxic effects on the soil and plants. KEYWORDS • • • • • • •

abiotic stress adenosine triphosphate ascorbate peroxidase biotic stress catalase micronutrients trace elements

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Akeel, A., & Jahan, A., (2020). Role of cobalt in plants: Its stress and alleviation. Contaminants in Agriculture Cham, 339–357. Springer. Akgül, M., Çöpür, Y., & Temiz, S., (2007). A comparison of kraft and kraft-sodium borohydrate brutia pine pulps. Building and Environment, 42, 2586–2590. Akoumianaki-Ioannidou, A., Barouchas, P. E., Ilia, E., Kyramariou, A., & Moustakas, N. K., (2016). Effect of vanadium on dry matter and nutrient concentration in sweet basil (‘Ocimum basilicum’ L.). Australian Journal of Crop Science, 10, 199–206. Aktas, H., Karni, L., Chang, D. C., Turhan, E., Bar‐Tal, A., & Aloni, B., (2005). The suppression of salinity‐associated oxygen radicals’ production, in pepper (Capsicum annuum) fruit, by manganese, zinc and calcium in relation to its sensitivity to blossom‐end rot. Physiologia Plantarum, 123, 67–74. Alabdallah, N. M., & Alzahrani, H. S., (2020). The potential mitigation effect of ZnO nanoparticles on [Abelmoschus esculentus L. Moench] metabolism under salt stress conditions. Saudi Journal of Biological Sciences, 27, 3132–3137. Alcázar, R., Altabella, T., Marco, F., Bortolotti, C., Reymond, M., Koncz, C., Carrasco, P., & Tiburcio, A. F., (2010). Polyamines: Molecules with regulatory functions in plant abiotic stress tolerance. Planta, 231, 1237–1249. Al-Hakimi, A. B., & HAMAdA, A. M., (2011). Ascorbic acid, thiamine or salicylic acid induced changes in some physiological parameters in wheat grown under copper stress. Plant Protection Science, 47, 92–108. Aloni, B., Karni, L., Deventurero, G., Turhan, E., & Aktas, H., (2008). Changes in ascorbic acid concentration, ascorbate oxidase activity, and apoplastic pH in relation to fruit development in pepper (Capsicum annuum L.) and the occurrence of blossom-end rot. The Journal of Horticultural Science and Biotechnology, 83, 100–105. Alscher, R. G., Erturk, N., & Heath, L. S., (2002). Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. Journal of Experimental Botany, 53, 1331–1341. Altaf, M. M., Diao, X. P., Ur Rehman, A., Imtiaz, M., Shakoor, A., Altaf, M. A., Younis, H., Fu, P., & Ghani, M. U., (2020). Effect of vanadium on growth, photosynthesis, reactive oxygen species, antioxidant enzymes, and cell death of rice. Journal of Soil Science and Plant Nutrition, 20, 2643–2656. Alves, L. R., Rodrigues, D. R. A., Prado, E. R., Lavres, J., Pompeu, G. B., Azevedo, R. A., & Gratão, P. L., (2019). New insights into cadmium stressful-conditions: Role of ethylene on selenium-mediated antioxidant enzymes. Ecotoxicology and Environmental Safety. Alzahrani, Y., Kuşvuran, A., Alharby, H. F., Kuşvuran, S., & Rady, M. M., (2018). The defensive role of silicon in wheat against stress conditions induced by drought, salinity or cadmium. Ecotoxicology and Environmental Safety, 154, 187–196. Amauri, P., Juliana, S., Tatiana, L., Victor, D., Caldas, H., Alessandra, R., & HermÃnio, A., (2017). Plant defense against leaf herbivory based on metal accumulation: Examples from a tropical high-altitude ecosystem. Plant Species Biology. Antoniadis, V., Levizou, E., Shaheen, S. M., Ok, Y. S., Sebastian, A., Baum, C., Prasad, M. N., Wenzel, W. W., & Rinklebe, J., (2017). Trace elements in the soil-plant interface: Phytoavailability, translocation, and phytoremediation—A review. Earth-Science Reviews, 171, 621–645. Arasimowicz-Jelonek, M., Floryszak-Wieczorek, J., Drzewiecka, K., Chmielowska-Bąk, J., Abramowski, D., & Izbiańska, K., (2014). Aluminum induces cross-resistance of potato to Phytophthora infestans. Planta, 239, 679–694.

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CHAPTER 2

Trace Elements and Their Role in Abiotic Stresses

SIMRANJIT KAUR,1 ANJALI JOSHI,2 KRITI GUPTA,3 ANUJ KUMAR,4 VAJINDER KUMAR,5 HARSH NAYYAR,6 and AVNEESH KUMAR1* Department of Botany, Akal University, Talwandi Sabo, Bathinda, Punjab – 151302, India

1

Center for Nanoscience and Nanotechnology (UIEAST), Panjab University, Chandigarh – 160014, India

2

3

Department of Botany, DAV College, Bathinda, Punjab – 151001, India

Center for Agricultural Statistics, ICAR–Indian Agricultural Statistics Research Institute, New Delhi – 11012, India

4

Department of Chemistry, Akal University, Talwandi Sabo, Bathinda, Punjab – 151302, India

5

6 *

Department of Botany, Panjab University, Chandigarh – 160014, India

Corresponding author. E-mail: [email protected]

ABSTRACT With an expanding global population, world food demand relies on agriculture. Due to rapid climate change, abiotic stresses are posing a negative effect on the productivity of plants and diminish the majority of crop production. To cope with adverse growing conditions, it becomes critical to understand the physiological effects of the abiotic stresses and search for ways to make plants more adaptive. Trace elements (TEs) are needed minimally for the ideal growth and development of plants. Recently, there have been several Biology and Biotechnology of Environmental Stress Tolerance in Plants: Trace Elements in Environmental Stress Tolerance, Volume 2. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

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successes concerning using TEs at their low levels to enhance plants’ abiotic stress tolerance. The role of TEs in ameliorating abiotic stresses is multifarious, such as regulating various metabolic processes, signal transduction, gene regulation, biosynthesis of proteins, sugars, and lipids, energy metabolism, and hormone perception. Here, we describe the role of some prominent TEs, their favorable aspects to boost crop production, and the part of TEs in conferring resilience to abiotic stresses in different plant species. 2.1 INTRODUCTION Food supply security is among the essential requirements and the primary significant concern worldwide (Condon et al., 2010; Brown & Funk, 2008). The earth’s population, consequently (~ 7 billion), is anticipated to rise to approximately 10 billion in the next half-century. Thus, total crop production may soon become insufficient to fulfill worldwide food demand (Glick, 2014). In contrast to this increasing demand, global climate change has also increased the magnitude of environmental stresses, which sporadically curb more than half of the crop production (Carmen & Roberto, 2011). In contrast to the previous decades, soil salinity, drought, heat, cold, metal/metalloid toxicity, flooding, and high radiation exposure are the significant abiotic stresses that have remarkably exacerbated (Mittler & Blumwald, 2010). Approximately 1–2 percent of the regions suited for cultivation are diminishing due to soil salinity annually, which is more significant in desiccated and semi-desiccated landforms (Rasool et al., 2013). Water stress has been recorded in 30% of the total area of the earth. It has many commonalities with salt stress that pose cataclysmic impacts on agricultural production compared to salinity stress (Bodner et al., 2015). The air temperature is envisaged to surge by 0.2°C per decennium globally that can cause hot spell 1.8 to 4.0°C over the existing level by 2100 (Intergovernmental Panel on Climate Change (IPCC), 2007). As sessile organisms, plants cannot move to more suitable environments; consequently, the growth and developmental processes of plants are considerably affected, usually fatal, by heat stress (Lobell & Asner, 2003; Lobell & Field, 2007). Low temperature is also major environmental stress which is alienated into chilling stress (less than 20°C) and freezing stress (less than 0C) in accordance with the environmental thermal ranges. Together with limiting the growth and development of the plant, low temperature drastically hampers the distribution of plants (Liu & Zhou, 2018; Shi et al., 2018; Guo et al., 2017). According to the reports published several important crops, for instance, potato, cotton, rice, soybean, corn, and tomato, are sensitive to chilling and not capable of acclimatization to cold. Unlike, some other crops such as oats are freezing

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sensitive but tolerant to chilling. On the contrary, wheat, rye, and barley are fairly capable of adjusting to freezing temperatures (Zhang et al., 2011). Presently, the level of toxic metals in soil is also rapidly increasing, leading to diverse environmental problems. Therefore, it has become a serious issue for the scientists owing to its long-term toxic effects on the environment (Etesami, 2017). Abiotic stresses lead to various physiological and metabolic alterations in plants’ life cycle such as nutritional and water imbalance, reduction in the growth, development, photosynthesis, dry matter assimilation, and final yield of plants (Paul & Lade, 2014). So, it has become crucial to attain food supply globally by investigating the plant’s abiotic stress responses and developing the potential strategies for making plants stress resilient (Condon et al., 2010). The most studied defense responses to abiotic stresses in plants are related to modifications in osmoprotectants, hormones, antioxidants, and several other indispensable metabolic substances. But there are some limitations of traditional crop improvement methods as these are laborious, extravagant, sometimes unpredictable, or futile and occasionally lead to crop loss due to evolution or dysgenics. Previous studies indicate that supplementation exogenous phytoprotectants in particular trace elements (TEs) could be effective strategies to combat abiotic stresses in plants (Nahar et al., 2015). TEs are elements that are essential in minute amounts to promote a variety of physiological activities in plants. TEs are not vital for many plants; however, they can boost plant growth and are indispensable for specific plants under definite conditions (Pilon-Smits et al., 2009). The exogenic application of these TEs at their low concentrations can put an advantageous effect on many vital processes and helps in alleviate biotic and abiotic stresses (Muszyńska & Labudda, 2019). Furthermore, these elements curtail the deleterious effects of other elements, and that they also can, has sometimes, provide specific role of essential nutrients, for example, the upkeep of osmotic balance, or promote plant’s adaptive responses to abiotic stresses (Pilon-Smits et al., 2009; Meimandi et al., 2019). Since abiotic stresses are among the core problem for the growth of plant that curb the crop production, the objective of this chapter is to outline the underlying defense strategies by which TEs like copper (Cu), cobalt (Co), boron (B), selenium (Se), silicon (Si), Zinc (Zn), and Nickel (Ni) could improve plant tolerance to abiotic stresses likewise drought, salinity, high and low-intensity radiations, extreme temperature stress, flooding, and heavy metal toxicity. Though much research has been accomplished on this topic, our study aims to gather recent evidence on the beneficial effects of these metal ion treatments on plants under stress conditions. Therefore, our focus is to discuss the involvement of TEs in the alleviation of environmental stresses by the activation of antioxidant machinery, which is recently one of the foremost studied issues.

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2.2 FUNCTIONAL ROLE OF TRACE ELEMENTS (TES) IN IMPARTING RESILIENCE AGAINST ABIOTIC STRESSES Despite the fact that TEs are needed in limited quantities, their essentialities are equivalent to macronutrients. A few TEs have not formerly been distinguished as essential elements, but they perform few crucial functions in plant growth and development. In addition, these elements have explicit metabolic functions and numerous roles in stress resilience, summarized in Table 2.1. But when exposed to high concentrations these elements caused toxicity in plants (Figure 2.1).

FIGURE 2.1 Trace elements-mediated abiotic stress tolerance in plants.

Crop or Plant Copper Catharanthus roseus Hordeum vulgare genotypes (Yan66, tolerant, and Ea52, sensitive) Nickel Triticum aestivum

Form and Dose of Type of Stress Trace Element

Growth Conditions

1.25 μM Cu (II)

Growth Lesser accumulation of terpenoid indole Chen et al. (2018) chamber alkaloids (TIA) Pot experiment Improved growth and photosynthesis, Lwalaba et al. an extreme fall in Co uptake and its (2019) transport from roots to aboveground parts

100 μM CuCl2.4H2O

20 mg kg−1 Ni(NO3)2.6H2O

Cd-toxicity (80 μM) Co-toxicity (100 μM; CoCl2.6H2O)

References

Salt stress (10 dS Pot experiment Nickel increased wheat growth by promoting antioxidative defense m−1; NaCl) mechanisms

Ain et al. (2016)

Moeinian et al. (2011)

Boron Drought Stress Triticum aestivum

0, 0.5, 1% B

Irrigation withdrawal

Triticum aestivum

50 mg B L−1

50, 75, and 100% Field irrigation experiment

50 and 100 ppm H3BO3

4% NaCl

Salt Stress Zea mays

Ameliorative Response

Field experiment

Enhanced leaf area index, overall crop growth rate, as well as plant net assimilation rate Improved chlorophyll and carotenoids content, declined H2O2 and proline levels

Pot experiment Improved height of the plant, no. of leaves, dry weight of shoot, as well as weight of grain

Trace Elements and Their Role in Abiotic Stresses

TABLE 2.1 Trace Elements and Their Function in Mitigation of Abiotic Stresses in Plants

Abdel-Motagally & El-Zohri (2016) Salim (2014)

71

(Continued)

Crop or Plant

72

TABLE 2.1

Growth Conditions

Ameliorative Response

References

2.5 and 20 μM

1.2 mM

Plant Culture

Zhou et al. (2015)

H3BO3

AlCl3 for 18 weeks

High dry weight, citrate, and malate secretion in roots

5 and 10 μM

50 mM NaCl

Manaf (2016)

Lactuca sativa L.

Na2SeO4 16, 32 μM Na2SeO4

Pot experiment Better growth, production, and protein contents

3.22 dS m–1 EC

Field experiment

Khalifa et al. (2016)

Lycopersicon esculentum-Mill.

0, 5, 10 μM Na2SeO3

0, 25, 50 mM NaCl

Hydroponic culture

Solanum melongena

0, 5, 10, 20, and 30 0, 30, 60, 120 mM NaCl μM Na2SeO3

Zea mays

1, 5 and 25 μM Na2SeO3

Heavy Metal Stress Citrus grandis

Selenium Salt Stress Vigna unguiculata

100 mM NaCl

Bedding sand culture Growth chamber

Improved growth, yield, and RWC, chlorophyll, carotenoids, K+/Na+, and total soluble sugar contents; decreased cell membrane permeability and malondialdehyde content Maintained water balance and reduced membrane damage; photosynthetic pigment contents increased; decreased proline, total phenolic content, improved plant’s growth Increased overall growth, higher yield, improved NPK content in fruit and leaf; enhanced K+/Na+ ratio Increased photosynthetic efficiency, antioxidative enzyme activities, and maintenance of Na+ levels

Mozafariyan et al. (2016)

Abul-Soud & AbdElrahman (2016) Jiang et al. (2017)

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 2

Form and Dose of Type of Stress Trace Element

(Continued)

Crop or Plant

Form and Dose of Type of Stress Trace Element

Growth Conditions

Ameliorative Response

References

Helianthus annuus

5 mg kg−1 Na2SeO4 15 dS M−1 NaCl

Greenhouse experiment

Habibi (2017)

Allium cepa

0.5 and 1 kg ha−1 Se

Field experiment

Enhanced antioxidant enzyme activity, regulated ratio of Na/K required for optimal photo-biochemical processes Enhanced yield in both qualitative and physiological attributes

Zea mays

20 and 40 mg L−1 Na2SeO4

Stevia rebaudiana

Bertoni

20 g ha–1 (2 ppt) Na2SeO3

Triticum aestivum L.

0, 0.5, 1, 4 mg kg−1 Na2SeO3 0, 5, 10 μM Na2SeO3

Phaseolus vulgaris L.

Triticum aestivum

5 and 10 μM Na2SeO4

Allium sativum

4, 8 and 16 mg L−1 Na2SeO4

8 dS m−1 Silt loam soil with salinity 12 dS m−1 Salinity

Reduced oxidative damage and elevating antioxidative enzyme activities at reproductive phase Enhanced rebaudioside-A, stevioside, Field 10, 30, 60, 90 and sweet steviol glycosides levels in experiment mM NaCl leaves 0.12, 0.30, 0.60 Pot experiment Improved chlorophyll a, b, and carotenoid contents dS m−1 salinity 0, 100 mM NaCl Pot experiment Enhanced MSI, photosynthetic efficiency, and RuBPCase enzyme activity hence improved growth and seed yield, Reduced the levels of signature oxidants, Greenhouse 100 mM NaCl stimulation in enzymatic antioxidants as experiment well as non-enzymatic one Lesser production of signature oxidants, Greenhouse 30, 60, and 90 increased concentration of different kind experiment mM NaCl of antioxidants Greenhouse experiment

Bybordi et al. (2018) Ashraf et al. (2018)

Aghighi Shahverdi

et al. (2018)

Trace Elements and Their Role in Abiotic Stresses

TABLE 2.1

Atarodi et al.

(2018)

Moussa & Hassen

(2018)

Elkelish et al.

(2019)

Astaneh et al.

(2019)

73

(Continued)

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TABLE 2.1

Form and Dose of Type of Stress Trace Element

Growth Conditions

Oryza sativa L.

2, 4, 6, 8, 10, 12 mg L−1 Na2SeO4

Sand culture

Vitis vinifera L. ‘Sultana’

Triticum aestivum L.

Olea europaea L. cv. Arbequina Drought Stress Hordeum vulgare Olea europaea

Zea mays

150 mM NaCl

Ameliorative Response

Increased plant biomass, chlorophyll, and water contents, K+/Na+ ratio, reduce malondialdehyde contents (MDA) and H2O2 contents 0, 5, 10 and 20 mg 0 or 75 mM NaCl Pot experiment Increased enzymatic and non-enzymatic L−1 Na2SeO4 antioxidant capacity thereby decreased vines leaves electrolyte leakage and lipid peroxidation 2, 4 and 8 μM 200, 250 mM Pot experiment Increased chlorophyll content, NPR, NaCl transpiration rate, stomatal conductance, SeCl2 RWC, MSI, excised leaf water retention, compatible solutes; stimulation of enzymatic and non-enzymatic antioxidative substances 10 and 30 mg L−1 200 mM NaCl Hydroponic Maintenance of proline content; culture restoration of ionic homeostasis, Na2SeO4 improved photosynthesis 30 g ha−1 Na2SeO4 70% of field Field capacity (FC) experiment 50 and 150 mg L−1 80% and 25% Field of the substrate experiment Na2SeO4 available water 5–15 μM Na2SeO3 PEG-6000 (25%) Hydroponic culture

References Subramanyam et al. (2019)

Karimi et al. (2020)

Desoky et al. (2021)

Regni et al. (2021)

Greater biomass accrual and stimulation Habibi (2013) of antioxidative enzymes Proietti et al. Enhanced ROS scavenging and (2013) maintained of water relations in plants Stimulation of antioxidative machinery, primarily the AsA-GSH cycle

Yildiztugay et al. (2017)

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 2

Crop or Plant

(Continued)

Crop or Plant

Form and Dose of Type of Stress Trace Element

Oryza sativa L.

0.5–2.0 mg kg−1 Na2SeO4 100 mg L−1 Na2SeO4

–50 kPa

Greenhouse experiment 110 m3 ha−1 and Field total water deficit experiment

Andrade et al. (2018) D’Amato et al. (2018)

Triticum aestivum

10 mL per pot Na2SeO4

40% FC (field capacity)

Sattar et al. (2019)

Brassica napus L.

30 g L−1 Na2SeO4

Cucumis sativus L.

1–10 μM Na2SeO3

Irrigation withdrawal Irrigation withdrawal 100 and 60% of soil FC

Increased photosynthetic capacity and reduced peroxidation of lipids Enhanced nutritional qualities, increased antioxidative substances and conferring extended shelf life. Pot experiment Enhanced growth, photosynthetic capacity, relative water content, as well as Chl levels; stimulation of antioxidative enzymes Field Reduction in ROS experiment Hydroponic Enhanced antioxidant capacity thereby culture reducing the ROS Greenhouse Enhanced antioxidants concentration experiment Hydroponic culture Growth chamber

Hasanuzzaman et al. (2014) Hawrylak-Nowak et al. (2014)

Olea europaea L.

Solanum lycopersicum 20–40 mM Na2SeO4 Temperature Stress 25 μM Na2SeO4 Brassica napus Cucumis sativus

2.5–20 μM Na2SeO4

38°C (HT), 24 h and 48 h 10°C/5°C (LT) for 24 hrs. for next 24 h at 20°C/15°C)

Growth Conditions

Ameliorative Response

Enhanced antioxidants (AsA and GSH) Improved shoot and root biomass and proline levels; lower levels of MDA content

References

Hemmati et al. (2019) J´o´zwiak et al. (2019) Rady et al. (2020)

Trace Elements and Their Role in Abiotic Stresses

TABLE 2.1

75

(Continued)

76

TABLE 2.1

Form and Dose of Type of Stress Trace Element

Growth Conditions

Ameliorative Response

References

Triticum aestivum

2 and 4 mg Se L−1 38±2°C (HT) Na2SeO4

Growth chamber

Iqbal et al. (2015)

Cucumis sativus

8 μM Na2SeO4

40/30°C day/ Growth night (HT), 40 d chamber

Valerianella locusta

50 mg Se L–1 Na2SeO4

35/22°C day/ night (HT), 7 d

Greenhouse experiment

Fragaria × ananassa

2.5–10 mg L–1 Na2SeO3

LT (0°C/5°C for 6 or 12 hrs.)

Growth chamber

Improved growth; decreased signature oxidants; enhanced enzymatic activities of antioxidants; increased contents of phenolic compounds and pigments of photosynthesis

Reduction in H2O2, O2•−, and MDA,

increased levels of compatible solutes; enhanced antioxidant enzyme activities Improved growth; reduced oxidative damage; increased anti-oxidative enzymes (GPX and CAT) activity; enhanced GSH concentration Increased intercellular CO2 and rate of photosynthesis, improved stomatal conductivity, decreased malondialdehyde and hydrogen peroxide levels; stimulation of antioxidative enzymes

Light Triticum aestivum L.

Triticum aestivum

10 mg L–1 Na2SeO4 UV+ and UV–

Field experiment

Seleniferous and nonseleniferous soil

Growth chamber (in vitro)

Visible and UV-B light

Increased UV absorbing compounds, power to reflect and transmit light increased, maintained redox balance Enhanced secondary metabolites to defend against lipid peroxidation

Balal et al. (2016)

Hawrylak-Nowak et al. (2018)

Huang et al. (2018)

Golob et al. (2017)

Jaiswal et al. (2018)

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 2

Crop or Plant

(Continued)

Crop or Plant

Form and Dose of Type of Stress Trace Element

Growth Conditions

Ameliorative Response

Glycine max L.

5, 10 or 20 mg L–1 UVC-light Na2SeO3

Growth chamber (in vitro)

Brassica oleracea L.

100 μmol L–1 Na2SeO3

Mata-Ramírez et Enhanced isoflavonoids (glycitein and al. (2019) genistein) content inhibit nitric oxide production and stimulate the antioxidant property as well He et al. (2020) Enhanced nutritional quality and activation of protective compounds

Heavy Metal Stress Oryza sativa

10 mΜ Na2SeO3

CK:1R1B1G LED, 1R1B1G + Se, 1R1B + Se, 1R2B + Se, 2R1B + Se

Growth chamber

50 μM CdCl2; 5, Pot experiment Reduced Cd accrual in plant parts like leaf, stem, grain, and root; lowered ROS 10 and 15 d production; enhanced CAT mediated detoxification Lowered As amassing and enhanced 0, 5, 10 and 25 μM 25 μM NaAsO2, Hydroponic Oryza sativa phenolic content Na2SeO3 culture 15 d Improved chlorophyll content; reduced Vicia faba 50 μM Pb(NO3)2, Hydroponic 1.5 or 6 μM MDA levels, H2O2, and superoxide ion culture Na2SeO3 14 d accrual Brassica campestris L. 0.1 mg L–1 Reduced Cr uptake 1 mg L–1 K2Cr2O7 Hydroponic culture Na2SeO4 Cucumis sativus L. Enhanced fruit production 4–8 mg L–1 20–25 mM CdCl2 Hydroponic Na2SeO3 and 60–100 mM culture PbCl2

References

Mozafariyan et al. (2014)

Trace Elements and Their Role in Abiotic Stresses

TABLE 2.1

Chauhan et al. (2017) Mroczek-Zdyrska et al. (2017) Zhao et al. (2019) Shekari et al. (2019) 77

(Continued)

78

TABLE 2.1

Form and Dose of Type of Stress Trace Element

Growth Conditions

Ameliorative Response

Brassica napus and Brassica juncea

3 μmol L–1 CdCl2 (50 μmol Na2SeO4, Na2SeO3 L–1) and Se-Met

Growth chamber

Zhang et al. (2020) Reduced levels of major oxidants; stimulation of antioxidants and improved photosynthesis.

Silicon Salt Stress Saccharum officinarum 1.4, 2.1, and 2.8 mM Si (calcium L. silicate) 2 mmol L–1 Si Brassica napus L. (sodium silicate)

Brassica napus L. Sorghum bicolor L.

1.7 mM sodium silicate (Na2SiO3) 0.83 mM Si

References

100 mM NaCl

Pot experiment Lowered Na+ content in shoots, enhanced yield and quality of sap

Ashraf et al. (2010)

150 mmol L–1 NaCl

Greenhouse experiment

Hashemi et al. (2010)

100 mM NaCl 100 mM NaCl

Oryza sativa L.

0.5, 1, 2 mM Si (Na2SiO3.5H2O)

100 mM NaCl

Abelmoschus esculentus

150 mg L–1 Si

6 dS m–1 EC (electrical conductivity)

Improved growth, lowered lignin content, lower lipid peroxidation and Na+ accrual; enhanced antioxidants and pigment content Hydroponic Reduced H2O2 and MDA content, culture increased antioxidative enzyme response Growth Reduced Na+ concentration, increased chamber glucose, fructose, and other osmolytes contents Growth Enhanced phytohormone contents and chamber antioxidative enzyme activities, lowered Na+ accrual, loss of electrolytes and lipid peroxidation Pot experiment Improved photosynthesis, osmolytes, antioxidative machinery, lowered Na+ and Cl– content

Farshidi et al. (2012) Yin et al. (2013)

Kim et al. (2014)

Abbas et al. (2015)

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 2

Crop or Plant

(Continued)

Crop or Plant

Form and Dose of Type of Stress Trace Element

Glycyrrhiza uralensis Fisch.

Zea mays L.

1, 2, 4 and 6 mM 50 mM NaCl K2SiO3 2 mM Si (H2SiO3) 60 mM NaCl

Oryza sativa L.

2 mM sodium metasilicate (Na2O3Si.9H2O)

Rapeseed (Brassica napus)

1 mM Silicon dioxide (SiO2)

Chinese liquorice 0.6 g per Kg (Glycyrrhiza uralensis) K2SiO3 Wheat (Triticum aestivum)

0.78 mM Na2SiO3

Wheat (Triticum aestivum)

2, 4, and 6 mM K2SiO3

Growth Conditions Growth chamber Greenhouse experiment

Ameliorative Response

Li et al. (2016) Khan et al. (2017)

Das et al. (2018)

Hasanuzzaman et al. (2018) Zhang et al. (2018)

Daoud et al. (2018)

Alzahrani (2018)

79

Reduced malondialdehyde levels, enhanced SOD, POX enzyme response Reduced levels of Na+ in shoots, accrual of K+ in roots and shoots, better quantum yield 25, 50 or 100 Growth Lesser free radicals’ accrual, increased mM NaCl chamber ascorbate and plummeted glutathione contents, enhanced responsiveness of multiple anti-oxidative enzymes like GST, GR, etc. NaCl solution, 2 Hydroponic Increased multiple anti-oxidative enzyme days culture mediated response, and the enhanced AsA and GSH concentration 3, 6, and 9 g of Pot experiment Enhanced free radical neutralizing NaCl mixed with enzymes like SOD, CAT, limit pot soils, 150 MDA content and plasma membrane days permeability. NaCl solution, Pot experiment Enhanced SOD and CAT activities, 120 days lesser H2O2 accumulation, and increased net photosynthesis and growth performance. NaCl solution, Pot experiment Enhanced proline, AsA, and GSH 45 days contents, and SOD, CAT, and POD enzyme response, reduced levels of MDA.

References

Trace Elements and Their Role in Abiotic Stresses

TABLE 2.1

(Continued)

80

TABLE 2.1

Form and Dose of Type of Stress Trace Element

Growth Conditions

Rock fire (Rosa hybrida)

1.8 mM K2SiO3

Hydroponic culture

Geranium (Pelargonium graveolens) Vigna radiata

0.5- and 1-mM NaCl solution, Potassium silicate 207 days (K2 SiO3) 2 mM Na2SiO3 NaCl solution, 14 days

Glycine max (L.) Merr. 2.0 mM sodium metasilicate (Na2SiO3.5H2O) Zea mays cv. (Hycorn 1 mM Na2SiO3 11 and P1574) Cannabis sativa L.

2 mM Na2SiO3

Drought Stress Solanum lycopersicum 0.5 mM Na2SiO3 L. 2.5 mM K2SiO3 Mangifera indica L.

25% K2SiO3 + 10% K2O3

NaCl solution, 15 days

Ameliorative Response

References

Stimulation of SOD, CAT, APX, and GPx enzymes, lower contents of MDA, O2•− and H2O2. Pot experiment Improved POD and CAT activities, reduced lipid peroxidation as well as electrolyte leakage. Pot experiment Boosted SOD, CAT, APX, and GR enzyme response, minimized H2O2 and MDA accumulation. Growth Lowered S-nitrosylation and enhanced chamber anti-oxidative enzyme actions

Soundararajan (2018)

Hydroponic culture

Enhanced RWC, MSI, and SOD, POD, APX, and CAT enzyme response and reduction in Na+/K+ ratio 200 mM NaCl Pot experiment Wider vessels lumen, stimulate the two times a week putative Si efflux transporter gene Lsi2 expression (low silicon 2).

Ali et al. (2021)

10% PEG-6000

Shi et al. (2014, 2016)

100 mM NaCl

80 mM and 160 mM NaCl

Growth chamber

–0.77 bars Water Field potential (Ψs) experiment

Reduced ROS and MDA levels, stimulation of SOD as well as CAT enzymes, enhanced ascorbate along with glutathione concentration Decreased response of POX, CAT, and SOD enzymes

Hassanvand (2019) Ahmed (2019)

Chung et al. (2020)

Berni et al. (2021)

Helaly et al. (2017)

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 2

Crop or Plant

(Continued)

Crop or Plant

Form and Dose of Type of Stress Trace Element

Growth Conditions

Ameliorative Response

References

Lens culinaris Medik

2 mM Na2SiO3

Growth chamber

Reduced ROS levels, enhanced amount of free radical neutralizing enzymes

Biju et al. (2017)

Triticum aestivum

1 mM Na2SiO3

Solanum lycopersicum 1.2 mM Na2SiO4 L.

2 mM K2SiO3

Vigna unguiculata Brassica napus

1 mM SiO2

18% polyethylene glycol-6000 PEG, 7 days

1% PEG Water withholding, 55 days 10 and 20% PEG, 48 h

Water withholding, 21 days Saccharum officinarum 600 Kg per hectare Water withholding, 60 of land calcium magnesium silicate days Zea mays

4 and 6 mM Na2SiO3

Hydroponic culture

Improved AsA and GSH content, increased SOD and CAT enzyme activities, attenuated H2O2, O2•−, and MDA accumulations Hydroponic Improved anti-oxidative enzyme culture activities, reduced ROS generation rate Greenhouse Improved response of SOD, POD, and experiment CAT enzymes, and lowered oxidative damage Hydroponic Alleviated CAT, APX, MDAR, DHAR, culture GR, GST, and GPx enzyme function, improved AsA as well as GSH, decreased contents of signature oxidants Pot experiment Stimulation of SOD, POD, and CAT enzymes lowered contents of MDA and H2O2 Pot experiment Enhanced SOD and APX enzyme response; improved proline level; detoxification of ROS

Xu et al. (2017)

Cao et al. (2017, 2020) Merwad et al. (2018)

Trace Elements and Their Role in Abiotic Stresses

TABLE 2.1

Hasanuzzaman et al. (2018)

Parveen et al. (2019) Bezerra et al. (2019)

81

(Continued)

Crop or Plant

82

TABLE 2.1

Form and Dose of Type of Stress Trace Element

Growth Conditions

Ameliorative Response

Increased activity of SOD shoot and roots; increased osmolytes and antioxidants content; lowered of H2O2 level; regulation of phytohormones Growth Improved photosynthesis, lower signature oxidants, enhanced chamber antioxidative enzyme activities Pot experiment Stimulation of SOD, POD, and CAT enzymes, decreased levels of oxidants

Moradtalab et al. (2018)

Pot experiment Reduced MDA, H2S and H2O2 levels, enhanced SOD and APX enzyme response

Hu et al. (2020)

50 and 100 μM NiCl2

Growth chamber

Khaliq et al. (2016)

Hordeum vulgare L.

56 mg L–1 Na2SiO3 5°C Cold/< 5°C freezing

Hordeum vulgare

1.5 mM Na2SiO3

Euphorbia pulcherrima 75 mg L–1 K2SiO3 Willd. Heavy Metal Stress Gossypium hirsutum L. 1 mM Na2SiO3

High temperature, 7 days 40°C HT or 4°C LT

Brassica napus L.

1.0 mM SiO2

0.5 and 1.0 mM CdCl2

Growth chamber

Pisum sativum L.

1.8 mM Si(OH)4

20 μM CdSO4

Growth chamber

Little Ni accretion, lower levels of free oxygen radicals, enhanced antioxidative enzyme activities Reduced Cd accumulation and oxidants levels, enhanced antioxidative enzyme responses Augmented CAT, POX, SOD, and GR enzyme responses, higher S containing metabolites, alleviation of ROS, lesser Cd accrual

Joudmand & Hajiboland (2019) Hussain et al. (2019)

Hasanuzzaman et al. (2017) Rahman et al. (2017)

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 2

Temperature Stress Zea mays L cv. Colisee 40 mg monosilicic 12–14°C Root Field acid kg−1 soil zone temperature experiment

References

(Continued)

Crop or Plant

Form and Dose of Type of Stress Trace Element

Growth Conditions

Triticum aestivum L.

1 mM Si(OH)4

Growth chamber

Oryza sativa L.

168 mg L–1 Na2SiO3

Hordeum vulgare L.

1.5 mM silicic acid Si(OH)4

Oryza sativa L.

0.50 mM Na2SiO3

Capsicum annuum L.

2.0 mM Na2SiO3

Cannabis annuum L.

2 mM Na2SiO3

Ameliorative Response

Improved performance of antioxidative enzymes like SOD, reduced loss of electrolytes, lower As amassing Enhanced performance of different 100 mg L–1 Growth antioxidative enzymes, GSH content p-arsanilic acid chamber increased, ascorbate concentration (ASA) alleviated while MDA concentration decreased Enhanced ascorbate level and Hydroponic 80 μm stimulation of APX, CAT, SOD, GSH culture NaFeIIIEDTA enzymes, lowered ROS accrual 0.25 and 0.5 mM Pot experiment Lowered Ni amassing, enhanced activities of antioxidative enzymes, NiSO4.7H2O reduced H2O2 and MDA content Greenhouse

Lesser Cd accumulation, augmented 0.1 mM CdCl2 Experiment

antioxidative activities, augmented NO, H2S as well as proline contents, reduced H2O2, MDA content and loss of electrolytes Greenhouse

Decreased boron accretion, activation 2 mM H3BO3 experiment

of different antioxidative enzymes, enhanced H2S, ascorbate, and GSH level, decreased oxidative damage 50 mM As V (Na2HAsO4)

References Hossain et al. (2018) Geng et al. (2018)

Nikolic et al. (2019) Hasanuzzaman et al. (2019)

Trace Elements and Their Role in Abiotic Stresses

TABLE 2.1

Kaya et al. (2020)

Kaya et al. (2020)

83

(Continued)

84

TABLE 2.1

Form and Dose of Type of Stress Trace Element

Growth Conditions

Ameliorative Response

References

Oryza sativa L.

1 mM K2SiO3

10 μM CdSO4

Hydroponic culture

Bari et al. (2020)

Trachyspermum ammi L.

1.5 and 3 mM K2SiO3

1.5 and 3 mM

Greenhouse experiment

Cannabis sativa L.

2 mM Si (H2SiO3) 20 μM cadmium Hydroponic culture (Cd)

Triticum aestivum

3 mmol L−1 Na2SiO3)

Reduced Cd levels, lowered oxidants content, enhanced phytochelatin, cysteine, and glutathione level and activation of common antioxidative enzymes, upregulation of PCS1 gene expression in roots Reduced Cd amassing, lowered content of major oxidants, enhanced anthocyanin content and activities of antioxidants Enhanced WUE via decreased water loss. Improved glutathione and phytochelatin synthesis Improved RWC; increased MSI, reduced Cd uptake, accumulation, and translocation; regulation of antioxidative defense mechanisms

CdCl2

0, 50, 200 μmol L−1 CdCl2

Hydroponic culture

Javed et al. (2020)

Luyckx et al. (2021) Ur Rahman et al. (2021)

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2.2.1 COPPER (Cu) The mineral nutrients are essential to the plants to support typical growth and development in plants, primarily from the soil. At the cell level, Cu is associated with a myriad of biophysiological measures inside the plants like involvement in mobilization of Fe, trafficking of protein, metabolism of cellwall components, mitochondrial respiration, electron transport during photosynthesis, and hormonal signal transduction (Ameh & Sayes, 2019). Within the plants, copper predominately shows two oxidation states, Cu2+ (the oxidation state) and Cu+ (the reduction state) and depending on its oxidation state can bind with different substrates (Ogunkunle et al., 2019). For example, Cu+ as often as possible reconciles with sulfur-containing compounds while Cu2+ ideally unites with imidazole nitrogen as well as oxygen groups (Whitby et al., 2018). Because of its double oxidation state, copper can bind with several organic molecules, for example, proteins (Ghazaryan et al., 2019). It has likewise been seen that copper is able to increase the generation of reactive oxygen species (ROS) via the Fenton reaction because of the dynamic nature of its redox state (Zhang et al., 2020; Da et al., 2019). It additionally behaves as a cofactor of the significant antioxidative catalyst SOD (superoxide dismutase) and controls the propagative chain reactions to detoxify the ROS. So, Cu shows a hermetic effect in plants: beneficial when steady state by attenuating ROS, and inhibitory by enhancing ROS, which can cause oxidative damage to fundamental cell constituents like lipids, proteins, and DNA (Manzl et al., 2004). In plants, Cu is an important constituent of plastocyanin protein, which transfers an electron from cytochrome f to P700+ in chloroplast (Aguirre & Pilon, 2016; Hope, 2000). There are considerable reports from the past pertaining to the crucial roles of copper in the biochemistry of plants. Not long ago, Gong et al. (2019) illustrated that exogenous copper application (100 mg/L) enhanced the plant biomass at low concentration but did not alter the levels of MDA (malondialdehyde), intercellular CO2 concentration, antioxidant enzymes activities, stomatal conductance, transpiration rate and net photosynthetic rate, hence, demonstrating that Cu application at low levels can be beneficial or have little adverse consequences on the growth and development of the plant. On the contrary, high supplemented concentrations of copper (800–1,000 mg/L) showed tremendously harmful on Spinacia oleracea seedlings. Additionally, Copper is deemed a beneficial element for plants at low concentrations due to its redox nature. As a result, copper can regulate growth and development of the plant by regulating the equilibrium of H2O2 that acts as a signaling

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molecule to activate the plant resistance mechanisms (Zhou et al., 2018). Subsequently, Copper stimulates many antioxidant enzymes activities in plants. It has been illustrated that the application of copper at different levels ranging between 0 μM and 800 μM showed variations in growth, protein content, and antioxidative enzymes behavior in plants (Gao et al., 2008). In Jatropha curcas seedlings, greater activities of enzymes were noticed at higher levels of Cu (200–400 μM), which is found to be plant organ-specific. Azooz et al. (2012) noticed that copper supplementation at 2–10 mM concentration showed magnificent improvement in growth and biochemical attributes, and thereafter remarkably decreased with increasing concentration. This suggests that the antioxidant enzymes activities such as APX, CAT, POD, and SOD got improved in concentration-dependent manners (Raldugina et al., 2016). For instance, the supplementation with second metals such as Cu (1.25 μM) significantly combats the Cd-induced toxicity (80 μM), including root rot and browning, oxidative stress, and internal Cd accretion in Catharanthus roseus. Also, the exogenous Cu application lessens the accumulation of most terpenoid indole alkaloids (TIA) (Chen et al., 2018). Recently, the effect of Cu on two barley genotypes with differential cobalt toxicity tolerance was investigated hydroponically to discover the interplay of these two metals. Copper counteracted the cobalt toxicity by antagonistic interaction of the Cu and Co in contrast with the individual metal treatment each, as shown by enhanced growth and photosynthesis, and much lower oxidative stress about a substantial reduction in uptake and transit of Co from the roots to shoots (Lwalaba et al., 2019). 2.2.2 BORON (B) Boron (B) is a vital trace element prerequisite for the normal reproductive and physiological functioning of plants. It has been discovered that B perform many crucial functions of plant for example, maintenance of cell structures and functions, cell wall and membranes structure, cell division, sugar translocation, plasmalemma-bound enzymes, and cytoskeletal proteins, nucleic acid and hormonal regulation, sugar metabolism, respiration, transport of membranes, and translocation and metabolism of other important elements (Herrera-Rodrígueź et al., 2010; Shaban et al., 2019). The plants deficient in boron showed impaired physiological and biochemical parameters, for example, root elongation, transport of sugar, carbohydrate, and nitrogen metabolism, etc., in plants that curtail plant growth and yield (Shaban et

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al., 2019). Boron applied plants yielded better quality fruit and seed by enhancing fertility, growth of pollen tube, and sugar consumption (Blevins & Lukaszewski, 1994). Several studies indicated that exogenous application of boron can alleviate stress by altering physiological and biochemical aspects owing to various abiotic stress conditions. For example, Moeinian et al. (2011) noticed that Boron when applied foliarly alleviates the drought-induced growth inhibition in Triticum aestivum and improved the growth rate of crop, leaf area index (LAI), and net assimilation rate thereby boosting the growth, yield, and quality of grain. Whereas boron foliar sprays enhance maize seedlings’ growth and yield parameters by adjusting the amino acids, proline, phenols, and soluble sugar levels when exposed to salt stress (Salim, 2014). Zhou et al. (2015) noticed that B alleviated the Al toxicity by regulating the genes associated with detoxification of ROS and aldehyde, metabolic activities, cell transport, Ca signaling, and regulation of hormones in Citrus grandis seedlings. Further, B confers a major role in conserving plant cell wall integrity because the cell wall of the plant exhibits the major proportion (70–90%) of copper, zinc, and cadmium, and boron assists in modulating Cd amassing and toxicity in Oryza sativa (Riaz et al., 2021; Chen et al., 2019) and Brassica sps. (Wu et al., 2020a, b). A number of studies were conducted on the beneficial role of Boron in ameliorating aluminum (Al) toxicity in the trifoliate orange plant. Riaz et al. (2018) revealed that B (10 mM as H3BO3) application defends Al-induced toxicity by enhancing root growth, reducing ROS, and Al uptake and accumulation in trifoliate orange plant parts under acidic conditions. Subsequently, the Al-detoxification mechanism by exogenous application of B in roots of the trifoliate orange was studied by Riaz et al. (2018). Boron improved the root growth and physiological attributes in Al-stressed plants by enhancing the activities of antioxidant enzymes such as catalase (CAT), peroxidase, and ascorbate peroxidase (APX) while lowering H2O2, MDA, and Al concentration in roots and leaves in rapeseed (Brassica napus L.) (Riaz et al., 2018). Further, the study was also carried out to explore the Al-stress alleviating role of B in Poncirus trifoliate roots by altering cell wall structure and minimizing the allocation of HG epitopes which ultimately limit Al3+ accumulation (Riaz et al., 2018). Later on, in Poncirus trifoliate (L.) rootstock X-ray diffraction (XRD) and Fourier transform infrared spectroscopy (FTIR) techniques were deployed to analyze the Al-induced alterations of cell wall components and found that boron counteracts the

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Al-phytotoxicity by protecting the possible binding sites of Al thereby diminishing Al-mediated modifications in the cell wall components such as pectin and cellulose (Yan et al., 2018). In the following year, Yan and coworkers (2019) suggested that B helps in regulating the AsA-GSH cycle thereby reducing the amassing of metabolites produced in the L-galactose pathway of ascorbic acid (AsA) synthesis in trifoliate orange roots against Al-induced oxidative stress. Under drought stress (DS) conditions, foliar sprays of B to wheat plants effectively increase the chlorophyll and carotenoid content and lower the stress signs such as H2O2 and proline content which eventually improve growth and yield (Abdel-Motagally & El-Zohri, 2018). Chen et al. (2019) revealed that the supplementation of boron (B), silicon (Si) in hydroponically grown rice plants and their mixture reduce the Cd accretion. The stress alleviating role of B and Si was attributed to reduced oxidants content such as O2−, H2O2, and MDA, and stimulation of major antioxidant enzymes activities. Whereas Yousefi and his coworkers (2020) reported that boron exogenous application (40–60 mM) helped rose plants improve relative water content (RWC), leaf area, and soluble carbohydrate contents in leaves, thereby maintaining the osmotic potential which is a prerequisite for plant performance under salt stress. Recently, enhanced photochemical efficiency of PSII and lower oxidative damage in rice seedlings were observed with sprays of B compounds under high-temperature stress (Calderón-Páez et al., 2021). 2.2.3 NICKEL (Ni) Nickel (Ni) is pervasive and recognized as a profoundly significant trace element. Its importance has been recognized lately owing to its function as a catalyst of the enzymes, for instance, urease, methyl-coenzyme reductase, SOD, acetyl-CoA synthase, carbon monoxide dehydrogenase (CODH) and hydrogenase enzyme (Fabiano et al., 2015). This element has its narrow window of essential, beneficial, and toxic concentration in plants and also varies with the plant-to-plant species. Several studies have discovered the stress alleviating role of Nickel to diverse abiotic stresses (Fabiano et al., 2015; Ameen et al., 2019). For instance, Ni plays an important role in activating OsGLY11.2 (glyoxalase I isoform), performing a crucial function in the degeneration of methylglyoxal (MG) (Mustafiz et al., 2014), a toxic compound that increases manifolds under a different type of stresses. The detoxification of

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MG occurs through activation of the glyoxalase system involving glyoxylase I and glyoxylase II enzymes. In the case of metal stress tolerance, nickel sustains reduced glutathione’s (GSH) redox state, which can act as a strong antioxidant. Fabiano and his coworkers (2015) demonstrated that Ni assists the antioxidant metabolism by maintaining the MG cycle and reduced GSH homeostasis, particularly in stressful environments (Fabiano et al., 2015; Hasanuzzaman et al., 2018). Salinity results in osmotic stress caused by ion toxicity, disturbance in homeostasis of Na+ concentration and other vital ions (Amjad et al., 2014), and activation of oxidative stress which leads to the formation of free oxygen radicals in the cell (Amjad et al., 2015; Ludwiczak et al., 2021). It has been illustrated that exogenous Nickel supplementation in a growth medium counteracts the absorption of Na+ ions and helps the plants to absorb K+ ions. Furthermore, a combative relationship between Na+ and Ni2+ uptake at a high concentration of Ni was noticed which leads to a decline in Na+ concentration in plant tissues. This recommends the divalent nature of Ni (Ni2+) ions which is more ideal over monovalent ions of Na+. Moreover, the presence of high levels of Ni2+ in the growth media upholds the uptake of K+ ions to adjust the decrease in Na+ uptake (Ain et al., 2016; Imtiaz et al., 2016). Nickel is the key constituent of the urease enzyme, which is vital for the catalysis of urea and arginine. The urease enzyme activity urease enzyme activity gets impaired in Ni deficient legumes and other dicotyledons, leading to necrosis on leaf margins. On the contrary, the mobility of Ni ions increases with the increase in moisture content in soil (Seregin & Kozhevnikova, 2006). Under drought conditions, decreased Ni uptake and inhibition in embryonic growth were observed in maize (Hordeum vulgare L.). Additionally, there were deformities in the endosperm due to decreased activity of the dehydrogenase enzyme. It has been proposed that nickel deficiency modifies nitrogen’s metabolic function and impaired urease enzyme functioning, which is the major cause behind the amassing of harmful urea in plant shoots under water-stressed conditions (Seregin & Kozhevnikova, 2006). The studies suggest that Ni generates hermetic effects in plants which is dose-dependent; at low application levels, it benefits in plant growth and development, while application at high levels of Ni causes growth retardation. However, there is still a gap in the knowledge about mechanisms of Ni essentiality and its stress mitigating roles in plants at the cellular, physiological, molecular, and genetic levels compared to other vital nutrients.

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2.2.4 ZINC (Zn) Zinc (Zn) is considered an essential micronutrient for plants as it is an integral component of several major enzymes and TFs (transcription factors) participating in the nucleic acids and lipids synthesis and metabolism. Moreover, zinc assists chlorophyll synthesis, biomass production, functioning of pollen, and fertilization processes of plants (Hafeez et al., 2013; Umair et al., 2020). For instance, Zinc at supra optimal levels (1–2 μM) facilitates the growth of the plant by increasing chlorophyll and crude protein content (Samreen et al., 2017). Waraich et al. (2011a, b) illustrated that zinc maintains water use efficiency (WUE) thereby helps in conferring DS tolerance. They found that Zn elevated the auxin levels in the plant by increasing the tryptophan (auxin precursor) content, hence promoting the root’s growth in drought conditions. Moreover, Zn downregulates the functioning of membrane-bound NADPH oxidase, thereby decreasing the ROS formation and enhancing antioxidative enzyme activities, for example, SOD, CAT, and peroxide dismutase (Px) to safeguard cells from oxidative injury under water stress. Zinc in trace amounts promotes the growth of plants and aids in mitigating salt-stressed conditions. In pistachio seedlings growing under saline conditions, application of Zn decreased the salt-induced oxidative stress by eliminating the major oxidants (H2O2, MDA, and lipoxygenase activities) via increasing the antioxidative enzymes (APX and CAT activity; Tavallali et al., 2010). Exogenously applied zinc improved fresh and dry weight, proline content, and SOD, CAT, and GST activities in sunflower leaves when subjected to salinity (Ebrahimian & Bybordi, 2011; Hasanuzzaman et al., 2018). Studies showed that zinc at its moderate range (1 mmol/L) along with NaCl (1%) acted synergistically to improve the yield in Spartina densiflora (Redondo-Gomez et al., 2011). Later on, Jan et al. (2017) demonstrated that zinc supplementation enhances the salinity tolerance in wheat plants by lowering the oxidative stress thus improve root, shoot, and spikelet growth. Moreover, the levels of osmolytes, total phenolics, total sugars, photosynthetic pigments, non-enzymatic antioxidant (Proline) content, and enzymatic antioxidants (SOD, CAT, and ascorbate peroxidase) activities were found to be greater in the Zn-applied salt-stressed plants as compared to the control. Under saline conditions, the efficacy of AsA and zinc when applied foliarly was quantified on the physio-biochemical parameters in barley (Hordeum vulgare L.). In combination, fertigation with AsA and Zn imparts salt stress tolerance and resulted in enhanced photosynthetic pigments, vegetative growth, synchronized ion uptake, and enzymatic and

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non-enzymatic antioxidants levels and harvest index in barley (Noreen et al., 2021). Lately, Al-Zahrani and his coworkers (2021) reported that the role of zinc (Zn) in salt stress mitigation and growth promotion varies to a great extent in the mungbean. Zn supplementation at 250 µM concentrations improved the activities of phenylalanine ammonia-lyase (PAL) and tyrosine ammonia-lyase (TAL) which bring on the secondary metabolism and resulted in the enhancement of total phenol and flavonoids. Furthermore, the scavenging activities of hydrogen peroxide (H2O2) and superoxide radicals were enhanced with the application of zinc in mungbean plants subjected to salt stress. Little work has been performed to investigate the role of zinc in providing resistance to abiotic stresses till now. Further, there is a need to investigate the potential approaches to enhance the Zn-induced abiotic stress tolerance and unravel the mechanisms of interplay between Zn and other nutrients. 2.2.5 SILICON (Si) Silicon (Si) is the second most extensive element after oxygen in the earth’s crust and is present abundantly in the form of silicate or Al silicates in soil. According to Epstein (1994), silicon ranges between 0.1 mM and 2.0 mM (pHtomato). It is an energy-dependent transport as metabolic inhibitors and low temperature impedes transport (Ma et al., 2004; Mitani & Ma, 2005; Tamai & Ma, 2003). Silicon has been transported from cortical cells to the xylem (i.e., xylem loading) and the concentration of silicon in the xylem sap is considerably higher in rice than cucumber and tomato. Moreover, the transporter mediates the xylem loading of Si in rice, whereas the loading of the xylem with Si is mediated by diffusion in tomato and cucumber. Due to this, the result concludes that xylem loading is the chief determinant for a high level of Si and so, in rice, a high level of Si is accumulated in shoots and a very little level of Si is accumulated in cucumber and tomato. This is due to the lower density of the transporter to transport Si from the outer solution to the cortical cells and the absence of transporter to transmit Si from cortical cells to the xylem (Ma et al., 2004; Mitani & Ma, 2005; Tamai & Ma, 2003). From here, we can conclude that the uptake of silicon involves two processes, i.e., the first is radial transport of Si from the outer solution to the cortical cells, and the second is the discharging from the cortical cells into the xylem (Mitani & Ma, 2005). In case of uptake of Si from roots, with the help of the xylem, it is transported to the shoots. When the concentration of silicic acid surpasses

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2 mM, it polymerizes to form silica gel (SiO2.nH2O) and due to this, a high concentration of silicic acid is present in xylem sap. In some plant species like rice, the concentration of silicon in the xylem is much higher than 2 mM, despite the major form of Si being present as monomeric silicic acid. In the shoots, loss of water leads to the formation of more concentrated silicic acid and is polymerized. The Si polymerization transforms silicic acid into silica gel with increasing silicic acid concentration. In the shoot of the rice plants, more than 90% of total Si is present as silica gel. The Si distribution in shoots is controlled by transpiration and older tissues acquire more Si because it is not mobile within plants (Ma et al., 2011). Figure 6.1 represents how silicon uptake by the plants from the soil, where Lsi1 (low Si 1) is a bidirectional protein channel function as influx transporter of Si and Lsi2 (low Si 2) helps to transport Si out from the plant cell across plasma-membrane by an energy-dependent process (increasing proton gradient). Actually, both the transporters (Lsi1 and Lsi2) facilitate the active transporter of Si.

FIGURE 6.1

Effect of silicon on heavy metal toxicity.

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6.5 GENE CONTROLLING SILICON UPTAKE IN RICE Low silicon rice (Lsi1) is the major transporter of Si into rice roots. The gene is composed of 5 exons and 4 introns, the complementary DNA of this gene is 1,409 base pairs, and the deduced protein is comprised of 298 amino acids (Ma et al., 2006). It is said that this gene encodes for a membrane protein that is somewhat similar to water channel protein, i.e., aquaporins (AQPs), the amino acid sequence consists of 6 transmembrane domains and two Asn-Pro-Ala motifs. Lsi1 was principally expressed in the roots, mainly in main roots and also in lateral roots but does not show its expression in the root hairs. From the research, it can be said that on a distal side of exodermis and endodermis a transport protein is situated on the plasma membrane, where Casparian strips exist. Passage of solutes through Casparian strips is difficult, so transporters are required to reach the stele for translocation from the roots to the shoots (Ma et al., 2006). Suppression of gene Lsi1 causes a reduction in the Si uptake, so, when cRNA-encoding Lsi1 was injected into Xenopus laevis oocytes there was an increased level of Si demonstrating Lsi1 as a major transporter (Ma et al., 2006). 6.6 ROLE OF SILICON AGAINST BIOTIC AND ABIOTIC STRESS In higher plants, Silicon is considered as an essential element because its deficiency causes various abnormalities in plants, and thus it can be said that Si shows beneficial effects on plant growth. Silicon is probably the only element that can strengthen the resistance against various multiple stresses. Silicon can protect plants from abiotic and biotic stresses (Tripathi et al., 2014). According to various studies, Si is effective in controlling the disease caused by fungi and bacteria in different plant species. Following are the types of mechanisms for Si-enhanced resistance to diseases and they are: (i) acts as a physical barrier; and (ii) modulates the host resistance to pathogens and the induction of phenolic compounds, phytoalexin/peroxidase/glucanase production, and it also regulates the pathogenicity or gene expression of stress-related to limit pathogen invasion and colonization (Belanger et al., 2003; Brunings et al., 2009; Chain et al., 2009; Sakr, 2016). 6.6.1 EFFECTS OF SILICON AGAINST ABIOTIC STRESS Silicon reduces abiotic stress including physical stress such as (drought, lodging, radiation, high temperature, UV, freezing, etc.), and chemical stress such as metal toxicity, salt, nutrient imbalance, and so on (Ma & Takahashi,

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2021). Silicon in response to the physical and chemical stresses are as in subsections. 6.6.1.1 ROLE OF SILICON IN RESPONSE TO PHYSICAL STRESS Owing to this abiotic stress, more than 50% of the crop losses occur worldwide (Allahmoradi et al., 2011; Wang et al., 2003) and due to this, the major physiological process such as respiration, translocation, photosynthesis, ion uptake, stomatal behavior, conductance, transpiration rate, seed germination, water relation, and mineral nutrition is affected. Silicon reduces the consequence of physical stresses, including radiation, low and high temperature, wind, drought, and waterlogging, low, and high light, and so on (Ma, 2004). The role of silicon against diverse physical stresses are discussed in subsections. 6.6.1.1.1 On Radiation Damage Due to depletion in the stratosphere ozone layer, an increase in the UV-B radiation, affect physiological processes such as growth, seed germination, photosynthesis, mineral elements, water balance, and other metabolic processes which cause negative impacts on crop production (Alexieva et al., 2001; Brown et al., 2005; Riquelme et al., 2007; Shen et al., 2010). The effect of UV-B radiation in the environment increases severe injury to plants tissues which further leads to the reduction of crop yield and quality in worldwide (Correia et al., 1999; Costa et al., 2002; Kakani et al., 2003; Riquelme et al., 2007). For example, if 30-day old rice seedling were irradiated with gamma rays, we can observe, the decrease in the dry weight was less noticed in the Si-supplied plant as compared to those in Si plants that had not been treated with Si, and hence this proves that presence of Si increases the resistance of rice against radiation stress (Takahashi, 1966). The exogenous application of Si decreases UV absorbance in the leaf blades of rice plants. Due to decreases in the level of phenolic biosynthesis, Si is accumulated in the plant leaves. This proves that the exogenous activity of Si increases the silica deposition in the rice plants, reducing the CAD activity, and ferulic and p-Coumaric acids which are connected to the changes in the UV defense system (Gotoa et al., 2003). Lsi1 gene regulates the UV-B tolerance in rice plants because exogenous application of Si increases the rate of accumulation of Si and activates the photolyase and associated antioxidant enzyme,

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which increases the repairing ability of DNA and decreases the injuries bring out by radiation. Severe damage is caused to soybean plantation by UV-B radiation, causing damage to the membrane, as evaluated by lipid peroxidation (LPO) and osmolyte leakage (Shen et al., 2010). In this case, Si plays a protective role by increasing the photosynthesis, growth, and antioxidant compound in wheat seedlings, intolerance against UV-B stress (Yao et al., 2011). Si enhances the translocation of K and Ca (mineral elements) and increases the dry mass production against UV B stress (Shen et al., 2009). In addition, when Si is supplied to plants it shows a faster recovery rate against radiation tolerance than non-supplied plants (Takahashi, 1996). 6.6.1.1.2 On Drought Stress (DS) Drought stress (DS) is also one of the major issues that is facing the world and it shows harmful and several deleterious effects on plant growth and metabolic processes such as water relations, nutrients uptake, decrease in photosynthetic pigments, and photosynthesis of plants (Cattivelli et al., 2008; Xiong et al., 2012). It leads to the closure of stomata and successive decreases in photosynthetic rate. According to the report, DS/water stress causes a decrease in the photochemical activities, and it inhibits the activity of the enzyme of the Calvin cycle (Monakhova & Chernyadev, 2002). It has been extensively reported that silicon increases the drought tolerance in plants such as wheat, rice, cucumber, sorghum, maize, sunflower, etc. Sometimes DS is caused due to high temperature and in that case, silicon increases the tolerance of heat stress by maintaining membrane stability (Ma et al., 2001a). Silicon application can notably improve the water status in non-irrigated crops because when the plants are exposed to drought conditions, the water content and water potential of the leaf decrease at the same time. The water deficit stress caused in wheat plants when exposed to polyethylene glycol (PEG) can be improved by adding silicon (Pei et al., 2010). Factors such as transpiration rate and stomatal conductance affect the plant water relations. In maize plants, silicon decreases the transpiration rate of plant leaf and water flow rate in xylem vessels and improves water use capability. So, according to the researchers, the decrease in transpiration rate is caused due to the formation of a silica cuticle double layer on the epidermal tissue of the leaf. The cuticular rate of transpiration is slow than the stomatal transpiration rate. The addition of silicon does not change the transpiration and conductance

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rate from the cuticle of leaves, but it decreases the rate and conductance from the stomata, which shows that silicon is involved in stomatal movement (Gao et al., 2006). Thus, reduction in the rate of transpiration is the mechanism for the observed silicon-mediated increase in drought tolerance (Zhu & Gong, 2013). The negative impact of silicon can also be observed in potted sorghum plants under DS by increasing the rate of transpiration and stomatal conductance of leaves (Hattori et al., 2005). In cucumber, the addition of silicon does not influence the rate of transpiration or stomatal conductance nonetheless whether osmotic stress was applied. Enhancement of silicon-mediated drought tolerance increases the antioxidant defense capability of the plant and alleviates oxidative damage. The number of non-enzymatic antioxidants is influenced by the application of silicon. One of the main antioxidants in plant cells is glutathione (GSH), which is several non-protein thiols. The toxicity of reactive oxygen species (ROS) caused due to drought can be reduced by increasing the content of non-enzymatic antioxidants. For example, in wheat plants, silicon partly nullifies the negative impacts of drought by increasing the activities of superoxide dismutase (SOD), glutathione reductase (GR), and catalase (CAT) (Gong et al., 2005). Whereas, on the other hand, it decreases the hydrogen peroxide (H2O2) content, acid phospholipase activity, and oxidative damage of protein (Gong et al., 2005). From the observation, it can be concluded that in drought-stressed wheat plants, silicon reduces phospholipid de-esterification, as hydrolysis of phospholipids does not take place due to a decrease in the activity of acid phospholipase. In drought-stressed wheat plants, it is observed that the addition of silicon increases the activity of GR and moderately increases the ascorbic acid (AsA) concentration in the leaves (Pei et al., 2010). Hence, these results show that silicon is involved in balancing the antioxidant defense mechanism and thus alleviating the oxidative damage in drought-stressed plants (Zhu & Gong, 2013). Water deficiency restricts the nutrient uptake through roots, shoots, and causes a reduction in nutrient availability and metabolism (Farooq et al., 2009). As we all know, the level of Ca is responsible for the expression of osmotic stress-responsive genes (Mahajan & Tuteja, 2005; Zhu, 2002) and on the other hand, osmotic adjustment is maintained by K+ ions (Ashraf et al., 2001). In the case of water-stressed maize leaves, the addition of silicon leads to the increase in the level of Ca2+ and K+. According to the report, silicon decreases the level of Ca2+, K+, and Mg2+ under water-stressed wheat shoots caused by 20% PEG (Pei et al., 2010). The concentration of all these minerals in shoots increases to improve the dry matter content of the shoot

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by the addition of silicon. The addition of silicon increases the consumption of K+ and Ca2+ to be assigned to a reduction in plasma membrane permeability and an increase in plasma membrane H+-ATPase activity (Kaya et al., 2006; Liang, 1999). In the xylem sap of maize, it is reported that the addition of silicon decreases the phosphorous uptake (Miyake, 1993). Silicon also increases the rice grain yield as well as nitrogen use efficiency (NUE). The addition of silicon in the culture solution enhances the root water uptake during water deficit conditions by accumulating soluble sugars and amino acids. During stress conditions, solute such as proline plays an important role in osmotic adjustment (Nayyar & Walia, 2003). Whereas, on the other hand, researchers consider that increase in the level of proline shows the symptoms of injury rather than a source of stress tolerance. In wheat leaves, the level of proline increases during water stress and the concentration of proline decreases by the addition of silicon (Pei et al., 2010). Hence, this shows that accumulation of proline is a symptom of stress-related injury. When we grow plants in soil culture and are subject to drought, then they have longer rooted with great surface area to increase the access to water, whereas, in the solution culture, plants frequently respond to water stress by enhancing their internal hydraulic conductivity in the water flow pathway because roots are always in contact with water. The contribution of cuticular transpiration to overall transpiration also shows some effect. Like in the case of rice, the contribution of cuticular transpiration is ∼25–39% of total transpiration (Matoh et al., 1991), 20–40% in barley (Millar et al., 1968), and up to 50% in Acer syriacium and Rhododendron poticum (Whiteman, 1965). Hence, this is the reason for the differential impact of silicon on stomatal conductance and rate of transpiration. When plants are exposed to major water deficiency then a reduction in the rate of photosynthesis is caused due to the closure of stomata, and this leads to the decrease in the CO2 influx. Many discussions are made on this stomatal closure by researchers. According to Meyer & Genty (1998), in Rosa rubiginosa, reduction in the photosynthetic rate was not mainly due to CO2 deficiency. Whereas Gong et al. (2005) suggested that the stomatal factor is not the major factor that inhibited the photosynthesis in drought-stressed wheat, as neither drought nor silicon treatment particularly affected the internal concentration of CO2 under their experimental conditions. When experiments are done with soilgrown rice, Chen et al. (2011) said that both factors such as stomatal and nonstomatal conditions are associated with silicon-mediated improvement in photosynthesis during drought conditions. In addition, it has been reported that in stomatal movement, photosynthetic pigments are affected by silicon

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addition. Silicon mediated help in the improvement of chloroplast ultrastructure, and increases the activity of antioxidant enzymes such as CAT, and SOD which in turn regulates the activity of photosynthetic enzymes like ribulose-bisphosphate. It also helps in increasing the basal quantum yield (FV/F0) and maximum quantum efficiency of photosystem II in plants like rice during drought conditions (Gong et al., 2005; Liang, 1998). The addition of Silicon enhances the growth of roots during drought conditions. In drought-stressed Sorghum, the ratio of shoot/root ratio is lower, and root dry mass accumulation is higher in plants treated with silicon, which shows that silicon promotes root growth during drought conditions (Hattori et al., 2005). Due to magnified cell wall extensibility in the growth zone adding silicon, is a major factor for enhanced root elongation (Hattori et al., 2003). Nutrient uptake by roots depends on the surface area and length of the roots because the larger the surface area more will be the intake of diffusible ions (Barber, 1984). Silicon increases the drought tolerance and nutrient absorption of plants. Sometimes the addition of silicon leads to the increase in water uptake during drought conditions is due to the enhanced hydraulic conductance of roots (Chen et al., 2011; Hattori et al., 2008a; Sonobe et al., 2011). Therefore, silicon plays an important role in maintaining the uptake, transport, and distribution of minerals in drought-stressed plants. 6.6.1.1.3 On Climatic Stress Climatic stress such as low temperature, typhoons, an inadequate amount of sunshine causes heavy damage to the crops (Ma et al., 2001a). High temperature affects the metabolic pathways causing extremely oxidative damage to cells and affects both primary and secondary metabolism. The addition of silicon helps in alleviating the damage caused by climatic stress, like typhoons, which causes lodging and sterility in rice plants leading to a considerable reduction in the rice yield. Silica deposition in the rice increases the thickness of the cell wall and the size of vascular bundles, which increases the strength of the stem, thus preventing lodging (Shimoyama, 1958). Deposition of silicon on the husks helps in preventing excess water loss because due to strong winds excess water loss takes place from the spikelets, which in turn results in sterility (Ma, 2003). Plants were grown in both tropical and subtropical conditions, of which sugarcane shows the most drastic response to cold stress leading to the changes in the photosynthetic parameters (Inman-Bamber et al., 2010). Therefore, plants like sugarcane

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show the impact of cold stress, which causes drastic changes like reduction in photosynthetic parameters, and activities of photosynthetic enzymes such as sucrose, NADP-malate dehydrogenase, pyruvate orthophosphate, phosphate synthase, and dikinase decreases during cold stress (Du & Nose, 2002). The content of aspartate and alanine in sugarcane leaves increases during cold stress (Du et al., 1999). Effects of high temperature on sugarcane lead to the reduction in biomass increase in the number of tillers, shorter internodes, and drying of older leaves. There is an increase in the levels of glycine betaine, soluble sugars, proline, flavonoids, and carotenoids during plant stress is important for mitigating the heat stress in the crop (Wahid & Close, 2007). Maintaining a proper temperature will be considered as an important parameter for the growth of plants, crop production, and development in near future. 6.6.1.2 ROLE OF SILICON IN RESPONSE TO CHEMICAL STRESS A significant amount of work is done on the effects of Si under chemical stresses, including nutrient imbalance, metal toxicity, salinity, and so on. Silicon helps in alleviating the damage caused by excess of chemicals such as phosphorous, Al, etc., and plays a crucial role in maintaining stability and increasing the nutritional value of primary products (Ma, 2004). 6.6.1.2.1 Effect of Silicon in Deficiency in or Excess of Phosphorous The deficiency of phosphorous (P) in the soil is a major worldwide problem. The advantageous effects of silicon can be seen in P deficiency caused in many plants like rice and barley (Ma, 2003). Previously it was believed that partial substitution of silicon is used to enhance the P availability in soil. But later on, after conducting many experiments it was concluded that the addition of silicic acid at various concentrations does not affect the P availability or fixation capacity of soil because, in soil solution, silicon in the form of silicic acid does not undergo dissociation at below pH 9. Whereas uptake of Fe and Mn decreases in silicon-treated plants (Ma et al., 1990). As we know that phosphorous is translocated and redistributed in plants in an inorganic form and as P shows high affinity with metals such as Mn, Fe, when the concentration of P is low, the level of Mn, Fe, and other metals control the level of internal availability of P. Plants growing under P deficiency stress, the addition of silicon is used to enhanced availability of internal P

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by decreasing excess Fe and Mn uptake (Ma, 2003; Nagaoka, 1998). An experiment was conducted in the field of barley, in which both the field is not treated to P fertilizer application. In one part of the field, Si application is applied, whereas in the other part it is not applied (Fisher, 1929). It is found that the part supplied with Si has a higher yield as compared to that of a field without Si treatment (Ma & Takahashi, 1990a). The useful effect of silicon is seen in many graminaceous species like rice, wheat, and maize. Silicon is applied in the form of sodium silicate or calcium silicate, and it increases the pH of the soil. In the case of acidic soil, Al toxicity is the major cause of factors limiting crop growth. So, if the pH value of soil is at or below five, then all the Al ions solubilized into the soil solution thereby inhibiting root growth and function, which in turn cause severe water impairing and nutrient acquisition by roots and hence leading to a significant reduction in crop yields. When the pH of the soil is increased by the application of the silicon, it improves the growth condition of roots of plants suffering from Al toxicity, which results in increased transpiration and, greater P uptake and utilization (Owino-Gerroh & Gascho, 2005). Excess of P is also not good for plants. P accumulation is essential for metabolism and plants storage, but a high level of P stops the enzymatic reaction and produces abnormal osmotic pressure, and decreases the amount of availability of essential metal elements in cells. For example, an increase in the level of P application decrease zinc uptake and bioavailability. Deficiency of zinc induced by P leads to some symptoms in plants like leaf necrosis and chlorosis. Zinc is one of the important nutritional sources (cereal grains and vegetables), so a decrease in levels of zinc in plants can cause insufficient Zn intake in humans (Cakmak & Marschner, 1987). To decrease the damage caused by an excess of P, Si is used, but due to this reduction in P uptake has occurred which decrease the concentration as well as accumulation of inorganic P in some plant species. The formation of cuticle-silica double layer during such event is due to deposition of Si in leaves reducing the plant transpiration rate or it could be due to the deposition of Si in endodermal cells of plant roots, which contribute to decreased P uptake, and alleviation of excess P stress (Ma & Takahashi, 2002). Another explanation for such an event is apoplastic barriers formation for P permeability across roots caused by deposition of Si in roots, which reduce the excessive uptake of P (Lux et al., 2003). The transpiration rate in rice plants is negative, corresponds to the SiO2 content in the aerial parts of the rice plants, thereby decreasing the transpiration rate between 20% and 30% (Ma & Takahashi, 2002). Hence, this shows that positive co-relation takes place between P content in the plant leaf and the

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rate of transpiration (Cernusak et al., 2011). Many of the plant species show less Si accumulation in their organs. Therefore, Si takes part in maintaining the regulation of responses of plants to excess P stress in other ways. Plants have developed different strategies to tolerate the deficiency of P-stress like secretion of organic acid anions (e.g., citrate, oxalate, and malate), by roots of plants. A strong application of Si stimulates the secretion of malate as well as citrate by roots and the amounts of anions liberated by roots are higher than in other tested treatments. It has been found that Si regulates the expression of the genes for the growth of plants under abiotic stress. Si decreased P uptake and accumulation in rice by downregulating the P transporter gene OsPHT1 six in roots. The expression of OsPHT1; six was decreased by the accumulation of Si in the shoot thereby decreasing the Pi uptake in rice (Hu et al., 2018). This study proves that Si helps in alleviating the damage caused by excess P and Si plays an important role in lowering the P content to sustain P balance and increases the nutrient value of primary products. 6.6.1.2.2 Ameliorative Effect of Silicon on Aluminum (Al) Toxicity Aluminum (Al) is a very common element, yet the toxicity of Al is the major growth-limiting factor for plant growth in acid soils. Ionic Al stops the growth of roots and nutrient uptake (Ma et al., 2001b). Impact of Al toxicity has been observed in Sorghum, maize, barley, rice, soyabean (Cocker et al., 1998). Although silicon is used to alleviate the effect of these plant species. Symptoms that occur during Al toxicity are the appearance of P and Ca deficiency in foliage and restricted root system with characteristically stocky and brittle roots (Foy et al., 1978). The formation of inert hydroxy aluminosilicates takes place in the soil solution to protect the plants from the destructive effects of Al. In tomato, plants grown in the greenhouse, it is observed that treatment with Si decreases the Al and Mn uptake into the tissues (Birchall & Chappell, 1988a, b). Two types of mechanisms are involved in the ameliorative effect of silicon on Al toxicity and the mechanisms are Solution chemistry and Planta mechanisms. Silicon decreases the level of toxic Al3+ concentration in a solution by forming Al-Si inactive HAS complexes (hydroxy aluminum silicates). The formation of the Al-Si complex depends on the pH and concentration of Al and Si. Low pH and low concentration of Al and Si are not beneficial for the formation of a complex in the nutrient solution. However, in the case of apoplast of root apex, high pH with high Al and Si concentration forms HAS complex (Ma,

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2005). High uptake of Al by roots inhibits the root elongation. Therefore, in the presence of Si, there is a decrease in Al uptake by roots. Many other mechanisms are proposed for the alleviative effect of Si on Al toxicity like solution effects, co-deposition of Al-Si, effects in cytoplasm or enzyme activity (Cocker et al., 1998), or indirect effects. The alleviative effect of Si on Al toxicity varies differently with different plant species, which may be due to differences in Al tolerance and/or differences in the mechanisms involved, the difference in the solution, or nutrient medium, in the initial Si state of the plants used, in plant age and development, and between cultivars. 6.6.1.2.3 Effect of Silicon on Salinity Stress Salt stress is the major cause of the environmental limiting factor for the growth of plants and crop production. An increase in the high osmotic potential of a soil solution leads to water deficiency in the plant cells and increases the concentration of certain ions such as Na+, Cl– that cause ion toxicity further leading to too much secondary stress such as nutritional deficiency and oxidative stress (Soylemezoglu et al., 2009; Yue et al., 2012). An increase in salt concentration affects the ion balance in plants. Water deficiency, which is caused by salt stress leads to the excessive production of ROS like superoxide anion, hydroxyl radical, H2O2, and singlet oxygen, and each of these can interrupt the normal metabolism (Zushi et al., 2009), which leads to the damage of the plasma membrane and endomembrane system (Gill & Tuteja, 2010; Liang, 1999). With the help of antioxidants such as GPX, SOD, ascorbate peroxidases (APX), CAT, dehydroascorbate reductase (DHAR), and GR defense system in plants, having both enzymatic and non-enzymatic constituents, they can hunt down the ROS. The major antioxidant scavenger is SOD as it converts superoxide to H2O2. Further on this H2O2, which is cytotoxic, is broken down into a variety of peroxidases with the help of CAT (Zhu et al., 2004; Soylemezoglu et al., 2009). Nonenzymatic antioxidants are GSH, nonprotein amino acids, AsA, and phenolic compound (Alaghabary et al., 2004; Gill & Tuteja, 2010; Hashemi et al., 2010; Kumar & Bandhu, 2005). According to the report, silicon decreases the concentration of malondialdehyde (MDA), which is the end product of membrane LPO which is mediated by ROS and is regarded to be a very damaging process caused in species like barley (Liang et al., 2003), maize (Moussa, 2006), and the addition of silicon decrease the LPO which helps in maintaining the membrane integrity and decrease plasma membrane

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permeability (Gill & Tuteja, 2010). The addition of silicon affects the antioxidant activity when added to growth media as it enhanced the activity of SOD leading to a decrease in the level of H2O2 under salt-stressed plants like tomato, maize, and cucumber (Al-Aghabary et al., 2004; Moussa, 2006; Zhu et al., 2004). As observed in wheat, silicon amplifies the activity of H+-ATPase activity of plasma membrane (Liang et al., 2006b), which leads to the decrease in oxidative damage to the protein during salt stress. The Liang et al. (2006b) put forward an observation that silicon can affect the membrane fluidity and enzyme activity indirectly since the addition of silicon does not affect membrane fluidity and H+-ATPase activity in in-vitro plants not treated with salt (Liang et al., 2006b). Silicon helps in the reduction of the damage which is caused during salt stress to protect the photosynthetic apparatus by decreasing the uptake of Na+ and increasing the uptake of K+ in salt-stressed plants. In wheat plants, the addition of silicon increases the level of chlorophyll during salt stress. In barley, silicon increases the level of chlorophyll and the photosynthetic function of leaf cell organelles with or without salt stress (Liang et al., 1996; Liang, 1998). These kinds of effects are also seen in tomato plants under salt stress. An increase in the concentration of salt leads to the increase in uptake of some Na+ and Cl– and decrease in uptake of K+ and Ca2+ (Guerrier, 1996; Khan et al., 2000; Wang & Han, 2007), which is very harmful to plants as it affects the cellular metabolism, leads to reduced plant growth, and excessive production of ROS (Mahajan & Tuteja, 2005). Due to all the events, silicon plays an important role in maintaining the balance of ions and protecting the plants from damage by decreasing the uptake of Na+ and increasing the uptake of K+ (Liang & Ding, 2002). In rice, silicon decreases the uptake of Na+ from shoots but not from the roots of salt-stressed plants (Gong et al., 2006). According to Gunes et al. (2007a), it is suggested that silicon decreased the translocations of Na+, Cl–, and also boron translocation from the roots of plants to its shoots in tomato plants when grown in sodic-B toxic soil. The addition of Si increases the activity of plasma membrane H+-ATPase’s, which facilitate the Na+ export from the cells as its compartmentation, is a very necessary mechanism for plants to prevent Na+ toxicity because Na+ can be used as an osmoticum to help maintain osmotic homeostasis (Blumwald, 2000; Zhu, 2001). In rice roots, induction of Siacts as a physical barrier as they are deposited on the exodermis and endodermis of the roots, which decreases transpirational bypass flow and Na+ accumulation. As lateral roots lack exodermis, the addition of Si enhances exodermal development in rice. Therefore, these depositions contribute to a reduction in the filling of salt

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ions into the xylem of the root, resulting in decreased salt ion accumulation in shoots. Sometimes this mechanism may not work in some species like grapevine (Gong et al., 2011). In tomato leaves, the inclusion of Si does not show any effects in the concentration of Na+ and Cl– but enhances the water storage in plants. High water accumulation contributes to salt dilution, thereby reducing salt toxicity and improving plant growth (RomeroAranda et al., 2006). As we all know, during salt stress conditions, there is an increase in the level of ROS scavenging enzymes, which cause greater lignin biosynthesis, which in turn hinders plant growth (Ortega et al., 2006). The addition of silicon decreases the lignin content in canola (Hashemi et al., 2010). According to Hattori et al. (2003); and Maksimović et al. (2007), Si can reduce lignification in tissues and may promote cell wall loosening and extensibility and promote further plant growth under salt stress conditions. The addition of Silicon also leads to the formation of Casparian bands in rice root in the exodermis and endodermis region, and the accumulation of lignin in sclerenchyma cells and all the modification leads to a decrease in the reduction of oxygen radical (Fleck et al., 2011). Abscisic acid (ABA), which is a stress hormone, is generated during high salt concentration and helps plants survive under stress conditions (Dodd & Davies, 2004; Wang et al., 2001). Upon addition of Si, the concentration of ABA decreases. Gibberellins, which is an important phytohormone, regulate many aspects of plant growth (Chakrabarti & Mukherji, 2003). During salt stress, the level of Gibberellins decreases but increases with the addition of Si (Lee et al., 2010). Si also shows some effects on polyamine. Polyamine is involved in a wide range of plant processes such as growth promotion, cell division, DNA replication, and cell differentiation. It shows a defense reaction in plants’ abiotic stress (Martin-Tanguy, 2001). The addition of Si increases the ratio of free spermine and spermidine to putrescine, perchloric acid-soluble covalently conjugated polyamines, and perchloric acid-insoluble covalently conjugated spermidine and spermine because salt stress effect the polyamine levels during the development of different plant species as the level of the putrescine decreases and its conversion to spermidine and spermine is crucial for comparing salt tolerance (Groppa & Benavides, 2008; Zapata et al., 2004). Hence, we can conclude that silicon during salt stress helps in the reduction of ion toxicity in plants by decreasing toxic ion accumulation and improving plant water status, alleviating oxidative damage in plants by modulating the plant antioxidant defense systems consisting of enzymatic or non-enzymatic constituents, and is also involved in the regulation of biosynthesis of lignin and amount of endogenous plant hormones and polyamines.

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6.6.1.2.4 EFFECT OF SILICON ON HEAVY METAL TOXICITY Si helps in mitigating toxic effects of essential as well as non-essential heavy metals when present in excess amount during stress conditions, which cause reduction and inhibition of plant growth, led by biochemical, physiological changes, and structural. Some common symptoms of heavy metal toxicity are chlorosis, inhibition of growth, photosynthesis, altered nutrient assimilation, low biomass accumulation, senescence, water balance, which finally leads to plant death. As silicon is introduced, it increases the pH which results in metal silicate precipitation which in turn decreases the metal Phyto-availability (Verma et al., 2020). Table 6.1 shows the detailed effect of silicon on heavy metal toxicity in various crop species. 6.6.2 ROLE OF SILICON AGAINST BIOTIC STRESS Biotic stress has become the major threat to agriculture as it causes a significant reduction in crop yield from all over the world. Biotic stress includes pests, insects, disease, pathogenic contamination, and infections in plants. Therefore, it has become a major global concern for sustainable agriculture production. It has been found that silicon availability in the plant cells protects plants from insects, pests, and diseases. Thus, it can be concluded that Si acts as a physical barrier to infection by producing dynamic resistance mechanisms (Anderson & Sosa, 2001; Belanger et al., 1995; Bockhaven et al., 2012; Chérif et al., 1994; Epstein, 1999; Massey et al., 2006; Reynolds et al., 2009). 6.6.2.1 SUPPRESSIVE EFFECT OF SILICON ON RICE BLAST DISEASE Rice blast disease is caused by Magnaporthe grisea (Hebert) Barr, and it is known to be the most disastrous fungal disease of rice. It can be seen in temperate areas, irrigated rice, and tropical upland rice (Onodera, 1917). The pathogen infects during the vegetative stage of growth on leaves causing leaf blasts. It also infects the panicle or neck nodes branches during the reproductive stage causing neck blasts and also spreads its infection in the above-ground parts of the rice plant. The incubation period was lengthened in rice—Magnaporthe grisea by Si accumulation and due to which the number of sporulating lesions, lesions size, lesion expansion, and disease leaf area is dramatically decreased. Si fertilizers are used in the area where

Heavy Metal Toxicity due to Silicon

Sl. No.

Heavy Crop Metals Species

Effects of Heavy Metals on Plant Species

Impact on Addition of Silicon

References

1.

Cd

• Trigger the synthesis of reactive oxygen species. • Inhibition of root growth and decrease in root diameter, width, and thickness of leaf midrib and diameter of xylem vessels. • The appearance of black spots in the cortex and pericycle. • Reduction in seed germination, decrease in plant nutrient content, reduced shoot and root length. • Reduction of Chla, Chlb, and carotenoids, decreased plant growth and biomass. • Decrease in plant dry weights, root length, and shoot height and leaves, alteration of photosynthetic pigments and lipid peroxidation. • Reduction of nodulation and leghemoglobin content. • Disruption of vascular tissues.

• It decreases the Cd concentration and translocation of Cd to shoots and grains. • Reduce shoot to grain translocation of Cd. • Cd co-precipitation with silicates, resulting in strong binding of Cd to cell walls, thus reducing the concentration of Cd in the symplast. • Formation of colloidal silicon in cell walls which has high specific adsorption property to Cd preventing Cd uptake into the cell. • Increase the activities of antioxidant enzymes and preventing membrane oxidative damage of plant tissue. • Inhibition of Cd transport from roots to shoots. • Increased diameter of xylem, thickness of leaf mesophyll and epidermis, and transversal area occupied by collenchyma and midvein. • Formation of apoplasmic barriers in endodermis closer to the wheat root apex. • Mediated extensive development of suberin lamellae in endoderm closer to the root tips.

Da-Lin et al. (2011); Dresler et al. (2015); Farooq et al. (2013, 2016); Greger et al. (2011); Hussain et al. (2015); John et al. (2012); Kasim (2006); Kherbani et al. (2015); Kleckerova et al. (2011); Liang et al. (2005, 2007); Li et al. (2008, 2014); Liu et al. (2014); Mondal et al. (2013); Naeem et al. (2014); Nwugo et al. (2008); Piršelová et al. (2016); Rizwan et al. (2012); Shi et al. (2005b, 2010); Thakur et al. (2014); Vatehová et al. (2012); Wang et al. (2007); Yourtchi et al. (2013); Žaltauskaitė et al. (2013); Zhang et al. (2008)

Rice, maize, wheat, cotton, peanut, barley, sorghum, chickpea, faba bean, garlic, rapeseed.

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TABLE 6.1

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Heavy Crop Metals Species

Effects of Heavy Metals on Plant Species

2.

Cr

Rice, barley, • Inhibition of shoot and root growth. maize, • Increase in lipid peroxidation, decrease in groundnut, photosynthetic pigments, induced oxidative onion, stress, Inhibition of germination process, tomato, reduction of plant biomass. wheat • Decrease in plant nutrient acquisition.

• Decrease the concentration of Cr in shoots and roots. • Increases plant height, number of tillers, root length and leaf size of barley plants.

3.

Zn

Barley, bean, pea, maize, cotton, rice

•

• Reduction in shoot/root biomass, decrease in length as well as dry weights of shoot/root and length of leaves. • The decrease in plant growth, development, and metabolism; induction of oxidative damage. • Reduction of photosynthetic pigments such as Chla and Chlb, disruption of absorption and translocation of Fe and Mg into the chloroplast.

Impact on Addition of Silicon

•

•

•

References

Zeng et al. (2011); Ali et al. (2013); Anwaar et al. (2014); Bokor et al. (2014a, b); Cakmak et al. (1993); da Cunha (2009); Doncheva et al. (2001); Gopal et al. (2014); Gu et al. (2011); Kaya et al. (2009); Khandekar et al. (2011); Kherbani et al. (2015); Kleckerova et al. (2011); Nematshahi et al. (2012); Neumann et al. (1997, 2001); Panda et al. (2000); Shim et al. (2014); Song et al. (2009); Tripathi et al. (2015); Vassilev et al. (2011) Suppressed Zn accumulation in various Abdi et al. (2014); Babula plant parts, i.e., roots, and leaves. et al. (2014a, b); Cakmak et Strong binding of Zn in the cell wall of less al. (2009); Doncheva et al. bioactive tissues, especially in sclerenchyma (2009); Ince et al. (2009); Kizek, R (2011); Koleva et al. of root. (1997); Lidon et al. (2011); Increased diameter of xylem, thickness Schwieger et al. (2001); Wang of leaf mesophyll and epidermis, and et al. (2001) transversal area occupied by collenchyma and midvein. Formation of less soluble zinc-silicates in the cytoplasm.

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TABLE 6.1 (Continued)

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4.

Mn

5.

Cu

Faba bean, pea, cucumber, cowpea

Effects of Heavy Metals on Plant Species

Impact on Addition of Silicon

Anshula et al. (2013); Kasim (2006); Keller et al. (2015); Meunier et al. (2015); Morel et al. (1997); Pokrovsky et al. (2011); Rizwan et al. (2013); Žaltauskaitė et al. (1997)

Anshula et al. (2013); Kasim (2006); Keller et al. (2015); Pokrovsky et al. (2011); Rizwan & Šliumpaitė (2013); Tang, Tian, Vardaka, & Žaltauskaitė (1997); Zhan (2018)

237

• Decrease in Chla and Chlb content, • Reduction of lipid peroxidation and reduction in relative growth rate, reduced increase of enzymatic and non-enzymatic photosynthetic O2 evolution activity and antioxidants levels. photosystem II activity. • Si increased Mn fraction in the cell wall of • Accumulation in shoot and root, reduction of shoots, thus reducing Mn concentration of the shoot and root length, chlorosis. symplast. • Si decreases the apoplastic Mn concentration and modify the cation binding capacity of the cell wall. Increased adsorption of Mn on cell walls reduces the amount of soluble apoplastic Mn. • Co-precipitation of Si and Mn in leaf apoplast of cowpea plants and increases Mn fraction in the cell wall of shoots. Wheat, • Reduction of root/shoot length and RWC, • Immobilization of heavy metals in culture barley, lipid peroxidation. media and decrease of phytoavailability, sorghum, which further suppressed metal uptake. • Root malformation and accumulation of Cu bean, in plant roots, reduction of root growth. • Cu form complex with organic acids and chickpea, reduced the Cu translocation to shoots. • The decrease in root diameter, width, and rice, thickness of leaf midrib and diameter of • Stimulated the genes responsible for the Arabidopsis xylem vessels, reduction of yield and yield production of metallothioneins (MTs) that contributing traits. can chelate toxic metals. • Reduction of plant dry weights, root length, • Si-mediated decrease in Cu uptake and and shoot height, alteration of photosynthetic translocation. pigments and lipid peroxidation.

References

Role of Silicon in Tolerance Against Different Environmental Stress

TABLE 6.1 (Continued)

Heavy Crop Metals Species

6.

Pb

7.

Hg

Effects of Heavy Metals on Plant Species

Brassica • Decrease in the plant growth like shoot/root juncea, length, shoot fresh/dry weights, number of wheat, tillers and biomass yield. pigeon pea, • Reduction in chlorophyll and carotenoid groundnut, pigments. cotton, • The decrease in the photosynthetic pigments soyabean, such as Chla, Chlb, and proline content. banana • Decrease in germination of seed, seedling growth, leaf area, root development. • The reduction in net photosynthetic rate, stomatal conductance, transpiration rate, water use efficiency, chlorophyll, carotenoids, and the soil plant analysis

development (SPAD) chlorophyll meter

value.

Soyabean, • Reduction in amount of germination pigeon pea, percentage, grain yield, tiller, panicle tomato, rice formation, root, and shoot length, fresh and dry weight of seedlings and decrease in plant height. • Reduction in content of oil, changes in major and minor fatty acid concentration in soybean seed. • Inhibition of root elongation. • Reduction in flowering and fruit weight, chlorosis.

Impact on Addition of Silicon

References

• Preventing Pb transfer from rice roots to aboveground parts and blocking Pb accumulation in rice grains. • Immobilization of heavy metals in culture media and reduction in phytoavailability, which further suppressed metal uptake. • Increase in the activities of antioxidant enzymes and prevents membrane oxidative damage of plant tissue. • Increases the pH of the soil and decreased proportion of exchangeable Pb in soil.

Bharwana et al. (2013); Bhatti et al. (2013); El et al. (2013); Gu et al. (2011); Imtiyaz et al. (2014); John et al. (2012); Lamhamdi et al. (2013); Li et al. (2012)

• It alleviates the growth inhibition induced by Hg and reduced the accumulation and translocation. • It decreases the Hg concentrations in the epidermis and pericycle of the roots and stems.

Yanhong et al. (2020); Patnaik & Mohanty (2013); Khan & Srivastava (2013); Kibra (2008)

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TABLE 6.1 (Continued)

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the soil is deficient in Silicon, and it acts as an effective fungicide application in controlling rice blast. Si fertilizers in the nursery are used to suppress the rice seedling blast significantly (Maekawa et al., 2001). 6.6.2.2 EFFECT OF SILICON ON POWDERY MILDEW DISEASE Powdery mildew disease is caused by Sphaerotheca fuliginea, in the number of plant species like cucumber, barley, strawberry, and wheat. By increasing the Si concentration in the culture, the solution leads to an increase in the Si content in the cucumber shoot, which causes a reduction in the incidence of powdery mildew disease (Miyake & Takahashi, 1983). When cucumber is grown in a nutrient solution containing a high concentration of Si, then the infection efficiency, colony size, and germination of conidia are reduced. Also, in the case of strawberry, the Si concentration was increased in culture solution which leads to an increase in Si content in the leaves, resulting in decreasing in the incidence of powdery mildew disease. In the case of barley and wheat, the deficiency of Si causes the poor growth habit and increases the chance of powdery mildew susceptibility (Menzies et al., 1991; Zeyen, 2002). The Si concentration is increased in the culture or nutrient solution because Si can produce phenolics and phytoalexins in response to these fungal infections. 6.6.2.3 EFFECTS OF SILICON AGAINST INSECTS AND PESTS Crop production has decreased due to the effect of insects and pests, which feed upon the crops. Therefore, it has become a major concern in agriculture, especially for those farmers who are not capable to purchase the expensive chemicals for the protection of crop (Anderson & Sosa, 2001; Belanger et al., 1995; Chérif et al., 1994; Epstein, 1999; Massey et al., 2006; Reynolds et al., 2009). From the various studies, we can be said that Si plays an important role in enhancing plant resistance against insect pests such as brown planthopper, stem borer, leafhopper, rice green, and white-backed planthopper, and non-insect pests such as mites and leaf spider (Coulibaly, 1990; Maxwel et al., 1977; Ota et al., 1975; Savant et al., 1997; Sawant et al., 1994; Sujatha et al., 1987; Tanaka & Park, 1966; Yoshida, 1975). Silicon is deposited in various plant tissues and acts as a mechanical barrier against probing and masticating insects, and the presence of silicified cells in plant tissues blocks the feeding of insects. The plants having high Si content in

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their tissue show great resistance against pest infection. Accumulation of a high amount of silica in the tissues of plants like rice, wheat, and sugarcane inhibits the feeding of insect larvae (Epstein, 1999). In rice plants, a positive relationship forms between the Si content of rice and insect pest resistance (i.e., resistance against brown planthopper) (Sujatha et al., 1987). 6.6.2.4 SILICON AND OTHER DISEASES In monocots, especially in the members of the family Poaceae, silicon is deposited abundantly and shows great potential against pathogen resistance (Carver et al., 1998; Datnoff et al., 1997; Shettya et al., 2012). Silica is accumulated underneath the cuticle forming a double layer of cuticle with Si, preventing the entry of fungal mycelium and infection in plant tissues. Apart from the blast and powdery mildew, the occurrence of brown spot, stem rot, sheath brown on rice plants, Fusarium wilt and Corynespora leaf spot on cucumber (Datnoff et al., 2002) Cynodon dactylon caused rust in cowpea and ring spot on sugarcane (Fawe et al., 2001), gray leaf spot in St. Augustine grass (Stenotaphrum sccundatum) is decreased by increasing the silicon supply. By adding Si supply in wheat and barley, it provides resistance against Blumeria graminis and rice from Pyricularia oyzae (Fauteux et al., 2005; Fawe et al., 1998). Si application protects the roots of cucumber plants from various insect pests like Pythium ultimum, Podosphaera xanthii, as Si enhanced the activity of chitinases, peroxidases, and polyphenol oxidases (PPOs). The bacterial blight of rice caused by Xanthomonas oryzae is a serious disease globally (Chang et al., 2002). According to Chang et al. (2002), the cultivator TN1 that is susceptible to this disease, the content of Si in the leaves is less than the resistance breeding line TSWY7 under the nutrient culture system. Increasing the amount of Si increases the degree of resistance to this disease. 6.7 SIGNIFICANCE OF USING SILICON DURING ENVIRONMENTAL STRESS CONDITION Silicon is considered as the second most abundant element in the earth’s crust. The content of silicon depends on the type of soil. The content of silica depends on the type of soil as Soils generally contain 50 to 400 g Si kg–1 (Kovda, 1973). In the case of clay soil, Silicon content varies between 200 g and 350 g of Si kg–1 while in sandy soil it varies between 450 g Si kg–1 and

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480 g Si kg–1 of soil (Kovda, 1973). Some of the positive effects of silicon during environmental stress are as follows: 1. The presence of silica in the soil improves the quality of the soil and hence leads to a large crop yield. Crystalline silicates form is the main Si-rich compounds that form the skeleton of the soil. Soluble H4SiO4, organosilicon compounds, and polysilicon acids constitute physically and chemically active Si substances in the soil (Matichenkov & Ammosova, 1996). H4SiO4 is absorbed by the plants, and they also maintain the chemical and biological properties of the soil P, Mn, Fe, Al, and heavy metal mobility, stability of soil organic matter the microbial activity, secondary minerals in the soil, and formation of polysilicic acids (Yoshida, 1975). Whereas polysilicic acid shows a notable effect on, water holding capacity, stability of the soil, adsorption capacity, and soil texture, thereby increases the fertility of the soil (Matichenkov et al., 2000). 2. Silicon is not present in the plant’s available form and is combined with other elements to form oxides or silicates. Plants generally absorb uncharged form of silicic acid in the form of Si(OH)4. The concentration of Si in plants depends upon the uptake and transport. Two types of Si uptake take place, one is active Si transport in Graminaceous species such as barley (Barber & Shone, 1966), rice (Ma et al., 2001b), ryegrass (Jarvis, 1987), and wheat (Rains et al., 2006), and second is passive Si transport some dicots such as soybean, cucumber, strawberry, melon (Liang et al., 2005). During water stress conditions, the addition of silicon decreased the transpiration rate and permeability of the membrane (Agarie et al., 1998), increase the water content and dry weight of plants, and modifies the architecture of the cell wall, which may be the cause for the increase in the cell wall extensibility Hossain et al. (2007). 3. Physiochemical properties change due to the high concentration of Si, which influences binding, sequestration of other elements, and solubility, ex planta and in planta. 4. The addition of silicon improves the nutrient imbalance, improvement of mechanical properties of plant tissues, reduction of mineral toxicities, and enhancement of resistance to other various abiotic (metal toxicity, lodging, salt, nutrient imbalance, high temperature, drought, UV radiation, freezing) and biotic stresses (Epstein, 1999; Ma & Yamaji, 2006). Stress tolerance capacity increases the

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concentration of polysilicic acid in plant tissues (Matichenkov et al., 2000). 5. The high concentration of salt in the plant cell leads to the generation of ROS, which activates phytotoxic reactions such as protein degradation, DNA mutation, and LPO (Ali & Alqurainy, 2006). Therefore, the addition of silicon decreases the porosity of the plasma membrane of leaf cells and remarkably improves chloroplasts’ ultrastructure, which was severely damaged by the addition of NaCl with the double membranes disappearing and the breakdown of grana in absence of Si (Liang et al., 2003). It also increases the activity of SOD and CAT activity during environmental stress conditions. 6. Silicon mediates the reduction of toxic heavy metals in higher plants and helps in the reduction of LPO, increases the soil pH, increases antioxidant enzyme activities, and prevents oxidative damage of membrane of plant tissue, and so on. 6.8 FUTURE PROSPECTS From the recent knowledge, the functions of silicon during stress condition is known but there should also be a clear understanding of its function in maximum species or during stress conditions, and in more complex interactions (such as, when higher temperatures are combined with optimal watering, UV-B radiation, and drought) like high temperature can be the major limiting factor affecting plant distribution, germination, and growth. It can also cause a reduction in crop production which leads to the increased production of ROS such as hydroxyl radicals (OH), superoxide radicals (O2–), and H2O2, causing loss of balance between productions and scavenging in the cell or organism. It causes LPO intensification. In another case, inducing silicon may lead to the binding with proteins such as effector proteins and receptors or with another binding process in the cell or on the surface of the cell. The evidence of this concept comes from the existence of Si transporters, which demonstrates the specificity of silica transport and recognition (Yamaji et al., 2008; Ma et al., 2006, 2007b). Therefore, Si metallomics screenings to identify high-affinity Si binding entities and to analyze the role of identified candidates should be initiated. Due to the increases in the concentration of the Silicon, its intrusion caused by the other cell processes but with very low affinity will be gained by the proteomic search for Si binding partners. To identify indirect effects,

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omics technologies should be done such as profiling of RNA to give some circumstantial evidence for processes to be involved (Tripathi et al., 2013). A new concept of Si-bio fortification of crop plants should be initiated because high levels of Si generally found in unrefined grains such as barley wheat, rice, and oat (Jugdaohsingh, 2007). Phytolithic silica which occurs in plants is linked to polysaccharide/carbohydrate constituents of the cell wall and is hardly absorbed in 1–20% depending on the food source (Martin, 2007). Thus, by increasing the content of silica in the edible part, we can increase the silica bioavailability by decreasing the anti-nutritional factors and increasing the expression of nutritional factors. According to recent researchers, the scientific community has issued various theories related to the possibility of micronutrients enrichment in the plant and using the soil-less condition as a tool for biofortification, Secondly, it enhances the nutritional quality of plant foods by using the molecular breeding technique as a strategy for improving the content of silica in the edible parts of the plant (Tripathi et al., 2013; Zhu & Gong, 2013). 6.9 CONCLUSION Silicon plays a crucial role in the growth of plants and development. Accumulation of silicon in plants helps in tolerating the various environmental stresses with the regulation of biochemical and physiological processes. The beneficial effect of silicon is seen when silica is deposited in the hull’s leaves and stems. Higher the accumulation of Si in the shoots larger will be the effect but accumulation of Si in shoots varies considerably on different plant species. As in dicot plants, the accumulation of Si in the shoot is very less because the accumulation of Si depends on the uptake of the Si by roots, which varies considerably on different plant species. The introduction of Silicon during salt stress leads to stress resistance by affecting the homeostasis of phytohormone. In salt-stressed soybean, the addition of silicon increases the levels of endogenous gibberellins, and it decreases the levels of ABA and proline. Silicon also interacts with many other components of plant stress signaling systems, which leads to induce resistance. Si affects the protein activity or its conformation by binding hydroxyl groups on amino acid residues, thus regulating the phosphorylation status of signaling proteins. To increase the resistance of plants against various stress conditions is to genetically modify the Si uptake ability. In case of Rice plants, the intake of Si by roots is maintained by a kind of transporter that has a low

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affinity for silicic acid. In the tomato plant, when Si is induced, it improves the water storage capacity resulting in the higher dilution of salt, thereby decreasing the toxicity of salt and improving growth. Silicon increases the formation of Casparian bands in the endodermis, exodermis, and depositions of lignin in sclerenchyma cells. Silicon also enhances the elongation of lateral roots such as in rice plants. According to Detmann et al. (2012), silicon increases NUE and stimulation of amino acid remobilization which changes the primary metabolism. Even though, more advances should be made in explaining the importance of silicon as it improves the plant stress tolerance at the whole-plant level. Detailed information is not mentioned on the molecular mechanisms of silicon inducing stress tolerance, which should be researched thoroughly for a better understanding. Technologies such as OMICS, transcriptome, and proteome platforms should be used for investigating the physiological, metabolic processes and to briefly understand the mechanisms of tolerance in plants. Hence, the use of these technologies will provide us with the transcriptional and post-transcriptional regulatory mechanisms of silicon-mediated tolerance to salinity and drought in plant stress. KEYWORDS • • • • • •

Cucumis sativus heavy metal toxicity lipid peroxidation monosilicic acid Oryza sativa reactive oxygen species

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Agarie, S., Agata, W., Kubota, K., & Kaufman, P. B., (1992). Physiological roles of silicon in photosynthesis and dry matter production in rice plants. Jpn. J. Crop Sci., 61, 200–206. Al-aghabary, K., Zhu, Z. J., & Shi, Q. H., (2004). Influence of silicon supply on chlorophyll content, chlorophyll fluorescence, and antioxidative enzyme activities in tomato plants under salt stress. J. Plant Nutr., 27, 2101–2115. Ali, B., Hayat, S., Hayat, Q., & Ahmad, A., (2010). Cobalt stress affects nitrogen metabolism, photosynthesis and antioxidant system in chickpea (Cicer arietinum L.). J. Plant Interact., 5, 223–231. Ali, M. A., Lee, C. H., & Kim, P. J., (2008). Effect of silicate fertilizer on reducing methane emission during rice cultivation. Biol. Fertil. Soils, 44, 597–604. Ali, M., (2013). The greenhouse effect. In: Ali, M., (ed.), Climate Change Impacts on Plant Biomass Growth (pp. 13–27). Springer, Dordrecht. Ali, S., Farooq, M. A., Yasmeen, T., Hussain, S., Arif, M. S., Abbas, F., Bharwana, S. A., & Zhang, G., (2013). The influence of silicon on barley growth, photosynthesis and ultrastructure under chromium stress. Ecotoxicol. Environ. Saf., 89, 66–72. Allahmoradi, P., Ghobadi, M., Taherabadi, S., & Taherabadi, S., (2011). Physiological aspects of mung bean (Vigna radiata L.) in response to drought stress. In: International Conference on Food Engineering and Biotechnology (Vol. 9, pp. 272–275). IPCBEE, IACSIT Press, Singapore. Anshula, S., & Gurpreet, S., (2013). Studies on the effect of Cu (II) ions on the antioxidant enzymes in chickpea (Cicer arietinum L.) cultivars. J. Stress Physiol. Biochem., 9. Arnon, D. I., & Stout, P. R., (1939). The essentiality of certain elements in minute quantity for plants with special reference to copper. Plant Physiol., 14, 371–375. Arya, S. K., & Roy, B., (2011). Manganese induced changes in growth, chlorophyll content and antioxidants activity in seedlings of broad bean (Vicia faba L.). J. Environ. Biol., 32, 707. Baylis, A. D., Gragopoulou, C., Davidson, K. J., & Birchall, J. D., (1994). Effects of silicon on the toxicity of aluminum to soybean. Commun. Soil Sci. Plant Anal., 25, 537–546. Bharwana, S., Ali, S., Farooq, M., Iqbal, N., Abbas, F., & Ahmad, M., (2013). Alleviation of lead toxicity by silicon is related to elevated photosynthesis, antioxidant enzymes suppressed lead uptake and oxidative stress in cotton. J. Bioremed. Biodeg., 4, 187. Bhatti, K., Anwar, S., Nawaz, K., Hussain, K., Siddiqi, E., Sharif, R., Talat, A., & Khalid, A., (2013). Effect of heavy metal lead (Pb) stress of different concentration on wheat (Triticum aestivum L.). Middle East J. Sci. Res., 14, 148–154. Birchall, J. D., & Chappell, J. S., (1988a). The solution chemistry of aluminum and silicon and its biological significance. In: Thornton, I., Doyle, H., & Moir, A., (ed.), Geochemistry and Health (1st edn., pp. 231–242). CRC Press, Boca Raton. Blumwald, E., (2000). Sodium transport and salt tolerance in plants. Curr. Opin. Cell Biol., 12, 431–434. Bockhaven, V. J., Vleesschauwer, D. D., & Höfte, M., (2013). Towards establishing broadspectrum disease resistance in plants: Silicon leads the way. J. Exp. Bot., 64, 1281–1293. Brenchley, W. E., & Maskell, E. J., (1927). The inter-relation between silicon and other elements in plant nutrition. Ann. Appl. Biol., 14, 45–82. Cakmak, I., & Marschner, H., (1987). Mechanism of phosphorus-induced zinc deficiency in cotton. III. Changes in physiological availability of zinc in plants. Physiol. Plant, 70, 13–20.

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Verma, K. K., Singh, P., Song, X. P., Malviya, M. K., Singh, R. K., Chen, G. L., Solomon, S., & Li, Y. R., (2020). Mitigating climate change for sugarcane improvement: Role of silicon in alleviating abiotic stresses. Sugar Tech., 22, 741–749. Verma, K. K., Song, X. P., Li, D. M., Singh, M., Rajput, V. D., Malviya, M. K., Minkina, T., et al., (2020). Interactive role of silicon and plant–rhizobacteria mitigating abiotic stresses: A new approach for sustainable agriculture and climate change. Plants, 9, 1055. Virta, R. L., (2004). Wollastonite—U.S. geological survey. Miner Yearb, 82, 1–3. Wang, L., Wang, Y., Chen, Q., Cao, W., Li, M., & Zhang, F., (2000). Silicon induced cadmium tolerance of rice seedlings. J. Plant Nutr., 23, 1397–1406. Wang, M., Zou, J., Duan, X., Jiang, W., & Liu, D., (2007). Cadmium accumulation and its effects on metal uptake in maize (Zea mays L.). Bioresour. Technol., 98, 82–88. Wang, W., Vinocur, B., & Altman, A., (2003). Plant responses to drought, salinity and extreme temperatures: Towards genetic engineering for stress tolerance. Planta, 218, 1–14. Wang, X. S., & Han, J. G., (2007). Effects of NaCl and silicon on ion distribution in the roots, shoots and leaves of two alfalfa cultivars with different salt tolerance. Soil Sci. Plant Nutr., 53, 278–285. Wang, Y., Stass, A., & Horst, W. J., (2004). Apoplastic binding of aluminum is involved in silicon-induced amelioration of aluminum toxicity in maize. Plant Physiol., 136, 3762–3770. Williams, L. A., & Crerar, D. A., (1985). Silica diagenesis. II. General mechanisms. J. Sediment. Petrol., 55, 312. Yadav, D. V., Jain, R., & Rai, R. K., (2010). Impact of heavy metals on sugarcane. In: Sherameti, I., & Varma, A., (eds.), Soil Heavy Metals (Vol. 19, pp. 339–367). Springer, Berlin, Heidelberg. Yamaji, N., Chiba, Y., Mitani-Ueno, N., & Ma, J. F., (2012). Functional characterization of a silicon transporter gene implicated in Si distribution in barley. Plant Physiol., 160, 1491–1497. Yamaji, N., Mitatni, N., & Ma, J. F., (2008). A transporter regulating silicon distribution in rice shoots. Plant Cell, 20, 1381–1389. Yamaji, N., Sakurai, G., Mitani-Ueno, N., & Ma, J. F., (2015). Orchestration of three transporters and distinct vascular structures in node for intervascular transfer of silicon in rice. PNAS, 112, 11401–11406. Yamaji, N., Takemoto, Y., Miyaji, T., Mitani-Ueno, N., Yoshida, K. T., & Ma, J. F., (2017). Reducing phosphorus accumulation in rice grains with an impaired transporter in the node. Nature, 541, 92–95. Yan, Z., Liu, P., Li, Y., Ma, L., Alva, A., Dou, Z., Chen, Q., & Zhang, F., (2013). Phosphorus in China’s intensive vegetable production systems: Over fertilization, soil enrichment, and environmental implications. J. Environ. Qual., 42, 982–989. Yang, X., & Post, W. M., (2011). Phosphorus transformations as a function of pedogenesis: A synthesis of soil phosphorus data using Hedley fractionation method. Biogeosciences, 8, 2907–2916. Yang, X., Post, W. M., Thornton, P. E., & Jain, A., (2013). The distribution of soil phosphorus for global biogeochemical modeling. Biogeosciences, 10, 2525–2537. Yoneyama, T., (1988). Problems on phosphorus fertility in upland soil; 5. Uptake and metabolism of phosphorus of plant. Agric. Hortic., 63, 16–20.

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CHAPTER 7

Role of Selenium in Tolerance Against Different Environmental Stress

UMAIR RIAZ,1* TAYYABA SAMREEN,2 MUHAMMAD ZULQERNAIN NAZIR,2 NATASHA KANWAL,3 SAFDAR BASHIR,4 and QAMAR-UZ-ZAMAN5

Soil and Water Testing Laboratory for Research, Bahawalpur – 63100, Agriculture Department, Government of Punjab, Pakistan, Phone: +92-3006208789, E-mail:

1

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

2

Regional Agricultural Research Institute, Bahawalpur – 63100, Agriculture Department, Government of Punjab, Pakistan

3

Department of Soil and Environmental Sciences, Ghazi University (GU), D.G. Khan, Pakistan

4

Department of Environmental Sciences, University of Lahore, Lahore, Pakistan

5

*

Corresponding author. E-mail: [email protected]

ABSTRACT Selenium (Se) is a vital microelement. Based on its abundance, Se is ranked at 69th in the list of elements on the earth. Selenium has received significant attention in recent years as a vital microelement. It is mainly produced from refining of different minerals as it is very rarely found in its pure form. Geological activities are the main source of Se on the earth. The beneficial Biology and Biotechnology of Environmental Stress Tolerance in Plants: Trace Elements in Environmental Stress Tolerance, Volume 2. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

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role of Se regarding plants is yet to be fully understood. However, according to different studies, when applied in small quantity, Se is very helpful in tolerating different stress conditions like drought stress (DS), cold stress, salt stress, extreme temperature stress, UV-B radiations-induced stress, and toxic metal stress. Its role is very important regarding enhancing plant’s growth and maturation. Selenium minimizes harm to chloroplast and elevate chlorophyll level when plants are under stress. Average concentration of Se in most soils is less than 1 mg/kg. If applied in excess amount, it causes the accumulation of reactive oxygen species (ROS) in plants and degrade plant growth and development. Selenium acts as a plant antioxidant, and due to this characteristic, it improves the physiological condition of the plant and exhibits a positive impact on the yield/productivity of the crop. It forms non-toxic Se-metal complexes in toxic metal stress conditions and reduces the chances of their absorption and accumulation in the plant. 7.1 INTRODUCTION Selenium is a hazardous metalloid and a trace element (Hasanuzzaman et al., 2020). Its atomic number is 34 and it is denoted by the symbol (Se) (Perrone et al., 2015). It is found in the VI A group, between sulfur and tellurium, and in the 4th period, between arsenic and bromine (Chauhan et al., 2019). Selenium is derived from the Greek word “Selene,” which means “moon” (Perrone et al., 2015). It is quite rare to find it in its pure form in the environment (Hasanuzzaman et al., 2020). It is found in various inorganic forms in nature, including selenide (Se2˗), selenate (SeO42˗) and selenite (SeO32˗). This element may be identified in the lithosphere region of the earth, water, soil, and the open environment, hence its availability varies around the world (Hasanuzzaman et al., 2020). It is among the most broadly dispersed elements, having an approximate abundance of 69th in the earth (Fishbein and toxicology, 1983). It was first discovered to be a poisonous substance for both animals and humans. When glutathione peroxidase (GPX) and other selenoproteins were discovered to constitute Se, it was later classified as an important element for microorganisms and many animals, including humans. For most species, the boundary between essentiality and toxicity of Se is extremely thin, and as a result, Se has been considered “the essential poison” (Chauhan et al., 2019). It was discovered in 1818 and can be found in metal sulfide ores as a partial replacement for sulfur (Perrone et al., 2015). Selenium is developed extensively as an extra outcome of purification of

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various ores, usually during manufacturing. Selenium is a semiconductor and is mainly used in photovoltaic cells (Shamberger, 1981). Glassmaking and pigments are the two most common commercial applications of Se today. 7.1.1 CHEMISTRY OF Se Selenium exists in a variety of oxidation states, allowing it to produce selenoamino acids and organo-selenium compounds. Selenium’s most common valence states are –2, 0, +2, +4, and +6. Selenium is found in a variety of chemical forms. Inorganic forms of Se, such as selenite [Se(+4)] and selenate [Se(+6)], are most commonly available to plants (Chauhan et al., 2019). Both forms of Se are highly poisonous, easily dissolvable, mobile, and accessible. Seleno-amino acids, seleno-peptides, and selenoproteins are the three main organic types. These are derived primarily from decaying plants that are rich in Se content. Where Se exists as an anion in minerals, it is chemically linked to metals, generating selenides like MexSe. Copper can combine with Se to generate compounds in which Se shows varying degrees of oxidation. It can partially replace sulfur in some minerals due to similarities in chemical composition (Sieprawska et al., 2015). Amorphous and crystalline forms are the two forms in which Se exists. The finely split brick-red forms of amorphous Se are the most well-known. The crystalline form, as well as the so-called “metallic” gray or black Se, ranging in color from red to brown. The hexagonal, crystalline form is the most thermodynamically stable form. Pure Se is a relatively less toxic and is considered as important trace element. Selenium compounds have more free pairs of electrons, and their pH lies in the acidic range than the corresponding sulfur compounds. Selenium has 6 natural isotopes, among them five are stable. Selenium and sulfur have the same valence electronic configuration, which explains the resemblance in their structural and compositional properties such as atom size, binding strength, potential to ionize and electronic conductivity (Perrone et al., 2015). 7.1.2 SOURCES OF Se Usually, Se exists as chemically linked to metals and form selenides as MexSe. Selenium has been discovered in coal strata in the form of unidentified minerals having Ni3As3S3Se. Another reason of the presence of Se in the environment is also due to volcanic eruptions. The eruption of Etna raised the amount of Se in neighboring region from 0.3 to 23 kg/year during 1976

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to 2007. The form of Se found in the air is SiO2, which is produced during the burning of coal (Sieprawska et al., 2015). Selenium is released into the atmosphere when seleniferous coals are incinerated. Rock development, rotations underneath the soil mantle, breakdown of the host substance, constant transportation of Se through air or water runoff, and supplementation of Se in soil due to mining activities are the main sources of Se in the soil. Selenium is mostly produced extensively as an extra outcome of copper purification (Fishbein and Toxicology, 1983). 7.1.3 REQUIREMENTS OF Se Animals, humans, and even microbes have been shown to get benefit from Se (Hasanuzzaman et al., 2020). Selenium is thought to have a firm capacity mixing with toxic metals like cadmium, mercury, silver, and titanium to produce harmless Se-metal complex compounds (Feng et al., 2013). When supplied at low concentrations to plants, Se has an important function in decreasing the damaging outcomes of nonliving stressors and may physiological nourishment of plants. It has been observed to have effective results on the development of plant by boosting antioxidant enzyme activity and promoting plant’s ability to withstand various nonliving stressors, like water shortage, salt stress, cold, metals, and so on (Hasanuzzaman et al., 2020). It also protects against Cd toxicity by lowering the harm because of stress due to UV-B radiations, elevating chlorophyll, and carotenoids level in leaves, and triggering the enzyme mediated and non-enzyme mediated antioxidant systems (Nawaz et al., 2015). Selenium controls the formation and the requirement of reactive oxygen species (ROS). Plants can accumulate ROS because of a variety of stressors. Plants may be damaged by increased ROS production. Selenium can affect the formation and fulfillment of ROS either directly or indirectly through antioxidant modulation. In plants exposed to a variety of environmental stressed conditions, adding a small amount of Se to the growing substrates can lower surplus ROS production. Selenium supplementation causes a disruption in the chain reaction of ROS, thus reducing harm to the fatty part of plant cellular membrane (Feng et al., 2013). Plants under stressed conditions result in damaged chloroplasts and impaired photosynthesis. The addition of suitable quantities of Se, on the other hand, can help to minimize chloroplast damage and increases total chlorophyll content. The recovery of photosynthesis in plants exposed to

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stress after Se is applied may have close relation to reduced ROS concentration, revival of antioxidants, recovered composition of disrupted chloroplasts and increased formation of further essential compounds (Feng et al., 2013). According to different studies, application of Se in low concentrations improves the growth of plants. In a research, 5 μM of Se was applied which results in enhancement of root development and increased the relative water content (RWC) up to 13% in contrast with treatments of known value. Likewise, the two concentrations (3 and 5 μM) of Se increased 25% leaf area, which eventually enhanced plant growth and biomass. Selenium also improves crop growth and development when applied in the form of fertilizer (Hasanuzzaman et al., 2020). 7.1.4 LIMITATIONS In most soils, the average Se level is usually > 1 mg/kg; Se levels in Se rich soils, on the other hand, can range from 4–100 mg/kg. Plants in most soils have Se levels of > 1 mg/kg biomass, however many crops growing in Se rich soils have Se content ranges from 1–10 mg/kg. This can reach from 1,000–15,000 mg/kg in the case of Se-hyperaccumulator plants (Garcia Moreno et al., 2013). However, too high a concentration of Se in plants results in the accumulation of a lot of ROS. For instance, when 1.5 μM Se was applied in the root zone of plants subjected to 50 μM lead, it enhanced cell growth, while when a higher level of Se, 6 μM, was applied, it greatly enhanced the oxygen concentration and reduced cell growth (Feng et al., 2013). It was observed that the concentration of Se oxide range within 0.1–0.5 μM reduced level of δ-aminolevulinic acid in elongated parts of leaves of maize. Furthermore, the rise in the SeO32˗ level resulted in a reduction of dependent-concentration in ALA deposition in both dark and light conditions (Hasanuzzaman et al., 2020). Threshold levels of sufficiency and hazardousness for Se are 0.05–0.10 and 4–5 mg/kg feed. It has been observed that soils holding < 0.5 mg/kg of Se produces vegetation that absorbs Se at dangerous quantity for livestock feed. Even when more than 5 mg/kg Se is deposited in plant tissue, species that are sensitive to Se may exhibit restriction in development (Rani et al., 2005). For positive impacts, the US government lately suggested nutritional Se intakes of 55–70 µg/day, while the present criterion established by UK’s health department has recommended concentration of Se at 400 μg/individual/day (Garcia Moreno et al., 2013). The toxic effects of Se restrict the development of most plants beyond threshold level of 0.1 mg/kg of biomass.

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7.2 GEOCHEMICAL CYCLE OF Se (FLOW CHART)

7.2.1 GLOBAL SELENIUM CYCLE IN NATURE Sulfur containing mineral, iron sulfide, and coal containing high sulfur content are the greatest sources of Se. In the environment, Se is discharged as SeO42˗ by geological and anthropogenic activities. At the bottom of the food chain, first micro-organisms and plants absorb Se from selenate or selenite, which is then eventually metabolized by animal species. In living organisms, Se is then converted into organoselenides. Degradation of perished microbes discharge Se back into the atmosphere. Extraction activities, fossil fuel burning, agronomic crop cultivation, explosions from the mountain activities, all discharge soluble forms of Se into the environment. In nature, microbes have a key performance in rotating Se substances (Nancharaiah et al., 2015).

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7.3 SELENIUM AND THE ENVIRONMENT

Drought stress (DS), high salt content in soil, low temperature, toxic heavy metal stress and high temperature are the usual harmful environmental circumstances that restrict production/yield of crops throughout the world (Rai Ashwani & Teruhiro, 2005). Selenium has been found to be beneficial against these abiotic stress conditions, although the mechanisms involved are complex and have yet to be fully understood. In some plant species, external implementation of Se has been reported to enhance the development and growth of plant in both stressed and non-stressed environments (Iqbal et al., 2015). 7.3.1 EFFECTS OF Se AGAINST STRESS Selenium is a biologically important trace element that helps plants to withstand stressed conditions. The function of Se as antioxidant, which increases growth and productivity of crop, is one of the most important reason of better plant resistance to various abiotic stressors. The increase in antioxidant defense system activity caused by Se enhances plant physiological condition, which has a positive impact on the production characteristics of crops (Hasanuzzaman et al., 2020). 7.3.2 EFFECTS OF Se AGAINST SALT STRESS Growth of the plant is affected by a variety of environmental stresses, including salinity stress being one of the most critical global agricultural issues. In plant cells, high salt concentration can induce hyperosmotic stress and ion imbalance, resulting in oxidative stress (Kong et al., 2005). Many experiments have been performed to understand the positive role of Se in protecting plants from stress conditions induced by salinity. According to the results of an experiment, under salt stress conditions, 1 μM Se improved the physical appearance of the crop, overall photosynthetic activity, potassium level of the plant, while the quantity of sodium dropped (Hasanuzzaman et al., 2020). 7.3.3 EFFECTS OF Se AGAINST EXTREME TEMPERATURE Extreme temperature is one of the environmental stresses that damages and hinders the productivity of plants (Balal et al., 2016). Selenium performs different functions under severe temperature by enhancing cell growth,

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reducing ROS formation, improving antioxidant defense, and regulating reproductive viability. Selenium is also a vital element for protecting crops during low temperatures (Hasanuzzaman et al., 2020). 7.3.4 EFFECTS OF Se AGAINST TOXIC METALS The toxic impacts of cadmium, lead, arsenic, mercury, aluminum (Al), antimony is termed as usual heavy metal stress. Other metals, including those required for optimal plant growth and development such as zinc, manganese, copper, and iron, function as sources of stress when present in higher amounts (Sieprawska et al., 2015). Various species of plants treated with Se have exhibited an increased resistance to metal/metalloid toxicity. Selenium supplementation to “hyper-accumulator” and “indicator” plant species reduces the impact of toxic metal stress (Sieprawska et al., 2015). In several studies, Se has been shown to protect plants by inhibiting the absorption and deposition of harmful substances, lowering movement to growth media, lowering transferring to higher sections of crops. In contradiction to the prevention of metal absorption, Se assists the plant in the absorption of iron, which is an essential component of the chloroplast and photosynthetic mechanism. Furthermore, Se contributes to the reduction of toxicity induced by metals/metalloids by promoting the formation of phytochelatin (PC) or non-toxic Se-metal complexes (Hasanuzzaman et al., 2020). 7.3.5 EFFECTS OF Se AGAINST WATER SHORTAGE CONDITIONS Dry condition in plants is commonly due to shortage of water in cells, which is accompanied by osmotic imbalances. It could be caused by a shortage of available water in the root system because of drought or salinity conditions in the soil. For a greater understanding of Se translocation within crop plants under water shortage conditions, the selection of an appropriate dose of Se and applying strategy is very important (Nawaz et al., 2014). Selenium ions, through activation of the antioxidant system of plant, can enhance the potential of crop to withstand excessive oxygen conditions induced by drought. The main process linked with the preventive activity under water shortage conditions is the role of Se in monitoring and establishing sufficient water conditions in cells. Increased water reservation in wheat tissues could be due to an increase in the amount of biological and non-biological protective materials stimulated by Se (Sieprawska et al., 2015).

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7.3.6 EFFECT OF Se AGAINST UV-B RADIATION STRESS

Stress due to ultraviolet (UV) radiations is amongst critical environmental concerns which can affect the development of crop and metabolic activity in nearly all possible ways. The damaging impacts of UV radiations are mainly due to the production of ROS, which eventually results in the accumulation of excess oxygen in plants. According to the results of an experiment, in contrast to control, UV radiations treatment caused a huge decline in shoot weight, root weight, and total biomass, as well as a noticeable rise in the root/ shoot ratio of wheat seedlings. Addition of Se resulted in a noticeable rise in shoot weight while lowering the root weight. Total biomass, root weight and shoot weight by the co-application of Se and UV-B was more pronounced than the treatment of UV-B applied alone (Table 7.1; Yao et al., 2011). TABLE 7.1 Uptake and Concentrations of Trace Elements in Roots, Stem, and Leaves in the Plants (mg/L) Trace Elements Zinc Iron

Form of Uptake Zn2+ Fe3+

Manganese Boron Copper Molybdenum Silicon Selenium

Mn2+ H3BO3 Cu2+ MoO42˗ H4SiO4 SeO42; SeO42˗

Roots

Stem

References

20–40 30–120 5–45 Sekara et al. (2005) 1.9–1,11,200 0.1–24,070 7.3–25,650 Ancuceanu et al. (2015) 42.89 60.63 91.14 Yang et al. (2008) 36 38 19 Gupta (1991) 6–26 5–10 2–11 Sekara et al. (2005) 1.26 1.23 0.62 Gupta (1991) 6–73 20–410 3–44 Collin et al. (2012) 196 387 191 Eiche et al. (2015)

KEYWORDS • • • • • • •

Leaves

ascorbate peroxidases drought nonselective cation channels plant antioxidant reactive oxygen species selenium yellow stripe like

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REFERENCES Ancuceanu, R., Dinu, M., Hovaneţ, M. V., Anghel, A. I., Popescu, C. V., & Negreş, S., (2015). A survey of plant iron content—A semi-systematic review. Nutrients, 7, 10320–10351. Balal, R. M., Shahid, M. A., Javaid, M. M., Iqbal, Z., Anjum, M. A., Garcia-Sanchez, F., & Mattson, N. S., (2016). The role of selenium in amelioration of heat-induced oxidative damage in cucumber under high temperature stress. Acta. Physiol. Plant, 38, 1–14. Chauhan, R., Awasthi, S., Srivastava, S., Dwivedi, S., Pilon-Smits, E. A., Dhankher, O. P., & Tripathi, R. D., (2019). Understanding selenium metabolism in plants and its role as a beneficial element. Crit. Rev. Environ. Sci. Technol., 49, 1937–1958. Collin, B., Doelsch, E., Keller, C., Panfili, F., & Meunier, J. D., (2012). Distribution and variability of silicon, copper and zinc in different bamboo species. Plant Soil, 351, 377–387. Eiche, E., Bardelli, F., Nothstein, A. K., Charlet, L., Göttlicher, J., Steininger, R., Dhillon, K. S., & Sadana, U. S., (2015). Selenium distribution and speciation in plant parts of wheat (Triticum aestivum) and Indian mustard (Brassica juncea) from a seleniferous area of Punjab, India. Sci. Total. Environ., 505, 952–961. Feng, R., Wei, C., & Tu, S., (2013). The roles of selenium in protecting plants against abiotic stresses. Environ. Exp. Bot., 87, 58–68. Fishbein, L., (1983). Environmental selenium and its significance. Fundam. Appl. Toxicol., 3, 411–419. Garcia, M. R., Burdock, R., Díaz, Á. M. C., & Crawford, J. W., (2013). Managing the selenium content in soils in semiarid environments through the recycling of organic matter. Appl. Environ. Soil Sci., 2013. Gupta, U. C., (1991). Boron, molybdenum and selenium status in different plant parts in forage legumes and vegetable crops. J Plant Nutr., 14, 613–621. Hasanuzzaman, M., Bhuyan, M. B., Raza, A., Hawrylak-Nowak, B., Matraszek-Gawron, R., Al Mahmud, J., Nahar, K., & Fujita, M., (2020). Selenium in Plants: Boon or Bane?: Environ. Exp. Bot., 104170. Iqbal, M., Hussain, I., Liaqat, H., Ashraf, M. A., Rasheed, R., & Rehman, A. U., (2015). Exogenously applied selenium reduces oxidative stress and induces heat tolerance in spring wheat. Plant Physiol. Biochem., 94, 95–103. Kong, L., Wang, M., & Bi, D., (2005). Selenium modulates the activities of antioxidant enzymes, and osmotic homeostasis and promotes the growth of sorrel seedlings under salt stress. Plant Growth Regul., 45, 155–163. Nancharaiah, Y. V., & Lens, P. N. L., (2015). Ecology and biotechnology of selenium-respiring bacteria. Microbiol. Mol. Biol. Rev., 79, 61–80. Nawaz, F., Ahmad, R., Ashraf, M. Y., Waraich, E. A., & Khan, S. Z., (2015). Effect of selenium foliar spray on physiological and biochemical processes and chemical constituents of wheat under drought stress. Ecotoxicol. Environ. Saf., 113, 191–200. Nawaz, F., Ashraf, M. Y., Ahmad, R., Waraich, E. A., & Shabbir, R. N., (2014). Selenium (Se) regulates seedling growth in wheat under drought stress. Adv. Chem., 2014, 1–7. Perrone, D., Monteiro, M., & Nunes, J. C., (2015). The chemistry of selenium. Selenium: Chem. Anal. Funct. Eff., 1. Rai, A. K., & Teruhiro, T., (2005). Abiotic Stress Tolerance in Plants Toward the Improvement of Global Environment and Food. Published by Springer. Netherlands. Rani, N., Dhillon, K. S., & Dhillon, S. K., (2005). Critical levels of selenium in different crops grown in an alkaline silty loam soil treated with selenite-Se. Plant Soil, 277, 367–374.

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Sekara, A., Poniedzialeek, M., Ciura, J., & Jedrszczyk, E., (2005). Zinc and copper accumulation and distribution in the tissues of nine crops: Implications for phytoremediation. Pol. J. Environ. Stud., 14, 829–835. Sieprawska, A., Kornas, A., & Filek, M., (2015). Involvement of selenium in protective mechanisms of plants under environmental stress conditions-review. Acta Biol. Crac. Ser. Bot., 57. Yang, S. X., Deng, H., & Li, M. S., (2008). Manganese uptake and accumulation in a woody hyperaccumulator, Schima superba. Plant Soil Environ., 54, 441–446. Yao, X., Chu, J., He, X., & Ba, C., (2011). Protective role of selenium in wheat seedlings subjected to enhanced UV-B radiation. Russ. J. Plant Physiol., 58, 283–289.

CHAPTER 8

Role of Nickel as a Potent Environmental Stress Reliever in Plants

DISHA DASGUPTA,1 KRISHNENDU ACHARYA,2 and NILANJAN CHAKRABORTY1

Department of Botany, Scottish Church College, 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 Plants are always subjected to a variety of environmental stresses, which will ultimately reduce the yield, and also affect the plant in certain other ways. Plants being exposed to heavy metal stress are also very common nowadays, out of which nickel (Ni) has gained considerable concentration because of its vigorously growing level in the atmosphere. Common household substances contain an adequate amount of Ni, and as a result, the concentration is being increased in water, air, and soil. On the immediate fixation of Ni in the soil, it is accumulated in plant body by their roots. Though, Ni is one of the most important micronutrients which is necessary for normal plant growth and development at a trace amount, but at high concentration it can cause toxic effect to the plant. At an excessive level, it may induce reactive oxygen species (ROS), which in turn can degenerate plasma membrane, can hamper certain physiological activates like photosynthesis, transpiration, and can deactivate certain metalloenzymes. But in contrast, it is a proven Biology and Biotechnology of Environmental Stress Tolerance in Plants: Trace Elements in Environmental Stress Tolerance, Volume 2. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

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fact that Ni plays an essential role in antioxidant metabolism in plant. Ni is the constituent element of several phyto-enzymes like Urease and glyoxalase I (Gly I). During stressed condition methylglyoxal (MG) is produced in the plant body, which is eliminated by glyoxalase enzyme, which confirms the indirect utility of Ni in stress management. In this chapter, we will discuss about the functionality of nickel in tolerance against a wide range of environmental stresses in detail. 8.1 INTRODUCTION Essential nutrients are those without which plant growth will be prohibited or plants can’t complete their life cycle, and these elements can’t be replaced by others. Normal plant growth and development is facilitated by the presence of some heavy metals viz. Copper, Iron, Cobalt, Molybdenum, Nickel, and Manganese. From a biological viewpoint, the term “heavy” refers to a number of metals or metalloids which show potent toxicity towards both plants and animals at certain concentration (Rascio and Navari-Izzo, 2011). Phytotoxicity by heavy metals can alter several physiological functions of plant body like distortion of membrane integrity, blocking functional pathways, disruption of genetic structure, unnecessary ion leakage, hazardous electron transport and many more (Quartacci et al., 2001; Navari-Izzo et al., 1999), such state of affairs encountered by plants are known as heavy metal stress. After entering the plant body these heavy metals are initially accumulated by the root cells, where their toxicity is neutralized by forming complex components with other organic compounds and isolated into vacuoles (Hall, 2002), but stress conditions occur when these heavy metals are racked by the plant body higher than the optimum level. Globalization has led to an enhanced level of environmental pollution, which not only can cause harm to human society but also can be a great threat to entire living organisms including the floral ecosystem and among multiple variety of pollutants heavy metals are one of the most severe components to look after at present and in coming future (Wo-Niak & Basiak, 2003). Plants are subjected to absorb a few heavy metals throughout their lifetime and nickel (Ni) is one of the main concerns. The source of this metal in the environment could be natural or could be due to human activities (Salt et al., 2020). The optimum level of nickel in the soil should be 0.1 gm/kg, and in water, the level should be around 0.005 mg/L, which is considerably very low as compared to certain other metals (McGrath, 1995).

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However, anthropogenic activities like mining, excessive use of fossil fuels, household, and industrial wastes, manufacturing construction materials can trigger atmospheric Ni level (Salt et al., 2000). Recently Ni pollution has been documented from Europe (Papadopoulos et al., 2007), Asia (Ahmad et al., 2007), Africa (Yabe et al., 2010) and North America (Kukier et al., 2004). A survey revealed that almost 150 K to 180 K metric tons of Ni are being added to the nature ever year (Kasprzak et al., 2003), which is an indication of a huge threat in the coming future. Huge rate on Ni contamination of soil should be taken into consideration and emphasis should be given to remediation of this problem. Brown et al. (1987) first identified Ni as an essential mobile element for plant. Nickel ranks 24 in orders to most abundant element in earth’s crust (Garrett, 2000) and is considered as an essential microelement to pursue multiple biological functions in plant body (Brown, 2007). Beside this, Ni is playing an active role in nitrogen (N2) assimilation, biosynthesis of certain enzymes like urease and glyoxalase-I and also helps plant body to combat against several biotic and abiotic stressed conditions (Barker, 2006; Wood & Reilly, 2007; Sreekanth et al., 2013). Being a heavy metal multiple damages can also be caused by increased level of Ni, its toxicity depends on certain conditions of plant body like age of the plant, growth phase, environmental condition, cultivation technique, type of flora and moreover Ni level and exposure period (Marschner, 1995; Kabata-Pendias & Pendias, 2001; Assuncao et al., 2003); but on the other hand, a plant body may face multidimensional problems if nickel deficiency occurs. Stunted growth, preaging, decreased level of iron uptake are some of the symptoms that could be seen in reduced Ni level (Brown, 2007; Chen et al., 2009). Increased concentration of Ni may cause a sharp fall in photosynthetic and respiratory rate, chlorosis of leaf, nutritional deficiency, normal plant growth will be prohibited and many more (Rahman et al., 2005; Seregin & Kozhevnikova, 2006). Reports suggest that nickel deficiency may lead to ill development of endosperm, embryo, and ultimately cease seed production (Brown et al., 1987). Photoautotrophs may experience different stressful conditions imposed by the environment or by some other living beings, i.e., both abiotic and biotic warning could be there. Stress is a condition where some stressor factors are imposed on an individual, and as a result of which its physiological, morphological rather entire biological functionality could be in a serious threat. To release this kind of stress plants may adapt multiple different strategies or may alter their behavior through morphological or physiological changes

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towards that cause. Experimental studies also support the role of Ni2+ in stress management. Ni can help the plant body to adapt certain deportment towards the stress imposing factor to cope up with those problems. By now it is evident that Ni is one of the most important trace elements (TEs) of plant body, which is associated with multiple biological functions. Both increased and decreased concentration of nickel can cause harmful effect to the plant. In this chapter, we will discuss about few important things regarding nickel, like its transport mechanism, positive, and negative effects in plants, its role in physiological activities, etc. Apart from this our main focus would be elaborating its working mechanism against biotic and abiotic stress in plants and to justify the title of the chapter. 8.2 ENVIRONMENTAL SOURCE OF Ni Nickel is most commonly present in the form of metal ion (Ni) in nature and within soil solution it is found as Ni (H2O)62+. Around 20% of total world’s Ni comes from Pentlandite mine, situated in Canada, which is a great source of Ni. Weathering of metamorphic and igneous rocks can also be a good Ni source (Yusuf et al., 2010). A sufficient amount of this cation is derived from the burning of coal, petroleum, and other fossil fuels (Ahmad & Ashraf, 2011). Traces of Ni could also be found in water bodies and the atmosphere. Among few popular anthropogenic sources of nickel industrial wastes, municipal garbage, household discharges are significant. Nickel is considered as metalo-pollutant, which is released from mines with other metals and dispersed throughout the atmosphere. These disseminated nickel particles settle down on the surface of water and soil (Orlov et al., 2002). A considerable amount of Ni is emitted directly to the air from power-generating trash and plant incinerators (Hilgenkamp, 2005; Lewinsky, 2007). Surprisingly the majority of Ni and its compounds are adsorbed by the sediments or particles of soil and become immobilized, a little proportion leaks to the groundwater as well. However, acidic soil can increase its mobility, and make them available for plant uptake (Zhang et al., 2006). As variable sources of nickel are accessible, thus each and every living organism is exposed to its toxicity either at present or in the coming future. 8.3 Ni STATUS IN SOIL Nickel can potentially resist against water, air, and alkali corrosion but dissolved in oxidizing acids (diluted). Ni enters the ecosystem through natural

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and anthropogenic venture and after spreading throughout the biosphere a very little proportion is taken up by plant bodies (Cempel & Nikel, 2006; Jin et al., 2006; Oorts et al., 2007). Availability of Ni for the plants is dependent on soil texture, structure, type, pH, free iron (Fe) and Manganese (Mn) oxides, organic matter, etc. (Kabata-Pendias & Pendias, 1999). Changes in any of these factors can result in phytotoxicity or deficiency of Ni in plant body and both come with their respective consequences. pH plays a vital role in uptake of nickel by plants, lower pH determines higher Ni availability (Li et al., 2009), and in higher pH (10 mM Glycine max L. >30 mM Zea mays L.

Zea mays L.

References Alam et al. (2007)

Kazemi et al.

(2010) Bazihizina et al. (2015) Brune & Deitz (1995) Brune & Deitz (1995) Shalygo et al. (1999) Arefifars et al. (2014) Lin & Kao (2005) Ruchi & Dubey (2009)

Rajni & Rajeev (2009) Liu et al. (1994) Liu et al. (1994) Liu et al. (1994) El-Shintinawy & El-Ansary (2000) Baccouch et al. (1998)

Ni alone or in com- Decreased dry matter of root. bination with Lead (Pb), Zinc (Zn), Copper (Cu), Cadmium (Cd), and Chromium (Cr) 20–500 mM Carbohydrates get accumulated towards Baccouch et al. the shoots which eventually prohibit (1998) roots growth. Chlorosis of leaves could be observed up to 100 mM concentration and above that necrosis could be seen.

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(Continued)

Plant Name

Toxic Concentration Effects

Zea mays L.

60 mM

Phaseolus vulgaris L. Helianthus annuus L.

200 mM 200 mg/L

Lemna gibba L. 0.5 mg L−1

Lens culinaris 50 mg kg−1 Medikus Vigna radiata 11.73 mg L−1 L. R. Wilczek Acer rubrum L. 1,600 mg kg−1 Solanum lycopersicum L. Phaseolus mungo L. Coronopus didymus L.

Medicago sativa L. Trifolium pratense L. Hordeum vulgare L. Cicer arietinum L. Hydrilla verticillata L.f. Royle

Vigna radiata L. Vigna radiata L. Eruca sativa L.

49 mg L−1 880.35 mg kg−1 70 mg kg−1 0.064 mg L−1

L’Huiller et al. (1996) Increased resistance of stomata. Rauser & Dumbroff (1981) Higher sugar content along with deHassanpour & creased protein and carotenoid content. Rezayatmand (2015) Retarded plant growth. Rahmani et al. (2017); Roveda et al. (2016) Reduced production rate and dry matter. Gautam & Pandey (2008) Prohibited growth and yield. Pandey & Pathak (2006) Genetic imbalance. Nkongolo et al. (2018) Reduced growth. Rehman et al.

(2016)

Reduced leaf area, root, and shoot Selvaraj (2018)

length.

Prohibited growth. Sidhu et al. (2018)

77 mg kg−1

Imbalance in potassium and hydrogen flux rates in roots. Reduced growth.

60 mg kg−1

Reduced height, biomass, and yield.

150 mg kg−1

Prohibited growth accompanied with reduced biomass.

Reduced biomass.

2.34 mg L−1

586.9 mg L−1 40 mg L−1 150–500 μg/g

References

Prohibited root growth.

Palm et al. (2017)

Shahbaz et al. (2018) Kumar et al. (2018) Batool (2018)

Song et al. (2018)

Reduced leaf area, root, and shoot Selvaraj et al.

length. (2010) Overall decrease in chlorophyll content. Ahmad et al. (2007) Chlorophyll content decreased along Kamran et al. with a sharp increase in proline content. (2016)

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8.6 ESSENTIALITY OF Ni IN PLANTS 8.6.1 GROWTH AND DEVELOPMENT Normal growth of plant is facilitated by an optimum level of nickel, which is majorly taken up by the roots. Evidence supports the role of nickel in the improvement of height, cellular biomass accumulation in many plant species (Aziz et al., 2007). Scientists suggests a probable working mechanism behind this growth promoting activity where they hypothesized that Ni is one of the integral constituents of few phyto-enzymes like urease, glyoxalases, and hydrogenase which in turn can promote growth of plant parts (Sundaramoorthy et al., 2008). Brown et al. (1987) had opined that nickel plays a vital role in seed germination and development in different species, not only this Ni can stimulate the yield of several plant and anthocyanins biosynthesis (Ragsdale, 1998; Lopez & Magnitskiy, 2011). 8.6.2 BIOLOGICAL FUNCTIONALITY Though required concentration of Ni may vary from species to species but numerous studies revealed that nickel is responsible for activation of multiple physiological processes which include hydrogen metabolism, methane biogenesis, ureolysis, and acetogenesis (Dixon et al., 1975; Evans et al., 1987; Mulrooney & Hausinger, 2003). The reason behind this could be its involvement in the biosynthesis of multiple enzymes. The first documentation was done by Dixon et al. (1975), where he has proved the involvement of Ni in usease formation, and after his success, multiple other trials were also made to find some kind of association of Ni with other enzymes. By far Ni has been reported to be a constituent of numerous plant enzymes like peptide deformylase, methyl coenzyme M reductase, Glyoxalases, hydrogenase, acetyl-S-coenzyme A synthase, Ni-containing superoxide dismutase (NiSOD), and peptide deformylases (Ermler et al., 1998; Mulrooney & Hausinger, 2003; Aziz et al., 2007). Ni was also reported to contribute to the activity of glyoxalase-I (Mustafiz et al., 2014) and Bai et al. (2013) identified its role in RNAase activity during urease formation. However, Sirko & Brodzik (2000) reported that in Glycine max, urease activity depends on its attachment to nickel and this attachment is carried out by two gene products viz. Eu2 and Eu3.

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8.6.3 NITROGEN FIXATION

Nitrogen metabolism is another important aspect where Ni plays a vital role (Khoshgoftarmanesh et al., 2011; Kutman et al., 2013, 2014; Alibakhshi & Khoshgoftarmanesh, 2015). BNF (biological nitrogen fixation) in leguminous plants is also promoted by the presence of nickel (Bertrand and De Wolff, 1973). de Macedo et al. (2016) had reported that nitrogen accumulation and urease activity increase rapidly when Ni concentration get increased in the soil. Nitrogen fixation is mainly carried out by the activity of hydrogenase enzyme, which is required for oxidation of hydrogen to provide ATP for N (nitrogen) reduction in NH3 (ammonia) and here comes the role of nickel, where it is required for root nodule formation and activation of hydrogenase (Dalton et al., 1985). Thus, now we are in a position where we could interpret that Ni is an obligatory micro element for plants to function normally and it cannot be substituted by any other element. Plants wheel of life will eventually stop without this mobile element. Multiple biological processes like photosynthesis, nitrogen fixation, respiration, numerous biosynthetic pathways may directly or indirectly rely on Ni concentration. Metalo-enzymatic activity, somatic growth and development, nutrient uptake, membrane viability all these phenomena are somehow maintained by Ni2+. 8.7 EFFICIENCY OF Ni IN STRESS MANAGEMENT Now, in the following part of the chapter, we will discuss about another important prospect of Ni in plants. Out of multiple positive effects of nickel in plant body, stress tolerance is a huge factor which should be taken into consideration. Plants are exposed to different types of stress factors throughout their lifetime; in this portion we will elaborately study the behavior of Ni, a trace element of plants in different stressed conditions. Our focus will be on covering the maximum plant stress conditions imposed by several environmental conditions. A hazardous condition subjected by a plant body due to some pathogenic or nonpathogenic organisms is called biotic stress. Living organisms like bacteria, fungus, viruses, nematodes, weeds, arachnids, and insects can cause biotic stress to a host body. On the other side, environmental factors like salinity, temperature, pH level, nutrition, drought, etc., can cause abiotic stressed condition (Singla, 2016). From an agricultural point of view, all these stressed conditions can cause huge preharvest and postharvest loss.

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As we are mainly focusing on the behavior of Ni2+ ion against environmental stress thus we will discuss all the probable aspects of it in details but beside this we will also consider biotic stress control process in a nutshell. 8.7.1 DEFENSE MECHANISM AGAINST ABIOTIC STRESS Environmental stress could be natural, or human made (Cairns, 2013), it could physical like thermal stress, drought stress (DS) or chemical offend imposed to a plant. A few such stressed conditions along with the nature of Ni in such situation, stress management techniques, and interrelation between this cation and plant body in disturbed condition are discussed in subsections. 8.7.1.1 SALINITY STRESS Salinity stress is considered as one of the most inimical abiotic stresses, where autotrophic organisms are subjected to osmotic stress, oxidative stress and even ionic toxicity (Tanveer & Shabala, 2018). Osmotic imbalance caused by salt stress may lead to reduced plant growth (Haryadi, 2017), and disparity between the concentration of sodium (Na+) and other important ions (Amjad et al., 2014). Simultaneously, due to increased oxidative stress huge amount of ROS is produced inside the plant body (Amjad et al., 2015). Transpiration pathway from root to the shoot of a couple of cations like Na+ and K+ are the same for higher plants, as a result of which a natural competition always persists between them (Rus et al., 2001). In stressed condition Sodium ion level get excessively high in the soil, which causes forceful entry of Na+ ions in plant body and eventually decrease the normal growth rate and production (Li-Juan et al., 2005). Considering the utilization of Ni in salt stress, reports had been made suggesting the inhibitory effect of Ni against Na+ ion uptake, Ni additionally can stimulate K+ (potassium) ion absorption (Ain et al., 2016). A contrasting relation is observed between Ni2+ and Na+ ion uptake, nickel accumulation level is always reversely proportional to the Na+ ion accumulation. The main reason behind this can be a preference towards divalent ions over monovalent ones. Thus, in saline condition higher concentration of Ni can actually prevent the uptake of Na+ ions and facilitates the absorption of K+ ions and eventually can improve plant growth. But a few studies also depict that excessively high level of nickel (40 mg kg−1) can also provokes the effects of salt stress in plants (Ameen et al., 2019).

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8.7.1.2 DROUGHT STRESS (DS) Drought stress (DS) can be broadly categorized as a part of water stress, which is experienced by phototrophs due to less rainfall, high light intensity, extreme low or high temperature and many more (Salehi-Lisar & Bakhshayeshan-Agdam, 2016). Zia-Ur-Rehman et al. (2018) opined that DS is a condition resulting from anthropogenic climatic change, and such a situation can further stimulate several complications in morphological and physiological characteristics of plant body and osmotic imbalance is one of them. Certain evidence was put forward which hypothesize that metal hyperaccumulation can release osmotic imbalance under DS condition. A similar depiction was made by Bhatia et al. (2005), according to him; hyperaccumulation of Ni can help in osmotic adjustment of Stackhousia tryonii. DS may show hazardous water potential, somatic biomass, and shoot Ni concentration. Ni level of plant shoots get significantly higher from 3,400 µg/g to 9,400 µg/g dry weight. Transportation of Ni is done via xylem in a chelated form, and the fact is that DS cannot alter the osmotic potential of xylem sap and thus change in nickel level within xylem is osmotically insignificant. Ni can definitely play a role as osmoticum during water stress besides the role of glycine, mannitol, proline, and betaine (Hare et al., 1998). A contrasting view opined that role of Ni against water stress is not consistent and rather accidental, which may differ from plant to plant and in some species Ni concentration, may not even associated with DS releasing strategies. 8.7.1.3 TEMPERATURE STRESS Temperature stress is nowadays a very common threat to all living beings, especially to plants. It can be either excessive (high temperature stress, HT) or very low (low temperature stress, LT) and can prohibit normal functioning of cell (Balla et al., 2009) and even can cause death. Heat stress may interfere with plant metabolism, protein structure membrane properties, Oxidative potential and other several aspects (Nahar et al., 2015). HT stress in plants can induce excessive ROS content which is again facilitated by high levels of Ni2+ (Suzuki & Mittler, 2006). High temperature can lead to the formation of oxidative imbalance that can induce lipid peroxidation (LPO) (Larkindale & Knight, 2002; Vacca et al., 2004). Enzymes such as catalases (CATs), glutathione (GSH) S-transferase, ascorbate peroxidases (APX), and superoxide dismutase (SOD) may play a vital role in protection against heat stress. Here,

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again the importance of Ni should be mentioned as SOD is a nickel-based enzyme (NiSOD) (Aziz et al., 2007), apart from this Ni is an essential for GSH homeostasis, and function of GSH is regulated by Ni concentration at certain level (Fabiano et al., 2015). Studies reported that increased level of ROS can be sensed by heat shock factors (HSFs) present inside plat body which may increase the efficiency of APX1 (Storozhenko et al., 1998). 8.7.1.4 OXIDATIVE STRESS, OSMOTIC STRESS AND OTHER ASSOCIATED STRESS FACTORS Oxidative stress is not caused by a single reason rather it is generated as a result of multiple other stressed conditions. It is considered as a complex physiological and biochemical phenomenon experienced by a plant body during adverse situations. Oxidative stress normally generated due to the over-accumulation of ROS within plant cell (Demidchik, 2015). At certain concentration Ni can induce ROS production within the cellular compartments but during overproduction of ROS or at a concentration higher than permissible limit Ni2+ can eventually act as stress reliever. ROS production can bring multiple other associated stress factors in combination like retarded cellular growth, reduced photosynthesis and respiration, prohibited embryonic development, osmotic imbalance (osmotic stress), excessive production of MG, hazardous cell signaling pathways, several physiological obstructions and what not? By the production of glyoxalase I (Gly I) and GSH (reduced glutathione) Ni can actually reduce the effectiveness of these stresses. Ni2+ acts as an activator of Gly I which degrade MG molecules to maintain the oxidative and osmotic balance of plant cell. It is also known for its role in the activation of certain other glyoxalase isoforms too is different plant species (Mustafiz et al., 2014). On the other side, Ni is not directly associated with activation of GSH rather Ni is considered as a key component for maintenance of equilibrium of reduced GSH inside plant body (Mustafiz et al., 2014). From the above discussions, it could be concluded that, though Ni is considered as one of the most recently added essential microelement but it still has a lot more to serve. Its functionality is not yet been explored to its maximum and is definitely a subject to be taken into consideration. Ni has proved its functionality against several environmental stresses, but still there is a huge opportunity to explore its significance against other stressed conditions.

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8.7.2 BIOTIC STRESS CONTROL

Biotic stress is a condition when a plant body is exposed to certain pathogenic organisms like insects, bacteria, viruses, fungi, nematodes, weeds, etc., which ultimately can alter the normal physiological metabolism of the plant body. Plants may face several other problems related to biotic stress like severe diseases with visible symptoms, retardation of growth and development, disputed metabolic pathways, etc. Table 8.2 is the representation of a few biotic stress management techniques with the help of Ni. TABLE 8.2

Role of Nickel (Ni2+) in Biotic Stress Management

Name of the Plant Species Streptanthus polygaloides Gray

Noccaea goesingensis (Hálácsy) F.K.Mey.

Stress Factor Response of Stress Factor Spodoptera exigua Tetranychus urticae Delia radicum Melanoplus femurrubrum Evergestis rimosalis Erysiphe cruciferarum

Senecio coronatus Helix aspersa (Thunb.) Harv. Alyssum Pythium serpyllifolium Desf. ultimum

Death at larval stage.

References

Sharp fall in population.

Boyd & Moar (1999) Jhee et al. (2005)

Reduced survival Reduced survival

Jhee et al. (2005) Jhee et al. (2005)

Reduced survival

Jhee et al. (2005)

Resistance against the pathogen through salicylic acid metabolites like catechol, salicyl glucose, etc. Toxic cellular condition which ultimately led to death. Increased toxicity.

Freeman et al. (2005) Boyd et al. (2002) Ghaderian et al. (2000)

Hyperaccumulation of heavy metals in some metal tolerant plants can serve as a stress reliever against a few biotic stressful conditions. Pathogenic attack may cause huge synthesis of salicylic acid (SA), but at a low concentration of metal ions, these plants cannot sense salicylate signals (Freeman et al., 2005). These plants are highly susceptible to pathogenic attack under low metal concentration (Ni level). Hyper accumulation of metals in plant shoot may increase their resistance against the pathogens, thus Ni being a heavy metal can efficiently show its therapeutic effect at stressed situations and can help the plant body to cope up with the changes imposed by these stresses. The probable mechanism of action of Ni against biotic stress is schematically represented in Figure 8.2.

286

FIGURE 8.2

Biology and Biotechnology of Environmental Stress Tolerance in Plants, Volume 2

Efficiency of Ni against biotic stressors and its defense mechanism.

Abbreviations: GR: Glutathione reductase; GSH: glutathione; PC: phytochelatins; SAT: serine acetyltransferase; ROS: reactive oxygen species.

8.8 MECHANISM OF ENZYMATIC FUNCTION IN STRESS ADMINISTRATION 8.8.1 GLYOXALASES Microorganism can produce an enzyme called glyoxalase I (Gly I), which is considered to be a potent stress reliever in plants (Kaur et al., 2013). Several studies had been conducted to understand the nature of this enzyme

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in microorganisms but in plant body extensive studies are required till date. Ni2+ or Zn2+ ions are responsible for Gly I production and functionality in microorganisms. The role of nickel, in the activation of the same enzyme in Oryza sativa have been recently reported by Mustafiz et al. (2014). Kaur et al. (2013) suggested that the requirement of Ni in Gly I formation may be due to the gene expansions, imposed by stressed conditions which have led to the activation of two-domain nickel-Gly I and multiple other enzymes, and these enzymes eventually help the plant to cope up against these tough situations. Several stressful conditions may give rise to a potentially toxic, mutagenic α-ketoaldehyde known as methylglyoxal (MG) inside the plant body (Kalapos, 2008). MG production is initiated with dihydroxyacetone phosphate (DHAP) in the process of photosynthesis and glycolysis (Kaur et al., 2014) and is considered as a lethal substance to normal cellular activities. Under abiotic stress, a sharp increase in MG level (Two to six folds higher than normal) could be seen which is accompanied by the disruption in photosynthetic and glycolytic processes (Yadav et al., 2007). Higher Mg level imposes higher oxidative stress due to increased level of ROS (reactive oxygen species) within the plant body (Maeta et al., 2005; Kalapos, 2008), and advanced form of glycation final products are generated (Thornalley, 2003). This situation may interfere with antioxidant defense mechanism and will alter cell division process (Martins et al., 2001). Here comes the role of glyoxalase enzyme, glyoxalase I and II (GLY-I and GLY-II) enzyme can degrade MG and can reduce its toxicity (Ray et al., 1994). Degradation process of MG begins with an interaction between reduced glutathione (GSH) and MG, and it will result in the formation of hemithioacetal, and with the help of GLY-I, hemithioacetal is then metamorphosed into S-D-lactoylglutathione. On the other hand, the role of GLY-II is to regenerate GSH by releasing D-lactate from S-D-lactoylglutathione. The process will go on in a cyclic manner where GLY-I functionality and GLY-II reactivation alternatively maintained throughout the stressed condition. Mustafiz et al. (2011) had reported that total 11 genes are responsible for GLY-I activity and three genes encode GLY-II in Oryza sativa. Though the enzymatic expression may differ from plant to plant and may vary depending on the environmental condition, developmental stage and the severity of stress, but the MG degradation pathway seems to be almost similar in most of the dicotyledonous and monocotyledonous plants (Mustafiz et al., 2011). An overall functional pathway of glyoxalase against stress is depicted in Figure 8.3.

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FIGURE 8.3 Schematic diagram showing the efficacy of glyoxalases enzyme during stressed condition. Abbreviations: RUBP: Ribulose bisphosphate; PGAld: phosphoglyceraldehyde; DHAP: dihydroxy acetone phosphate; MG: methylglyoxal; GSH: glutathione; Gly I: glyoxalase I; Gly II: glyoxalase II.

Beside these enzymes a few isoforms have already been identified and their functionality may slightly vary from the original one under environmental stress. In seeds the gene like OsGLYI-3 and OsGLYI10 are expressed, whereas few other isoforms are reported from variable developmental stages of endosperm or embryo. An experimental study on two rice varieties, one is resistant to salinity stress and another one is susceptible, was conducted by Mustafiz et al. (2011) had revealed that in both cases, different mechanisms were adapted by the plant body due to the formation of different isoforms. Under salt stress, genes viz. OsGLYI-6 and OsGLYI-11 was over expressed. He had also added that a similar situation could be observed under extreme oxidative or osmotic stress level. From the above elaboration, we could infer that these isoforms are vital for MG metabolism, but in contrast they are much essential for stress release and to maintain normal cellular pathways. 8.8.2 GLUTATHIONE (GSH) Hazardous cellular mechanism due to oxidative imbalance in plant body can cause upraise of ROS, and this condition can be neutralized by a vital

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phytoenzyme called reduced GSH. Under stressful situation as well as in normal condition formation of GSH is necessary along with its transport and degradation (Noctor et al., 2012). GSH is always being converted to oxidized glutathione (GSSG) and then again will be converted to GSH with the help of glutathione reductase (GR), which is an NADPH dependent enzyme (Fabiano et al., 2015). GSH is also popular for its role in antioxidant metabolism (Galant et al., 2011; Noctor et al., 2012). GSH biosynthesis is an energy dependent process where two molecules of ATP are required, and two distinct phyto-enzymes were so far reported to be responsible for GSH production. The biosynthetic pathway of GSH formation is described schematically in Figure 8.4. An experiment conducted on Arabidopsis thaliana, reveals that the enzyme, gamma-EC synthase (γ ECS) which is responsible for the first step of GSH biosynthesis, is restricted to the chloroplast and is encoded by GSHI gene, whereas the second enzyme GSH synthetase is available throughout the chloroplast and cytoplasm and is encoded by GSH2 gene. Total GSH content is also comparatively higher in chloroplast (30%) and cytoplasm (50%) in Arabidopsis thaliana (Queval et al., 2011).

FIGURE 8.4 Role of Ni in activation of glutathione which eventually can release plant stress. Abbreviations: Gly: Glyoxalase; Glu: glutathione; ROS: reactive oxygen species; γ ECS: gamma-EC synthase; ATP: adenosine triphosphate; GSGS: glutathione synthetase.

Noctor et al. (2012) also added that GSH is a mobile substance which can be transported to the extra and intra-cellular compartments. Evidence suggests that GSH could be found from different cellular parts including phloem and apoplastic pathway. Despite having such amazing activities

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against oxidative stress, more extensive studies are yet required. Ni plays a vital role in GSH homeostasis, Mustafiz et al. (2014) reported the significance of nickel as an activator of GLY-I isoform, OsGLY11.2 in Oryza sativa. During oxidative stress Ni could maintain the cellular redox potential. In the process of GSH regeneration, GLY-I activation is totally dependent on nickel and thus Ni can be considered as a key component for degradation of MG through the activation of GSH under stressed situations. 8.8.3 UREASE Ni is mainly known for being an active constituent of urease enzyme of plant body, which can hydrolyze urea (Eskew et al., 1983, 1984). Urease can metabolize ammonia (NH3) from toxic urea (Figure 8.5) and the nitrogen from NH3 is further used for the biosynthesis of polyamine, amino acids and other nitrogenous compounds (Gerendás & Sattelmacher, 1997, 1999).

FIGURE 8.5

Utility of urease enzyme to cut off the toxicity of urea.

Inside the plant body urease is present in two different forms, one in vegetative tissues and another one in seeds. The forms present in vegetative tissues are comparatively less reactive, this only serves as an important component in nitrogen recycling (Hogan et al., 1983), and the forms in seeds

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are highly reactive (Polacco et al., 2013). Urea can be accumulated at an excessive level under multiple stressed conditions; thus, urease activity is very much essential for a plant body to release the toxicity produced by urea. 8.9 FUTURE PROSPECT Environmental stress or abiotic stress is something, which a plant cannot avoid. Even in certain cases, the effectiveness of these natural factors imposed to a plant is so high that it can cause more harm than many pathogenic infections, and thus plants have shown many altered physiological activities which can eventually either neutralize these stress conditions or help them to adapt the stress condition. On contrary, metals are those elements that can cause severe stress to a plant body at a higher concentration. Hyperaccumulation of many of these metals can lead to severe injury to photoautotrophs, and nickel is one of them. Nickel is considered as comparatively new metal to be grouped under essential micro-elements for plants, and it is the main reason behind its unexplored prospective. Several research works had been made to understand its role in plant body, to evaluate the effects of its hyperaccumulation and even its status in soil or the transportation process in plants, but when it comes to stress management scenario then it’s quite true that nickel is far behind as compared to all the other microelements. Though a few reports were made regarding the role of nickel against certain abiotic and biotic stress factors but the documentation made so far is not sufficient enough to understand the mechanism of action against these stressors. Even many abiotic stress conditions are there against which the exact functionality of this microelement is still not known. And this can give a firm platform for researchers to evaluate the efficiency of Ni against environmental stress. Apart for this multiple experimental works can be conducted to recognize the mode of action against environmental stress and along with this, it will give a golden opportunity to the researchers to evaluate whether there are some other abiotic stress factors against which nickel have some functional activity or not. 8.10 CONCLUSION Stress is considered as a hazardous or abnormal situation where plants metabolism gets affected with multiple different anomalies. This tensity can either be caused by some environmental stress factors, i.e., abiotic stress or

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by the interaction of some living organism, i.e., biotic stress. Whatever may be the cause, this situation can bring multiple alterations in photoautotrophs like retarded physiological activities, inhibited growth and development, reduced nutritional uptake and the list continues. To combat against these stresses, plants can show variable adaptations under stressful conditions. Among multiple stresses subjected to plant body heavy metal stress is one of the major concerns. Sustainable development has led to huge production of these heavy metals from industrial and municipal practices, and nickel (Ni) is amongst them. It is dispersed throughout the atmosphere, weather be soil, water or air but at a very trace amount. Similar to most other heavy metals, Ni also contributes in phytotoxicity. Hyperaccumulation of Ni can cause multiple significant damages to the plant body and this condition is popularly known as Ni toxicity. But the most contrasting feature was put forward by some scientists when they observed that Ni at a low level can serve several positive functionalities of plants like nitrogen metabolism, phyto-enzyme activation or biosynthesis, development of embryo, etc. Reports also suggest the positive participation of this cation in autotrophic growth and development, besides this Ni is recently categorized under essential micro elements of plants. Photoautotrophs can access the available Ni content from soil in soluble ionic form, and after absorption through the roots, Ni molecules are transported to upper areal parts via xylem and get distributed to the whole body. Ni accumulation depends on a few factors like plant species, soil type, environmental conditions, etc., and in post-accumulation phase Ni molecules are compartmentalized and mainly stored in vacuoles. The most surprising fact is that being a heavy metal also, Ni can serve as a plant-stress reliever. Ni can activate and produce certain enzymes in plant body which in turn can act as stress controlling agents. Enzymes like urease, hydrogenase, glyoxalase, NiSOD, and reduced GSH can top the list. Studies also revealed that hyperaccumulator plants of Ni can naturally show resistance against pathogenic or herbivores attack, in these species, deficiency of nickel can provoke the fragility towards those biotic stress factors. Thus, it could be inferred that Ni has the efficiency to control both biotic and environmental stresses either by direct interaction or indirectly by forming some other stress suppressing agents. Although, Ni is being acknowledged for its utility in plant defense mechanism in plants but it should be kept in mind that furthermore extensive studies are required to understand its working mechanism fully. Moreover, as nickel has been recently categorized under mobile essential microelements, not much information is yet available, which gives a strong platform for future experiments and studies.

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KEYWORDS

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A. thaliana cobalt herbivores attack nitrogen parts per million salinity stress soil ecology

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CHAPTER 9

Role of Cobalt in Plant Growth and Tolerance Against Different Environmental Stress

DEBABRATA PANDA,1* PRAFULLA K. BEHERA,1 and JAYANTA K. NAYAK2 Department of Biodiversity and Conservation of Natural Resources, Central University of Odisha, Koraput – 764021, Odisha, India, Tel.: 91-6852-251288, Fax: 91-6852-251244

1

Department of Anthropology, Central University of Odisha, Koraput – 764020, Odisha, India

2

*

Corresponding author. E-mail: [email protected]

ABSTRACT Cobalt plays a critical role in the overall growth process of plants, and it is considered as one of the emerging novel bio-stimulants and beneficial elements that help in productivity at its lower concentrations/dosages. Cobalt is a transition element and plays a vital role in nitrogen fixation in leguminous plants and somewhat, essential component of various enzymes and co-enzymes. Additionally, Cobalt alleviates different stresses such as salinity stress, heavy metal stress and drought stress (DS), promotes uptake of other nutrients, etc., and it also showed toxicity levels in different plants at its higher concentration. In brief, at its lower concentration Co enhances plant growth and yield and also maintains mineral composition; however, at its higher concentrations, Co decreases germination rate, seedling growth, suppresses root nodulation, photosynthesis, etc. Thus, proper application of Co at its lower dosages might be useful for crops growth and productivity. Biology and Biotechnology of Environmental Stress Tolerance in Plants: Trace Elements in Environmental Stress Tolerance, Volume 2. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

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In this chapter, we focus mainly on the properties of Co, its physiological effects, Co uptake, translocation, and its accumulation in plants, as a beneficial element in alleviating different stresses and its toxicity effects in various plants have been discussed. 9.1 INTRODUCTION Plant requires essential nutrients elements and some beneficial elements as nutrients for their growth and production in their life cycle (Rashmi et al., 2020). In most plants, beneficial elements are said to be not requisite, however, these elements can advance and be helpful in growth and development for certain plants under specific circumstances (Gómez-Merino & Trejo-Téllez, 2018). Among 10 beneficial elements, Cobalt plays a critical role in the overall growth process of plants, and it is considered as one of the emerging novel bio-stimulants and beneficial elements that help in productivity at its lower concentrations/dosages (Gómez-Merino & TrejoTéllez, 2018). Cobalt (Co), a heavy metal and transition element, which is a crucial component of various enzymes and coenzymes, is found in nature in a variety of chemical forms (Palit et al., 1994; Marschener, 1995; Lwalaba et al., 2017; Akeel & Jahan, 2020). Cobalt is an important element for Vitamin B12 synthesis, and its requirement is for human and animal nutrition. The Co is also safe for human ingestion, with daily dose up to 8 mg posing no health risk (Young, 1983; Minz et al., 2018). Based on different concentration and levels of Co in soil found to be altering growth, physiological processes and metabolism in varying degrees in different plant species (Palit et al., 1994). In comparison with other heavy metals or trace elements (TEs), Cobalt can have both positive and negative impacts by preventing the uptake of harmful elements like Cd, Pb, as well as decreasing the uptake of important elements like Ca and Fe (Lwalaba et al., 2017). Cobalt has been found in high concentration in acidic or calcareous soil along with peaty soils (Lwalaba et al., 2017). Furthermore, due to industrial operations as well as automobile and aviation emission, Co concentration and pollution level in soils going increasing day-by-day and has become worse (Chatterjee & Chatterjee, 2000; Sree & Appenroth, 2015; Lwalaba et al., 2017; Akeel & Jahan, 2020). The distribution of Co in different plants said to be crop-specific and co-toxicity proportions are determined by plant species-specific, soil type and soil chemistry (Akeel & Jahan, 2020). At higher Co concentration and toxicity, it affects various physiological and biochemical processes in several plants like

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affecting seed germination, photosynthesis, leaf chlorosis and necrosis, root browning, plant height (Pandey & Sharma, 2002; Sree & Apprenroth, 2015; Akeel & Jahan, 2020). Some literature also revealed that Cobalt suppresses root development by slowing down cell division, transportation of water and blocking nutrient uptake in plants has been reported (Jayakumar et al., 2008; Akeel & Jahan, 2020). However, supplementation of Cobalt at lower concentration or dosages, have a positive impact on various critical processes and they can also enhances tolerance mechanism to abiotic stresses, as well as improve the intake of other nutrients (Gómez-Merino & Trejo-Téllez, 2018). Moreover, various studies have revealed about beneficial biological activities of Cobalt in plants such as drought stress (DS) tolerance, nitrogen fixation in leguminous plants, salinity tolerance, chlorophyll b biosynthesis, alkaloid accumulation, etc., in different plants at its lower dosage/concentration (Kaur et al., 2016; Gómez-Merino & Trejo-Téllez, 2018; Khan et al., 2018). Based on above circumstances, the present chapter described about sources of Cobalt, its associated properties, impact of Cobalt at lower and higher concentration in different plants, the potency of Co in different stress alleviation, and effect of Co on leguminous plant has been presented in a lucid manner. 9.2 SOURCES OF COBALT AND ITS DIFFERENT FORMS IN THE ENVIRONMENT The representation of Cobalt in the periodic table as transition metal and it seems to have chalcophile, lithophile, and siderophile characteristics (Kosiorek & Wyozkowski, 2019), i.e., occurrence of sulfides forms of Co in Earth’s mantle (below part) manifests Chalcophile properties, presence of Cobalt at Earth’s crust silicate layer represents lithophility characters of Cobalt (Lock et al., 2006; Koch et al., 2007; Kosiorek & Wyozkowski, 2019), while occurrence of Cobalt at core part of earth’s crust is due to low affinity of Co towards O2 and Sulfur which symbolizes siderophile characteristics of Cobalt occurrence in the Earth’s crust (Lock et al., 2006; Kosiorek & Wyozkowski, 2019). Sheppard et al. (2007) documented that presence of Co in its natural form not more than 12 mg/kg and alkaline igneous rocks assumed to be biggest accumulator of Co with about 200 mg/kg but acidic igneous rocks containing 15 mg/kg of Co only (Kosiorek & Wyozkowski, 2019). Luo et al. (2010) revealed about minerals such as cobalite, linnaeite, safflorite, smaltite, and spherocobaltite are the various sources of Cobalt (Kosiorek

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& Wyozkowski, 2019). The soil pollution due to Co has an influence on different TEs, which may cause enhancement of Pb, Cr, Ni, and Zn in the soil (Li et al., 2009; Swarnalatha et al., 2013; Kosiorek & Wyszkowski, 2019). Naturally, alluvial, and loamy soils having higher Co content (12 mg/kg) but silty and podsolic soil with 5.5 mg/kg Co (Tappero et al., 2007). The mobility of Co in soils is modest and after being introduced into the soil, it is anticipated that 95% of Co remain under depth of 5 cm and generally does not move (Edwards et al., 2012; Narendrula et al., 2012; Kosiorek & Wyozkowski, 2019). Improper fertilizer application, pesticides, and sludge from municipal sewage plants are the main causes increasing amount of Cobalt in the soil (Ebrahimi et al., 2009; Li et al., 2014; Saaltink et al., 2014; Defarge et al., 2018). 9.3 PHYSICAL AND CHEMICAL ATTRIBUTES OF COBALT According to Arnon & Stout (1979), an element is said to be essential, it must fulfill three criteria such as: (i) a plant need mineral element to complete its life cycle; (ii) the function of one element cannot be replaced by other element; and (iii) the element is directly regulates and functions in plant metabolism (Kaur et al., 2016). Cobalt (Co) is a heavy metal and transition element (Akeel & Jahan, 2020) and an important component of various enzymes and co-enzymes (Palit et al., 1994; Akeel & Jahan, 2020) and naturally occurring in the atmosphere in many various chemical complexes and different forms (Akeel & Jahan, 2020). In terms of abundance in nature, the element Cobalt (Co) has been given 32nd rank in comparison to all the elements and considered as 19th position of the TEs (Liu, 1998). Co has the following properties: cubic crystalline shape, atomic number (27), atomic mass about 58.9, density of 8.9 g/cm3, melting and boiling point is about 1,495°C and 2,870°C, respectively (Lison, 2007, 2015). 57Co, 58Co, and 60 Co are the primary radioactive isotopes of Cobalt have 272, 71, and 5,271 years of half-lives, respectively, and generate γ-rays (Lison, 2007, 2015). Cobalt has two oxidation states such as Co (II) and Co (III), among them Co (II) oxidation state is a most stable form (Lison, 2007, 2015). Vitamin B12 is the biologically significant Co molecule, where Co is making complex compound with four pyrrole nuclei connected in a corrin ring, which is comparable to porphyrins (Lison, 2015). Co (II) ions can create hydroxyl radicals through a Fenton-like process in the presence of H2O2 and chelating agents can modify Co (II) oxidation potential to facilitate the radical formation (Mao et al., 1996; Lison, 2007, 2015).

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9.4 BIOCHEMICAL ASPECT OF COBALT IN PLANTS Nitrogen (N2) fixation in blue-green algae and leguminous plants by involvement of Cobalt has been a well-established fact (Pilot-Smits et al., 2009). Although some experiments have shown that Co availability is beneficial for growth and metabolism of plants (Akeel & Jahan, 2020). The mechanism through which Cobalt works as a “beneficial” agent on plant metabolism at low doses is currently unknown or little research has been done; however, some beliefs that interaction of Co with other metals in a cross-linked manner shows positive responses under low concentrations (Akeel & Jahan, 2020). Many growth mechanisms are linked to Cobalt salts such as hypocotyls hook opening, extension of stem and coleoptile, enlargement of leaf disc, and bud development (Thimann, 1956; Klein, 1959; Akeel & Jahan, 2020). According to available literature on Cobalt’s role in nitrogen fixation, it has been believed that Cobamide coenzymes are involved in H atom migration during ammonia (NH3) synthesis with the support of rhizobia (Nicholas, 1975). Several studies have revealed that in higher plants, maintenance of various biochemical and physiological processes has been regulated by Co at its lowest concentration (Nagajyoti et al., 2010). DalCorso et al. (2014) reported that Co decreases transpiration rate and regulation of plant water status resulting in maintaining many vital biological processes occurring in plants (Akeel & Jahan, 2020). As per Dilworth et al. (1979) deficiency or unavailability of Cobalt lead to decreased in nitrogen fixation due to restrain of leghemoglobin generation in case of legumes. 9.5 IMPACTS OF COBALT IN VARIOUS PLANTS The beneficial elements like Cobalt has beneficial effects in different plants like cowpea, tomato, maize, rice, and finger millet, etc., at lower concentration of Co, however the higher dosages of Co in various plants shown to having toxicity and detrimental effects at multilevel like seed germination inhibition, decreasing plant growth and biomass, chlorosis, necrosis, etc., (Figure 9.1) as reported by various researchers in their experimental work has been presented in Figure 9.1; Tables 9.1 and 9.2 (Khan & Khan, 2010; Gad et al., 2013; Arif et al., 2016; Asati et al., 2016; Kaur et al., 2016; Akeel & Jahan, 2020). The lower concentrations of Co have positive effects in different plants like increase in growth and yield, nodulation, and nitrogen fixation and boosts nutrient uptake, etc. (Figure 9.1).

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FIGURE 9.1 Impact of Cobalt in different plants at lower and higher concentration (Akeel & Jahan, 2020).

9.5.1 EFFECTS OF LOWER COBALT CONCENTRATION IN DIFFERENT PLANTS The literature regarding beneficial elements has provided that beneficial elements like Co, Fe, etc., plays a beneficial role in different plants at its lower concentration (Arif et al., 2016). Previous studies on Co effect in different plants at lower concentration was described by Zhu et al. (2000); Jayakumar et al. (2008); Khan & Khan (2010); Jaleel et al. (2008); Nagajyoti et al. (2010); Gad et al. (2013); and DalCorso et al. (2014) (Table 9.1). An experiment by Nagajyoti et al. (2010) illustrated that Co stimulates critical biochemical and physiological processes in plants at lower concentrations or within an optimal range. DalCorso et al. (2014) also studied cobalt benefits in plants at optimum condition to plant growth development because it regulates plant water use and reduces transpiration (Arif et al., 2016). In a study, the cobalt level (0.1–10 µg/g) was enhanced the positive benefits and normal functioning of plants at lower concentration (Bakkaus et al., 2005). The effects

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of Cobalt in tomato plant has been studied by Gad & Hassan (2013) revealed that 7.5 ppm of Cobalt was improved the growth, nutritional status, chemical constituents, fruits quality and yield of tomato found in their experimental investigation (Gad & Hassan, 2013; Arif et al., 2016). Similarly, the effects of lower cobalt concentration, i.e., 5 µg/L in finger millet and rice genotypes studied by Jayakumar et al. (2008) revealed about enhanced seed germination rate, increment of radical and plumule length in the studied genotypes was observed (Jayakumar et al., 2008; Arif et al., 2016) (Table 9.1). In another study reported that 50 mg/kg of Co concentration caused positive responses in maize plant shown that enhancement of seedling growth, sugar, starch, chlorophyll content, protein, and mineral content has been observed by Jaleel et al. (2008) in their experiment (Table 9.1). TABLE 9.1 Plants Studied Cowpea

Tomato Maize

Rice and finger millet Chickpea

Effect of Cobalt (Co) Concentration on Various Plants at Low Concentration Low Cobalt Effects on Different Plant Concentration 8 ppm The plant growth and yield of tomato plant was increased, induction of nodule, maintenance of chemical components and mineral level was also observed. 20 mM CoSo4 Improvement of growth, antioxidant enzyme (SOD and CAT) was increased 50 mg/kg Enhancement of seedling growth, total sugars, starch, chlorophyll a, chlorophyll b, total chlorophyll content, amino acids, mineral, and protein content was visualized in maize plant. 5 µg/L Seed germination improvement, plumule length and radical length were enhanced. 0, 10, and 50 Maintains of seed germination, plant ppm growth, biochemical constituents

References Gad et al. (2013); Arif et al. (2016)

Zhu et al. (2000); Kaur et al. (2016) Jaleel et al. (2008); Arif et al. (2016)

Jayakumar et al. (2008) Khan & Khan (2010)

9.5.2 EFFECTS OF HIGHER COBALT CONCENTRATION ON DIFFERENT PLANTS Beneficial heavy metals in large concentrations can disrupt the soil ecology, negatively impacting soil fertility, plant growth, and development (Arif et al., 2016). Previously various studies by different researchers such as Parmar &

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Chanda (2005); Khan et al. (2006); Liu et al. (2000); Jayakumar et al. (2008); Khan & Khan (2010); Kaur et al. (2016); and Akeel & Jahan (2020), etc., has been revealed about toxic, harmful effect of higher concentration of Co on different plants (Table 9.2). The higher concentration of Cobalt (25–100 µg/L) in finger millet and rice genotypes decreased seed germination, radical, and plumule length and growth of studied plants was observed (Jayakumar et al., 2008). The higher toxicity level of Cobalt was shown to decrease the growth of shoot and biomass of tomato, barley, and oilseed rape plant (Li et al., 2009). The study on chickpea plant at high dosages of Cobalt, i.e., 100, 200, and 400 ppm resulted in toxicity level in chickpea-like inhibition of seed germination, growth, and biomass, root nodulation, and chlorophyll content was observed (Khan & Khan, 2010; Arif et al., 2016). The study on the effects of higher cobalt concentration on maize plant decreased the seed germination and germination index in maize genotypes was observed (Ebru, 2014). Moreover, the experiment on seedlings of cucumber and tomato also revealed that high amount of Co concentration (> 18 ppm) impeded ethylene generation in studied plants (Gad & Atta-Aly, 2006). TABLE 9.2 Plants Studied Mung beans

Effect of Cobalt (Co) on Various Plants at Higher Concentration

High Cobalt Effects on Different Plant Concentration 5 µM The higher cobalt level decreased seedling growth, chlorosis, and Fe level decrement in leaves, and Mn level decreased in roots. Maize 125, 250 mg/L Decreased in seed germination and genotypes Co and 160 negatively affects seed germination index mg/L Ni in maize plant was observed. Chickpea 100, 200, and Seed germination decrement, reduction 400 ppm in plant growth and biomass, chlorophyll content, root nodules, and inhibiting of functional nodules.

References Liu et al. (2000); Arif et al. (2016) Ebru (2014)

Khan & Khan (2010); Arif et al. (2016)

9.6 ABSORPTION AND UPTAKE MECHANISM OF COBALT IN PLANTS Understanding the uptake and transport processes of beneficial or TEs like Cobalt in plants and within between tissues and cell compartments, are critical to demonstrate their beneficial effects in various plants (Kaur et al., 2016). Soil pH is considered to be a critical factor in Co uptake in roots

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and inversely proportional to its uptake process, i.e., enhancement of Co uptake with declining of pH (Kaur et al., 2016). The absorption of Cobalt from soil occurs in plants due to the availability of mobile Cobalt content in the soil as well as Co supplementation in solution forms (Akeel & Jahan, 2020). Some researchers reported that “IRT1 – an Iron (Fe) transporter of Arabidopsis thaliana” to aid in the cobalt uptake into plant cells, as a result ‘IRT1’ transporter are involved in Co2+ absorption in roots (Korshunova et al., 1999; Kaur et al., 2016). Co-absorption in plants is similar to that of other heavy metals (e.g., Fe, Mn) and is carried by complex organic molecules (MW 1,000–5,000) with a negative charge (Akeel & Jahan, 2020). Cobalt (Co2+ ion) is transported across cortical cells by active transport and passive diffusion and transpirational flow is the primary mode of upward transport in the xylem tissue (Kaur et al., 2016). Chemical fertilizers and liming are also known to alter Co solubility and are a key source of Co for plants (Akeel & Jahan, 2020). Kloke (1980) discovered that leafy plants such as cabbage and brassica tend to acquire and accumulate a substantial quantity of Co in their life cycle. 9.7 PHYSIOLOGY OF COBALT ACCUMULATION AND TOLERANCE Cobalt is a transition metal with 7 potential oxidation states and out of which Co (II) and Co (III) oxidation states are considered as suitable for physiological conditions in plants which symbolizes it as catalyzer in Fenton processes (Lange et al., 2017). The availability of Co in soil determines the level of Cobalt in plants and those plants which are growing in Co-enrich soil said to have a higher amount of Cobalt in their tissues (Johnston & Proctor, 1977; Akeel & Jahan, 2020). The potency of a plant to absorb Co is another aspect that contributes to its accumulation. Generally, Co is a rare metal, and it is less abundance with concentrations ranging from 15 to 25 parts per million (ppm) in soils and 0.04 ppm in natural waterways and 0.1–10 ppm in plants (Palit et al., 1994; Pilon-Smits et al., 2009). The review on hyperaccumulators plant had reported about 26 numbers of Cobalt hyperaccumulators, with over 1,000 ppm Co concentration in their leaf tissues and among the hyperaccumulators most of them are belongs to Asteraceae, Fabaceae, Lamiaceae, and Scrophulariaceae families (Baker et al., 2000; Pilon-Smits et al., 2009). In case of plants, Co affects Fe homeostasis and compete with Fe for accessibility to transporters and in case of A, thaliana plant ‘IRT1’ transporter can transport Co into epidermal cells of root (Barras & Fontecave,

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2011; Lange et al., 2017). IREG1/FPN1 and IREG2/FPN2 transporters have a function in remediation of Co once within cells and ‘IREG2/FPN2’ transporter transports Co2+ into vacuoles of cortical and epidermal cells of roots, allowing Co to be sequestered in the root’s outer layers (Lange et al., 2017). Morrissey et al. (2009) reported that ‘FPN1’ transporter loads Co in xylem tissue and transport it into the shoots of plant (Lange et al., 2017). According to Morrel et al. (2009) ‘HMA3’ transporter also transports Co2+ into vacuoles with other metallic ions. The mechanisms behind Co accumulation and tolerance are little known. Cobalt’s direct role in abiotic stress tolerance is primarily through antioxidant regulation in plant systems, which indirectly scavenge ROS and inhibit toxicants (Khan et al., 2018). Plants that hyperaccumulate Cobalt have most likely acquired Fe homeostatic systems to deal with the targets of Co toxicity (Pilon-Smits et al., 2009; Sahanmugam et al., 2011; Lange et al., 2017). An efficient Co detoxification mechanism is also to minimize the accumulation of free ions that can cause oxidative stress (Lange et al., 2017). 9.8 BENEFITS OF COBALT SUPPLEMENTATION IN ALLEVIATION OF VARIOUS ENVIRONMENTAL STRESSES IN PLANTS Cobalt has various beneficial biological activities in plants, including drought tolerance, biosynthesis of chlorophyll b, N2 fixation in leguminous plants, salinity resistance, etc. (Kaur et al., 2016; Khan et al., 2018; Akeel & Jahan, 2020) has been described in subsections. 9.8.1 DROUGHT STRESS (DS) TOLERANCE IN PLANTS Drought stress (DS) has a detrimental effect on the growth and yield of different plants, some research studies have proved to be supplementation of Co has enhanced the drought resistance capacity in different plants (Gad et al., 2019). The study on tomato and potato plant by supplementation of Co about 3 mg Kg–1 dry soil has enhanced the water absorption ability, leaf water content, decreased water scarcity and wilting coefficients as a result enhancing drought tolerance in tomato and potato plant as reported by Egrove (2000) in their experiment (Gad et al., 2019). Similarly, in 2001, Duan & Auge revealed about cobalt solution that when seeds of soybeans were soaked in prepared solution of Co reduced the impact of moisture stress on growth of soybean to some extent (Gad et al., 2019). Further studies on

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beneficial effects of Co in maintaining soil moisture stress by Anter & Gad (2001) reported that cobalt treatment decreased the transpiration rate and under water deficit or drought circumstances, the low Co-treatment has beneficial effects like maintaining leaf water potential, hormonal levels (auxin, gibberellins, and abscisic acid (ABA)), and regulating xylem and phloem tissue (Anter & Gad, 2001). Some research studied on P. vulgaris also shown that Co-treatment has enhanced hormones (ethylene and ABA) under DS which in turn decreases plant water loss (Schautmann & Wenzel, 2002). Furthermore, the application of Cobalt on bean plant subjected to irrigated water level revealed that growth, mineral composition and yield of bean plant was enhanced (Gad et al., 2019). The experiment on potato seedlings subjected to osmotic stress revealed that application of Cobalt in the nutrient medium has shown positive responses and helps in decreasing polyamine, antioxidant enzymes which adapts protective effects in the leaves of potato by reducing membrane damage (Li et al., 2004; Akeel & Jahan, 2020). 9.8.2 SALINITY STRESS ALLEVIATION Salinity stress is also considered as precarious stress and has adverse effect on growth and yield of plants by altering physiology and metabolic activities in different plants (Akeel & Jahan, 2020). Hence, it is important to identify and explore cobalt benefits in alleviating salinity stress in plants as it is a beneficial element at lower concentration pointed out by several researchers through their experimental work (Gad, 2005; Gad & Kandil, 2011; Gad and El-Metwally, 2015; Gad et al., 2018; Akeel & Jahan, 2020). Gad (2005) studied the effect of different Cobalt concentration in enhancing salinity tolerance in Tomato plant and the authors revealed that positive effect of 7.5 ppm Co concentration supplementation in enhancing salinity level in tomato plant by maintaining spongy, lower epidermis and blade thickness tissues (Gad, 2005). The study on wheat plant regarding Cobalt potency in alleviating salinity stress has been reported that 15 ppm dosages of Co has increased growth and yield of salinity treated plants and also significant tolerant capacity of wheat seedlings to salinity treated soil as compared with control (Gad & Kandil, 2011; Akeel & Jahan, 2020). Similar study on maize plants under salt stress condition reported that Co (15 ppm to 17.5 and 20 ppm) application increased growth parameters like shoot and root length, leaf area, fresh and dry weight, etc., and hormones (auxins, cytokinins, and

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gibberellins), micronutrients and macronutrient content under salinity condition was observed (Gad & El-Metwally, 2015; Gad et al., 2018; Akeel & Jahan, 2020). The above-studied experimental findings showed that Cobalt can be used to alleviate salt stress in areas where saline water is used to irrigate plants (Akeel & Jahan, 2020). 9.8.3 HEAVY METAL (CADMIUM) STRESS ALLEVIATION Some research studies revealed that Co alleviates cadmium stress in plants. Cadmium is one of the heavy metals which toxicity level affects growth and physiological processes in different plants. Plants exposed to cadmium experience oxidative stress in plants led to inhibit photosynthesis and respiration metabolism causing yield reduction (Akeel & Jahan, 2020). In an experimental investigation on the function of Co in alleviating Cd stress in different soybeans seedlings was carried out by Chmielowska-Bak et al. (2014) presented by Akeel & Jahan (2020) in their chapter on Cobalt. The authors carried out Cd stress treatment by application of Cobalt (CoCl2) and without Co as control and reported that Cobalt modulates expression of 1-aminocyclocyclopropane-1-carboxylic acid synthase enzyme which is involved in ethylene production in different plants (Akeel & Jahan, 2020). Further the authors also reported that following few hours of treatment in soybeans seedlings, the expressed gene was repressed, hence they concluded that under Cd stress treatments Co (CoCl2) can be used as ethylene inhibitor (Chmielowska-Bak et al., 2014; Akeel & Jahan, 2020). 9.9 IMPACTS OF COBALT ON LEGUMINOUS PLANTS Based on classification, Co is assumed as beneficial element due to its nitrogen fixation ability in leguminous plants, and in addition to that, it is also having several other metabolic activities in leguminous plants (Reisenauer, 1960; Akeel & Jahan, 2020). Previously various studies by Kandil (2007); Jaleel et al. (2008); Jayakumar & Jaleel (2009); Khan & Khan (2010); Sahay & Singh (2012); Gad et al. (2013); and Kandil et al. (2013), etc., has been carried out the experiment about effects of Cobalt treatment on various leguminous plants. The experiment on Soybean in responses to Cobalt was reported that the growth parameters like shoot and root length, leaf number, fresh and dry weight of seedlings, nodules number

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were enhanced under 12 mg/kg Co-treatment in soybean seedlings (Kandil et al., 2013) and with the increasing dosage of Co decreased the growth parameters (Minz et al., 2018). The field experiment on Faba bean by the application of Cobalt (CoSO4) concentration of 0 ppm, 5 ppm, 10 ppm, 15 ppm, 20 ppm revealed that the elevated level of growth and yield parameters were observed in response to 20 ppm of CoSO4 treatment (Kandil, 2007; Minz et al., 2018; Akeel & Jahan, 2020). The impact of Co on growth and yield parameters of lentil carried out by Sahay & Singh (2012) revealed that at 6 kg/ha Co-treatment, increased the growth, yield parameters, also grain and straw yield was observed as compared to lentil grown without application of Cobalt (control condition) (Sahay & Singh, 2012; MInz et al., 2018; Akeel & Jahan, 2020). In leguminous plants, nodulation involved in nitrogen fixation occurs, and an elevation in nodulation also resulted in enhancement of nitrogen fixation in legumes (Kandil, 2007; Gad, 2012; Vijayarengan, 2012; Minz et al., 2018; Akeel & Jahan, 2020). It has been well-established fact that, at lower dosage/concentration, Cobalt (Co) promotes greater nodulation and, as a result, better growth and yield; yet, at maximum concentration, Co reduces the bacterial community resides in the rhizosphere, causing modulation to be hampered, resulting in decreased crop growth and production (Minz et al., 2018). The experiment on Co impact on Cowpea and soybean plant nitrogen fixation was carried out by Yadav & Khanna (1983) revealed that Co (1.5 ppm) fixed nitrogen about 3.5% and 7.0% in two cowpea genotypes, but in case of soybean, Co (2.5 ppm) increased 3.3% and Co (3.5 ppm) treatment showed 13.4% increment in nitrogen fixation respectively in their experiment (Yadav & Khanna, 1983). Some research studies also showed that Cobalt treatment in Faba beans, groundnut, and hyacinth bean had enhanced the nodule number (Kandil, 2007; Younis, 2011; Gad, 2012; Akeel & Jahan, 2020) which in turn helpful in increased amount of nitrogen fixation. In brief, the addition of Co boosted the production of nodules in the roots and nitrogen fixation by microorganisms, resulting in a higher amount of nitrogen in leguminous plants (Minz et al., 2018). Some researchers like Basu et al. (2006); Kandil et al. (2013); and Manal et al. (2016) also suggested that exogenous supplementation of Co shown to enhance nutrient uptake capacity in leguminous plants (Akeel & Jahan, 2020). Kandil et al. (2013) reported that Co (12 mg/kg) treatment in soybean seedling enhanced the NPK (Nitrogen, Phosphorus, and Potassium) level. Similarly, 0.24 g/L and 0.48 g/L Cobalt supplementation in broad bean (foliar treatment) suggested beneficial effects of nutrient uptake (Manal et al., 2016; Akeel & Jahan, 2020).

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9.10 IMPACT OF COBALT ON NON-LEGUMINOUS PLANTS In the case of medicinal plants, increased drought resistance, delayed leaf senescence, regulation of ethylene production, and control of alkaloid accumulation are all stimulatory function of Cobalt involved (Akeel & Jahan, 2020). The low dosage of Cobalt enhances quality and grain yield in Triticum aestivum plant (Wen-Hua et al., 2004). Jayakumar et al. (2008) investigated the effect of lower cobalt application about in rice and finger millet genotypes shown that positive impact on studied genotypes in the form of seed germination improvement, increment in plumule and radical length. Similarly, in case of maize plants showed growth and biochemical function improved and at 50 mg/kg Co containing soil enhanced the chlorophyll pigment, nutrient status as compared to maize plants grown under control condition (Jaleel et al., 2009; Akeel & Jahan, 2020). In another study on maize also revealed about beneficial effects on growth and yield with the application of Cobalt as a treatment in maize seedlings (Gad & El-Metwally, 2015). The authors also suggested rising of Co-treatment ranges from 15 to 20 ppm has significantly hiked the biomass, seedling height and area of leaves has been reported in maize plant subjected Co application (Akeel & Jahan, 2020). 9.11 CONCLUSION AND FUTURE OUTLOOK The authors have concluded that Cobalt is a beneficial element for regulating different functions and metabolic activities in higher plants, but it is essential and plays an important role in nitrogen fixation and nodule development in leguminous plants. Cobalt, at its lower concentration, plays a vital role in growth, yield, nitrogen fixation, and nutrient uptake in legumes, alleviation of environmental stresses like drought, salinity, osmotic stress, and heavy metal (cadmium stress) in various plants has been reported. However, Cobalt at its higher concentration poses adverse effects in different plants, which alters physiological and metabolic activities like growth retardation, photosynthesis, respiration, chlorosis, and necrosis in young leaves, etc., eventually reduces plant productivity which is a challenge for food security in the modern world. The mechanism associated with positive responses of Cobalt at its lower concentration is not fully understood. The impact of beneficial element like Cobalt at lower dosages demand additional investigation, not only because it will throw more light on basic plant nutrition function and processes, but also due to application of fertilizing with beneficial nutrients may enhance crop output and have an impact on the nutritional value of plants as feed or food.

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KEYWORDS

• • • • • • •

abiotic stress abscisic acid beneficial elements cobalt indole-3 acetic acid leguminous plants nitrogen fixation

REFERENCES Akeel, A., & Jahan, A., (2020). Role of Cobalt in plants: Its stress and alleviation. In: Naeem, M., Ansari, A., & Gill, S., (eds.), Contaminants in Agriculture (pp. 339–357). Springer, Cham. Anter, F., & Gad, N., (2001). Cobalt absorption in relation to plant water balance. Egypt. J. Soil Sci, 41(1, 2), 111–122. Arif, N., Yadav, V., Singh, S., Singh, S., Ahmad, P., Mishra, R. K., Sharma, S., et al., (2016). Influence of high and low levels of plant-beneficial heavy metal ions on plant growth and development. Front. Environ. Sci, 4, 69. Arnon, D. I., & Stout, P. R., (1939). Experimental methods for the study of the role of copper, manganese, and zinc in the nutrition of higher plants. Am. J. Bot, 26, 144–149. Asati, A., Pichhode, M., & Nikhil, K., (2016). Effect of heavy metals on plants: An overview. Int. J. Appl. Innov. Eng. Manage, 5(3), 56–66. Baker, A. J. M., McGrath, S. P., Reeves, R. D., & Smith, J. A. C., (2000). Metal hyperaccumulator plants: A review of the ecology and physiology of a biological resource for phytoremediation of metal polluted soils. In: Terry, N., & Banuelos, G. S., (eds.), Phytoremediation of Contaminated Soil and Water (pp. 85–107). Edited by Boca Raton: CRC Press. Bakkaus, E., Gouget, B., Gallien, J. P., Khodja, H., Carrot, H., Morel, J. L., & Collins, R., (2005). Concentration and distribution of Cobalt in higher plants: The use of micro-PIXE spectroscopy. Nucl. Instrum. Methods Phys. Res. B, 23, 350–356. Barras, F., & Fontecave, M., (2011). Cobalt stress in Escherichia coli and Salmonella enterica: Molecular bases for toxicity and resistance. Metallomics, 3, 1130–1134. Basu, M., Bhadoria, P. B. S., & Mahapatra, S. C., (2006). Influence of microbial culture in combination with micronutrient in improving the groundnut productivity under alluvial soil of India. Acta Agric. Slov., 87, 435–444. Chatterjee, J., & Chatterjee, C., (2000). Phytotoxicity of Cobalt, chromium and copper in cauliflower. Environ. Pollut, 109, 69–74.

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Chmielowska-Bąk, J., Lefèvre, I., Lutts, S., Kulik, A., & Deckert, J., (2014). Effect of cobalt chloride on soybean seedlings subjected to cadmium stress. Acta Soc. Bot. Pol., 83, 201–207. DalCorso, G., Manara, A., Piasentin, S., & Furini, A., (2014). Nutrient metal elements in plants. Metallomics, 6, 1770–1788. Defarge, N., Spiroux De, V. J., & Séralinia, G. E., (2018). Toxicity of formulants and heavy metals in glyphosate-based herbicides and other pesticides. Toxicol. Rep, 5, 156–163. Dilworth, M. J., Robson, A. D., & Chatel, D. L., (1979). Cobalt and nitrogen fixation in Lupinus angustifolius L. II. nodule formation and function. New Phytol, 83, 63–79. Duan, X., & Auge, R. M., (2001). Effect of Cobalt on soybean response to moisture stress. Plant Physiol., 1, 166–170. Ebrahimi, M., Panahi, R., & Dabbagh, R., (2009). Evaluation of native and chemically modified Sargassum glaucescens for continuous biosorption of Co (II). Appl. Biochem. Biotechn, 158(3), 736- 746. Ebru, O. G., (2014). Nickel and Cobalt Effects on Maize Germination. Canakkale.

Edwards, A. C., Coull, M., Sinclair, A. H., Walker, R. L., & Watsun, C. A., (2012). Elemental

status (Cu, Mo, Co, B, S and Zn) of Scottish agricultural soils compared with a soil-based risk assessment. Soil Use Manag., 28(2), 167–176. Egrove, V. E., (2000). The role of Cobalt increasing tomato and potato drought resistance. Reverativnyi Zhurnal, 8, 152–162. Gad, N., & Atta-Ally, M. A., (2006). Effect of Cobalt on the formation, growth and development of adventitious roots in tomato and cucumber cuttings. J. Appl. Sci. Res, 2(7), 423–429. Gad, N., & El-Metwally, I. M., (2015). Chemical and physiological response of maize to salinity using cobalt supplement. Int. J. Chem. Tech. Res, 8, 45–52. Gad, N., & Hassan, N. M., (2013). Role of cobalt and organic fertilizers amendments on tomato production in the newly reclaimed soil. World Appl. Sci. J, 22, 1527–1533. Gad, N., & Kandil, H., (2011). Maximizing the tolerance of wheat plants to soil salinity using Cobalt. 1- growth and mineral composition. J. Appl. Sci. Res, 7, 1569–1574. Gad, N., (2005). Interactive effect of salinity and Cobalt on tomato plants II- some physiological parameters as affected by Cobalt and salinity. Res. J. Agric. Biol. Sci, 1(3), 270–276. Gad, N., (2012). Role and importance of cobalt nutrition on groundnut (Arachis hypogaea) production. World Appl. Sci. J, 20(3), 359–367. Gad, N., Abdel-Moez, M. R., & Ali, M. E. F., (2019). Maximization of drought tolerance of bean plants using cobalt supplementation, B- physiological and chemical contents in plants. Plant Arch, 19(2), 2282–2287. Gad, N., Abdel-Moez, M. R., Fekry, A. M. E., & Abou-Hussein, S. D., (2018). Increasing salt tolerance in cucumber by using Cobalt. Middle East J. Appl. Sci, 8, 345–354. Gad, N., Mohammed, A. M., & Bekbayeva, L. K., (2013). Response of cowpea (Vigna anguiculata) to cobalt nutrition. Middle East J. Sci. Res, 14, 177–184. Gómez-Merino, F. C., & Trejo-Téllez, L. I., (2018). The role of beneficial elements in triggering adaptive responses to environmental stressors and improving plant performance. In: Vats, S., (ed.), Biotic and Abiotic Stress Tolerance in Plants (pp. 137–172). Springer, Singapore. Jaleel, C. A., Jayakumar, K., Chang-xing, Z., & Azooz, M. M., (2008). Effect of soil-applied Cobalt on activities of antioxidant enzymes in Arachis hypogaea. Global J. Mole. Sci, 3(2), 42–45.

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CHAPTER 10

Role of Molybdenum in Tolerance Against Different Environmental Stresses LEKSHMY SATHEE,1* R. SURIYAPRAKASH,1 JYOTI PRIYA,1 SINTO ANTOO,1 and SHAILENDRA K. JHA2

Division of Plant Physiology, ICAR–Indian Agricultural Research Institute, New Delhi – 110012, India 1

Division of Genetics, ICAR–Indian Agricultural Research Institute, New Delhi – 110012, India

2

*

Corresponding author. E-mail: [email protected]

ABSTRACT Molybdenum (Mo) is an important trace element for higher plants and plays an important regulatory role in developmental processes, photosynthesis, nitrogen (N) metabolism, hormone signaling, and stress tolerance. Molybdenum is an important element for more than 40 enzymes, four of which have been extensively studied in plants and include nitrate reductase (NR), and nitrogenase which is involved in nitrogen fixation and assimilation, respectively, xanthine dehydrogenase/oxidase (XDH), which plays an important role in purine catabolism, aldehyde oxidase (AO), which plays an essential part in the synthesis of indole-3 acetic acid (IAA), abscisic acid (ABA), and sulfite oxidase (SO) which has a role in sulfur metabolism. Molybdenum application increased the synthesis of nitric oxide (NO) through regulating NR and NO as a signal molecule regulates a series of growth modules including primary root growth, root meristem growth, root hair development, and lateral root formation. Therefore, it could be speculated that Mo application might improve root system growth through NO accumulation Biology and Biotechnology of Environmental Stress Tolerance in Plants: Trace Elements in Environmental Stress Tolerance, Volume 2. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

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and NR regulation. Molybdate is the dominant form of Mo available to plants. Although Mo participates in various redox reactions, it is required at very low levels and the required amount of Mo is considered to be one of the lowest among the essential micronutrients. There are several possible ways by which Mo could enhance the development of stress tolerance in plant cells; Mo may increase the anti-oxidative defense by increasing the activity of the anti-oxidative enzymes. Molybdenum also activates AO and thereby increasing the ABA content. ABA accumulation can trigger bZIP transcription factors (TFs) and downstream stress signaling. 10.1 INTRODUCTION Molybdenum (Mo), an essential transitional trace element, can exist in multiple oxidation states (0 to VI). It dominates in agricultural soils as soluble oxoanionic molybdate (VI) which is the major form accessible to plants. It was not until 1939, the requirement of Mo as an essential element for plant growth was established by Arnon and Stout (Arnon & Stout, 1939). Its ability to exist in multiple oxidation states aids it to participate in various redox chemistry. It is available to the plant in the soil pH Fe > Zn > B > Cu > Mo pattern, these micronutrients get accumulated by the plants (Fageria et al.,

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2002). Micronutrients are vital for appropriate plant growth, development, biosynthesis of proteins and nucleic acids, gene expression, redox reaction, electron transfer, stress tolerance, and other important metabolic processes in plants throughout their life cycle (Jatav et al., 2020). Many soil factors like pH, soil organic matter, redox potential, temperature, and moisture affect the availability of micronutrients to crop plants. Both micronutrient deficiencies and toxicities in crops are found throughout the world and have been investigated in various soils. Micronutrient deficiencies, also known as ‘hidden hunger’ (India ranking 94 out of 107 countries on the Global Hunger Index score as recorded in 2020), is a prime health menace for humans in most of the world’s developing countries (Kennedy et al., 2003; Shukla et al., 2018). According to World Health Organization (WHO), about two billion people are sufferers of micronutrient deficiency worldwide. In plants, micronutrient deficiencies affect cell division and leaf size negatively and promote necrosis, chlorosis, wilting, bleaching, panicle sterility, etc. (Fageria et al., 2002). Escalating the micronutrient status of the plants in situations of inadequate supply of micronutrients from the soil has been found to increase yield. In crop plants, the methods for treating micronutrients are soil treatment, foliar sprays, micro-dosing, or seed treatments. So, micronutrient application has been a favored and frequently practiced method for improving plant growth and development and combating atrocities of various environmental stress. Copper (Cu), originating from the Latin ‘cuprum’is the 25th most abundant element after zinc among the micronutrients, with an average concentration of 60 ppm on the earth’s crust. Cu is a soft, ductile, reddish-brown element that reacts with atmospheric oxygen forming copper oxide. Naturally, copper is found within many minerals like copper sulfosalts (enargite, and tetrahedrite-tennantite), copper carbonates (azurite and malachite) copper sulfides (bornite, chalcocite, chalcopyrite, covellite, and digenite), cuprite and tenorite. Rapid urbanization and industrial growth had augmented levels of Cu in soil and sediments (Kumar et al., 2020). Though insoluble in water, Cu can be dissolved in concentrated hydrochloric acid or ammonia owing to the formation of complex ions. It usually exists in two oxidation states, Cu1+ and Cu2+. Cu being a redox metal can participate in Fenton reactions. Several members of the copper transporter protein (COPT) family are involved in Cu uptake and distribution in plants (Yuan et al., 2011). Copper is a cofactor of many antioxidant enzymes and is involved in photosynthetic and respiratory electron transport chains (Alaoui-Sossé, 2004). Copper has a marked effect on the chemical composition of cell walls. Cu2+ is likely to complex with cell wall polymers (especially histidine-rich

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glycoproteins such as extensions, some arabinogalactan-proteins) which in turn form Cu+ by electron donors of the apoplast (ascorbate and superoxide). The resultant Cu+ can participate in the Fenton reaction with H2O2 from the apoplast and leads to the formation of hydroxyl radicals. Ultimately it causes non-enzymatic scission of cell wall polysaccharides and thereby loosens the cell wall (Fry et al., 2002). It improves the fertility of male flowers. A deficiency of copper is known to cause ‘dieback’ or ‘exanthema’ of fruit trees and ‘reclamation disease’ of cereal crops (Rao et al., 2018). However, the presence of Cu above critical threshold concentration can be toxic to both plants and animals as it unsettles a varied range of metabolic (biochemical and physiological) processes, such as pigment synthesis, photosynthesis, membrane integrity, and protein metabolism (Yang et al., 2002). Using micronutrient-efficient crop plants serves as an important aspect for alleviating food-chain micronutrient deficiency by reducing fertilizers use, improving seedling vigor, and providing resistance to abiotic and biotic stresses. Also, soil and foliar fertilization, exogenous application of organic amendments in crop systems have been demonstrated to reduce micronutrient deficiency and increase crop yield (Khoshgoftarmanesh et al., 2010). Simultaneously, environmental deterioration is generating huge stress in all forms of life. This environmental deterioration is mainly contributed by prominent exposure to environmental factors like drought, salinity, heavy metal toxicity, ultraviolet-B (UV-B) radiation, pesticides, extreme temperature and pathogen invasion that causes enhanced reactive oxygen species (ROS) accumulation and oxidative stress. ROS such as hydroxyl radicals, singlet oxygen, and H2O2 are produced in significant quantities in the plant cells and activate signaling pathways leading to interruptions of physiological, biochemical, molecular, and cellular metabolism (Xie et al., 2019). Free radicals (ROS) displace electrons from lipids in the cell membrane causing disruption of membrane architecture mainly PUFA (polyunsaturated fatty acids), causing lipid peroxidation (LPO) damaging the phospholipids (Banerjee & Roychoudhury, 2018). However, several antioxidants play a depressive effect on the increased accumulation of ROS. Many strategies have been evolved by plants to counteract environmental stress. Among them, the application of microelements exhibits a propitious approach to mitigate the stress condition of plants by upregulating stressresponsive genes. Those genes are associated with the biosynthesis of antioxidants (enzymatic or non-enzymatic) and solutes (proline, polyamines) (Banerjee & Roychoudhury, 2018). This chapter encompasses the general

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role of Cu in plants, translocation of Cu, deficiency, and toxicity syndromes. It also compiles available information about the pivotal role of copper in alleviating various biotic and abiotic stress in plants and provides insights on available ways to combat them. 11.2 ROLE OF Cu IN PLANTS Extensive research during the 1920s revealed that Cu influences numerous physiological functions in plants. It has roles in electron transport, protein, and carbohydrate metabolism, chlorophyll biosynthesis, polyphenol metabolism, and also the lignification of cell walls. Thus, Cu is considered as one of the most essential micronutrients for plants (Droppa & Horváth, 1990). The role of Cu in plant growth and metabolism have been discussed in subsections. 11.2.1 ROLE IN PHOTOSYNTHESIS Plastocyanin, a component of the photosynthetic electron transport system that transfers an electron from membrane-bound cytochrome b6f complex in PSII to membrane-bound complex P700 in PSI, contains one copper atom per molecule (Freeman & Guss, 2011). Cu is the key contributor of plastocyanin synthesis and Cu content has a close relationship with plastocyanin content and maintaining activities of photosystem complexes (Droppa & Horváth, 1990). 11.2.2 ROLE IN ENZYME ACTIVITY 11.2.2.1 COPPER-ZINC SUPEROXIDE DISMUTASE (CU-ZN SOD) Various types of SOD isoenzymes have been observed for the detoxification of superoxide radicals. Among them, the Cu-Zn SOD (EC No: 1.15.1.1), found in mitochondrial cytoplasm, are homodimers with a molecular weight of 32 kDa, and each subunit contains one copper at the active site and one zinc atom that is associated by common histidine nitrogen. This Cu-Zn SOD serves in the detoxification of superoxide radicles generated during photosynthesis (Marschner, 1983; Bannister et al., 1991).

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11.2.2.2 CYTOCHROME OXIDASE Cytochrome oxidase (EC No:1.9.3.1), the terminal catalyst of the electron transport chain, contains four redox-active metal centers – two of which are copper atoms and the other two are haem A groups. This enzyme catalyzes the electrons transfer from reduced cytochrome c to molecular oxygen (Saraste, 1990). 11.2.2.3 ASCORBATE OXIDASE (AO) AO (EC No: 1.10.3.3) is a large, homodimer that comprises a multi-copper oxidase family of enzymes that catalyzes the oxidation of AsA with oxygen to yield dehydroascorbic acid and water. Each subunit is formed by three distinct domains and contains at least four copper ions (Venere et al., 2011). 11.2.2.4 POLYPHENOL OXIDASE (PPO) AND LACCASES Another Cu-containing enzyme is polyphenol oxidase (PPO) (EC No: 1.10. 3.1) containing only two copper ions at one reaction site in each functional unit of the enzyme, laccases (EC No: 1.10. 3.2) containing four copper ions at the active site of each enzyme molecule or functional unit. PPO can oxidize only o-diphenols with hydrogen abstraction whereas laccases are capable of oxidizing both p-diphenols as well as o-diphenols (Burton, 2003). 11.2.3 ROLE IN CELL WALL LIGNIFICATION Cu also increases the activity of Peroxidases (POD). This POD and laccases are mainly involved in lignin biosynthesis. Among the PODs, anionic PODs are precursors of cell wall lignification. Lignin in turn forms complexes with other polysaccharides, cellulose, and proteins of the cell wall that give mechanical strength, water transmission, and blocking the growth of pathogen so increasing resistance against pathogen by host defense mechanisms (Lin et al., 2005). 11.2.4 ROLE IN SEXUAL REPRODUCTION The role of copper is highly associated with photosynthesis and carbohydrate metabolism that positively influence micro-sporogenesis in the tillers

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leading to the formation of viable pollen, fertilization, flowering, and grain formation (Graham, 1976). 11.2.5 ROLE IN NITROGEN FIXATION In legumes, Cu plays a powerful role in nodulation and N2 fixation through overexpression of the meIA gene of bacteroids, which is a copper-containing enzyme tyrosinase specifically associated with nif genes (Weisany et al., 2013). 11.2.6 ROLE IN CELL WALL LOOSENING Cu performs central functions in plant cell wall loosening. Cu2+ forms complex with histidine-rich glycoproteins. Those cell wall polymers are reduced to Cu+ by apoplastic electron donors (ascorbate and superoxide). Reduced Cu+ can then generate hydroxyl radicals (·OH) undergoing Fenton reaction with apoplastic H2O2, resulting in pectin cleavage and loosening of the cell wall and ultimately supporting several physiological processes such as cell expansion, fruit softening, and organ abscission (Fry et al., 2002; Printz et al., 2016). 11.2.7 OTHER ROLES IN PLANTS In plants, Cu also plays a crucial role in signaling, iron mobilization, transcription, and protein trafficking machinery and oxidative phosphorylation at the cellular level (Syuhada et al., 2014). In addition, Cu solution increases the level of ABA during germination of wheat seeds due to the expression of ABA biosynthesis genes (OsNCED2 and OsNCED3) which leads to the cessation of heavy metal translocation from roots to shoots (Bücker-Neto et al., 2017; Munzuroğlu et al., 2007). In cucumber, seed germination percentage decreased, and ABA content increased under Cu2+ stress by activating expression of ABA-responsive genes such as CsPYL1, CsPYL3, CsPP2C5, CsABI1, CsSnRK2.3, and CsSnRK2.4 (Wang et al., 2014). Also, increased production of endogenous ABA level due to lead (Pb) toxicity in germinating chickpea (Cicer arietinum) seeds under Cu-exposed conditions has been reported (Bücker-Neto et al., 2017).

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11.2.8 ROLE OF Cu IN ANIMALS As a trace micronutrient, Cu has an important role in mammalian metabolism. Cu is directly required for activating multiple cuproenzymes, such as Cu-Zn SOD (free radical detoxification), ceruloplasmin (iron transport), lysyl oxidase (cross-linking collagen and elastin), cytochrome c oxidase (cellular energy production), and tyrosinase (melanin production), etc. (Vonk et al., 2008). In addition, Cu causes tumor angiogenesis by stimulating tumor cells to secrete angiogenic factors. It also affects the migration and proliferation of endothelial cells (Lowndes & Harris, 2005). 11.3 DEFICIENCY SYNDROMES Copper has an immense role in the biological system of plants and its deficiency is considered to be a major constraint in Indian agriculture. Cu concentration below a threshold level of 2–5 mg/kg, is considered as Cu deficiency in plants (Jatav et al., 2020). Soil pH, redox potential, and soil organic matter are the main limiting factors of Cu deficiency. Generally, plant phenotypes associated with Cu deficiency are chlorotic symptoms that appear first at the tip of the young leaves and then extend toward the leaf base (Printz et al., 2016). Being immobile, copper deficiency symptoms tend to appear first in younger leaves. Young leaves become yellow and later leaves become brown at the margins. Leaves may occasionally be wilted or twisted in vegetable crops (Nutrifact copper http://www.ipni.net/nutrifacts-northamerican). The most striking effect of Cu deficiency in citrus is characterized by red rust, die-back (dying back of the twigs), multiple buds, or peach leaf conditions. In severe cases, the twigs start to die and some of them bear small yellowish-green leaves. Later yellowish blotches are formed on the shoots just below the leaf nodes leads to diminution of carbohydrate movement from the leaves into the stem and fruits. So that small swellings or lumps along the stem are produced. When these swellings are punctured reddish-brown droplets of gum exude from slits on the bark of stems that cover the twigs. The phenomenon is called ‘exanthema’ (excrescences on the surface of the twigs and fruit) (Zekri & Obreza, 2003; Elavarasan & Premalatha, 2019). Lack of adequate Cu is also associated with ‘reclamation disease’ or ‘white tip’ in annual crops. The disease produces a characteristic distortion of young leaves that become bleached due to chlorosis or necrosis appearing at the apical meristem and then extending up to leaf margins (Rao, 2013; Broadley et al., 2012). Cu deficiency impedes the photosynthetic electron transport chain and causes a reduction in non-photochemical quenching. The

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most prominent and established reason behind such anomalies is the lack of proper functioning of copper-containing protein plastocyanin (PC) and disintegration of the thylakoid membrane (Ghany & Pilon, 2008). Cu deficiency represses the expression of Cu/Zn superoxide dismutase (SOD) mRNA, making plants more susceptible to ROS (Yamasaki et al., 2008). Apart from these, Cu deficiency has been found to hinder nodulation, nitrogen fixation, crop yield, and acetylene depletion per gram nodule in subterranean clover (Snowball & Robson, 1980). Transition to flowering is directly linked with the decrease in miR156 expression and associated upregulation of miR172 and flowering locus T (FT) genes, but under copper deficiency expression of FT and miR172 are found to decline in leaves. In addition, it activates floral repressors such as flowering locus C (FLC), successively reducing FT gene expression and causing a delay in flowering. In copper-deficient plants, reduced Cu/Zn SOD activity, cytochrome c oxidase (COX) activity lead to over generation of ROS to cell, depletion of cellular ATP production, and consequently impairs male fertility by inhibition of pollen tube growth, pollen germination, fertilization also. However, plants grown under copper-deficient conditions exhibit a dramatic reduction of lignin deposition that ultimately changes the architecture of the cell wall (Ishka & Vatamaniuk, 2020). Interestingly in rice, severe Cu deprivation leads to increased auxin synthesis through interaction with PIN1 (Andrés et al., 2017). Besides Cu deficiency results in low pollen viability, hampers germination rate and retards grain fertility in rice (Zhang et al., 2018). Cu deficiency causes the formation of iron plaques on rice roots that dramatically escalates the capacity to adsorb heavy metals like Cd, Cr, Cu, and Zn that in turn become detrimental to human health by entering the food chain and (Peng et al., 2018). In addition, Cu has a depressive effect on Arsenic (As), i.e., Cu deficiency increases As accumulation in rice grain causing phytotoxicity and enhancing incidences of its entry into the food chain (Liu et al., 2018). As fungicides (Bordeaux mixture), Cu can denature the spores and conidia of fungus and prevent spore germination, but it has been reported that rice becomes more susceptible to blast disease caused by a fungus Pyricularia grisea, and also results in a reduction of yield on exposure to Cu fungicides (Liew et al., 2012). 11.4 Cu UPTAKE AND TRANSLOCATION Plant metabolism requires specific elements (besides water and light) for ensuring optimum growth and development. Minerals that enter from the soil matrix to the root cells of the epidermis are then transferred through the

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parenchyma up to the center of the roots, endodermis, and finally reaches the xylem. In the course of evolution, plants have developed various transporters, pumps, and channels to establish proper access, uptake, translocation, and balanced distribution (Kumar, 2020). Being an essential micronutrient, plants possess a specific mechanism for Cu uptake. The mechanism of Cu uptake by root cells shows striking resemblance with that of iron uptake and follows a reduction based strategy (both dicotyledons and non-graminaceous monocotyledons) involving reduction of Cu2+ to Cu+ by Cu 2+ chelate reductase at root surface (Printz et al., 2016). This reduced form of Cu+ is in turn taken up by the roots through specific transporters namely, COPT, P-type ATPase COPT, Zinc Iron Regulated Transporter-like Protein (ZIP) family transporters, and natural resistance-associated macrophage protein (NRAMP) family transporters (Kumar, 2020) (Figure 11.1).

FIGURE 11.1 Overview of copper transport and translocation. Copper uptake is occurred in its reduced form (Cu+) by highly selective plasma membrane Cu-transporters, COPT1/2. Cu uptake is also carried out by non-selective ZIP proteins (ZIP2/4) present in the root cells. Cu is usually chelated by intracellular MTs or some specific chaperones (e.g., ATX1) in the cytoplasm, and are delivered to different organelles. Cu mobilization to-and-fro the vacuole is mediated by HMA5 and COPT5, respectively. HMA6 and HMA8 help in the transport of Cu in the chloroplast and thylakoid, respectively. ATX1 delivers Cu to HMA5 that in turn loads Cu+ into the xylem. Cu2+ complexes are transported to the leaf cells by YSL1/2/3 whereas reduced Cu are imported to the leaf by COPT6. Cu2+ complexes are transferred to the phloem from senescing organs by YSL16. HMA7 delivers Cu to ETR1. Long-distance transport of Cu through xylem and phloem is aided by MTs and several Cu-binding proteins (e.g., CCH). Abbreviations: COPT: Copper transporter; MTs: metallothioneins; ATX1: antioxidant protein 1; HMA: heavy metal ATPase; YSL: yellow stripe like; ETR1: ethylene receptor 1; ZIP: zinc iron-regulated transporter-like protein.

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In plants, uptake of reduced Cu is mainly aided by COPT (CTR-like highaffinity Cu transporters protein family). In Arabidopsis, six putative CTR/ COPT transporters, i.e., COPT 1–6 regulate copper uptake (Li et al., 2014), whereas, in rice, the COPT-transporter family consists of seven members (COPT1-7) (Yuan et al., 2011). The key player in Cu acquisition from the soil is a plasma membrane-bound high-affinity transporter protein, COPT1, distributed in many organs but concentrated at the root tips in Arabidopsis (Gayomba et al., 2013). SPL7 (SQUAMOSA promoter-binding protein-like) is the keeper of Cu homeostasis and under Cu deficiency plants seem to activate COPT1 in an SPL7 dependent manner to ensure optimum Cu uptake (Sancenón et al., 2004). COPT2, another Cu(I) transporter of the COPT/Ctr-like family is primarily localized in the epidermal cells of the root, root hairs but are absent in the meristematic zones and shows upregulation in response to Cu depletion in an SPL dependent way. It primarily mediates the secondary pathway of root Cu incorporation and is mainly present in the reproductive organs (Puig, 2014; Gayomba et al., 2013). COPT3 and COPT5 transporters possess an intermediate rate of Cu affinity and transportation and constitute a secretive pathway for indirect transport of Cu (Kumar, 2020). COPT5 mobilizes Cu from the tonoplast and vacuolar compartment. It is reported that COPT5 mutants are more sensitive to cadmium stress-causing Cd accumulation in aerial parts and thereby reducing Cu content leading to Cu deficiency in plants (Carrió-Seguí et al., 2015). In contrast, COPT6 facilitates translocation of Cu to leaf photosynthetic zone via shoot (Migocka & Malas, 2018). Cu is mainly translocated from roots through the shoots as Cu-complexes along the xylem and OsHMA5 (located in the pericycle and vascular tissues of rice) aids this process. However, in dicots, Cu is mainly translocated as Cu (II) by metal chelators. Cu gets complexed either with free amino acids (mainly histidine) or non-proteinogenic amino acids (mainly nicotianamine) in the xylem and such metal-chelates are transported by YSL2 or YSL3 (in Arabidopsis) and YSL16 (phloem localized YSL in rice). Metallothioneins (MTs) are Cys-rich proteins that help in the remobilization of Cu from senescing organs such as old leaves to sink organs such as developing seeds or leaves, and their expressions are regulated by Cu availability (Guo et al., 2003). Cu binding proteins (like CCH) are also suggested to have a role in the long-distance transport of Cu in vascular plants (Andrés-Colás et al., 2006).

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The P-type heavy metal transporters within the plasma membrane allow the movement of metals such as Cu2+, Zn2+, Cd2+, and Pb2+ using ATP as an energy source for pumping them across the cell membranes. Cu-transporting ATPases belong to the 1B P-ATPase family of heavy metal transport proteins consisting of eight characteristic transmembrane helices (TMHs). Among them, AtPAA1/AtHMA6 facilitates the transport of Cu to the stroma of the chloroplast. AtPAA2/AtHMA8 involves the transfer of Cu across the thylakoid membrane and protects thylakoids from Cu overload under high Cu concentrations (Kumar et al., 2020; Migocka & Malas, 2018). HMA7/RAN1 helps in ethylene receptors (ETRs) biogenesis by delivering Cu to ETR1 (ethylene response). OsHMA4 is a P-type ATPase, isolated from rice plants that regulate Cu accretion in rice grains and aids sequestration of Cu in the root vacuoles, reducing their accumulation in grains (Huang et al., 2016). Another novel metal transporter family in plants is members of the ZIP gene family that mediate the transport of divalent cations. This transporter has eight potential transmembrane domains whose amino- and carboxyterminal ends reside on the outer surface of the cell membrane. Excess Cu has been found to induce expression of ZIP4 whereas Cu deprivation has been documented to upregulate ZIP2 expression in Arabidopsis (Yamasaki et al., 2009; Wu et al., 2015). In rice, however, OsZIP1 functions to distribute Cu within the cells (Guerinot, 2000; Kumar et al., 2020). Lastly, the NRAMP family of transporters also plays a role in transporting many heavy metals like Co, Cu, Cd, Fe, Mn, Ni, and Zn in plants (Komal et al., 2015) but there is a dearth of reports elucidating the particular roles of NRAMP in Cu transport in plants. 11.5 APPLICATION OF Cu AGAINST ENVIRONMENTAL STRESS Plants are often subjected to unfavorable environmental conditions which can restrict plant growth and development. The term ‘stress’ actually refers to external conditions that adversely limit plant growth, development, productivity, or yield. These stress conditions potentially trigger various responses like altered gene expression, cellular metabolic activity, changes in growth rates, etc. Environmental stress can be broadly classified as abiotic stress and biotic stress (Gull et al., 2019). Abiotic stress mainly includes climatic factors, i.e., temperature, salinity, flood, drought, cold, and chemical components such as radiation, whereas biotic stress includes attack by various pests and pathogens, i.e., bacteria, fungi, viruses, nematodes, and insects. These

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factors ultimately reduce average yields by more than 50% for most crop plants (Bijlsma & Loeschcke, 2005; Atkinson & Urwin, 2012). Recently global warming, as a consequence of human activities, is becoming a major environmental issue worldwide, which drives drastic change in our climate and increases the frequency of abiotic and biotic stress instances (Zandalinas et al., 2021). Several strategies have been well documented that help to combat environmental stress and address related problems in various economically important crop plants. Foliar application of glycine-betaine, before initiation of flowering, can increase the yield of potatoes, grapevines under cold and moisture stress. Similarly, seed treatment with betaine increases seed germination, seedling vigor in salt-stressed crops (Naidu, 2003). Seed coating by Vermiculite (V), Kaolin (K), and Perlite (P) (3:1.5:2) and biopriming with Pseudomonas fluorescens and Trichoderma harzianum fungi helps to improve physical properties of the seed in drought-stressed crops by enhancing antioxidant enzymes (Piri et al., 2019). Wheat straw-derived biochar application can reduce herbicide fomesafen stress by improving the soil microbial ecology thus balancing the structure and diversity of the microbiome and improving plant performance under abiotic stresses (Meng et al., 2019). Molecular markers are extensively used in breeding to combat drought conditions. Biotechnology has been successfully used where genes involved in stress resistance are cloned and incorporated into stress-sensitive plants (Smirnoff, 1998). Attention has been paid to generate transgenic plants and natural genetic variants that confer salt tolerance (Hussain et al., 2008). In addition, “shot-gun” is an emerging approach to plants under stress conditions via exogenous application of proline and glycine betaine (Ashraf & Foolad, 2007). Among all the prevalent methods of imparting stress tolerance or mitigating stress-related atrocities in plants, micronutrient application, is another popular approach. Several successful cases of micronutrient mediated stress management in plants have been already reported worldwide and more are being added up frequently. Soil application of iron nanoparticles (Fe-NPs) has been found to mitigate Cd and drought-stressed wheat by improving Fe concentration, reducing oxidative stress and Cd concentrations (Adrees et al., 2020). Seed priming with zinc had improved biomass production and mineral nutrient status of plants under salt stress conditions (Imran et al., 2018). Foliar application of zinc has been an effective way to combat drought stress (DS) in plants by reducing photo-oxidative damages (Toor et al., 2020). Application of magnesium sulfate (MnSO4) has been reported

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to induce the Mn-SOD gene and result in lowered ROS levels in cucumber under low-temperature stress (Ye et al., 2019). Exogenous application of Mn also provided salt stress tolerance by expressing antioxidant defense enzymes, i.e., dehydroascorbate reductase (DHAR), SOD, and catalase (CAT), and glyoxalase systems in rice crops (Rahman et al., 2016). Molybdenum (Mo) application had notably alleviated oxidative stress of winter wheat by enhancing ABA contents and upregulating activities of ROS scavenging enzymes (Imran et al., 2020). Nickel can also be applied in tissue culture growth media to reduce leaf damage and metabolic stress by improving urease activity (Witte et al., 2002). Boron can also act as an inducer of antioxidant glutathione (GSH) pool in sunflower and maize plants under aluminum (Al) stressed plants (Camacho-Cristobal et al., 2008). Copper application has appeared to be a promising approach to mitigate the harmful effects imparted by various environmental stress in plants (Figure 11.2). Various approaches of copper application against several abiotic and biotic stress in plants have been discussed in subsections (Table 11.1).

FIGURE 11.2 Summary of stress-induced damages in plants and their alleviation through the copper application. Various abiotic and biotic stress poise several detrimental effects on plant cells such as membrane disruption, improper ionic balance, cellular damage, tissue necrosis, oxidative stress via ROS formation that results in erratic germination, stunted growth, and concomitant yield loss. The copper application could mitigate the stress-induced atrocities in the plants through upregulation of antioxidant enzyme activities, accumulation of compatible solutes, enhanced expression of defense-related genes and inhibition of pathogen invasion or spore germination.

Sl. Treatment No. 1. Cu foliar spray 2.

Type of Stress Plant Under Combated Study Salt stress

Zea mays L.

Cu NPs+ NaCl

Salt stress

Foliar spray, 250 mg L , 78 days −1

Solanum lycopersicum

Mode of Action

References

Proline, glycine betaine, antioxidant Dutta et al. (2020) activity PAL, APX, GPX, SOD, GSH, and CAT Pérez-Labrada et al. (2019) phenols, and flavonoids, vitamin C, lycopene

ROS

3.

CuSO4 + salinity stress

Salt stress

Nutrient solution (NO3–, N, K, PO43–, P, Ca, Mg, Na, Cu, Zn, Mo, SO42˗, S, B, Fe, Mn) 4.

60 μM Cu + 150 mM NaCl, 10 days Sod1 (a cytosolic Cu/Zn SOD) Salt stress

from Avicennia marina in Yoshida medium

Mentha spicata L.

Limonene, Ca, Mg (in leaves)

Chlorophyll, polyphenols, antioxidants,

Zn, N, K (in leaves), K, Ca, P, Mg (in roots)

CuSO4 + NaCl in Hoagland nutrient Salt stress

solution, 0–1 µm CuSO4 + 0–100 mM NaCl, 3 months

6.

Copper chlorophyllin (Cu-chl) seed Salt stress

priming, 0, 100, and 200 µM, 3 days

7.

Cs-PVA + Cu NPs, soil application, Salt stress

10 mg Cu NPs + 1gCs-PVA, 20 days

Solanum lycopersicum

H2O2 JA, CAT, APX, GPX Na , ROS +

Prashanth et al. (2008)

Mehrizi et al. (2012)

Islam et al. (2021)

Hernández-Hernández et al. (2018)

365

5.

Indica rice var Sod1 gene expression Pusa Basmati-1 Methyl viologen mediated stress response Rosmarinus Total phenol content officinalis L., Lipid peroxidation, membrane Lamiaceae permeability Arabidopsis Class III peroxidases, glutathione thaliana S-transferases

Chrysargyrisa et al. (2019)

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TABLE 11.1 Summary of Different Types of Cu Treatment in Plants Against Diverse Environmental Stress and Their Possible Mechanism to Action to Ameliorate the Stress Mediated Adversities

(Continued)

Sl. Treatment No.

9.

Colloidal solution of Cu and Zn Drought stress Triticum sp. NPs, seed treatment (mother colloid solution:water::1:100), 4 hours Copper NPs (nano-Cu), seed Drought stress Zea mays L. priming, 3.333 mg L–1, 4.444 mg L–1, 5.556 mg L–1, 8 hours

10. Cu + PEG in Hoagland solution (0.5–1.5 mM CuSO4.5H2O + 20% PEG), 5 days

Drought stress Zea mays L.

11. CuO NP, seed treatment, 0–1,000 mg L–1, 6 days

Osmotic stress Oryza sativa (var. Jyoti)

Mode of Action

References

SOD, CAT, carotenoid biosynthesis

Taran et al. (2017)

TBARS, ROS Anthocyanin, carotenoid, SOD, APX, Chl-a, Chl-b, seed number, yield ROS SOD, CAT, GR, APX, GST, RWC, proline

Nguyen et al. (2021)

Cetinkaya et al. (2014)

MDA level

12. Combination of micronutrients (Cu, Osmotic stress Triticum sp. Zn, and Mn), foliar application

Proline and APX, SOD Photosynthetic rate, transpiration rate and stomatal conductance Albumin, globulin gliadin

13. Cu NPs, soil application, 0–800 mg Osmotic stress Cucumis sativus Benzoic acid, gallic acid hydrate, caffeic, and p-coumaric acid, kg–1, 60 days transpiration, and stomatal conductance rates α-tocopherol, reduced glutathione and vanillic acid photosynthetic rate, biomass of root, stem, leaf, fruit, and ROS

Costa & Sharma (2015) Dutta et al. (2020); Pierre et al. (2007); Ye & Guo-Ping (2020); Fischer et al. (2017) Huang et al. (2019)

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TABLE 11.1

(Continued)

Sl. Treatment No.

Type of Stress Plant Under Combated Study

14. CuNPs using Klebsiella pneumonia, Heavy metal soil application, 0–100 mg kg−1, 30 stress days

Triticum sp.

17. CuO-NPs, NP amended media, 0–1,000 μg mL–1; 4 days

Biotic stress

18. CuSO4 soluble in water

Biotic stress

B. cinerea, A. alternata, F. solani, V. dahliae, C. gloeosporioides, M. fructicola Against Late blight disease in potato by Phytophthora infestans against S. aureus, B. cereus, P. mirabilis, E. tarda, A. caviae, A. hydrophila and V. anguillarum against E. coli and S. aureus

Spray method 0.1–10 μM, 4 hr. prior to P. infestans inoculation 19. CuO NPs suspension using actinomycetes, 5–100 µg mL–1

Biotic stress

References

Growth, biomass, and CAT, POD, proline, and total phenolic contents

Noman et al. (2010); Yousef (2012)

Cr concentration, ROS Mycelial growth

Malandrakis et al. (2019)

StACS genes, ET production

Liu et al. (2020)

ABA

Growth of bacteria, fungi, viruses, and Nabila & Kannabiran (2018) algae

Antibacterial activity

Amer & Awwad (2021) 367

20. Synthesized copper NPs (CuNPs) Biotic stress from CuSO4.5H2O and Citrus lemon fruits aq. extract

Mode of Action

Role of Copper in Tolerance Against Different Environmental Stress

TABLE 11.1

(Continued)

Sl. Treatment No.

Mode of Action

References

Form protective film

Lamichhane et al. (2018); Menkissoglu & Lindow (1991)

Toxic level of copper ions

Ottesen et al. (2014)

21.

Cu(OH)2, spray application, 100 ppb, 20 days

Biotic stress

22.

Copper oxychloride culture-based methods

Biotic stress

CuChNp, foliar spray

Biotic stress

23.

0.01%, 0.05%, 0.1%, 0.15%, 40 days

Against Plasmopara viticola in grapes Against Salmonella and Paenibacillus Against blast disease caused by P. grisea

Growth of these genera Chitinase and chitosanase

Sathiyabama & Manikandan (2018)

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Type of Stress Plant Under Combated Study

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11.5.1 Cu AGAINST ABIOTIC STRESS 11.5.1.1 SALT STRESS Plant salt stress is defined as a condition where a higher concentration of salts decreases the osmotic potential of the soil and inhibits normal plant growth or metabolism due to severe water deficit or osmotic stress (Zhu, 2007). Soil salinity is potential abiotic stress that adversely influences plant growth, results in high sodium uptake, causes sodicity resulting in an increase in soil resistance; reduction in root growth, and water movement through the root and a net decrease in hydraulic conductivity (Ramón Acosta-Motos et al., 2017). As salt stress reduces crop quality and productivity, these crops appear to be necessary for achieving sustainable food production (Hussain et al., 2008). By definition, salt stress induces inhibition of plant growth because of an increased rate of ROS accumulation in cellular organelles, which causes osmotic stress, and alteration of morphological traits. Some researchers have reported that in salt‐treated rosemary cultivars phenol and malondialdehyde (MDA) accumulation were decreased by exogenous application of Cu, which led to enhanced membrane permeability, ionic homeostasis, and nutrient uptake as compared with control varieties. Similarly, foliar Cu application has been effective in ameliorating the detrimental effects of salt stress by improving antioxidant activity and accumulation of osmolytes (proline and glycine betaine) that is usually sufficient to protect osmotic stress conditions (Dutta et al., 2020). Again, foliar spray using copper nanoparticles (Cu NPs + NaCl) improved the Na+/K+ ratio and provided better fruit quality in tomato plants under saline stress. It also sharply increased the activity of PAL, APX, GPX, SOD, and CAT enzymes and secondary metabolites such as phenols, and flavonoids, also vitamin C, lycopene that helped to mitigate damage caused by salt stress in tomatoes (Pérez-Labrada et al., 2019). Salinity stress has also been reported to impair growth, photosynthetic rate, and stomatal conductance in Spearmint species. Combined exposure of Cu and salinity stress was found to activate secondary metabolism in Spearmint plants that helped to defend oxidative stress damage by scavenging ROS. It was also reported to bring down effects of salinity stress by restoring SOD activity. In addition, limonene content (monoterpene that serves as the main constituent of essential oil biosynthesis) increased with a concomitant decrease in 1,8-cineole content followed by alterations in chemical structure and quality of the essential oil due to interference in their biosynthetic pathways (Chrysargyrisa et al., 2019).

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Increased level and activity of SOD, especially Sod1, a cytosolic copper-zinc superoxide dismutase (Cu-Zn SOD), has been observed in halophytic plants like mangroves to provide defense against severe abiotic stresses. This Sod1 cDNA when inserted into indica rice var Pusa Basmati-1 produced transgenic Sod1 protein that provided tolerance against a high degree of salt stress and abiotic stress by the over expression SOD in rice (Prashanth et al., 2008). Salt stress is highly associated with LPO and electrolyte leakage which includes augmented MDA content representing membrane injury. The application of copper resulted in a higher accumulation of phenolic compounds in plant roots indicating defense against ROS and thereby decreasing LPO. Copper nutrition ameliorated salt-induced oxidative damage in rosemary (Mehrizi et al., 2012). Foliar application of copper chlorophyllin (Cu-chl), a semisynthetic water-soluble chlorophyll derivative is an efficient way to decrease salinity stress through modifying cellular H2O2 levels. Cu-chl treated plants upregulated leaf antioxidant enzyme activities such as class III peroxidases and GSH S-transferases that scavenge ROS leading to increased ROS/H2O2 detoxification and osmotic adjustment thereby improving tolerance to high salinity stress in Arabidopsis thaliana (Islam et al., 2021). The mechanism to reduce salinity stress can be achieved either by overproduction of jasmonic acid (JA) signaling pathway that mitigates the effect of salt stress on plants or by antioxidant enzyme activation, i.e., CAT, APX, and GPX, converting highly toxic ROS species into less toxic ones and scavenging of H2O2. The addition of Cu-NPs along with chitosan-polyvinyl alcohol hydrogels (Cs-PVA) aided this mechanism by promoting the expression of JA and SOD genes in tomatoes and enhancement of plant growth under salt stress environment (Hernández-Hernández et al., 2018). 11.5.1.2 DROUGHT STRESS (DS) Drought stress (DS) may be defined as a water-limited condition that hampers plant productivity. DS has been reported to interfere with normal morphological and physiological processes such as leaf size, photosynthesis, yield, membrane integrity, pigment content, stem, and root growth, plant water relations, and water-use efficiency. Due to its negative impact on the plant, DS is classified as one of the major adverse factors threatening sustainable crop production (Farooq et al., 2009; Anjum et al., 2011). The damage of cells imposed by drought conditions has been ameliorated by the application of Cu. It has been reported that the treating seeds with colloidal solution of Cu NPs rescued the negative effect of drought by maximizing activity of anti-oxidative enzymes

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like SOD and CAT in leaves by 22% and 21% under drought conditions respectively which in turn decreased thiobarbituric acid reactive substance (TBARS) accumulation in leaves. Altering the ratio of chlorophyll (Chl a to Chl b) in the leaves with a higher rate of carotenoid biosynthesis has been put forth as a mechanism to neutralize DS by quenching ROS in the wheat plant. It also changes plant phenotypic indexes such as relative water content (RWC) and area of leaves, promoting adaptation mechanism at drought-stressed conditions (Taran et al., 2017). A promising approach to protect plants against DS is seed priming with Cu-NPs. It has been effective in enhancing leaf water content and plant biomass by regulating leaf water status, chlorophyll, and carotenoid content by preventing chlorophyll degradation under DS. It also escalates SOD and APX enzyme activities and anthocyanin content that helps in the maintenance of photosynthesis. Histochemical analyzes with nitro blue tetrazolium and 3,3’-diaminobenzidine (NBT) validated active ROS scavenging and detoxification in plant cells. Furthermore, under DS, the treatment of Cu-NPs increased the grain yield (Nguyen et al., 2021). A report also indicated that the application of Cu with polyethylene glycol (PEG) could alleviate drought response in maize. Increased RWC has been observed by combined treatment of PEG and 1 mM Cu. The treatment protected leaves from dehydration by the uplifting accumulation of compatible solutes like proline that reduced damage to the membrane which was evident with low MDA levels. Also, the most important antioxidants such as SOD, APX, and CAT increased to develop DS tolerance in maize (Cetinkaya et al., 2014). It was reported that CuNP treatment in soybean plants can help to overcome DS. One of the most prominent underlying effects of CuNP application was enhanced expression of drought-responsive genes GmDREB2, GmERD1, GmNAC11, and GmMYB174 in roots and GmDREB2, GmERD1, GmNAC11, GmWRKY27, GmMYB118, and GmMYB174 in leaves at a molecular level in significant quantities. Among these genes, induced expression of GmWRKY27 in leaves was associated with induction of ABA biosynthetic pathway and resultant stomatal closure. Another reason behind drought resistance by CuNPs is cell water retention which showed an 8%–10% increment in leaves of wheat seedlings (Linh et al., 2020). 11.5.1.3 OSMOTIC STRESS Osmotic stress is generally caused either due to drought, salinity, or cold stress, and happens to be one of the important abiotic factors that induce various cellular damages including morphological and developmental anomalies like

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stunted shoot growth, increase in root growth and changes in the life cycle; disrupted ion transport regulation such as uptake, extrusion, and sequestration of ions and metabolic changes such as alteration of carbon metabolism (Xiong & Zhu, 2002). In response to an osmotic stress condition, different types of compatible, low molecular weight, highly soluble, usually nontoxic organic solutes accumulate in plant cells (e.g., proline and glycine betaine). They serve as osmoprotectants by adjusting cellular osmotic balance, detoxifying ROS, protecting membrane integrity, and stabilizing enzymes/proteins facilitating water uptake mechanisms in plants to adapt to water stresses (Ashraf & Foolad, 2007). Seed treatment by CuO NP was found to be effective in elevating proline and AsA levels in Oryza sativa (var. Jyoti) (Costa & Sharma, 2016). Increased expression of enzymatic antioxidants, APX and SOD via CuO NPs, has been frequently reported to protect against the development of oxidative stress in the plants subjected to osmotic stress. Similarly, winter wheat subjected to water stress showed increased levels of albumin, globulin (smaller monomeric seed storage protein fraction regulating metabolic activity or structural function), and gliadin (large monomeric proteins, crucial seed storage protein) contents on foliar application of a combination of micronutrients (Cu, Zn, and Mn) that aided to overcome abiotic stress otherwise these soluble proteins concentration lowered in water-stressed condition (Dutta et al., 2020; Pierre et al., 2007; Ye & Guo-ping, 2020; Fischer et al., 2017). As mentioned earlier, copper-containing nano pesticides (Cu NPs) are used to scavenge ROS which in turn tends to increase levels of low molecular weight antioxidants such as benzoic acid, gallic acid hydrate, caffeic, and p-coumaric acid that triggers activation of the anti-oxidative defense system of plants. When ROS is produced as a consequence of oxidative stress, ∝-tocopherol also acts as chain-breaking inhibitors of LPO and inhibit free radical propagation cascades ultimately ameliorating oxidative stress in cucumber (Cucumis sativus) (Huang et al., 2019). 11.5.1.4 HEAVY METAL STRESS Heavy metal toxicity, one of the major abiotic stresses, poses severe health hazards in animals and plants by entering the food chain (Maksymiec, 2007). Unlike other organic pollutants, these heavy metals such as Cd, Cr, Pb, and Hg are not degraded in the environment and so can persist in soil (Purakayastha & Chhonkar, 2010). Being toxic and reactive, they can directly interfere with ultrastructural, biochemical, and molecular processes in plants culminating in stunted growth, chlorosis of leaves, necrosis, loss of turgor, decrease in the rate of seed germination, a crippled photosynthetic apparatus, impairs

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energy synthesis processes in plants, leads to early senescence or death in plant tissues (Gill, 2014; Maksymiec, 2007). The basic characteristic of heavy metal stress is the generation of ROS and subsequent damage of the biomolecules through LPO, alteration of protein functions, gene mutation, chlorophyll degradation, and disruption of metabolic pathways (Rastgoo & Alemzadeh, 2011). Oxidative damage of cells imposed by Cr has been reported to be ameliorated by treatment of CuNPs from Klebsiella pneumoniae (Gram-negative, non-motile, encapsulated, facultative anaerobic bacterium most frequently present in the normal flora of the mouth, skin, and intestine. It can synthesize selenium, gold, and other metal NPs strain in wheat. Here, an isolated strain of K. pneumoniae SN35 was mixed with CuSO4, incubated, and a powdered form of CuNPs was procured from the supernatant. Treatment of these CuNPs has been efficient in reducing Cr translocation and accumulation in different plant parts, checking ROS generation by improving anti-oxidative enzyme status and thereby mitigating Cr-induced stress in the plants. In addition, a significant increase in the growth of root and shoot was observed. CuNPs application significantly influenced the cellular antioxidants’ activities by elevating the CAT, POD, proline, and total phenolic contents that relieve ROS as compared to the control plant (Noman et al., 2020; Yousef, 2012). 11.5.1.5 TEMPERATURE STRESS Temperature stress is another major threat to the environment that is associated with global warming. Hot or cold temperature stresses may cause detrimental effects to all phases of plant development in agricultural fields. The specific symptoms of this stress are changes in membrane fluidity, nucleic acid and protein structures, photosynthesis inhibition with Rubisco activity reduction, the disparity in metabolite and osmolyte concentrations, induction of ROS resulting in oxidative damage, and cell death (Zinn et al., 2010). During cold stress, chloroplastic Cu/Zn-SOD from barley seedlings was investigated to exhibit a response to cold stress. The results suggested that Hordeum vulgar Cu-Zn SOD gene expression was induced in leaf tissues to scavenge ROS produced by chilling stress and as a consequence provided tolerance to oxidative stress caused by low temperature. But no significant induction of HvSOD expression was noticed during the heat-stressed condition in barley (Romman & Shatnawi, 2011). As temperature stress imposes a negative effect on plants and is ameliorated by increasing SOD activity. The genes encoding cyt Cu/Zn SOD were uplifted to cope with chilling stress,

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whereas the expression of Cu/Zn-SOD was lightly downregulated under high-temperature conditions (Hernandez-Nistal et al., 2002). 11.5.2 Cu AGAINST BIOTIC STRESS As mentioned before, biotic stress is well-defined stress that may result in severe damage to crops throughout the world. The components of biotic stress mainly involve live organisms such as fungi, bacteria, viruses, parasitic nematodes, insects, and weeds. Among them, bacteria, fungi, viruses, and nematodes are major pathogens responsible for plant diseases. Leaf spots, vascular wilts, and cankers may be caused by fungi and bacteria, and nematodes can absorb all plant cell content and subsequently attack all plant sections, such as roots, stems, leaves, flowers, and seeds. Viruses also form local lesions and systemic damage, causing malformations, stunting, and chlorosis in various plant parts without killing their hosts (MoustafaFarag et al., 2020). To eliminate the depressive effect of pathogen, Cu2+ based fungicide, Bordeaux mixture has been traditionally used since 1885, as a potential substance to provide defense against plant disease caused by bacteria, fungi, and oomycetes. For example, the application of Cu nanoparticles (NPs) reduced biotic stress by limiting the mycelial growth of fungal species (Malandrakis et al., 2019). Cu has been successfully and extensively used to protect potato plants from Phytophthora infestans (late blight disease in potatoes caused by the oomycetes pathogen, hampers yield, and quality of potato tubers) and Arabidopsis against bacterial pathogens. As we know, ethylene is one of the important phytohormones that is crucial for plant defense responses, application Cu as copper sulfate has been found to overexpress StACS genes (ethylene synthesis pathway contains major rate-limiting step, including the conversion of S-adenosylmethionine to ACC catalyzed by ACC synthase (ACS) promoting ET production) resulting in rapid biosynthesis of ethylene through promoting StEIN3 gene (negatively binds to the promoter of StABA1 and StNCED1 decreasing ABA content). This negatively affects the biosynthesis of ABA by blocking the transcription of StABA1 and StNCED1 genes. Thus, CuSO4 ions appear to be beneficial in providing greater resistance to late blight disease (Liu et al., 2020). Actinomycetes, a group of grampositive bacteria, acts as an efficient candidate for the synthesis of metal NPs like CuO NPs that displayed higher antibacterial activity against both human and fish bacterial pathogens (viz. Aeromonas caviae, A. hydrophila, Bacillus cereus, Edwardsiella tarda, Proteus mirabilis, Staphylococcus aureus, and

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Vibrio anguillarum). Being reactive, Cu NPs have a high surface-to-volume ratio that allows them to interact with the bacterial cell membranes through its surface, resulting in inhibition of bacterial cell growth, death of the bacteria, and providing increased antimicrobial properties. Owing to antimicrobial properties like limiting the growth of bacteria, fungi, viruses, and algae, CuO NPs can be successfully used as both antibacterial and antifungal agents. It is reported that bacterial pathogens such as A. caviae B. cereus, and P. mirabilis, were inhibited by the biosynthesized CuO NPs at 5 µg/ mL concentration. Similarly, green-synthesized CuO NPs from Ocimum sanctum leaf extract exhibited antibacterial activity against S. aureus (Nabila & Kannabiran, 2018). Also, green synthesized Cu-NPs using Citrus limon fruits extract displayed excellent antibacterial activity against E. coli and S. aureus pathogenic bacteria. Cu application is a cost-effective, eco-friendly antibacterial agent (Amer & Awwad, 2021). Copper sulfate displaying antifungal properties against smut spores in wheat was already known before the discovery of the Bordeaux mixture. After the advent of the Bordeaux mixture, its efficacy to defend against diseases caused by Plasmopara viticola in grapes has been documented. On foliar application, Cu(OH)2 particles form a protective film over the leaves which releases Cu ions slowly when comes in contact with water at low pH. This imparts toxicity to the microbial cells. A large number of Cu-based antimicrobial compounds has been used for serving defense against diseases caused by oomycetes (downy mildew of grapevine, late blight of potato), and pathogenic bacteria (tomato spot, citrus canker, fire blight of pome fruits, walnut blight, stone fruit canker, mango apical necrosis, and olive knot). Hence, it can be concluded that Cu is vehemently applied on a large scale to combat plant pathogens and ensure disease management (Lamichhane et al., 2018; Menkissoglu and Lindow, 1991). Research on the evaluation of the role of Cu as a pesticide has also been reported. The growth of Gammaproteobacteria and other taxa in this class are significantly reduced in copper‐treated plants. The foodborne illness of tomatoes caused by Salmonella is prevalent in extensive areas throughout the world. Copper oxychloride (pesticide) effectively diminished the incidence of Salmonella and Paenibacillus sp. in the phyllosphere of copper‐treated tomato plant by blocking cellular growth of these genera via induction of toxic level of copper ions into the phylloplane and exhibiting toxicity symptoms such as stunted fungal and bacterial cell growth (Ottesen et al., 2015). Cu NPs are a novel eco-friendly promising alternative to synthetic conventional chemical fungicides. Cu-NP is the most effective nano-sized

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compound to limit mycelial growth of fungal species, i.e., Fusarium sp., Aspergillus niger, Rhizoctonia solani, Alternaria solani, A. alternata, Phoma destructive (Malandrakis et al., 2019) as well as inducing the production of intracellular ROS that subsequently oxidize fungal cell wall components such as glucan and chitin, that ultimately damage cell membranes of the pathogens. Thus, copper nanoparticle is an excellent anti-fungicide that controls pathogenic fungi (Pariona et al., 2019). Similarly, copper-chitosan nanoparticle (CuChNp) application shows the suppression of blast disease caused by P. grisea with increasing defense enzymes like chitinase and chitosanase on finger millet plants (Sathiyabama & Manikandan, 2018). 11.6 EXCESS COPPER AND REMEDIATION STRATEGIES The presence of an excessive amount of Cu in the plant body elicits a wide range of responses. When Cu crosses a threshold value (5–30 mg/kg) that may cause severe stress conditions in a plant. Cu exposure ranging between 100 mg/kg and 200 mg/kg is generally considered to be toxic for the plants (Jatav et al., 2020). Cu toxicity poses a serious threat to plants’ morphophysiological processes. Several aspects of plant growth and metabolism and the activity of several enzymes are inhibited by an excessive amount of Cu. It also impedes photosynthetic electron transport, causes LPO, and results in stunted growth. Additional effects of Cu toxicity include degradation of chloroplastids (grana stacking and stroma lamellae), increase in size and number of plastoglobuli, and production of intra-thylakoidal inclusions (Yruela, 2005). Cu toxicity may slow down fatty acid and protein metabolism, cause disturbances in respiration and nitrogen fixation (Fernandes & Henriques, 1991). Excess Cu induces oxidative stress due to ROS formation. Often proline accumulation in Cu stressed plant acts as an osmoprotectant to provide an additional defense system against oxidative stress (Thounaojam et al., 2012). Cu toxicity in plants results in erratic germination of seeds, stunted growth of leaf and root, ultrastructural, and various anatomical alterations, reduced yield. Few studies have been reported that Cu toxicity results in inhibition of seed germination, decrease in biomass and fresh weights of roots, shoots, and leaves of wheat; reduction of height (root and shoot elongation), leaf area, and diameter in maize. Moreover, total chlorophyll contents in wheat leaves have been found to drop linearly with high Cu levels in the soil and chlorosis has been occurred on leaves. Excess Cu concentrations may be attributed to genotoxicity by damaging DNA in cucumber, pea plants, tomato, onion, and

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root tips of sunflowers. Excess Cu induced rate of chromosome aberrations in anaphase and telophase of mitosis in wheat plants. Similarly, in rice roots, high Cu altered gene expression that was imposed a negative effect on fatty acid metabolism and cellular component biogenesis (Adrees et al., 2015). Excess Cu causes a marked increase of carbohydrates in leaves. This starch accumulation in the source leaves decreases phloem loading which has been reported to alter the source-sink relationship of Cu-stressed cucumber leaves (Alaoui-Sossé et al., 2004). The impact of Cu toxicity is associated with the uptake of other essential nutrients. A sharp decline of K and S content, and increased Mg, Ca, Fe, and Zn content has been observed due to high Cu accumulation in the root, and also decreased shoot concentrations of Ca, K, P, and Mn in Arabidopsis plants (Lequeux et al., 2010). Cu accumulation in plants negatively regulates Fe content and Fe addition has been found to ameliorate Cu toxicity in spinach (Fageria et al., 2002). It has been observed that in a waterlogged environment iron plaque formation dramatically blocks Cu uptake resulting in a reduction of Cu concentration in plant roots and shoots by 89% and 78% respectively (Peng et al., 2018). Plants have also been reported to limit ethylene biosynthesis via a decrease of Aminocyclopropane-1-carboxylic acid (ACC) synthase activity in leaf, root tissues due to excess Cu concentration (Lidon et al., 1995). Metal accumulation in plant systems is becoming a major environmental issue worldwide, particularly, in the agricultural ecosystem. Treatment of ampicillin to the nutrient solution has been found to rescue Cu accumulation by about 24–44% in shoots and 20–44% in roots of Elsholtzia splendens (Chen et al., 2005). Grafting is another way that has been effective in reducing Cu toxicity by improving higher net assimilation rates, crop performance of cucumber (Rouphael et al., 2008). After the discovery of the fact that Cu-Fe ions are antagonists to each other, ryegrass plants fertilized with Fe-EDTA, was found to replace binding of free Cu2+ thereby lowering Cu toxicity in soil with reduced accumulation both at the root and shoot (Conti et al., 2020). Exogenous application of Si improves morpho-physiological attributes such as growth, photosynthetic pigments, and gas exchange which may confer tolerance to Cu and detoxify Cu concentrations in roots, stem, and leaves as compared with the non-treated plants (Ali et al., 2016). Application of 24-epibrassinolide (EBR, an active form of Brassinosteroids) and putrescine (Put), spermidine (Spd) (active form of polyamines) act as direct response to enhance Cu stress tolerance (Pal Choudhary et al., 2012). All these strategies have been recorded to avoid the excess Cu concentration in the plant body and thus prevent the onset of toxic symptoms.

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11.7 CONCLUSION Micronutrient application in crop plants to promote plant growth and mitigate plant stress has gained impetus over the years. The main reason behind it lies in the fact that micronutrients are the most authentic organic substitute for harmful chemical fertilizers and pesticides. Agro-chemicals does not only cause environmental degradation but also result in consumer health menace. Application of plant nutrients through methods like soil treatment, microdosing, foliar application, seed treatment, appears to be the environmentally friendly alternative to bulk usage of chemicals. In addition, the increasing environmental pollution poise its harmful effects on plants leading to stress conditions and micronutrient application is beneficial in mitigating stressmediated atrocities. Copper is one such important micronutrient that has diverse roles in plants. Investigations on the role of copper against environmental stress reveal that copper can be used to combat various biotic and abiotic stress in economically important plants. However, there is a dearth of detailed understanding of the mechanism of how copper can do so. Moreover, most of the studies fail to deliver the results in terms of ultimate crop yield. Also, increasing reports of the use of Cu-NPs creates room for understanding the mechanism of action and safety of usage of them. Thus, future investigations might fill the voids and help in establishing copper as a potent alternative to harmful agrochemicals. KEYWORDS • • • • • • • •

antioxidant enzymes copper copper nanoparticles copper transporters cytochrome-C oxidase hydrogen peroxide stress yield

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Pariona, N., Mtz-Enriquez, A. I., Sánchez-Rangel, D., Carrión, G., Paraguay-Delgado, F., & Rosas-Saito, G., (2019). Green-synthesized copper nanoparticles as a potential antifungal against plant pathogens. RSC Advances, 9(33), 18835–18843. Peng, C., Chen, S., Shen, C., He, M., Zhang, Y., Ye, J., Liu, J., & Shi, J., (2018). Iron plaque: A barrier layer to the uptake and translocation of copper oxide nanoparticles by rice plants. Environmental Science & Technology, 52(21), 12244–12254. Pérez-Labrada, F., López-Vargas, E. R., Ortega-Ortiz, H., Cadenas-Pliego, G., BenavidesMendoza, A., & Juárez-Maldonado, A., (2019). Responses of tomato plants under saline stress to foliar application of copper nanoparticles. Plants, 8(6), 151. Piri, R., Moradi, A., Balouchi, H., & Salehi, A., (2019). Improvement of cumin (Cuminum cyminum) seed performance under drought stress by seed coating and biopriming. Scientia Horticulturae, 257, 108667. Prashanth, S. R., Sadhasivam, V., & Parida, A., (2008). Overexpression of cytosolic copper/ zinc superoxide dismutase from a mangrove plant Avicennia marina in indica rice var Pusa Basmati-1 confers abiotic stress tolerance. Transgenic Research, 17(2), 281–291. Printz, B., Lutts, S., Hausman, J. F., & Sergeant, K., (2016). Copper trafficking in plants and its implication on cell wall dynamics. Frontiers in Plant Science, 7, 601. Puig, S., (2014). Function and regulation of the plant COPT family of high-affinity copper transport proteins. Advances in Botany, 2014. Purakayastha, T. J., & Chhonkar, P. K., (2010). Phytoremediation of heavy metal contaminated soils. In: Soil Heavy Metals (pp. 389–429). Springer, Berlin, Heidelberg. Rahman, A., Hossain, M. S., Mahmud, J. A., Nahar, K., Hasanuzzaman, M., & Fujita, M., (2016). Manganese-induced salt stress tolerance in rice seedlings: Regulation of ion homeostasis, antioxidant defense and glyoxalase systems. Physiology and Molecular Biology of Plants, 22(3), 291–306. Rahmati, I. M., & Vatamaniuk, O. K., (2020). Copper deficiency alters shoot architecture and reduces fertility of both gynoecium and androecium in Arabidopsis thaliana. Plant Direct, 4(11), e00288. Rao, B. S., Patil, D. B., & Puli, M. R., (2013). Delineation of copper (Cu) and zinc (Zn) status in soils of central research station Akola. Journal of Progressive Agriculture, 4(1), 131–134. Rao, B. S., Patil, D. B., Puli, M. R., & Jayalakshmi, M., (2018). Withdrawn: Delineation of copper (Cu) and zinc (Zn) status in soils of central research station Akola. Withdrawn: Delineation of Copper (Cu) and Zinc (Zn) Status in Soils of Central Research Station Akola. Rastgoo, L., & Alemzadeh, A., (2011). Biochemical responses of Gouan (‘Aeluropus littoralis’) to heavy metals stress. Australian Journal of Crop Science, 5(4), 375. Rouphael, Y., Cardarelli, M., Rea, E., & Colla, G., (2008). Grafting of cucumber as a means to minimize copper toxicity. Environmental and Experimental Botany, 63(1–3), 49–58. Saint, P. C., Peterson, C. J., Ross, A. S., Ohm, J., Verhoeven, M. C., Larson, M., & Hoefer, B., (2007). Change in grain protein composition of winter wheat cultivars under different levels of N and water stress. In: Wheat Production in Stressed Environments (pp. 535–542). Springer, Dordrecht. Sancenón, V., Puig, S., Mateu-Andrés, I., Dorcey, E., Thiele, D. J., & Peñarrubia, L., (2004). The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development. Journal of Biological Chemistry, 279(15), 15348–15355. Saraste, M., (1990). Structural features of cytochrome oxidase. Quarterly Reviews of Biophysics, 23(4), 331–366.

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CHAPTER 12

Role of Sulfur in Plant Tolerance to Environmental Stresses

LALICHETTI SAGAR,1 SULTAN SINGH,2 DEEPAK KUMAR,2 SUBHASHISA PRAHARAJ,1 SUDEEPTA PATTANAYAK,3 GANESH CHANDRA MALIK,4 BISWAJIT PRAMANICK,5 TANMOY SHANKAR,1 AKBAR HOSSAIN,6 and SAGAR MAITRA1*

Department of Agronomy and Agroforestry, Centurion University of Technology and Management, Paralakhemundi – 761211, Odisha, India 1

Division of Agronomy, Sher-e-Kashmir University of Technology and Management, Jammu – 180009, Jammu and Kashmir, India

2

Division of Plant Pathology, ICAR–Indian Agricultural Research Institute, Pusa Campus, New Delhi – 110012, India

3

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

4

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

5

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

6

*

Corresponding author. E-mail: [email protected]

ABSTRACT Management of sulfur (S) is vital in crop plant nutrition, especially under an intensive agriculture system. Sulfur has a distinct role in essential physiological and metabolic processes such as electron transport, structure, and Biology and Biotechnology of Environmental Stress Tolerance in Plants: Trace Elements in Environmental Stress Tolerance, Volume 2. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

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regulation and is also linked to photosynthetic oxygen production, biotic, and abiotic stresses tolerance, and secondary metabolism. Sulfate uptake, reductive assimilation, and integration into important amino acids, namely, cysteine (Cys), and methionine are the important processes that direct oxidized and reduced forms of organically bound S into their various functions. S-containing compounds that enhance tolerance to various stresses are elemental S, phytochelatins (PCs), hydrogen sulfide (H2S), S-rich proteins glutathione (GSH), and numerous secondary metabolites. These compounds are formed depending on the need of the plants, removal of applied or soil containing S and its assimilation. The chapter highlights the role of S in the amelioration of abiotic stresses in plants inclusive of S metabolism and response during environmental stress conditions. Also, based on the available literature, the future scope of research has been narrated. 12.1 INTRODUCTION Plants face various biotic and abiotic stresses which limit their growth and yield by disturbing their normal physiological and metabolic pathways. This environmental stress can alter ideal growth conditions like salinity, temperature, ozone, heavy metal or acidification of soil, water pollution, etc., leading to a reduction in yield or causing permanent damage and death (Bulbovas et al., 2014; Nougirol et al., 2015). A sudden modification in environmental conditions can reflect stress in a plant. The presence of some toxic compounds or hazardous chemicals in water, air, or soil may create stresses for plants (Su et al., 2014; Iannone et al., 2015). Plants are exposed to a variety of abiotic stresses continuously due to the constant change of climatic conditions. Different categories of abiotic factors are heat, dehydration, salinity, etc. Among the abiotic stresses, cadmium (Cd) toxicity is one of the major threats disturbing the molecular and physiological mechanism of plants as they are most sensitive to the Cd concentration. This heavy metal is mixed with agricultural lands through industry or municipality wastes and taken up by roots and then transported to leaves (Rodríguez-Serrano et al., 2009). High salt concentration creates salinity stress by accumulating Na+ and Cl– ions causing ionic toxicity. Salinity stress can disturb the plant growth processes by damaging the cellular components, inhibiting enzyme activities through altering the growth regulator, and disturbing the nutritional homeostasis of minerals (Munns & Tester, 2008; Hasanuzzaman et al., 2013a). The burdens due to high atmospheric temperature is another critical challenge causing

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severe damage to the plant. It was observed that heat stress can lower pollen fertility, fail or disturb pollination which severely affects both the vegetative and reproductive stages of the plant (Fahad et al., 2016). The responses of plants to different stresses occur in a complex as well as dynamic way. Abiotic stresses increase the production of reactive oxygen species (ROS) through the perturbation of cellular homeostasis (Das & Roychoudhury, 2014). Plants have very effective defense pathways which protect the cell from oxidative damage by allowing the scavenging of ROS. The soils having low fertility are due to a lack of application of all essential nutrients into the soil during the crop production process. Low S content in the soil can be a reason for inefficient functions of other nutrients, such as nitrogen (N) or carbon (C) which can reduce the chlorophyll content or decrease the protein biosynthesis (Iqbal et al., 2013). The research evidence documented the key role of S metabolism against the different types of plant stress. The primary role is to manage sulfur fluxes in response to environmental fluctuating conditions. The plant mainly focuses on the optimization of available sulfur to reach the demands of plant growth and resistance to a different type of stresses. Before incorporation into organic nitrogen and sulfur compounds, nitrate, and sulfate need to be reduced first. Plant roots absorb the sulfur from roots and assimilation of sulfur occurs. Similarly, when the leaves absorb the H2S, plants use this sulfur for its developmental activity. 12.2 ROLE OF SULFUR IN PLANT NUTRITION Sulfur, the fourth major plant nutrient after nitrogen, phosphorus, and potassium, is recognized as an essential nutrient for plants. Sulfur plays many important roles in plants (Figure 12.1). Sulfur has many regulatory, structural, and catalytic functions. The productivity of plants is mainly dependent on S or S-compounds. Sulfur is a major component of proteins, vitamins, cofactors, and secondary metabolites (Mazid et al., 2011). In addition to this, S is also a constituent of polysaccharides, iron, sulfur clusters, peptides, etc. (Khan et al., 2013). Sulfur is a key constituent of three major amino acids, i.e., cysteine (Cys), cystine, and methionine which are also known as building blocks of protein. S can activate different enzymes to start the function of many biochemical reactions in the plant. It has an indirect role in the production of sugar, starch, vitamins, fats, etc., by chlorophyll production and nodule formation (Sarker & Oba, 2018). It can also improve the crop quality, oil percentage, and flavor, quality of tobacco and forage quality, etc. The presence of the correct amount

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of S improves the odor and flavor quality of garlic, onion, and mustard. The main source of sulfur is sulfates or sulfur oxides like H2S. H2S is absorbed by the stomata of plant leaves from the air while sulfates are obtained from the soil through sulfate transporters. Most S elements are present in topsoil with soil organic matter. S is available in the soil as elemental S, which cannot be taken by the plants directly and need to be converted to the sulfate (SO4–) form by the soil microorganisms (Raza et al., 2018).

FIGURE 12.1

Multiple roles of sulfur in plant.

Sulfur reclamation in alkaline and saline soil has proved its potential role in improving the physicochemical and biological properties of soil, decreasing the pH content, increasing the efficiency of other fertilizers, and availability of plant nutrients for the crop such as phosphorus and other micro-nutrients. S has a major role in reducing the possibility of copper toxicity by creating a

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Cu-S complex. Oxidation of S improves the manganese (Mn) availability to the plant (Reich et al., 2016). The specific nutrient requirement for the crop can be defined as “the minimum content of that nutrient-related with the maximum yield.” Therefore, the slight up and down in the concentration of S can lead to a decrease in the marketability, quality, and yield of the crop. The requirement and uptake of S greatly vary among species, cultivars as well as crops. Most halophytes contain a high amount of S while maize and small grain contain the least amount of S. S is mostly required at 0.1 to 1.0% on a dry weight basis for the growth and development of the crop. The adequate supply of S needs to be assessed properly as it has multiple sources and varying utilization efficiencies, limited S reuse, and high S reserve accumulation in the plant. Sulfur can be applied through different fertilizers (Table 12.1). TABLE 12.1

Different Sulfur-Containing Fertilizers

Sulfur Source Ammonium sulfate Single superphosphate (SSP) Potassium magnesium sulfate Potassium sulfate Magnesium sulfate

Sulfur Content (%) 24 10–14 22 17 13

The S deficiency symptoms can easily be identified by visualizing some prominent symptoms in the plant, such as chlorosis and reduced growth. Chlorosis spreading to older leaves, cupping of leaves or upright leaf structure, reddening or purpling of stems and petioles is observed often in some plants. Similarly, S toxicity is also a challenge in crop plants which can be observed as the reduction in leaf size, yellowing or scorching at leaf edges, or stunted growth of the plant. Many sulfur compounds in plants have been found to overcome diseases and stress resistance (Table 12.2). TABLE 12.2

Sulfur Compounds Involved in Overcoming Disease and/or Stress Resistance

Sulfur Compounds Involved in Disease and/or Stress Resistance Phytoalexins Glucosinolates Glutathione Cysteine

References Bloem et al. (2015); Yadav (2010) Bloem et al. (2015)

Cobbett (2000); Vanacker et al. (2000) Alvarez et al. (2012)

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12.3 SULFUR AMELIORATION OF SALINITY Salinity is a major constraint in crop production that renders farmland to non-arable land (Joseph & Mohanan, 2013). Recently, most of the areas in the world are subjected to salinity stress which in turn triggers several socio-economic constraints. The concentration of salt in excessive amounts in the soil primarily reduced the soil water potential influencing the osmotic potential; thus, nutrient uptake was seriously affected by soil salinity rendering highly fertile soil as unproductive (Aslam et al., 2017; Sheldon et al., 2017). The loss of soil productivity due to salinity stress is mainly attributed due to the osmo-ionic imbalance that adversely impairs nutrient concentration and its availability within the plant (Dodd & Perez-Alfocea, 2012). Physiologically, an increase in soil salinity reported a significant reduction of turgidity of leaf cells leading towards severe reduction of cell elongation and in turn the leaf growth rate (Shrivastava & Kumar, 2012). Due to its influence on soil water potential, uptake of nutrients and water was seriously hampered. Furthermore, this results in an increased number of free radicals and subsequent over release of ROS (Karuppanapandian et al., 2011). Overproduction of ROS initiates oxidative stress ensuing structural disintegration of biomolecules, viz., proteins, lipids, nucleic acids, etc., and membrane properties, respectively (Ahange et al., 2017). Upregulation of ROS is a natural response to stress; hence the adoption of any adaptation strategy to normalize ROS production could be an efficient and best strategy to tolerate stress (Maremonti et al., 2020). Henceforth, mechanisms triggering the expression of ROS regulatory genes as a response to scavenge ROS enhances the plant tolerance to salinity (Zhang et al., 2016). Crops subjected to salinity stress resulted in the activation of sodium and hydrogen antiporters present on the plasma membrane leading to simultaneous activation of the salt overly sensitive complex to improve salinity tolerance. SOS signaling is one of the important pathways which primarily elicits different adaptive mechanisms to tolerate salinity stress. Studies indicate, when the plant is subjected to salt stress calcium-mediated signaling gets activated and upon activation calcium minds at the myristoylation site of SOS3 which further binds to the C-terminal of SOS2 resulting in activation of kinase enzyme that initiates phosphorylation of SOS1 resulting in extrusion of Na+ ions from cell (Gupta & Huang, 2014) In Arabdiopsis, salt stress tolerance was reported due to activation of mitogen-activated protein kinase (MAPK) cascade produced as a response to ROS upregulation, in turn lowered ROS levels significantly due to improved signaling which

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could contribute for high concentration of antioxidants (Gupta & Huang, 2014; Goharrizi et al., 2019). However, it is challenging to impart tolerance to salinity stress because this trait is governed by multiple gene responses. Nowadays, the role of sulfur is increasingly getting widespread which could be due to the constituent nature of sulfur in many organic molecules such as Cys, glutathione (GSH), etc. (Joshi et al., 2009). ROS signaling pathway contributes a vital role in activating stress ameliorating pathways in the plant thereby, adapting it to stress (Di Meo et al., 2016). Plants with high concentrations of antioxidants have enhanced tolerance to stress which can otherwise detoxify the adverse negative impact of ROS (Ahmad et al., 2008; Sharma et al., 2012). Among the various antioxidants, the role of GSH, a sulfur-containing compound, is very effective (Gaucher et al., 2018). Sulfur Sulfur-containing compounds have immense practical utility in imparting stress tolerance to various crops. In case a crop is exposed to salinity stress GSH synthesis was emphasized to tolerate induced oxidative stress due to its role in ROS detoxification; while during sulfur deficiency, sulfate transport was accelerated to keep up the rate of GSH synthesis (Badea & Antoce, 2015). However, during severe deficiency synthesis of Adenosine-5-phosphosulfate was accelerated which was reported to be acted upon by adenosine-5-phosphosulfate reductase (APR) enzyme resulting in the formation of sulfite targeting the synthesis of sulfur-based analogs (Grant et al., 2011). Henceforth, during salinity stress, the role of GSH synthesis is gaining importance and this rate is regulated by an increased supply of sulfur to meet its demand. ROS scavengers like GSH could decrease the formation of hydroxyl radicals which may seriously impair various proteins and membranes, respectively (Zhang et al., 2012). In case of deficiency external supply of sulfur is essential and if the demand for sulfur exceeds then channelization of sulfur through more efficient sulfur transporters takes place preferably under the influence of APR resulting in GSH formation to meet its demand (Henchion et al., 2017). In an experiment, it was observed that Giza 9 variety of Egyptians lentil was highly tolerant to salinity stress compared with Giza 4 under normal conditions while when the seeds of Giza 4 were primed with GSH this was reversed which might be attributed due to the role of GSH (Gaafar & Seyam, 2018). Sulfur is usually uptake by roots and moves within the plant system through the xylem pathway and phloem uptake of sulfur is only possible in polluted environments (Tan et al., 2010). Cys is a sulfur-containing amino acid. Studies indicated upregulation of Cys concentration as a protective role in response to a variety of environmental stresses (Yin et al., 2016).

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ATP-sulfurylase and adenosine 5-phosphosulfate reductase enzymes were very important enzymes involved in sulfur assimilation (Herrmann et al., 2014). Sulfur assimilation usually occurs in plastids of the leaf wherein with the induction of salinity stress adenosine 5-phosphosulfate in the plastids of the plant cell is reduced to adenosine 5-phosphosulfate in the presence of an enzyme adenosine 5-phosphosulfate reductase (Van den Boom et al., 2012). Further, this adenosine 5-phosphosulfate is converted to a sulfide in the presence of an enzyme sulfite reductase (SiR) which upon supplied to active serine compound through O-acetyl-serine-lyase (OASTL) results in the production of Cys, respectively. The importance of Cys in stress tolerance was mainly attributed due to its role as a precursor for the synthesis of GSH and in ethylene synthesis (Wirtz et al., 2012; Birke et al., 2012). Phytochelatin is certain secondary sulfur molecules that were observed to increase in concentration upon overexpression of phytochelatin synthase 2 enzymes in Arabidopsis thaliana (AtPCS2) in response to salinity and consequently, realized better seed germination and seedling growth under stress due to salinity (Kim et al., 2019). A study clearly revealed that foliar application of Cys @40 ppm on soybean helps in alleviating the crop from salinity stress; this might be due to enhanced production of ROS scavenging enzymes, viz., superoxide dismutase (SOD) and catalase (CAT) and further reported elevation of nutrient as well as pigment concentration within the cell (Sadak et al., 2020). Similarly, in Arabidopsis, upregulation of genes involved in thiamine biosynthesis when induced with artificial salt stress for 48 hours (Rapala-Kozik et al., 2012). 12.4 SULFUR TO FIGHT AGAINST DROUGHT Globally, drought is considered as a foremost constraint for raising crops. Each plant requires water, and the requirement varies from one crop to another (Farooq et al., 2009). The plant requires water to achieve water demand, mainly to balance evapotranspiration losses of the crop and very minor quantity of water is required for plant metabolic activities (Jaleel et al., 2009). Plants face low soil moisture stress when potential evapotranspiration losses exceed water availability for an extended period of time (Kubov et al., 2020). Water deficits have an adverse impact on several parameters determining crop growth and yield viz. water relation of the crop, photosynthesis, respiration, hormonal changes, etc. (Wang et al., 2019). Several experimental studies indicated that cell expansion is manifested due to

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turgor pressure within the plant cell (Osmolovskaya et al., 2018). In addition, when the plants are subjected to drought stress (DS) initially, there was an increased rate of transpiration, raising the demand for moisture (Feller & Vaseva, 2014). Consequently, water absorption from the soil increases along with minimization of stomatal conductance influencing the transpiration rate aiming to maintain cell turgidity (Desoky et al., 2020). Once the soil moisture gets exhausted, canopy temperature was reported to raise gradually impairing cell turgidity resulting in minimization of cell division and subsequent growth of the crop (Guan et al., 2015). Several studies indicated dry matter accumulation was impaired due to a reduction in photosynthesis under moisture stress. This might be due to increased stomatal resistanceconferring reduction in carbon dioxide (CO2) intake which is a basic raw material for photosynthesis (Xie et al., 2011). In addition, leaf area reduction is also attributed to the reduction in photosynthetic rate leading towards poor grain filling resulting in less photosynthate accumulation (Moonmoon et al., 2017; Gregoriou et al., 2007). On the other hand, DS also induces free radical oxygen species as a response to stress activating the signaling pathways to get adapted to the abiotic stress and consequently, targeting the lipid peroxidation (LPO) affecting the structural integrity of the membrane resulting in leaky membranes (Cruz de Carvalho et al., 2008). Furthermore, this also elicits hormonal imbalance promoting the production of growthregulating hormone production (Lipiec et al., 2013). All those anatomical and metabolic changes occurred as a response to drought, manifests tolerance and improves adaptivity to survive and grow under environmentally unfavorable conditions compromising the yield (Abdel-Kader et al., 2015). Proper understanding of the mechanisms involved in tolerating the stress conditions is essential to adopt certain strategies to withstand stress overcoming its limitation as a whole (Hussain et al., 2019). Nutrient management during stress is one such strategy which when not planned appropriately might decrease its efficiency (Da Silva et al., 2011). Since stress adaptation was mainly influenced by certain nutrients whose uptake and assimilation from soil was also restricted due to DS raising concerns. Similarly, in recent days, the role of S and its compounds to fight the drought was widely recognized. The mechanism of sulfur in DS tolerance is usually classified into two mechanisms namely primary sulfur metabolic and secondary sulfur metabolic pathway (Musilova et al., 2016). In the primary, metabolic pathway with the induction of DS sulfate transporters present on the plasma membrane were activated and led to accumulation of sulfur in the form of sulfate from the

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soil solution (Gallardo et al., 2014). The sulfate upon entry acted by ATP in the presence of enzyme ATP-sulfurylase, resulting in the formation of Adenosine phosphor-sulfate which were further acted upon by Adenosine phosphor-sulfate reductase enzyme resulting in Adenosine phosphor-sulfite and thereby, it gets reduced to Adenosine phosphor-sulfide in the presence of sulfide reductase enzyme. Ultimately, Cys is produced which is involved in the biosynthesis of GSH imparting tolerance to DS. Moreover, Cys’s role in abscisic acid (ABA) biosynthesis minimizes the evapotranspiration losses attributed due to the role of ABA in stomatal closure (Lee et al., 2011; Khan et al., 2010). Under severe DS the zeaxanthin present in the plastids undergoes epioxidation in the presence of zeaxanthin epioxidase enzyme resulting in the violaxanthin which is further undergoes isomerization into neoxanthin followed by it is subjected to cleavage by of NCED enzyme resulting into xanthaxin which is further oxidized to ABA aldehyde and later it is again subjected to oxidation in the presence of ABA aldehyde resulting in the biosynthesis of growth-regulating hormone ABA (Cao et al., 2010; Seiler et al., 2011). As a known fact availability of sulfide and OASTL enzyme determines the rate of synthesis of Cys under DS conditions and biochemically the role of Cys in ABA biosynthesis was signified as it acts as a vector for sulfur resulting in the formation of sulfur molybdenum co-factor which is very essential for the activation of ABA aldehyde enzyme that which acts as a catalyst during the last step of ABA biosynthesis (Zhang et al., 2020). Sulfur molybdenum cofactor was catalyzed by ABA3 enzyme and upregulation of both ABA3 provoking S-Moco and NCED provoking xanthoxin production in ABA biosynthesis signifies the DS (Batool et al., 2018; Vishwakarma et al., 2017). On the other hand, Cys being very unstable rapidly oxidizes into gamma-glutamyl synthase (Badea & Antoce, 2015). Further synthesis of GSH is an ATP-dependent process wherein two catalysts, namely gamma glutamine Cys synthase and GSH synthase hasten the process significantly (Yang et al., 2015). GSH when exposed to oxygen free radicals oxidize to glutathione reductase (GR) and immediately GR was observed to revive back to GSH upon reduction, establishing a redox cycle attributing to its role in efficient detoxification of ROS (Couto et al., 2016; Dumanovic et al., 2020). Glucosinolate compounds were observed to get provoked in Brassica rapa spp. chinensis when subjected to DS (Park et al., 2021). Further, glucosinolate production stimulates the production of growth-regulating hormones, viz., ABA contributes towards Cys synthesis that plays a significant role

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in imparting DS tolerance to crops (Gupta et al., 2020). Lipoic acid was reported to establish drought resistance in maize seedlings which were artificially induced with drought by using polyethylene glycol (PEG). Further, exogenous application of alpha-lipoic acid minimized membrane damage due to its ROS scavenging activity and increased relative water content (RWC) ensuring normal crop growth during drought (Sezgin et al., 2019). 12.5 SULFUR IN AMELIORATION OF TEMPERATURE STRESS The atmospheric temperature greatly influences the growth processes of plants (Hasanuzzaman et al., 2013b). Each plant needs a specific cardinal temperature, and the rate of growth is normal until the temperature is within an optimum range (Bartley et al., 2015; Hatfield & Prueger, 2015). However, extremities in temperature reported having an adverse negative impact on the crop phenology and directly affecting the duration of the crop (Sehgal et al., 2018). According to an estimate, by the end of the 21st century, the global average temperature may rise 1.8–5.8°C, respectively (Bita & Gerats, 2015). Rapid industrialization and mechanization lead to a spike in greenhouse gas concentration in the atmosphere (Wadanambi et al., 2020). Consequently, resulting in high-temperature stress (Kumar et al., 2012). In fact, at the cellular level, the production of ROS is commonly induced by high-temperature stress resulting in deformed cell organelles in response to denaturation of proteins and enzymes which in turn considered quite essential for maintaining structural integrity and metabolic functioning of the cell (Sharma et al., 2012). In general, PS-II is most sensitive to high-temperature stress while on the other hand, PS-I exhibits mild tolerance to high temperatures and adversely affects the photosynthetic rate (Martinez et al., 2018; Chandra et al., 2008). In addition, contributing towards the substantial reduction of yield and yield attributes of a crop accompanied by loss of chlorophyll and creating a significant imbalance in its ratios, respectively (Awasthi et al., 2017). Moreover, temperature rise accompanied by photoperiod plays a direct role in determining the crop duration (Daba et al., 2016). All the plant’s metabolic and biochemical functioning was accelerated with the rise in temperature above the threshold, which in turn curtailed the crop duration (Farooq et al., 2009; Rani & Sen, 2020). In a study conducted by Reena et al. (2019) reported an increased sensitivity of temperature stress on wheat phenology viz. Flowering, anthesis, and maturity in late sown wheat (Dec 28) occurred

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11.4, 11.7, and 9.1 days earlier than normally sown wheat (Nov 28), comparatively. Further, high-temperature stress often affects pollination in the crop ensuing pollen grain sterility, reduced number of pollens, or induced pollen incompatibility (Harsant et al., 2013). Pollen grains are comparatively more sensitive to high temperatures than stigma (Fahad et al., 2016). This might adversely affect fertilization attributing to poor grain development. In this context, the S compounds positively impact in amelioration of temperature stress, which is acquired due to its role as a structural constituent of certain metabolites like methionine, Cys, and GSH, respectively (Anjum et al., 2015; Ahmad et al., 2016). In addition, sulfur also helps in improving stress signaling intracellularly and thereby helps in improving communication between different cell organelles which in turn helps in quick activation of different stress ameliorating mechanisms (Sehgal et al., 2016; Kopriva et al., 2019). High temperature initiates degradation of protein resulting in the accumulation of ammonia in the plant cells contributing towards ammonium toxicity which is tolerated with subsequent accumulation of amino acid asparagine (Samsel & Seneff, 2016). Methionine is another important amino acid that is concentrated as a response to heat stress playing an important role in the translation of mRNA (Laxman et al., 2013; Zhang et al., 2015). In addition, special proteins, namely heat shock proteins (HSPs) are released as a resistant mechanism by different crops, basically to protect structural integrity PS-II (Hasni et al., 2015). The increased synthesis of ROS is quite significant inside the plant cell as a response to heat stress which in turn work as a defense mechanism and imparts enhanced resistance to extreme temperatures, but on the other side, this accumulation negatively affects the growth and development of the plant through improper balance on ion homeostasis (Devi et al., 2017; Ulhassan et al., 2019). Hence ROS scavenging is very important during stress to overcome ROS’s negative impacts on cell functioning (Karuppanapandian et al., 2011). GSH, a metabolite of sulfur plays an important role in ROS scavenging during heat stress and helps safeguard the cell functioning (Wisedpanichkij et al., 2010). GSH acts as an electron donor, and with induction of stress either heat or drought it donates its electrons and gets oxidized to GR and these donated electrons help to minimize ROS thus escaping oxidative stress induced by high temperatures (Achary et al., 2015). Thioredoxins (Trx) are sulfur-containing proteins that help in sensing the heat stress and induce the signal that enhances the production of HSPs; thus, imparting stress resistance to the crop (Lee et al., 2018; Wang et al., 2018). In a study, it was observed that increased expression of NADPH-Trx reductase inducing holdase chaperon function and that

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was responsible for high-temperature tolerance in Arabidopsis (Chae et al., 2013). According to some recent studies, the role of lipoic acid during heat stress is getting popular as an efficient antioxidant significantly focusing on ROS detoxification which is increased due to high-temperature extremes (Terzi et al., 2018). Glucosinolate is another important metabolite having sulfur as a basic constituent, usually present in crucifers as an anti-nutritional factor reported to increase in concentration when the crucifers are subjected to heat stress (Soundararajan et al., 2018). 12.6 SULFUR AGAINST LIGHT STRESS Light is the most important factor essential for the growth and development of any plant. Since many physiological and biochemical processes were influenced by wavelength and intensity of light thus plays a key role in affecting seed germination, expansion of leaf, flower initiation, fruiting, and crop duration, etc. (Chen et al., 2014). Solar radiation is the major source of light in the earth’s atmosphere that supplies the energy required for various metabolic and biochemical processes in the plant (Kazem & Chaichan, 2016). The light within the UV range is harmful and adversely known to affect plant metabolism (Jirous-Rajkovic & Miklecic, 2012). Similarly, the light within the visible range (400 to 700 nm) is reported to influence activity and amount of key photosynthetic enzymes, pigmentation, and leaf orientation which in turn is attributed to influence growth and yield of the crop; hence, this wavelength is popularly known as photosynthetically active radiation (PAR) (Bayat et al., 2018; Kumar et al., 2017). Further, higher wavelengths beyond red light could not have photosynthetic effects, while possessing only thermal and photoperiodic effects in plants (Cao et al., 2016). Light intensity determines the surface characteristics of the leaf. At higher light intensity, CO2 assimilation increases due to an increment in stomata per unit area (Holisova et al., 2012). In addition, increased light intensity is also reported to stimulate the activity and production of photosynthetic enzymes, viz., phosphoenolpyruvate carboxylase and ribulose 1,5 bisphosphate carboxylases, respectively (Giuliani et al., 2019). Although light is renewable and available continuously during daytime either as direct or diffused radiation, interception of light by plant canopies is influenced by both spatial and temporal factors, viz., time of sowing, plant stand, surrounding, and overhanging vegetation, latitude, season, altitude of a place and adopted crop management practices (Marchiori et al., 2010). In addition, the requirement

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of light intensity is crop-specific, those crops that have higher photosynthetic capacity can be adapted to higher light intensity and vice versa (Zervoudakis et al., 2012). All the agronomic management practices such as time of planting, crop geometry, plant population per unit area, nutrient management, weed management, etc., usually aim at facilitating enhanced interception of light by crop canopies attributing towards increased photosynthetic efficiency (Liu et al., 2011). Shading of crop canopies usually reduces the photon flux thus affecting the photosynthesis, adversely resulting in low light stress seriously impairing the chlorophyll formation and carbon assimilation, respectively (Feng et al., 2014). While plants raised under excess light are reported to have waxy leaf surface and less exposed leaf area; thus, adapted to reflect excess light, minimizing the excess light intake flux consequently (Paul et al., 2019; Aparecido et al., 2017). However, light-sensitive or shade-loving plants when exposed to excess light were subjected to oxidative stress due to stimulation of ROS (Staneloni et al., 2008). These ROS were released as a signaling mechanism to adapt against abiotic stresses, but their accumulation impairs the DNA and membrane structure of several cell organelles leading to cell death (Sachdev et al., 2021). In a study, when a plant is subjected to high light intensity observed to increase the concentration of OAS and GSH. However, the Cys concentration remained unchanged due to the rapid conversion of Cys to GSH to abate light stress, respectively (Speiser et al., 2015). Similarly, sulfur also plays a vital role in photo-acclimatization to high-intensity light this could be due to its regulatory role in the last step of ABA biosynthesis signifying its role in stomatal opening and closing (Caliandro et al., 2013; Sun et al., 2009). 12.7 SULFUR IN COMBATTING HEAVY METAL STRESS Heavy metal pollution is a rising concern at current times, significantly deteriorating the productivity of arable agricultural lands (Hu et al., 2014). In General, heavy metals viz. cadmium (Cd), copper (Cu), lead (Pb), nickel (Ni), chromium (Cr), cobalt (Co), arsenic (As) and zinc (Zn) plays a key role in crop growth and development (Arif et al., 2016). Heavy metal stress could be primarily induced due to overuse of fertilizers (viz. phosphatic), improper application of sewage and sludge, irrigation using poor quality water, etc. (Zhang et al., 2018). The plants induced with heavy metal stress primarily triggered the production of ROS; this could be due to induced disruption of electron transport chains adversely affecting the antioxidant activity in the

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plant (Madkour, 2020). In addition, this also induced membrane instability due to its significant role in LPO and thereby, resulting in leakage of protoplasm and cell death, respectively (Hameed et al., 2012). The crops cultivated on cadmium-rich soils have a negative impact on the photosynthetic mechanism, water, and nutrient uptake thus reflecting in crop growth inhibition (Asati et al., 2016). Usually, cadmium is accumulated in the agricultural soils through fertilizers or by using Industrial wastewater for irrigation prior to treatment (Mojiri & Aziz, 2016). High mobility of cadmium in the plant system attributes to easy uptake and translocation resulting in yellowing of leaves, LPO, impaired pollen tube formation and germination, inactivation of several enzymes involved in various metabolic activities, etc. (Emamverdian & Ding, 2017). Copper (Cu) is another heavy metal that plays a key role in cell signaling (Jaishankar et al., 2014). Plastocyanin is a copper-based mobile electron carrier that is involved in electron transfer during non-cyclic electron transfer of photosynthesis, in turn, plays a vital role in supplying electrons from PS-II to PS-I, respectively (Weigel et al., 2003; Jha et al., 2016). Under high concentrations of accumulated copper, it gets oxidized to Cu2+, resulting in the production of ROS; thus, it induces oxidative stress (Duanghathaipornsuk et al., 2021). Copper-induced oxidative stress impairs DNA structure, stability of lipid membrane, etc. (Husain & Mahmood, 2019). Zinc (Zn) is an important heavy metal that plays a vital role in plant metabolism (Asati et al., 2016) and acts as a cofactor for many enzymes. The Zn deficiency causes a substantial reduction in the yield of the crop (Shoja et al., 2018). The Zn-toxicity has a severe impact on photosynthesis because of its ability to replace magnesium ions from the center of the chlorophyll molecule, thus impairing chlorophyll structure and on the other hand zinc regulates the movement of stomata and upon an increase in zinc concentration reduces its conductivity thus accelerates the intake of CO2 (Farhat et al., 2016; Acosta-Motos et al., 2017). A high concentration of cobalt also inhibits several metabolic activities and the growth of a plant. During prophase, the excess concentration of cobalt was reported to result in chromosome despiralization and impairs the structural integrity of the plastids (Aziz et al., 2011; Moyroud, 2011). Similarly, lead (Pb) plays a key role in the biosynthesis of chlorophyll and inhibits the activity of CAT enzymes attributing to the increased production of ROS species, respectively (Sharma et al., 2012). Additionally, lead also inhibits key enzymes involved in the Calvin cycle attributing to poor photosynthesis (Yang et al., 2017).

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Sulfur plays an important role in combatting heavy metal stress because of the complexation and accumulation of toxic heavy metals into the vacuoles pivotally mediated by several sulfur containing compounds such as metallothioneins (MTs), Cys, GSH, and PCs; thus, improving stress tolerance (Wuana & Okieimen, 2011; Anjum et al., 2015). In addition, sulfate analogs gain their entry through sulfate transporters. GSH, a sulfur-based thiol usually presents in cytosol, mitochondria, endoplasmic reticulum, chloroplast, and vacuole of a plant cell (Finnegan & Chen, 2012). During oxidative stress induced by heavy metals, the GSH plays a pivotal role in interfering with the hydrogen peroxide (H2O2) degradation and checks the redox signaling pathway upon oxidation of GSH to GR (Dias et al., 2013). Thus, GSH acts as an antioxidant limiting the oxidative stress induced by heavy metals. However, in the presence of a glutathione-S-transferase enzyme, GSH forms certain conjugates and is subsequently absorbed by the vacuole of the cell in turn, improves the tolerance to heavy metal toxicity (Adwas et al., 2019; Hossain et al., 2006). Under heavy metal stress conditions, GSH could act as a precursor and promote the production of PCs in the presence of phytochelatin synthase (PCS) (Yadav, 2010). PCs are oligopeptides dominated with Cys characterized as the best heavy metal chelator, thereby imparting tolerance to various heavy metals, especially cadmium (Tennstedt et al., 2009). All these metals are involved either directly or indirectly in the metabolism of the plants till they reach their maximum threshold and when the threshold limit of these metals exceeds, leading to unusual binding to various functional groups, ultimately results in protein disruption (Dubey et al., 2018). Chelated and immobile metals are comparatively less toxic than free ions and PCs being metal-binding peptides play a key role in chelating various free metal ions rendering them inactive to express toxicity (Dipu et al., 2012). This heavy metal tolerance helps the plants to yield up to their potential over contaminated soils and further helps in ameliorating the soils seriously contaminated with toxic heavy metals (Farid et al., 2015). 12.8 FUTURE SCOPE OF RESEARCH The above paragraphs clearly mentioned that sulfur plays many pivotal roles in improving abiotic stress tolerance. Based on the available literature and studies, the below-mentioned future lines of work can be suggested further: • Nutrients interact with each other. The result of such interaction can either be positive or negative. The interaction of other nutrients with

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• •

• •

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sulfur may change the activity of the nutrient. The role or effect of these interactions in altering plant stress tolerance must be studied. The biochemical and molecular basis of stress tolerance in response to the sulfur application need to be investigated further. Understanding of these mechanisms will help in improving the crop performance through different breeding approaches for stress-resilient crops. Study may be conducted on sulfur acquiring efficiency of plants and its correlation with stress tolerance traits for the development of a stress-tolerant variety of crops. The specific role of sulfur in improving stress tolerance at the phenological level needs to be investigated further. The phenological changes in response to sulfur application need to be quantified for a better understanding of its role in environmental stress alleviation. The response of sulfur to multiple stress tolerance or a combination of stresses tolerance may also be studied. A comprehensive study on 4Rs (right source, right time, right dose and right place) of sulfur application for different crops and different agroclimatic conditions may be carried out to ensure proper sulfur nutrition for different crops.

12.9 CONCLUSION Sulfur, being an essential nutrient, is indispensable for the growth and development of plants. However, intensive agricultural activity, lower addition of organic fertilizer, the low external sulfur application increases the risk of sulfur deficiency in agricultural soil. Soil deficient in sulfur may adversely affect crop productivity in those regions. In addition to its well-known functions or involvement in activities such as amino acid synthesis, oil synthesis, electron transport mechanism, protein synthesis, enzymatic activity, etc., it also plays a crucial role in multiple abiotic stress tolerance such as salinity stress, DS, heavy metal stress and light stress. Sulfur imparts stress tolerance through different mechanisms such as enzymatic action and complexation, production of PCs, etc. Proper sulfur nutrition to crops can thus help in improving stress tolerance in crops, while the deficiency of the same may make the plant more vulnerable to these stresses. Hence, care must be taken to ensure proper sulfur nutrition of crops by maintaining soil sulfur level at an optimum level by exogenous application of S from different sources of plant nutrients, especially when the soil is deficient of sulfur.

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KEYWORDS • • • • • •

abiotic stresses glutathione physiological mechanisms single superphosphate sulfur superoxide dismutase

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Seiler, C., Harshavardhan, V. T., Rajesh, K., Reddy, P. S., Strickert, M., Rolletschek, H., Scholz, U., et al., (2011). ABA biosynthesis and degradation contributing to ABA Homeostasis during barley seed development under control and terminal drought-stress conditions. J. Exp. Bot., 62(8), 2615–2632. Sezgin, A., Altuntaş, C., Demiralay, M., Cinemre, S., & Terzi, R., (2019). Exogenous alpha lipoic acid can stimulate photosystem II activity and the gene expressions of carbon fixation and chlorophyll metabolism enzymes in maize seedlings under drought. J. Plant Physiol., 232, 65–73. Sharma, P., Jha, A. B., Dubey, R. S., & Pessarakli, M., (2012). Reactive oxygen species, oxidative damage and antioxidative defense mechanism in plants under stressful conditions. J. Bot., 2012, 26. Sheldon, A. R., Dalal, R. C., Kirchhof, G., Kopittke, P. M., & Menzies, N. W., (2017). The effect of salinity on plant-available water. Plant. Soil, 418(1), 477–491. Shoja, T., Majidian, M., & Rabiee, M., (2018). Effects of zinc, boron and sulfur on grain yield, activity of some antioxidant enzymes and fatty acid composition of rapeseed (Brassica napus L.). Acta Agric Slovenica., 111, 73–84. Shrivastava, P., & Kumar, R., (2015). Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J. Biol. Sci., 22, 123–131. Soundararajan, P., & Kim, J. S., (2018). Anti-carcinogenic glucosinolates in cruciferous vegetables and their antagonistic effects on prevention of cancers. Mol., 23, 2983. Speiser, A., Haberland, S., Watanabe, M., Wirtz, M., Dietz, K. J., Saito, K., & Hell, R., (2015). The significance of cysteine synthesis for acclimation to high light conditions. Front. Plant Sci., 5, 776. Staneloni, R. J., Rodriguez-Batiller, M. J., & Casal, J. J., (2008). Abscisic acid, high-light, and oxidative stress down-regulate a photosynthetic gene via a promoter motif not involved in phytochrome-mediated transcriptional regulation. Mol. Plant., 1, 75–83. Su, Y., Liu, J., Lu, Z., Wang, X., Zhang, Z., & Shi, G., (2014). Effects of iron deficiency on subcellular distribution and chemical forms of cadmium in peanut roots in relation to its translocation. Environ. Exp. Bot., 97, 40–48. Sun, X., Hu, C., Tan, Q., Liu, J., & Liu, H., (2009). Effects of molybdenum on expression of cold-responsive genes in abscisic acid (ABA)-dependent and ABA-independent pathways in winter wheat under low-temperature stress. Ann. Bot., 104(2), 345–356. Tan, Q., Zhang, L., Grant, J., Cooper, P., & Tegeder, M., (2010). Increased phloem transport of S-methyl methionine positively affects sulfur and nitrogen metabolism and seed development in pea plants. Plant Physiol., 154(4), 1886–1896. Tennstedt, P., Peisker, D., Bottcher, C., Trampczynska, A., & Clemens, S., (2009). Phytochelatin synthesis is essential for the detoxification of excess zinc and contributes significantly to the accumulation of zinc. Plant Physiol., 149(2), 938–948. Terzi, R., Saruhan, G. N., Guven, F. G., & Kadioglu, A., (2018). Alpha lipoic acid treatment induces the antioxidant system and ameliorates lipid peroxidation in maize seedlings under osmotic stress. Archiv. Biol. Sci., 70, 503–511. Ulhassan, Z., Huang, Q., Gill, R. A., Ali, S., Mwamba, T. M., Ali, B., Hina, F., & Zhou, W., (2019). Protective mechanisms of melatonin against selenium toxicity in Brassica napus: Insights into physiological traits, thiol biosynthesis and antioxidant machinery. BMC Plant Biol., 19(1), 1–6.

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Van, D. B. J., Heider, D., Martin, S. R., Pastore, A., & Mueller, J. W., (2012). 3′-phosphoadenosine 5′-phosphosulfate (PAPS) synthases, naturally fragile enzymes specifically stabilized by nucleotide binding. J. Biol. Chem., 287(21), 17645–17655. Vanacker, H., Carver, T. L. W., & Foyer, C., (2000). Early H2O2 accumulation in mesophyll cells leads to induction of glutathione during the hypersensitive response in the barleypowdery mildew interaction. Plant Physiol., 123, 1289–1300. Vishwakarma, K., Upadhyay, N., Kumar, N., Yadav, G., Singh, J., Mishra, R. K., Kumar, V., et al., (2017). Abscisic acid signaling and abiotic stress tolerance in plants: A review on current knowledge and future prospects. Front. Plant Sci., 8, 161. Wadanambi, R. T., Wandana, L. S., Chathumini, K. K., Dassanayake, N. P., Preethika, D. D., & Arachchige, U. S., (2020). The effects of industrialization on climate change. J. Res. Technol. Eng., 1, 86–94. Wang, B., Liu, C., Zhang, D., He, C., Zhang, J., & Li, Z., (2019). Effects of maize organspecific drought stress response on yields from transcriptome analysis. BMC Plant Biol., 19(1), 1–9. Wang, Q. L., Chen, J. H., He, N. Y., & Guo, F. Q., (2018). Metabolic reprogramming in chloroplasts under heat stress in plants. Int. J. Mol. Sci., 19, 849. Weigel, M., Varotto, C., Pesaresi, P., Finazzi, G., Rappaport, F., Salamini, F., & Leister, D., (2003). Plastocyanin is indispensable for photosynthetic electron flow in Arabidopsis thaliana. J. Biol. Chem., 278(33), 31286–31289. Wirtz, M., Beard, K. F., Lee, C. P., Boltz, A., Schwarzländer, M., Fuchs, C., Meyer, A. J., et al., (2012). Mitochondrial cysteine synthase complex regulates O-acetylserine biosynthesis in plants. J. Biol. Chem., 287(33), 27941–27947. Wisedpanichkij, R., Chaicharoenkul, W., Mahamad, P., Prompradit, P., & Na-Bangchang, K., (2010). Polymorphisms of the oxidant enzymes glutathione S–transferase and glutathione reductase and their association with resistance of plasmodium falciparum isolates to antimalarial drugs. Asian Pacific J. Tropic. Med., 3(9), 673–677. Wuana, R. A., & Okieimen, F. E., (2011). Heavy metals in contaminated soils: A review of sources, chemistry, risks and best available strategies for remediation. Int. Schol. Res., 20. Xie, X. J., Shen, S. H., Li, Y. X., Zhao, X. Y., Li, B. B., & Xu, D. F., (2011). Effect of photosynthetic characteristic and dry matter accumulation of rice under high temperature at heading stage. Afr. J. Agric. Res., 6(7), 1931–1940. Yadav, S. K., (2010). Heavy metals toxicity in plants: An overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. South Afr. J. Bot., 76, 167–179. Yang, B., Liu, J., Ma, X., Guo, B., Liu, B., Wu, T., Jiang, Y., & Chen, F., (2017). Genetic engineering of the Calvin cycle toward enhanced photosynthetic CO2 fixation in microalgae. Biotechnol. Biofuels., 10(1), 1–3. Yang, X., Yao, H., Chen, Y., Sun, L., Li, Y., Ma, X., Duan, S., et al., (2015). Inhibition of glutathione production induces macrophage CD36 expression and enhances cellularoxidized low density lipoprotein (oxLDL) uptake. J. Biol. Chem., 290(36), 21788–21799. Yin, J., Ren, W., Yang, G., Duan, J., Huang, X., Fang, R., Li, C., et al., (2016). L‐cysteine metabolism and its nutritional implications. Mol. Nut. Food Res., 60(1), 134–146. Zervoudakis, G., Salahas, G., Kaspiris, G., & Konstantopoulou, E., (2012). Influence of light intensity on growth and physiological characteristics of common sage (Salvia officinalis L.). Brazil. Arch. Biol. Technol., 55, 89–95. Zhang, J., Zhou, M., Ge, Z., Shen, J., Zhou, C., Gotor, C., Romero, L. C., et al., (2020). ABA-triggered guard cell L-cysteine desulfhydrase function and in-situ hydrogen sulfide

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production contributes to HY1-modulated stomatal closure. Plant. Cell. Environ., 43, 624–636. Zhang, L. J., Wang, K. F., Jing, Y. P., Zhuang, H. M., & Wu, G., (2015). Identification of heat shock protein genes hsp70s and hsc70 and their associated mRNA expression under heat stress in insecticide-resistant and susceptible diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Eur. J Entomol., 112(2), 215. Zhang, L., Yan, C., Guo, Q., Zhang, J., & Ruiz-Menjivar, J., (2018). The impact of agricultural chemical inputs on environment: Global evidence from informetrics analysis and visualization. Int. J. Low-Carbon Technol., 13(4), 338–352. Zhang, M., Smith, J. A. C., Harberd, N. P., & Jiang, C., (2016). The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses. Plant Mol. Biol., 91, 651–659. Zhang, Y. P., Jia, F. F., Zhang, X. M., Qiao, Y. X., Shi, K., Zhou, Y. H., & Yu, J. Q., (2012). Temperature effects on the reactive oxygen species formation and antioxidant defense in roots of two cucurbit species with contrasting root zone temperature optima. Acta. Physiol. Plant, 34(2), 713–720.

CHAPTER 13

Role of Chloride and Organic Acid Anions in Environmental Stress Tolerance TITIR GUHA, PREETI VERMA, and RITA KUNDU*

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

Corresponding author. E-mail: [email protected]

ABSTRACT Plants being sessile, maintain an active interaction with their environment, have to face several kinds of stresses in their lifetime, and evolve the tolerance mechanism to survive; hence the enhancement of environmental stress tolerance has been a primary focus for researchers to maintain crop performances and productivity. According to recent studies, several exogenous treatments of plants with chemical compounds can elicit strong stress defense responses. In this chapter, the role of two such chemical compounds, i.e., chloride ions and organic acids in enhancing stress tolerance in plants have been elucidated. Both chloride and organic acids can play paramount roles in increasing stress defense responses. Although previously chloride was considered to be toxic, it is now regarded as a beneficial macronutrient involved in increasing plant growth, photosynthetic efficiency, water, and nitrogen utilization efficiency. Chloride ions can also orchestrate well-concerted defense responses in plants by means of a series of molecular and biochemical pathways contributing to draft and salinity tolerance. Similarly, amendments of organic acids in the soil can be another sustainable tool to protect plants from heavy metals. Organic acid metabolism is fundamental in maintaining several biochemical reactions involved in energy production, amino acid synthesis, in modulating plant’s adaptation towards the environment. Chelating heavy metals with carboxyl Biology and Biotechnology of Environmental Stress Tolerance in Plants: Trace Elements in Environmental Stress Tolerance, Volume 2. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

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groups of organic acids can reduce their phyto-availability and help in heavy metal stress tolerance. Since, these chemicals are widely available, ecofriendly, and cost-effective tools for increasing stress tolerance, their roles in the elicitation of plant defense responses must be explored further to open up new perspectives about sustainable agriculture. 13.1 INTRODUCTION Presently, the global agricultural system is plagued by several challenges, and also with increasing population growth; the food demand is also escalating worldwide. According to United Nations (2017), the total world population is expected to reach 9.8 billion from 7.8 billion by 2050. To meet the food demand, agricultural production needs to be expanded by 70%. Since natural resources like water, land area, and fertile soil are constant limiting factors in increasing agricultural productivity, proper management of agricultural resources is absolutely crucial. Also, with the abrupt changes in climate, development in agriculture is in further distressful condition (Raza et al., 2019). Draught and heat stress are the direct impacts of rapid climate change and global warming are often associated with the decline in crop yield (Barnabás et al., 2008). The overuse of agrochemicals like pesticides, herbicides, and chemical fertilizers by farmers is another major concern. Although the application of such agrochemicals can provide immediate benefits like enhanced growth and yield, in the long run it results long-term environmental hazards (Zhang et al., 2018a). Indiscriminate uses of agrochemicals are reportedly detrimental to overall soil health and soil microbiota (Ikoyi et al., 2018). Thus, to ensure the elimination of hunger and poverty, sustainable development of agriculture is a universal goal in the 21st century. A variety of physical and chemical factors like, low or high temperature, water scarcity or flood, saline soils, heavy metals or nutrient unavailability are hostile for proper plant growth. These stresses are collectively known to be abiotic stresses which are quite common yield-limiting factors for crops and about 90% of arable lands are under abiotic stress conditions (Dos Reis et al., 2012). According to IPCC-2014, the earth’s average temperature is predicted to rise by 2 to 4.5°C in the 21st century (Pachauri et al., 2014). Zhao et al. (2017) analyzed the impacts of climate changes on yields of major crops and found a significant decline in yields of wheat, rice, soybean, and maize by 6%, 3.2%, 3.1%, and 7.4%, respectively. Under drought and high-temperature conditions, the activities of Rubisco get disrupted which is the direct cause of the decline in cereal yields (Griffin et al., 2004). Salinity

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stress is another pressing concern. In the recent two decades, saline soil area has increased by 37%. Plant growth, biomass, and yield are negatively associated with the intensity of soil stress (Stavridou et al., 2017). Since plants are directly dependent on soil for nutrient acquisition, their growth and development are strongly associated with soil health and quality. Enhanced contamination of arable lands with heavy metal is very distressful for plant survival and productivity (Proshad et al., 2018). Improper irrigation systems, excessive use of chemical fertilizers, and other synthetic growth enhancers are a huge threat in this regard. Some heavy metals like copper, aluminum (Al), nickel, zinc, cobalt, iron, and selenium are considered to be essential for plant growth but when such elements are present in excess, they can significantly impair crop performances (Narendrula-Kotha et al., 2019). In addition to this, non-essential elements like arsenic, chromium, lead, mercury, and cadmium can be the cause of reduced crop yield even when they are present in trace amounts (Khalid et al., 2018). Typically, industrial and sewage wastes, fuel burnings, urban run-off, garbage disposals in river and water channels are the chief causes of heavy metal contaminations in arable soils and such contaminations are harmful for crop production and human health also (da Rosa Couto et al., 2018; Waqas et al., 2019). In the course of evolution, plants have developed several efficient mechanisms which can help them to combat several environmental stress situations. Under growth-limiting situations, plants activate their stress tolerance mechanisms. Plant stress tolerance mechanism comprises a wide range of signaling which induces several changes at molecular, metabolomic, anatomical, and structural levels (Atkinson & Urwin, 2012). After sensing any stress condition, some specific stress-responsive genes get induced or repressed, which can be the first trigger for the regulation of the elaborate stress gene networks which are directly involved in imparting stress tolerance. Expressions of signaling molecules like transcription factors (TFs), protein phosphatases, and kinases also play an integral part in imparting stress tolerance by regulating signal transduction pathways. As the first line of defense against environmental stresses, different osmoprotectants, antioxidant enzymes, transporters, proteases, and chaperones usually get triggered (Délano-Frier et al., 2011; Grativol et al., 2012; Shinozaki & YamaguchiShinozaki, 2007; Krasensky & Jonak, 2012; Wang et al., 2009). These early responses are very helpful in the alleviation of the damages induced by plant stress and allow proper plant growth (Peleg et al., 2011). A well-developed stress defense system is directly associated with crop yield enhancement. Plant yield enhancement can be achieved despite the

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prevalence of abiotic stress if plant stress tolerance can be boosted (Singh et al., 2018). High throughput knowledge about plant stress defense responses can be the major contributing factor in developing high stress-tolerant crop varieties which is a major aim of scientists in the context of ensuring present and future food security. Metabolomic profiling of different crop plants under stress conditions has revealed that organic acids are one of the most important metabolites having significant effects on the plant during stress. Organic acids are major metabolites involved in the Krebs cycle, C4 cycle, CAM (crassulacean acid metabolism) cycle, and glyoxylate cycle (Lopez-Bucio et al., 2000; Igamberdiev & Eprintsev, 2016). Organic acids are stored in cytosols and vacuoles to maintain ionic balances (Osmolovskaya et al., 2007). They often act as precursors of amino-acid synthesis and takes part in energy generation in plant’s cell which is vital during stress defense (Lopez-Bucio et al., 2000). Organic acids also play significant roles in metal detoxification by sequestration of metals via the carboxyl groups (Anjum et al., 2015). Also, chloride anion is one of the most predominant halogens present in the soil. There has been a recent paradigm shift in understanding the role of chloride ions which was mostly considered to be a toxic ion that gets absorbed by the plants along with nitrate transporters (NRT) but very recently chloride ions are considered as a beneficial macronutrient (Colmenero-Flores et al., 2019). Chloride as a vital plant nutrient has significant roles in photosynthesis, enhancement of plant growth, biomass, etc. (Franco-Navarro et al., 2016). This chapter mainly deals with the understanding of the roles of organic acids and chloride anions in the context of imparting plant stress tolerance. The participation of organic acids in stress mitigation needs a thorough understanding. Since they are essential metabolites for plants and are widely available in nature, proper exploitation of their benefits can be helpful to establish sustainable crop development. Also, the positive roles of chloride ions have recently come into the focus of plant research. Since chlorides are available and highly abundant in soil, careful exploitation of this anion can show us new prospects in boosting plant stress tolerance. 13.2 ORIGIN OF ORGANIC ACIDS AND CHLORIDES IN SOIL 13.2.1 CHLORIDES Chloride (Cl–), is the anion of Group VII halogen element chlorine, with atomic number 17 and atomic weight 35.453. Chloride was considered to be only toxic for plants and its beneficial roles were overlooked for a long time.

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Recent reports by Franco-Navarro et al. (2016); Raven (2017) highlight several positive roles of chlorides. Chlorides are readily available in the soil as a result of depositions from rainfall, upon application of fertilizers mainly KCl, irrigation water, air pollution, dust, and sea spray. Proximity to salt waters can greatly influence the amount of chlorine in rain (White & Broadley, 2001). Irrigation with saline waters can easily deposit up to 1,000 kg Cl– per hectare soil annually (Xu et al., 1999). Chlorine also gets deposited in the soil from anthropogenic sources such as soil chlorination, disposal of domestic wastes, dechlorination of organic compounds, etc. Industrial sources are also remarkably responsible for chloride contamination of soil. Coal burning, waste combustions easily contaminate soil with excess chloride (Gelfius et al., 2019). Since exchange sites on the silicate layers of soil are negatively charged, chlorine gets repelled from the possible binding sites and thus fails to form complexes. Thus, chlorides are highly mobile not being strongly adsorbed to soil compared to other soil anions like sulfates and nitrates (White & Broadley, 2001). 13.2.2 ORGANIC ACIDS The origin, roles, and dynamics of soil organic acids need further exploration in the context of crop improvements. Organic acids can be released from plant roots, due to microbial activities and organic decompositions, and often the status of soil organic acid is the index of biotic or abiotic stress imposed on biological systems. Soil organic acids have notable contributions in heavy metal remediation, nutrient mobilization, and mineral weathering (Adeleke et al., 2017). Soil organic acids are weak acids that comprise a significant water-soluble fraction of soil. They are classified into two groups based on molecular weights (Perminova et al., 2003): 1. High Molecular Weight Organic Acids (HMWOAs): These are insoluble with molecular weights ranging from a few hundred to million Daltons with more than 3 carboxylic acid groups. For example, humic acid and fulvic acids. 2. Low Molecular Weight Organic Acids (LMWOAs): These have higher solubility with molecular weights ranging from 46 Daltons to a few 100 Daltons and 1–3 carboxylic acid groups. For example, citric, oxalic, malic, succinic, malonic, and maleic acids, etc.

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These organic acids are known to be abundant constituents of soil and play vital roles in the maintenance of soil ecology, phyto-availability of nutrients, and productivity. The distribution and concentrations of soil organic acids vary hugely depending on several edaphic factors. LMWOAs like oxalic acid, citric acid, malic acid, acetic acid, tartaric acid, and formic acid are found in abundance and play the dominant role in soil productivity. The concentrations of the LMWOAs like malic, oxalic, tartaric, malonic, succinic, and citric acids (di/tri carboxylic acids) vary typically between the range of 0 to 50 μM and for the monocarboxylic acids like formic, propionic valeric, acetic, butyric, and lactic acids, the soil concentration ranges between 0 mM and 1 mM (Strobel, 2001). Several studies also revealed that the concentrations of organic acids vary depending on the type of crops grown in the soil. High levels of organic acids can be found under plant litter (Jonnes et al., 2003). Bacteria, fungi, and lichen also produce significant proportions of organic acids. Veneklaas et al. (2003) reported that organic acid concentrations around the plant root and in soil solution amounted to 58 mM and 84 mM, respectively. Organic acid concentrations as high as 330 mM were found in soil growing Solanum nigrum and on the contrary, in sandy-clay soils with lupin plantation had organic acid concentration ranging from 43–140 mM (Mimmo et al., 2008). It is reported that soil organic acid profile is linked to plant root exudates, leaching of leaf litter, microbes, and decomposition of organic matter (Adeke et al., 2017). Plant root exudates generally comprise different complex compounds like sugar, amino acids, phenolics, flavonoids, purines, nucleosides, vitamins, proteins, and organic acids (Ryan et al., 2001). Among these wide arrays of chemical compounds, organic acids are released in high concentrations. The levels of exudation of organic acids are highly variable and mostly governed by plant developmental stages, biotic, and abiotic stress (like drought, heavy metal stress, nutrient unavailability, damages to root morphology) or edaphic factors (like temperature, moisture levels, pH levels, presence of insoluble P) (Nwoke et al., 2008; Badri & Vivanco, 2009). Al tolerant cultivars of Zea mays and Fagopyrum esculentum are reported to release citric acid and oxalic acid, respectively (Pellet et al., 1995; Ma et al., 1997). According to Arcand & Schneider (2006), there is a significant link between soil acidification and the release of organic acids. The release of organic acids occurs mainly during environmental stress like P deficiency or mental stress, and the amount of organic acid exudated from roots is strongly associated with soil physicochemical status, root metabolism, and

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it also varies based on plant species. According to the findings of Dinkelaker et al. (1989); and Hinsinger et al. (2003), maize can release almost 0.3% of organic acid and on the contrary, lupins release both citrate and H+ in large amount (11%–23% of total dry weight) leading to a significant lowering of soil pH, from 7.5 to 4.8. Similarly, in a pot experiment, soil pH was found to decline up to 4.1 upon release of organic acid by Brassica napus (Hoffland et al., 1989) Alfafa or Medicago sativa are found to release only 0.3% of citric acid (Lipton et al., 1987). Mangrove plants can also release organic acid as an adaptive response during cadmium toxicity (Haoliang et al., 2007). Pine seedlings also release organic acids in the soil in response to nutrient deficiency (Adeleke et al., 2012). 13.3 FLUXES OF ORGANIC ACIDS AND CHLORIDES WITHIN PLANTS 13.3.1 CHLORINE Since chloride is highly mobile and also has various physiological roles in plants, hence are actively taken up by roots. However, during excess salinity, the uptake and translocation of chlorides are regulated. The different patterns of Cl– uptake under low Cl– and high Cl– concentrations of soil are depicted in Figure 13.1. 13.3.1.1 CHLORIDE UPTAKE IN NON-STRESS CONDITION Chloride generally follows a symplastic pathway after being taken from soil (Brumos et al., 2010). The movement of chloride up to the root xylem also depends on the concentration gradient between root cytosol and soil solution. According to Geilfus (2019), chlorine levels in the soil are often significantly lower as compared to that of root cells. Hence the uptake of chlorine must be an active process. Due to higher concentrations of chloride in the soil and negative membrane potential, chloride uptake is energetically coupled to the symport (influx) of H+ (Felle, 1994). ZmNPF6.4 has been identified by Wen et al. (2017), to be acting as Cl– selective proton-coupled symporter channel, localized in the plasma membrane. Thus, ZmNPF6.4 aids the active uptake of chloride in maize, which then follows a symplastic route radially across the root, along the concentration gradient, and reaches the xylem parenchyma. Other NRT (i.e., AtNPF2.4, AtNPF7.3) further facilitate the loading of chlorine in root xylem (Li et al., 2016, 2017a). S-type anion channel proteins

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FIGURE 13.1 Uptake of Cl– from soil having low concentration (active uptake by proton symporters like ZmNPF6.4) and excess concentrations of Cl– (passive uptake by anion channels) followed by radial movements across roots following symplastic routes along concentration gradient and eventual xylem loading occurs with the help of different transporters (like, AtNPF2.4, SLAH1, etc.). Translocation of Cl– leads to its accumulation in the shoot. In Cl-stressed condition plant sequester excess Cl– in vacuoles with aid of transporters like (CLC, ALMTs) and other thus protects plants from salinity stress.

SLAH1 and SLAH3 are also expressed in pericycle cells and are associated with translocation of chloride in root xylem (Cubero-Font et al., 2016). 13.3.1.2 CHLORIDE UPTAKE UNDER SALINITY STRESS The mechanism of chloride uptake shifts dramatically during excess soil salinity. Under salt stress, the concentrations of Cl– in the xylem increase significantly and it eventually gets translocated up to shoot causing leaf injury and reducing plant photosynthetic efficiency (Li et al., 2017b; Geilfus, 2018). Under extremely high soil chloride levels, the dramatic increase in root chloride concentration occurs because the entry of Cl– is aided by anion

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channels, and the passive influx of chlorides has been reported (Hedrich, 1994; Barbier-Brygoo et al., 2000). Glycophytes can tolerate the extreme salinity stress by restricting the transfer of chloride in root xylem by downregulation of transporters like AtNPF7.3 which mediates xylem loading (Chen et al., 2012). The stress hormone, abscisic acid (ABA) also mediates down-regulation of NPF2.4 and SLAH1 (Li et al., 2016; Qiu et al., 2016) and thus restricts the transfer of chlorides to shoot. Additionally, some root cortical cell localized transporters (NPF2.5, NRT1.5) mediate the efflux of Cl– from the root cells into soil solution becomes functional in response to salinity (Li et al., 2017a; Henderson et al., 2014). 13.3.1.3 CHLORIDE SEQUESTRATION IN THE SHOOT Upon accumulation of excess chloride in the shoot, chlorides are restricted from photosynthetic sites and dividing cells through inter and intracellular compartmentalization (Teakle & Tyerman, 2010). Sequestration of chlorides in leaf vacuoles has been reported to be an adaptive mechanism during salinity stress (Storey et al., 2003). Wege et al. (2017), reported that glycophytes can store up to 40 mM chloride in vacuoles. CLC family anion transporters in Glycine max, (GmCLC) are Cl–/H+ antiports located in tonoplasts that can sequester chloride in vacuoles (Nguyen et al., 2016). CLC transporters have also been identified in Arabidopsis. AtCLCa has been reported to be involved in vacuolar sequestration of chlorides during salinity stress (Lorenzen et al., 2004). AtCLCc is also localized in tonoplast membranes and helps in the accumulation of chlorides in vacuoles of guard cells during stomatal opening and also helps in inducing salt tolerance by maintaining the chloride homeostasis (Jossier et al., 2010). Aluminum activated malate transporters (ALMTs) located in the tonoplast of leaf mesophyll, vasculature, endodermis, pericycle, guard cells, and root vasculatures are also responsible for chloride sequestration in vacuoles during salinity stress and maintenance of cytosolic ion homeostasis (Barbier-Brygoo et al., 2011; Baetz et al., 2016). 13.3.2 ORGANIC ACID Organic acids represent the group of compounds having carboxylic groups which are negatively charged at neutral pH and to a lesser extent at acidic pH. Thus, the functions can change based on solution pH. Excretion of organic acids can result in proton release leading to acidification of soil, apoplast, and vacuole.

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13.3.2.1 ORGANIC ACIDS IN TCA CYCLE Organic acids are synthesized by the incomplete oxidation of photosynthetic products and represent the stored pools of fixed carbon accumulated due to different transient times of conversion of carbon compounds in metabolic pathways. During active photosynthesis, the redox level in the cell increases, and the tricarboxylic acid (TCA) cycle in mitochondria is transformed to a partial cycle which supplies citrate for 2-oxoglutarate and glutamate synthesis (via citrate valve), and malate is accumulated and participates in maintaining redox balance (via malate valve). Thus, malate and citrate are the most accumulated acids in plants. These carbon skeletons also act as intermediates for amino acid biosynthesis. The partitioning of the organic acid metabolites between cytoplasm and mitochondria is carried out with the help of mitochondrial carriers. The transport processes are mainly driven by electrochemical gradient, proton motive force across the inner mitochondrial membrane. In plants, the mitochondrial carriers associated with TCA cycle operation are mainly of three types as mentioned below: 1. Dicarboxylate Carriers (DICs): These are members of the mitochondrial carrier family (MCF) and can facilitate the transport of dicarboxylates like malate, and related compounds as well as phosphate, sulfate, and thiosulfate. 2. Dicarboxylate/Tricarboxylate Carriers (DTC): These are also a class of mitochondrial carrier proteins that participate in the transport of dicarboxylates such as malate and 2-oxoglutarate and tri-carboxylates, such as citrate. 3. Succinate/Fumarate Carrier (SFC): These proteins are involved in the exchange of succinate and fumarate.

13.3.2.2 MECHANISMS DRIVING THE ROOT EXUDATION OF ORGANIC ACIDS The root tip is the plant part that explores a new soil environment and plays a pivotal role in regulating root responses to environmental stimuli. According to Sasse et al. (2018); Doan et al. (2017), the majority of root exudation is localized near root rip and root exudation determines the interaction of plants with the soil environment.

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Root exudation involves driving the C transport to roots and followed by its exudation from roots to the soil. From the source organs, the long-distance C transport occurs via phloem according to Munch’s pressure-driven phloem flow (Münch, 1930). The transport is driven based on the difference in turgor between the sink and source organs (De Schepper et al., 2013). The unloading of the metabolites from the phloem to the growing root tips is vital for root exudation. Ross-Elliott et al. (2017) reported the occurrence of phloem unloading through plasmodesmata. Low-molecular-weight proteins and solutes like organic acids are transported into the phloem-pole pericycle, by means of specialized “funnel plasmodesmata.” Upon unloading, the organic acids move out of the phloem-pole pericycle through the symplastic pathway and organic acids pass through at least one plasma membrane barrier before their soil exudation. The process is briefly summarized and depicted in Figure 13.2. Recent discovery highlights that efflux of the organic metabolites occurs through specific efflux carriers and channels, and the up/downregulation of their gene expression or post-translational modifications, plays a significant role in regulations of root exudations (Badri et al., 2008). Ryan and coworkers (2011) reported that ALMT and multidrug and toxic compound extrusion (MATE) gene families encode membrane proteins that aid the efflux of organic anion across plasma membrane under stress conditions. 13.4 PHYSIOLOGICAL ROLES OF CHLORIDES AND ORGANIC ACIDS AND THEIR ROLE IN STRESS MITIGATION Both chloride and organic acids are found to be involved in numerous physiological and metabolic functions in plants and thus are also involved directly in stress mitigation or development of stress tolerance in plants. Some of the roles are briefly summarized in Figure 13.3. Cl- are recently defined as beneficial and it represents the dominant inorganic anion in the vacuole, determining central functions in cell osmoregulatory and turgor-driven processes (Colmenero-Flores et al., 2019). Since Cl– is accumulated at significant levels, and helps in improving plant performances, Cl– has gained a status of macronutrient. Tobacco plants with high Cl– levels display higher water use efficiency (WUE), nitrogen utilization efficiency, and carbon/energy utilization and production. All of these lead to enhanced plant growth. Since Cl– helps in improving WUE, it can play a pivotal role in increasing the ability of plants to tolerate water deficit. Several reports

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FIGURE 13.2 Representation of the events which leading to root exudation of organic acids following the phloem unloading. After phloem unloading radial movement of organic acids occurs via both symplastic and apoplastic pathways and influx carriers help to cross the Casparian strip barrier. The ultimate exudation process occurs with the help of efflux channels like ALMT and MATE.

also suggest that Cl– plays an important role in increasing NUE, which can be correlated with the increase of plant biomass. External supplementations of Cl– are also reported to have positive effects on plant biomass since they can help to boost photosynthetic performances also. Cl– can regulate thylakoid swelling, improve photosynthetic electron transport, and also activates several photoprotective mechanisms. Chloride also promotes cell elongation as a consequence of its osmoregulatory and turgor-generating ability. Hence auxin triggers the influx of Cl– into plant cells and ABA has the antagonistic effect. Thus Cl– fertilization can indeed help to improve crop performance, yield, and stress resilience if utilized properly. Organic acids directly participate in the central metabolic pathways of plants such as the TCA cycle, C3, C4, CAM cycle, and glyoxylate cycle.

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FIGURE 13.3 Summary of physiological roles played by chlorides and organic acid and their possible implications in enhancing biotic and abiotic stress tolerance.

Organic acids, such as malate, fumarate, lactate, and citrate, are involved in biochemical pathways mediating energy production, amino acid biosynthesis, and impart environmental stress tolerance (Igamberdiev & Eprintsev, 2016). Organic acids are involved in the phosphorous acquisition, stomatal

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function, Al tolerance, and temporary carbon storage, interchange of reductive power among subcellular compartments, pH regulation, and the response to biotic and abiotic stresses (Meyer et al., 2010a). The organic acid and chloride, both being anions are responsible for some of the common physiological functions like maintenance of charge balance, osmoregulation, turgor, stomata movement, proper nutrient acquisitions, etc. Some of the key roles are discussed in detail in subsections. 13.4.1 CONTROL OF CHARGE-BALANCE, OSMOREGULATION, TURGOR Different anions like chloride, nitrate, sulfate, and malate are involved in the maintenance of charge balance, osmoregulation, and cellular turgidity, and their concentrations in the cell are regulated by the activity of different anion channels (Figure 13.4). Chloride being highly mobile and remains unutilized in anabolic metabolism and thus serves as the most preferred anion as compared to others (Colmenero-Flores et al., 2019). It can accumulate in significantly high proportions, as compared to nitrates (4-fold), sulfates (3 folds), and phosphates (3 folds) and thus generate more negative charge potential and high turgor (Franco-Navarro et al., 2016). Thus, chloride regulates the water movement and retention capacity based on the charge and osmotic balance. In general, the electric potential (Em) is negative inside due to the activity of H+-ATPase (Armstrong, 2003). In absence of chloride, the movements of cations are osmotically balanced. Hence during Cl– conductance, the equilibrium of the Em is maintained by adjusting the cell volume, and thus the Cl– conductance determines the rate and amount of water movement which has impacts on cell volume (Dmitriev et al., 2019). In plant cells, the Cl– exclusion is also achieved by its compartmentalization in vacuoles, and this is mediated by activation of proton pumping vacuolar V-type ATPases in the presence of Cl– (Sze, 1985). Thus, the chloride fluxes in vacuoles also have impacts on the maintenance of turgor and cell volume (Zonia et al., 2002). On the contrary, the activation of chloride efflux channels leads to membrane depolarization and activates the outward rectifying K+ channels leading to the release of salts and water. Thus, chloride ion flux is the main controller of cell turgor (Sanders & Bethke, 2000). These events regulate the nyctinastic, seismonastic movement of leaves and stomatal guard cells (discussed in section 4.5) (Colmenero-Flores et al., 2019).

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FIGURE 13.4 Anion channels and transporters involved in charge balance, osmoregulation, etc., through uptake of chlorides, sulfates, nitrates, and organic acids.

13.4.2 CONTROL OF CELL ELONGATION According to the report by Terry (1977), the accumulation of Cl– occurs uniformly when present in abundance. But when Cl– are available in low levels, the accumulation of chloride occurs typically at the actively growing immature leaves. This finding is the first indication of the possible involvement of Cl– in regulating cell growth and increasing or maintaining the cell division rate. Later, the roles of chloride in pollen tube elongation, elongation of the stigma of the grass, coleoptiles of grass seedlings were discovered (Colmenero-Flores et al., 2019). This was further confirmed when disruption of transporter genes involved in the vacuolar sequestration of Cl– during cellular expansions (DXT33 and DXT35 genes) stunted the root hair length and pollen tube growth. Mutations in cation-chloride cotransporter (CCC) proteins led to inhibition of cell elongation mainly in the inflorescence

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stem of Arabidopsis and root cells of rice due to changes in Cl– homeostasis (Colmenero‐Flores et al., 2007; Chen et al., 2016). 13.4.3 CONTROL OF TISSUE HYDRATION, WATER USE EFFICIENCY (WUE), AND PHOTOSYNTHESIS

Since chloride promotes high cellular osmolarity, turgor, cell volume, etc., this also leads to the enhancement of the water storage capacity of cells. FrancoNavarro et al. (2016) confirmed that Cl– nutrition can enhance the relative water content (RWC) and succulence of tobacco plants. This is also accompanied by low stomatal conductance (gs) and consequent reduction in the leaf transpiration. The Cl– induced enlargement of leaf cells leads to a reduction of stomatal density, which is the key contributor in decreasing the rate of transpiration, water loss, and increasing the water-use efficiency (WUE). It is quite interesting that although Cl– lowers stomatal conductance (gs) but increases the mesophyll conductance (gm), which is the index of CO2 diffusion from sub-stomatal cavities to the carboxylation sites in chloroplasts. This phenomenon is chiefly attributed to the increase in leaf cell size owing to chloride nutrition which reduces the stomata density, and the gm increases due to the consequent increase in the chloroplast surface area which is exposed to the intercellular air space (Franco-Navarro et al., 2016). This phenomenon of increasing the WUE along with a simultaneous increase in photosynthetic rate is challenging for C3 plants which can be achieved by Cl– nutrition. Cl– being the most abundant anion of the stroma in chloroplast has a crucial function in maintaining the performance of the cellular organelle (Neuhaus & Wagner, 2000). During light reaction protons get accumulated in the thylakoid lumen which is electrically counter-balanced due to Cl– influx via thylakoid membrane-localized Cl– channels and thus regulates the pH gradient between stroma and lumen. Thus, chloride fluxes have a major role in maintaining the electron transport during photosynthesis (Bose et al., 2017; Enz et al., 1993) and also stabilize the oxygen evolution complex of PSII (Kawakami et al., 2009). 13.4.4 CHLORIDE ENHANCES NITRATE UTILIZATION IN PLANTS Generally, chloride is mainly considered to be toxic because of its antagonistic interaction with nitrate uptake which consequently reduces the N availability and yield capacity in plants. Recent reports by Rosales et

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al. (2020), indicate that an optimum supply of chloride can benefit plant water relations, photosynthetic performances, growth potential, and at the same time it can also enhance nitrogen use efficiency (NUE). Generally, nitrate and chlorides are the two major anions utilized for maintaining osmolarity (Colmenero‐Flores et al., 2019). However, the utilization of chloride is considered to be energy cost-efficient or “cheap” mainly due to the differences in the transport mechanism of the two anions (Wege et al., 2017). The vacuole sequestration of chloride is entirely dependent on the functions of anion channels and on the contrary NO3– mainly depends on secondary active transport which requires the expenditure of ATP (Baetz et al., 2016; De Angeli et al., 2006). Recent studies by Rosales et al. (2020), in tobacco plants, showed that optimum Cl– input can significantly increase the NUE by decreasing the amount of NO3– sequestered in the vacuoles. This increases the levels of free N which can be easily used in N assimilation for the biosynthesis of organic N. Thus Cl– nutrition management can help to reduce overuse of excess N fertilizer applications in agricultural fields and pave a new way for sustainable agricultural yield enhancement. 13.4.5 CONTROL OF STOMATA MOVEMENT Stomatal function is vital for photosynthesis since they help in CO2 uptake and also cools plants by transpiration. The functions of stomata are mainly controlled by the guard cell turgidity which can be adjusted according to diurnal cycles and other environmental cues. Upon changes in osmotic pressure, the water uptake pattern by guard cells changes, and thus the stomata pore sizes are controlled (Buckley, 2005). Mobilizations of osmotically active metabolites are chiefly involved in this process. Blue/red light, low CO2 levels, and high humidity can activate membrane H+-ATPases which results in proton export (Kim et al., 2010), which causes hyperpolarization of plasma membrane leading to K+ uptake by inward rectifying K+ in channels (Kim et al., 2010). In response to the K+ uptake, anions like chlorine and nitrate ions enter the vacuoles leaving the guard cell apoplast (Guo et al., 2003). This is also accompanied by mobilization of starch, sugars to form malates which accumulate in vacuoles leading to an increase in turgor pressure of guard cells and initiates water uptake by guard cells via aquaporins (AQPs) causing stomatal opening (Outlaw, 2002; Padro & Maurel, 2013). For stomata closure, H+

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export is first inhibited and Ca2+ channels are activated which increases the cytosolic Ca2+ levels by mediating Ca2+ influx (Pei et al., 2000). The rise in concentrations of internal Ca2+ activates anion efflux channels. Thus, stomatal closure is mediated by membrane depolarization which involves efflux of Cl–, NO3– and malate via plasma membrane-localized anion channel (Saito & Uozumi, 2019). During environmental stress like draft, salinity, or bacterial invasions, rapid stomatal movement can impart stress tolerance. Stomatal closure can prevent bacterial entrance and regulates water loss which is crucial to prevent abiotic and biotic stresses. This is chiefly attributed to the regulation of the ion channels employing complex regulatory networks. As mentioned previously the stomatal closure is hugely dependent on anion efflux from guard cells and Cl– and organic acids like malates are major anions responsible for stomatal closure. Activities of the anion channels are often regulated by environmental changes leading to changes in the distribution of anions in the guard cells and thus control the volume of guard cells. Upon perception of any stress, anions are driven into vacuole or outside the cells, which alter the turgor pressure and reduces guard cell volume. There are two basic types of anion channels located in the guard cells which are directly involved in the regulation of stomatal movement. They are broadly classified into two types, i.e., (rapid) R-type which are activated with 50 ms by depolarization and (slow) S-type channels shows slow activation and deactivations depending on cellular voltage (Saito & Uozumi, 2019). The S-type channels are crucial for stimulus-induced stomatal closure and carry out passive efflux of Cl–, NO3, and malate (Kim et al., 2010). The S-type slow anion channel-associated 1 (SLAC1) genes encode plasma membrane proteins with 10 transmembrane helices (TMHs) are involved chiefly in stomatal closure and act as a dicarboxylate/malate transporter (Mur et al., 2013). A phenylalanine residue situated at (Phe450) blocks the channel pore and maintains the inactive state of the transporter. Phosphorylation by some specific kinases can shift the Phe450 residue due to conformational changes and help in activating the anion efflux channel (Chen et al., 2010; Li et al., 2000a, Schmidt et al., 1995; Maierhofer et al., 2014). Kinases like, LRR-RLK (leucine-rich repeat kinase), SnRK (sucrose non-fermenting-related kinase), MAPK (mitogen-activated protein kinase), CBL (calcineurin-B like protein), CPK/CDPK (calcium-dependent kinase), and CIPK (CBL-interacting protein kinase) are responsible for SLAC1 activations (Saito & Uozumi, 2019).

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Another R-type anion channel protein, i.e., Al-activated malate transporters also constitute a major group of guard cell anion channels involved in the regulation of stomatal movements (Barbier-Brygoo et al., 2011; Sasaki et al., 2010; Meyer et al., 2010b). AtALMT12 is first discovered in 2010 as a guard cell localized anion channel and was found to be permeable to Cl–, NO3– and malates. The activation of these R-type anion channels is not dependent on kinases or the presence of Al3+ (Meyer et al., 2010b, Hoekenga et al., 2006). Stress hormones ABA, Ca2+, and CO2 are found to be involved in the regulation of AtALMT12 activities. The cytosolic C-terminus domain of AtALMT12 protein is known to be a voltage sensor and can mediate rapid inactivation of the channel protein during membrane hyperpolarization (Mumm et al., 2013). Other 3 ALMT transporters AtALMT4, 6, and 9 are also found in tonoplast membrane of guard cell of Arabidopsis (Meyer et al., 2011; De Angeli et al., 2013; Kovermann et al., 2007; Dreyer et al., 2012; Eisenach & De Angeli, 2017). AtALMT6 are Ca2+ activated channel proteins responsible for the transport of fumarate and malate, and the activity of channel proteins is regulated by vacuolar pH (Meyer et al., 2011). AtALMT9 is a chloride efflux channel that is controlled by cytosolic malate levels and mediates stomatal opening (De Angeli et al., 2013). Atalmt4 mutant plants displays impairment of ABA-mediated stomatal closure, and these tonoplast localized anion efflux and influx proteins were found to be regulated by serine phosphorylation at Ser382 (Eisenach et al., 2017). Thus, it is evident that malate is also a strong player in the regulation of stomatal movements. Malate release from guard cells and upregulation of malate synthesis in guard cells is strongly associated with regulation of stomatal opening and closure (Daszkowska-Golec & Szarejko, 2013). ABC transporter AtBCB14 are malate influx channels localized in guard cell plasma membranes and helps in the stomatal opening (Lee et al., 2008). Another family of voltage regulated chloride channel and anion transporter protein CLC are found to be the regulator of stomatal movement (Saito & Uozumi, 2019). There are 7 members of CLC proteins (ATCLCa-g) in Arabidopsis and among them, AtCLCc is found in the tonoplast membrane of guard cells (Hechenberger et al., 1996; Lv et al., 2009). The clcc mutants are reported to be involved in ABA and NaCl-induced stomatal closure by changing the nitrate/chloride homeostasis (Jossier et al., 2010). The other two vacuolar chloride influx channel proteins of detoxification efflux carrier (DTX)/multidrug and toxic compound extrusion (MATE) family proteins, DTX33 and 35 were found to reside in Arabidopsis guard cell tonoplast

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membrane and their mutation can impair stomatal opening (Li et al., 2002; Omote et al., 2006; Zhang et al., 2017a). Thus, allocations of Cl– and malates are hugely involved in maintaining guard cell ion homeostasis and can promote adaptation against biotic and abiotic stresses. Modulation of these transporters through transgenic approaches can help in developing stresstolerant crops. 13.4.6 DROUGHT RESISTANCE Drought stress (DS) is known to affect crop growth and production universally. Hence one of the major objectives of agricultural biotechnology is to increase tolerance of plants during water deficit along with high yield. Plants possess some inherent qualities which help them to combat draft stress which mainly comprises of the following strategies: 1. Escape Strategy: This strategy is mainly found in desert ephemerals, pasture plants, and annual crops. These plants complete their life cycle before encountering the drought sessions by upregulating their metabolic rate, shortening the vegetative phase, rapid growth, and early flowering. 2. Avoidance Strategy: This is prevalent in annual and perennial plants where water loss is prevented by regulating stomatal movement and cuticular conductance. 3. Tolerance Strategy: This mainly involves the development of low water potential withstanding capacity which is imparted by lowmolecular-weight proteins and other osmoprotectants which protect from damages due to water deficiency (Bacelar et al., 2012). 13.4.6.1 MEMBRANE TRANSPORTERS AND DRAUGHT STRESS REMEDIATION Recently some membrane-bound transporters are found to be involved in draft avoidance, and tolerance strategies (Figure 13.5). Plasma membranelocalized anion channel SLAC1 which transports Cl– and NO3– were found to be under the control of ABA, CO2, Ca2+, NO, and H2O2 concentrations (Geiger et al., 2009; Vahisalu et al., 2008). According to Negi et al. (2008), mutations in SLAC1 can cause excessive Cl– accumulations and thus can disrupt stomata closure.

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FIGURE 13.5 Different chloride transporters involved in the regulation of stomatal movement during draft stress.

Plant chloride channels (CLCs) are also known to play a pivotal role in stomatal movements. The disruptions in AtCLCc channel transporters reportedly lead to delay in the stomatal opening (Guo et al., 2003). Changes in the phosphorylation patterns of AtCLCa enable the transporters to sequester anions during stomatal opening and stomatal closure in response to ABA, these transporters also participate in anion release (Wege et al., 2014). The expressions of CLCs are strongly linked with plant stress responses. Um et al. (2018) showed that over-expression of OsCLC1 genes promoted tolerance in rice seedlings by upregulating jasmonic acids (JAs) and ABA levels. Also, the overexpression of ZmCLC-d in Arabidopsis reduced Cl– levels in transgenic plants imparted higher drought resistance as compared with wildtype plants (Wang et al., 2015).

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De Angeli et al. (2013) reported that mutations in AtALMT9 can cause changes in stomatal movement patterns which are associated with increased tolerance. The atalmt9 knockout mutants of Arabidopsis showed slower wilting under draft stress as compared to wild-type plants. This showed that genetic modifications of vacuolar CLCs can help to increase tolerance. Another report by Lee et al. (2008), highlighted that mutation of malate importer AtABCB14 can accelerate stomatal closure. Vacuolar chloride influx channel proteins (AtDTX50) are also involved in increasing DS tolerance as reported by Jarzyniak & Jasiński (2014). It was found that this transporter can control ABA accumulations. They are localized in plasma membranes and show high activity during apoplastic pH-7 which corresponds to stress. Due to dysfunction of AtDTX50, excess ABA accumulated in guard cells, and this aided in slowing down the rate of wilting and provided higher tolerance to stress. Thus, genetic engineering for drought resistance can be achieved by targeting the anion transporter genes which are responsible for stomatal movements. 13.4.6.2 ORGANIC ACID AND DROUGHT STRESS REMEDIATION The role of acetic acids in the mitigation of drought stress has been recently highlighted by Kim et al. (2017) who observed over-accumulations of acetic acid in Arabidopsis at the onset of drought. An increase in acetic acid biosynthesis triggered a signal cascade which also initiated jasmonate acid (JA) signaling and helped in developing drought stress tolerance. In different draft tolerant mutants, high expression levels of the genes related to acetic biosynthesis like pyruvate decarboxylase-1 (PDC1) and acetaldehyde dehydrogenase 2B7 (ALDH2B7) was found due to epigenetic regulations by histone deacetylase 6 (HDA6). HDA6 acted as a negative regulator of PDC1 and ALDH2B7 gene expression. Kim et al. (2017) proved that JA signaling, and acetate synthesis were involved together in enhancing tolerance since JA biosynthesis and signaling gene mutants were drought-sensitive, and exogenous acetic acid treatments failed to rescue the mutant plants. 13.4.7 SALINITY STRESS REMEDIATION Almost 50% of all irrigated agricultural lands face excessive soil salinity which is detrimental to crop yield (Fita et al., 2015). Generally, adverse

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effects from soil salinity are mainly attributed to Na+ toxicity (Hanin et al., 2016). However, during NaCl stress, increase in Na+ levels are always associated with Cl– hyper-accumulation and K+ loss (Munns & Tester, 2008; Tavakkoli et al., 2010; Wu et al., 2018). K+ is a macronutrient that has various roles in plant metabolism and stress responses (Wang et al., 2013). Cl– also acts as a micronutrient but high concentrations are harmful as it can damage growth and plant photosynthetic ability due to its excess accumulation in chloroplasts (Tavakkoli et al., 2010, 2011; Geilfus, 2018). According to Bazihizina et al. (2019); Cl– can have a pivotal role in increasing plant stress tolerance. Enhancement in Cl– exclusion and control of Cl– transport in plants is reported to be potential means of generating salt stress-tolerant crops (Raven, 2017; Li et al., 2017b). According to White & Broadley (2001), some plants like soybeans, citrus, etc., are more prone to Cl– toxicity because they are equipped with Na+ exclusion mechanisms but cannot prevent the uptake of Cl– (Munns & Tester, 2008). Li et al. (2017b) reported antagonism between Cl– and NO3– uptake which is solely responsible for shortage in N supply during salinity stress which leads to a decline in protein synthesis and disrupts various metabolic processes. There are several channels and transporters responsible for Cl– transport in plants under salt stress (like AtCLC, SLAC, ALMT, DTX/MATE, CCC, NRT, NAXT (nitrate excretion transporter family), NPF (nitrate transporter 1/peptide transporter), etc.) and proper study about the roles of these transporters in controlling Cl– exclusion can help in establishing salt tolerance in crop plants (Wu & Li, 2019) (Figure 13.6). SLAC1 is a major plasma membrane-localized channel protein for malate and Cl– transport (Negi et al., 2008). According to the reports by Kurusu et al. (2013), overexpression of AtSLAC1 in tobacco BY-2 cells was triggered by cryptogein levels which induced downstream immune responses and also enhanced the Cl– efflux. This study showed evidence about the involvement of the SLAC family of anion channels in the early stages of immune response generation through signaling cascades (cryptogein induced ROS wave) and induction of hypersensitive cell death. The role of SLAC1 in the Cl– exclusion process was further confirmed by the reports of Negi et al. (2008), where mutations in slac1 showed increased Cl– levels in guard cells. Qiu et al. (2016), reported the artificial miRNAmediated knockdown of AtSLAH1 genes localized in the plasma membrane of root stele cells can reduce the Cl– accumulation in the shoot. On the contrary, upon over-expression of stele localized AtSLAH1 enhancement

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FIGURE 13.6 Transporters and channel proteins involved in increasing Cl– stress mitigation; upon sensing salt stress the sequestration of Cl– anions in vacuoles takes place through ALMT9 and CLC transporters and upon activation of CCC, ALMT, NPF2.5, SLAC1, SLAH1, and NRT transporters mediates efflux of excess Cl– anions preventing Cl– mediated cytotoxicity.

of Cl– uptake in shoots and decreases in NO3–/Cl– ratio was noted. Thus, SLAH1 can regulate salt tolerance in Arabidopsis. Another report by Liu et al. (2014) showed that upregulation of HvSLAH1 and HvSLAC1 genes in barley leaves can be associated with nitrogen homeostasis, regulation of stomatal movement which mainly helped in rapid stomatal closure and thus optimized water balance and imparted salt stress tolerance and higher grain yield in field conditions. Other chloride ion channel of CLC family AtCLCe (located in thylakoid) has been proved to be involved in the maintenance of photosynthetic efficiency and also in nitrate homeostasis (Herdean et al., 2016a). Wei and coworkers (2019) revealed the role of GsCLC-c2 in the alleviation of salt stress. Under salinity stress upregulation of GsCLC-c2 genes were noted in the roots of soybean which contributed to sequester the excess Cl– into the vacuoles of root cells and thus limited translocation of Cl– in the shoot which prevents salinity induced damages. Over-expressions of GsCLC-c2 genes in

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transgenic Arabidopsis, lead to Cl– and NO3– homeostasis and conferred salt tolerance (Liu et al., 2021). Li et al. (2017a) identified another potential Cl– transporter (AtNPF2.5) present in the root cortical cells and mutation of the AtNPF2.5 gene resulted in impairment of root Cl– exclusion and lead to higher Cl– accumulation in the shoot. Thus, overexpression of the AtNPF2.5 gene can lead to enhanced salt tolerance. Another candidate gene of the CCC (cation chloride co-transporter) family from Vitis vitifera was reported by Henderson et al. (2015). It was found that expression of the VviCCC gene in ccc knockout lines of Arabidopsis can reduce shoot Cl– levels and thus can play a crucial role in increasing salt tolerance. During salinity stress, vacuolar sequestration of Cl– can be an effective solution for preventing damages from extreme saline conditions. Cl– channels and transporters like AtCLCa, AtCLCb, AtCLCc, AtCLCg, and AtALMT9 are localized in tonoplast membranes (De Angeli et al., 2013; Wei et al., 2015), and they might contribute to vacuolar sequestration of Cl–. Recent findings by Nguyen et al. (2016) highlight the role of AtCLCc transporters which are responsible for anion storage in vacuoles and thus helps in detoxifying Cl– from cytoplasm which can increase overall salinity stress tolerance in Arabidopsis. The role of Cl–/H+ antiporter GmCLC1 of Glycine max was further tested in salt-stressed transgenic Arabidopsis where Cl– levels in shoots were decreased significantly. Also, over-expression of GmCLC1 in soybean leads to high Cl– sequestration and also prevented shoot translocation of Cl– which caused lesser damages. From these results, Wei et al. (2016), emphasized the protective roles of GmCLC1 under salinity stress. The link between vacuolar sequestration of anions and its further distribution in whole plants during saline conditions was validated by Baetz et al. (2016). almt9 knockout mutants of Arabidopsis showed reduced Cl– contents in the shoot. This alteration in the distribution of Cl– was mainly due to the changes in vacuolar anion sequestration pattern and regulated xylem loading of Cl–, since ALMT9 are highly expressed along the root and shoot vasculature. Thus, the above-mentioned examples strongly suggest that the involvement of Cl– transporters leading to vacuolar sequestration of Cl– to be strongly associated with modulating the stress tolerance of plants during salinity stress. 13.4.8 HEAT STRESS REMEDIATION Organic acid like citric acid is a TCA intermediate, which is involved in the respiratory pathway (DaSilva, 2003). A recent report by Hu et al.

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(2016), highlights the potential of citric acid amendments in the mitigation of the heat stress in tall fescue plants (Festuca arundinacea). With citric acid treatment increase in endogenous levels of citric acids was reported in the heat-stressed plants which lead to the upregulation of several cellular metabolic functions like, increase in photosynthetic efficiency, root activity, and antioxidant enzyme activities. Additionally, HSP gene expressions were also upregulated in the heat-stressed plants which played a major role in the enhancement of heat stress tolerance. 13.4.9 HEAVY METAL STRESS REMEDIATION According to Von Uexküll & Mutert (1995), approximately 50% of the world’s total arable lands are comprised of acidic soil (pH lower than 5.5). This acidic soil limits crop growth rate and productivity. Under acidic soil conditions, the solubility and bioavailability of heavy metals increase. As reported by Kochian et al. (2004), toxic levels of Al, Mn, Fe, and a limited supply of mineral nutrients like P are predominant in acidic soils. Under acidic soil conditions, organic acids not only reduce heavy metal toxicity but also can play a vital role in improving nutrient availability in soil. Organic acids (like citrate, malate, malonate, oxalate, tartarate, acotinate, etc.) can form bonds with heavy metals with the aid of carboxyl groups. The presence of heavy metals in soil often acts as an inducer for organic acid (like oxalate, malate, citrate, etc.) exudations from the roots which help in reducing the bioavailability of the heavy metals. Organic acid and heavy metals are reported to be less harmful owing to their low solubility. Detoxification of several toxic heavy metals like Al3+, Zn2+, Cd2+, Cu2+ is achieved by means of the secretion of organic acids to the rhizosphere (Osmolovskaya et al., 2018). Among different heavy metals, Al toxicity remediation and P utilization by means of organic acid secretions have been mostly studied in detail. 13.4.9.1 Al TOXICITY Aluminum (Al) is the most abundant mineral and is very toxic to plants under high concentrations (Kar et al., 2021). Primary symptoms of Al stress include deterioration in root growth and nutrient uptake efficiency. Root growth can be inhibited by Al3+ as a result of its interaction with actins and microtubules. Al3+ toxicity is also associated with disruption of Ca2+

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homeostasis, Ca2+ signaling, and ROS generation causing mitochondrial disruption, etc. Al3+ in toxic concentrations can also hinder the uptake of K+, Mg2+, NH4+, Ca2+, NO3– by directly interacting with the transporters (Kar et al., 2021). Several Al3+ tolerant plant species are already present, and they have developed strong mechanisms to prevent Al stress which mainly involves either Al3+ exclusion from root tip regions or by intrinsic detoxification of root absorbed Al3+ (Ma & Furukawa, 2003; Kochian et al., 2005; Sade et al., 2016). It is quite interesting that Al3+ tolerant plants have been identified to be capable of exudating organic acids (like malate, oxalate, citrate, and acetate) from roots which are considered as most effective in preventing the entry of Al3+ upon formation of stable complexes with Al3+ (Matsumoto, 2000; Chen & Liao, 2016; Sharma et al., 2016; Igamberdiev & Eprintsev, 2016). In response to high external Al3+ levels, plants generally upregulate the process of organic acid secretion from the root tips (Yang et al., 2008) and the primary function of those amino acids is to shield the root tip region upon formation of a defensive scabbard (Klug & Horst, 2010). Since it is impossible to detoxify all of the soil Al3+, plants only neutralize the Al3+ which is in close proximity with the root apex (Delhaize et al., 1993). Secretion of organic acids from roots can be categorized into two patterns. For Pattern I, there is no significant delay between the encounter of Al and secretion of organic acids (15 to 30 mins) since the presence of Al is enough to induce the transporters (Ma & Hiradate, 2000; Ryan et al., 2001). On the contrary, for Pattern II, a relatively longer delay for 4 to 48 h takes place between the two events as there is involvement of other signaling proteins or genes associated with the synthesis of organic acids followed by its transportation through plasma membrane-localized anion channels and transporters (Li et al., 2000b, Ma et al., 2001). 13.4.9.1.1 Role of Al-Activated Malate Transporters Malate is one of the major organic acids, capable of inducing Al tolerance is often exudated into the soil by inducing the activation of the malate transporters (Ryan et al., 1995). This group first identified that the rate of malate efflux upon induction by Al3+ varied significantly based on tolerance. Al tolerant wheat cultivar ET3 had a higher efflux rate than that of Al sensitive ES3 cultivar almost by 10 folds. This increase in efflux was also independent of activities of enzymes associated with malate synthesis like

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NAD-malate dehydrogenase, Phosphoenolpyruvate Decarboxylase. Ryan et al. (1995), also reported that the malate efflux can be inhibited upon treatments with niflumic acid, NPPB (5-nitro-2-(3-phenylpropylamino) benzoic acid), and IAA-94 (anion channel blockers). Zhang et al. (2001), first concluded that malate exudation from roots was carried by specific anion channels located in the root apical region. Sasaki et al. (2004) first identified a family of transporters named Al-activated Malate Transporter (TaALMT1) isolated from wheat which is involved in malate efflux in response to Al. Functional analysis of TaALMT1 was carried out by heterologous expression of the TaALMT1 gene in cultured tobacco cells, where strong malate efflux was found in the cells expressing TaALMT1 and TaALMT2 genes in response to Al3+. Delhaize et al. (2004) also reported that expression of TaALMT1 in transgenic barley can increase Al3+ resistance. Recent work by Silva et al. (2018) confirms that TaALM1 is directly responsible for malate efflux which provides tolerance to Al3+ in low pH soils. Several other ALMT transporters have been also identified in different plant species like Brassica napus, Arabidopsis thaliana, Zea mays, Hordeum vulgare, Solanum lycopersicum, Vitis vinifera, Oryza sativa, and Camelina sativa which are all involved in Al-induced malate secretion (Riaz et al., 2018). This was further confirmed by Park et al. (2017), who identified CsALMT1 gene encoding a plasma membrane-localized Al-activated malate transporter in Camelina sativa to be homologous to TaALMT1. CsALMT1 expression was found to be upregulated only in root tissue in response to Al stress which directly correlated to the degree of malate efflux and correspondingly with the tolerance of plants towards Al3+. Overexpression of CsALMT in transgenic lines also showed welldeveloped root architecture in comparison to wild types (WTs) under Al3+ stress. 13.4.9.1.2 Role of MATE Transporters Another family of transporters Multidrug and Toxic Compounds Extrusion (MATE) is responsible for the exudation of citrate upon induction by Al stress (Upadhyay et al., 2019). Multiple homologs of the MATE proteins are identified in different species, but Magalhaes et al. (2007) first identified the MATE proteins during the investigation of the Al-tolerance locus in sorghum. Functional analysis of MATE proteins was carried out by expressing the

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gene in Xenopus oocytes and electrophysiological studies revealed a rapid rate of citrate efflux in response to Al3+ (Lei et al., 2017; Liu & Zou, 2018). A study by Zhou et al. (2014) revealed that the presence of CEM (citrate exuding motif) in the MATE protein is primarily essential for citrate efflux. HvAACT1 was isolated from Hordeum vulgare which is Al sensitive in nature and was transformed with AtFRD3 and SbMATE followed by an expression in transgenic barley which then showed enhanced Al tolerance. Also, AtFRD3 transformed barley had a high rate of citrate efflux (Zhou et al., 2014). In japonica rice cultivar upon Al toxicity, Ferric Reductase Defective like 4 (OsFRDL4) is found to be upregulated and aluminum resistance transcription factor 1 (ART1) modulated the expression of MATE family genes which functions as citrate transporters (Yokosho et al., 2011). Another citrate transporter ScFRDL2 has been identified in rye which acts as a citrate transporter (Yokosho et al., 2010). According to Furukawa et al. (2007), Al-activated citrate transporter 1 (HvAACT1) is responsible for imparting Al tolerance in barley. Yang et al. (2011b) identified a family of MATE transporters in Vigna umbellata (VuMATE) which participates in the exudation of citrate under Al stress in acidic soil conditions. Citrate exudations via MATE transporters are generally characterized by two phases. In the 1st phase, citrate exudation occurs right after the encounter with Al (within 1.5 h), as in the case of VuMATE2 (proton-coupled citrate channel) mediated citrate efflux, and another surge of citrate exudation is noted after 6 h carried out by VuMATE1 (Liu et al., 2013; Liu & Zou, 2018). Upadhyay et al. (2020) also identified AtDTX30, a MATE transporter in Arabidopsis localized in the distal transition zone of the root which is involved in citrate release under Al stress and imparting Al resistance in Arabidopsis. 13.4.9.1.3 Role of H+-ATPases The plasma membrane-localized H+-ATPases (P-ATPase) and vacuolar H+-ATPases (V-ATPases) are also involved in the regulation of Al toxicity. In Cucurbita pepo, Al3+ is known to be responsible for inhibiting H+-ATPase activity thus altering membrane potential and increase Al3+ toxicity (Ahn et al., 2002). H+-ATPases mainly generate a gradient of protons across the membrane and thus facilitate the exchange of ions across the membrane and recent studies also elucidate that the functions of H+-ATPases are correlated

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with the exudation of organic acids (Yu et al., 2016; Zhang et al., 2017b). Shen et al. (2005) first reported simultaneous activation of H+-ATPases and exudation of citrates from soybean root tips in the presence of toxic Al3+. Application of H+-ATPases inhibitors like fusicoccin and vanadate can inhibit the Al stimulated citrate exudation simultaneously. Similarly, the citrate exudation rate was directly proportional to the increase in H+-ATPase activity. According to Chen et al. (2015a), H+-ATPase undergoes post-translational modifications which render its interaction with 14-3-3 proteins, and thus upregulate citrate efflux via MATE transporters under Al stress. H+-ATPase activities are vital for Al tolerant species like tea where a high rate of H+ efflux is found via H+-ATPases upon exposure to Al treatment (Qing et al., 2018). Another study carried out by Zhang et al. (2019) showed that mutation in VHA-a2 and VHA-a3 subunits of the Arabidopsis V-ATPase can prevent the accumulation of high levels of Al in roots and there is simultaneous upregulation in PM H+-ATPase activities and ALMT1 gene which increased Al resistance in the mutants. However, in few reports, it is highlighted that citrate exudation is completely independent of H+-ATPase in tomato and white lupin (Yang et al., 2011a, Zeng et al., 2013). 13.4.9.1.4 Regulation of Genes Involved in Al Exclusion and Sequestration Recent studies have unfolded various TFs and protein kinases that are involved in Al tolerance depicted briefly in (Figure 13.7). In Arabidopsis, the sensitive to proton rhizotoxicity 1 (STOP1) gene is associated with upregulation of expression of AtALMT1, AtMATE, and AtALS3 genes by interacting with their corresponding promoters (Iuchi et al., 2007). RAE1, an F-box protein (regulation of AtALMT1 expression 1), is identified to be the regulator of STOP1 stability and AtALMT1 level. RAE1 promotes STOP1 degradation by 26S proteosome and STOP1 binds the promoters of RAE1 and upregulates its expression, thus a negative feedback loop operates between RAE1 and STOP1 (Zhang et al., 2019). AtCBL1 (calcineurin B-like protein 1) is also involved in the activation of AtSTOP1, which controls the expression of AtALMT1 (Ligaba-Osena et al., 2017). STOP1 orthologs have been also identified in tobacco and maize. OsART1 (aluminum-resistance transcription factor 1) is an ortholog of AtSTOP1 which regulates the expression of STAR2 and OsFRDL4 proteins

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FIGURE 13.7 Summary of the roles of organic transporters involved in amelioration of aluminum toxicity by vacuolar sequestration and root exudation of organic acid with the help of efflux channels which are upregulated in response to stress.

which are homologs of AtALS3 and AtMATE (Yamaji et al., 2009; Daspute et al., 2017). Another transcription factor, calmodulin binding transcription activator 2 was reported to be the regulator of AtALMT1 expression (Tokizawa et al., 2015). Li et al. (2020) recently reported that wrky47 mutants of Arabidopsis, displayed high expressions of AtALMT1, AtMATE, and AtALS3 proteins and thus it was proved that the AtWRKY47 transcription factor had a direct role in the modulation of Al mediated responses. AtWRK46 also acted as an AtALMT1 repressor according to Ding et al. (2013). OsWRKY22 is also known to bind to the promoter of OsFRDL4 and activate its expression thus enhancing the citrate exudation in rice (Li et al., 2018). The knowledge about TFs mediated regulation of the organic acid efflux is increasing. Further investigations about the mechanism of Al sensing and signal transduction involved in the activation of Al-tolerance genes are needed for engineering Al-tolerant crops in the future.

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13.4.9.2 Mn TOXICITY Under acidic soil conditions, the level of free Mn increases gradually (Hu et al., 2019). Although Mn is an essential micronutrient, under very high concentrations, Mn becomes toxic. In such a scenario of Mn stress, organic acid exudation can help in Mn detoxification. Fernando et al. (2010) reported that organic acids like oxalate, malate, and citrate can mediate Mn stress remediation by chelating the cations in photosynthetic and non-photosynthetic tissues. Under Mn stress, high levels of oxalate and citrate exudation by ryegrass root have been reported by de la Luz Mora et al. (2009) which confirms the involvement of organic acids in Mn detoxification. Chen et al. (2015b) reported that upon exposure to Mn stress an increase in malate synthesis is found due to high malate dehydrogenase activity, and simultaneous root malate exudation via SgALMT1 was noted in Stylosanthes guianensi. These events together increased Mn stress tolerance. 13.4.9.3 ARSENITE TOXICITY LMWOAs such as citric acids can be effective chelators for arsenic (Almaroai et al., 2013). Ma et al. (2008); and Chen et al. (2017) reported a silicon transporter Low Silicon rice 2 (OsLsi2), which participates in arsenite [Ars(III)] efflux in rice, and Garbinski et al. (2019) reported that citrate efflux transporters in rice are close homologs of OsLsi2. Yu et al. (2012) also reported about the participation of citrate transporters in vacuolar sequestration and detoxification of arsenite. 13.4.9.4 CADMIUM TOXICITY LMWOA exudations from roots are also helpful in Cd detoxification. The negatively charged carboxylic acid groups bind the cations which can lead to the immobilization of metals. Organic acid acts either by causing precipitation of Cd in the rhizosphere or by organic acid mediated sequestration of Cd in the vacuoles (Clemens et al., 2002; Ding et al., 2014). Pinto et al. (2008) and Zhu et al. (2011) reported exudation of malates and oxalates from sorghum roots and tomato roots respectively in response to Cd stress which helped in resistance against toxic Cd. Organic acids upon exudation into the rhizosphere can also bind protons which leads to

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an increase in soil pH and reduced the phytoavailability of heavy metals (Javed et al., 2013). A recent study by Javed et al. (2017) showed that Cd tolerance in Zea mays cultivars, varied due to differential patterns of organic acid exudation from roots when grown in Cd spiked soils. It was found that upon exposure to toxic levels of Cd, tolerant cultivar cv. 3062, exudated malic formic, citric, acetic, glutamic, succinic, and oxalic acids in higher rate compared to that of Cd sensitive cultivar cv. 31P41. The antioxidant activities were dependent upon the rate of organic acid exudation. Since organic acid can increase the availability of essential macro and micronutrients to the plants, this may also help in improving the nutrient uptake efficiency of the Cd stressed plants and increase the activity of antioxidant enzymes. The effects of exogenous citrate and malate on Cd tolerance were studied by Sebastian & Prasad (2018), in Oryza sativa L. cv MTU 7029. They found that organic acid aided in the upregulation of antioxidant activities, the photosynthetic performance of the Cd stress plants, and also increased sequestration of Cd in vacuoles due to the upregulation of HMA3 (tonoplast localized heavy metal ATPase). 13.4.10 NUTRIENT AVAILABILITY In response to nutrient deficiency, plants undergo a series of changes to maximize nutrient uptake efficiency of plants. These changes include, modulation of the root system, changing soil pH by means of various root exudates which renders the dissociation of minerals from their bound forms, or the establishment of symbiotic relationship with beneficial soil bacteria and fungi which are capable of solubilizing minerals (Gruber et al., 2013; Mehra et al., 2017; von Tucher et al., 2018; Almario et al., 2017). According to reports by Panchal et al. (2021) organic acids can increase beneficial microorganism growth and alters the soil environment which aids in increasing the phytoavailability of nutrients. 13.4.10.1 MICRONUTRIENT DEFICIENCY It is well reported that deficiencies of micronutrients like Fe, Zn, and Mn can enhance the exudation of a range of organic acids like malate, citrate, oxalate, succinate, lactate, tartarate, etc. (Martinez-Cuenca et al., 2013; Bandyopadhyay et al., 2017; Rengel, 2015). These micronutrients form

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complexes with citrates and are translocated through the vascular tissues with the help of various citrate transporters. In Arabidopsis, AtFRD3 (citrate transporter) helps in the translocation of Fe-citrate complex (Durrett et al., 2007). OsFRDL1 and ScFRDL1 also help in iron transport in rice and rye plants (Yokosho et al., 2009, 2010). Another report by Sebastian & Prasad (2018) highlighted that organic acid treatments can prevent the Cd stressinduced Fe deficiency by upregulating the expression of OsIRT1 transporters which help in Fe uptake and this was also accompanied by a rise in the ferric chelate reductase activity, and stabilized Fe3+ – organic acid complex which can be readily taken up by plants via OsFRD1 transporters. 13.4.10.2 P DEFICIENCY The primary requirement for triggering the root responses in case of P deficiency involves the direct contact of the roots with the area of low P. Upon sensing the P deficiency, several changes in root architecture like an increase in root hair and root surface area takes place (Kellermeier et al., 2014; Nadira et al., 2016). Even if the shoot P contents was high, the arrest in the primary root growth, cell division, elongation, and changes in the merismatic activities can be found in response to the decline in soil P levels as reported by (Chevalier et al., 2003; Ticconi & Abel, 2004; Svistoonoff et al., 2007). Plants are also known to secrete organic acids (LMWOAs) as root exudates under P deficiency which is quite prominent in the Proteaceae family. These plants are characterized by specialized root clustered termed as ‘proteoid’ roots, which are dedicated for organic acid release in response to P deficiency (Dinkelaker et al., 1995; Zhang et al., 1997). The organic acids exudation from the roots of Proteaceae and other plants generally occurs from the young parts of roots, mainly the root apex (Shane & Lambers, 2005; Ryan et al., 2014). Positively charged cations like Al, Mg, etc., are known to form insoluble complexes with soil Pi and plants fail to absorb Pi in bound forms. Now upon exudation of the negatively charged organic acids (mainly citrate and malates), they react freely with the cations and in turn releases Pi from the cation-bound insoluble complexes (Zhang et al., 2018b, Shahbaz et al., 2006). According to reports by Krishnapriya & Pandey (2016); Giles et al. (2017); Mora-Macías et al. (2017), both citrate and malates are exuded for mobilizing the bound Pi from the soil. The entire signaling mechanisms involved in this event are depicted in (Figure 13.8).

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FIGURE 13.8 Under P deficiency, the uptake of organic acids in the root tip induces RAM exhaustion which cause a temporary rise in sugar levels followed by changes in root architecture, enhances root surface area.

Mora-Macías et al. (2017) reported that exudation of malate is required for accumulating Fe in the meristematic cell apoplasts which can trigger the modulations in root meristematic cell activities. STOP1 induces ALMT1 in malate exudation which accumulates Fe in the apoplast. Followed by this, the LPR1 (low phosphate root 1) dependent Fe redox cycling causes cell wall stiffening leading to root growth inhibition (Muller et al., 2015; Balzergue et al., 2017). LPR1 mediates the conversion of Fe2+ to Fe3+ in the apoplast

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region of root apical meristematic cells. Due to the accumulations of Fe3+ and, generation of ROS, the expression of CLE peptide gets upregulated which leads to exhaustion of root apical meristem (RAM) causing the loss of meristematic potential and arrest of cell proliferation, ultimately leading to inhibition of primary root growth and consequently lateral root proliferation. Malate exudation and Fe uptake are also associated with sugar accumulation due to the exhaustion of the apical meristem which leads to damages in the symplastic connections upon the deposition of callose and blocks cell differentiation (Shishkova et al., 2008; Ogden et al., 2018). This would also decrease the rate of exudation of organic acids from the roots. The increase in sugar concentrations acts as the main signal for modulating the root architecture (Canarini et al., 2019). Low-Pi insensitive mutants (lpi5 and lpi6) displayed long roots even when grown in low-Pi conditions and exogenous malate could reverse the growth pattern in a dose-dependent manner (Mora-Macías et al., 2017). Also, in transgenic tobacco having enhanced citric acid synthesis and citric acid secretion rate, a higher rate of Pi uptake was noted due to the dissolution of soil-bound immobilized Pi compounds (Lopez-Bucio et al., 2000). Overexpression of TaALMT1 in transgenic barley increased both Al tolerance and Pi uptake from low pH soils (Delhaize et al., 2004, 2009). Also, in Arabidopsis plants, malate exudation via AtALMT3 was found in response to Pi deficiency (Maruyama et al., 2019). These reports confirm the involvement of membrane transporters which are mainly associated with the exudation of organic acid and help in increasing P uptake. 13.4.11 PLANT BIOTIC STRESS TOLERANCE Organic acids also have significant roles in modulating plant responses to biotic stress. Sharma et al. (2016) reported salicylic acids (SAs) and their derivatives having complex benzene rings with carboxylic groups can induce local and systemic resistance in plants. Rudrappa et al. (2008) first reported that infection of Arabidopsis, with a foliar pathogen Pseudomonas syringae pv tomato (Pst DC3000), can induce AtALMT1 expression which consequently leads to malate secretion via root. This malate secretion helps in the recruitment of beneficial rhizobacterium Bacillus subtilis FB17 in a dosedependent manner. Upon the root colonization by the beneficial bacteria, the Pst DC3000 infected plant displayed reduced symptoms of leaf chlorosis and pathogen multiplication also reduced significantly. This inter-organism

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signaling between above ground and below ground tissues also leads to the development of induced systemic resistance (ISR) in the host which was evident from the upregulated levels of PR1 genes and SA in the leaves (Figure 13.9). Later Lakshmanan et al. (2012), discovered that upon Arabidopsis leaf infection with Pseudomonas syringae pv tomato (Pst DC3000), pathogenderived microbe-associated molecular patterns (MAMPs) relayed signals for recruitment of the Bacillus subtilis FB17. MAMPs like flagellar peptide, flagellin22 (flg22) were found to be the inducer of AtALMT1 expression which lead to malate secretion and root colonization with Bacillus subtilis FB17.

FIGURE 13.9 Inter-organism signaling involving enhanced root exudation of organic acids, for the development of induced systemic resistance against a virulent bacteria Pseudomonas syringae pv tomato (Pst DC3000) in Arabidopsis.

A recent study by Takanashi et al. (2016), showed the possible involvement of malate transporter LjALMT4 in the nitrogen fixation process of Lotus japonicas. It was found that the transporter protein was localized in the parenchyma cells of nodule vascular bundles and supplied necessary dicarboxylates and other anions required for symbiotic N2 fixation across the nodule vasculature. Recent findings also highlight the role of oxalic acids in inducing immunity against fungus Sclerotinia in tomatoes. Oxalic acids in low levels can

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act as an activator of host defenses by enhancing the innate immunity but when present in high concentrations, they suppress the ROS based immunity and induces programmed cell death (Kim et al., 2008; Cessna et al., 2000; Ghosh et al., 2016; Lehner et al., 2008). Kumar et al. (2016) reported that overexpression of oxalate decarboxylase (OXDC) gene degrades oxalic acid and thereby reduces the oxalate levels in transgenic grass pea and soybean and this has a tremendous impact on host resistance and develops host innate immunity against pathogenic fungi. 13.5 FUTURE PERSPECTIVES 13.5.1 CHLORIDE Chlorine nutrition for plants is one of the most overlooked topics. Most of the research is focused on chloride toxicity rather than its beneficial roles. However, recent findings have suggested that Cl can be regarded as a beneficial micronutrient for plants. High levels of Cl in the tobacco plants have led to an increase in water, carbon, and NUE, and all of this contributed to the enhanced growth rate. The increase in WUE through Cl nutrition can help to combat water deficit and drought situations. Further studies in this regard can eventually lead to the development of drought-resistant crops. Cl can also help in increasing the C and N metabolism since it can replace the anions like malate and nitrates in case of vacuole sequestration events. This increases the available C and N pool for other primary metabolic processes. Cl can also improve photosynthetic efficiency. Thus, crops can be benefited from the proper management of Cl fertilizations. Identifications of the transporters involved in Cl acquisition are very vital for further studies regarding Cl nutrition. To date the substrate-binding region of NPF proteins is unidentified, and this discovery can also play a part in improving Cl nutrition and uptake studies. Research regarding hormonemediated signaling and regulations of Cl nutrition are still urgently required to improve Cl nutrition. Different transporters are already found to be involved in soil-root, xylem-symplast, and cytosol-vacuole transfer interfaces which needs further explorations (Table 13.1). Endomembrane Cl transporters like GmCLC1, GsCLC2, AtALMT9, and GmSALT3/CHX1 are involved in maintaining intracellular Cl homeostasis and can regulate shoot Cl levels and maintaining salinity tolerance in plants. Also, the process of intracellular compartmentalization of Cl in the vascular cells is unknown. But since this particular event

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plays a crucial part in controlling ion (like Cl– and Na+) distribution in whole plants, further studies in this field can hold a bright future in the development of salinity tolerant plants. TABLE 13.1 Transporter Genes ZmNPF6.4

Some Transporters Involved in Chloride Flux in Plants Origin

Functions

References

Zea mays

Cl– selective proton-coupled symporter channel, active uptake of chloride Nitrate transporters, chlorine loading in root xylem S-type anion channel proteins, translocation of chloride in root xylem, SLAH1 is a salt tolerance regulator Efflux of Cl− from the root cells into soil

Wen et al. (2017)

Li et al. (2016, 2017) Cubero-Font et al. (2016); Qiu et al. (2016) Arabidopsis Li et al. (2017); AtNPF2.5 thaliana Henderson et al. NRT1.5 (2014) Glycine max Cl–/H+ antiports sequestering chloride Nguyen et al. GmCLC in vacuoles (2016) Arabidopsis Vacuolar sequestration of chlorides, Lorenzen et al. AtCLCa thaliana anion release (2004); Wege et al. (2014) Arabidopsis Accumulation of chlorides in vacuoles Jossier et al. AtCLCc thaliana of guard cells during stomatal opening, (2010) induces salt tolerance by chloride homeostasis Arabidopsis Chloride sequestration in vacuoles Barbier-Brygoo et ALMTs thaliana during salinity stress and maintenance al. (2011); Baetz of cytosolic ion homeostasis et al. (2016) – DXT33DXT35 Arabidopsis Vacuolar sequestration of Cl during Colmenero-Flores thaliana cellular expansions, helps in stomatal et al. (2019) opening Arabidopsis Cation-chloride cotransporter, cell CCC Colmenero‐Flores thaliana, elongation (inflorescence, root cells) et al. (2007); Chen Oryza sativa et al. (2016) Arabidopsis Stomatal closure, dicarboxylate/malate, Mur et al. (2013); SLAC1 thaliana chloride (efflux) transport Negi et al. (2008) Arabidopsis Guard cell localized R-type anion AtALMT12 Meyer et al. channel, permeable to Cl–, NO3– and (2010), Hoekenga thaliana malates et al. (2006) Arabidopsis Chloride efflux channel, mediates De Angeli et al. AtALMT9 thaliana stomatal opening (2013)

AtNPF2.4, AtNPF7.3 SLAH1, SLAH3

Arabidopsis thaliana Arabidopsis thaliana

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TABLE 13.1

(Continued)

Transporter Genes

Origin

Functions

References

ZmCLC-d

Arabidopsis thaliana Arabidopsis thaliana Arabidopsis thaliana

Reduced Cl– levels in transgenic plants imparted higher drought resistance Vacuolar chloride influx channel, involved in drought stress tolerance Chloride ion channel, maintenance of photosynthetic efficiency, nitrate homeostasis Sequestration of excess Cl– into the vacuoles of root cells Cation chloride co-transporter, related to salt tolerance

Wang et al. (2015)

AtDTX50 AtCLCe

GsCLC-c2

Glycine soja

VviCCC

Vitis vitifera

AtCLCb AtCLCg

Arabidopsis thaliana

GmCLC1

Glycine max

Jarzyniak & Jasiński (2014) Herdean et al. (2016a) Wei et al. (2019)

Henderson et al. (2015) – Tonoplast membrane Cl channels and De Angeli et al. (2013); Wei et al. transporters, vacuolar sequestration (2015) of Cl– Cl–/H+ antiporter, Cl– sequestration, chlorine homeostasis

Wei et al. (2016)

13.5.2 ORGANIC ACID The role of organic acids in the mitigation of DS and biotic stress tolerance has been recently highlighted by researchers. However, the viability of these approaches in field conditions is yet to be explored. Presently there are plenty of research regarding the role of organic acid exudation in nutrient acquisition and detoxification of toxic heavy metals. The organic acid exudation from the roots involves the utilization of a certain extent of carbon pool and thus it is a metabolically expensive process. However, the research regarding the regulation of the root exudation of organic acids have not been carried out to the full extent. Few studies have been carried out which highlight the role of different transporters in organic acid exudation and their simultaneous role in helping plants to combat stress situations (Table 13.2). According to very recent studies, it can be concluded that STOP1–ALMT1 modules are involved in root organic exudation during both Al toxicity and Pi deficiency. Recently identified TFs like AtWRKY46, OsWRKY22, and CAMTA2, have been identified to be involved in the regulation of the detoxification of Al3+ by organic acids. The roles of these TFs in mineral uptake and stress response can be further analyzed. The interplays between organic acid secretions and phytohormones under various stresses are yet to be explored.

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Some Transporters Involved in Organic Acid Flux in Plants

Transporter Gene AtALMT6

Origin

Functions

References

Arabidopsis thaliana

AtABCB14

Arabidopsis thaliana

Meyer et al. (2011) Lee et al. (2008)

SLAC1

Arabidopsis thaliana

AtABCB14

Arabidopsis thaliana

OsCLC1

Oryza sativa

AtDTX50

Arabidopsis thaliana

TaALMT1, TaALMT2 AtFRD3 HvAACT1

Triticum aestivum

ScFRDL2

Secale cereale

Transport of fumarate and malate Malate influx channels, helps in stomatal opening Dicarboxylate/malate transporter, plays a role in stomatal closure Guard cell malate influx channel, aids stomatal opening Upregulates jasmonic acid and abscisic acid to counter draft stress Controls ABA accumulations, aids in draft tolerance Malate efflux channels in roots. Citrate efflux transporter Al sensitive, citrate efflux transporter Citrate transporter

VuMATE

Vigna umbellata

VuMATE1 VuMATE2

Vigna umbellata Vigna umbellata

AtDTX30

Arabidopsis thaliana

SgALMT1 CsALMT1 AtALMT1

Stylosanthes guianensi Camelina sativa Arabidopsis thaliana

LjALMT4

Lotus japonicas

Arabidopsis thaliana Hordeum vulgare

Exudation of citrate under Al stress Citrate efflux Proton-coupled citrate channel, citrate efflux Citrate release under Al stress

Mur et al. (2013)

Lee et al. (2008)

Um et al. (2018)

Jarzyniak & Jasiński (2014) Sasaki et al. (2004) Zhou et al. (2014) Zhou et al. (2014) Yokosho et al. (2010) Yang et al. (2011c) Liu et al. (2018) Liu et al. (2013)

Malate exudation from root

Upadhyay et al. (2020) Chen et al. (2015)

Malate exudation Malate exudation in response to Pi deficiency malate transporter, plays role in nitrogen fixation

Park et al. (2017) Maruyama et al. (2019) Takanashi et al. (2016)

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13.6 CONCLUSION Chloride uptake by plants and the process of organic acid exudation by roots can be both considered as necessary evil. Excess Cl uptake is indeed toxic to the plants and the exudation of organic acids from roots can be considered to be a metabolic loss. High production and exudation of organic acids lead to high levels of C loss and thus it is an expensive process for fast-growing annual crops. However, Cl as a micronutrient participates in various physiological functions like osmotic regulation, stomatal regulation, and environmental stress tolerance. Thus present practices of avoiding the application of fertilizers having metallic salts of Cl increase chances of Cl deficiency in areas of high-yielding deep sandy soils with low organic matter. But based on recent evidence, proper Cl nutrition management can be a cost-effective source to mediate sustainable enhancement of agricultural productivity. Organic acid exudations by roots are also vital for increasing nutrient use efficiency of crops despite its energy cost. To prevent the C loss the tissuespecific exudation of organic acids is found in some plants like Arabidopsis where only the root tip mediates organic acid release in response to Al stress. The negative regulators like GABA (gamma amino-butyric acid) can also play a part in the regulation of organic acid release. However, there are various physiological functions of organic acids which are yet to be explored to full extents, and they can have a strong possibility of increasing crop productivity and the development of stress-resistant crops. Overuse of fertilizers can be prevented with the help of transgenic plants with enhanced synthesis capacity of organic acids and exudation. Thus, organic acids can also help in the development of sustainable agriculture, prevent soil pollution from heavy metals and eutrophication in water bodies and at the same time ensure an increase in agricultural output and environmental resilience in crops. KEYWORDS • • • • • •

chloride crassulacean acid metabolism organic acids stress tolerance sustainable approach transporters

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Wu, H., Shabala, L., Shabala, S., & Giraldo, J. P., (2018). Hydroxyl radical scavenging by cerium oxide nanoparticles improves Arabidopsis salinity tolerance by enhancing leaf mesophyll potassium retention. Environ. Sci. Nano, 5(7), 1567–1583. Xu, G., Magen, H., Tarchitzky, J., & Kafkafi, U., (1999). Advances in chloride nutrition of plants. Adv. Agron., 68, 97–150. Yamaji, N., Huang, C. F., Nagao, S., Yano, M., Sato, Y., Nagamura, Y., & Ma, J. F., (2009). A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell, 21(10), 3339–3349. Yang, J. L., Li, Y. Y., Zhang, Y. J., Zhang, S. S., Wu, Y. R., Wu, P., & Zheng, S. J., (2008). Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiology, 146(2), 602–611. Yang, J. L., Zhu, X. F., Peng, Y. X., Zheng, C., Ming, F., & Zheng, S. J., (2011). Aluminum regulates oxalate secretion and plasma membrane H+-ATPase activity independently in tomato roots. Planta, 234(2), 281–291. Yang, X. Y., Yang, J. L., Zhou, Y., Pineros, M. A., Kochian, L. V., Li, G. X., & Zheng, S. J., (2011). A de novo synthesis citrate transporter, Vigna umbellata multidrug and toxic compound extrusion, implicates in Al‐activated citrate efflux in rice bean (Vigna umbellata) root apex. Plant Cell Environ., 34(12), 2138–2148. Yokosho, K., Yamaji, N., & Ma, J. F., (2010). Isolation and characterization of two MATE genes in rye. Funct. Plant Biol., 37(4), 296–303. Yokosho, K., Yamaji, N., & Ma, J. F., (2011). An Al‐inducible MATE gene is involved in external detoxification of Al in rice. Plant J., 68(6), 1061–1069. Yokosho, K., Yamaji, N., Ueno, D., Mitani, N., & Ma, J. F., (2009). OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. Plant Physiol., 149(1), 297–305. Yu, L. J., Luo, Y. F., Liao, B., Xie, L. J., Chen, L., Xiao, S., Li, J. T., et al., (2012). Comparative transcriptome analysis of transporters, phytohormone and lipid metabolism pathways in response to arsenic stress in rice (Oryza sativa). New Phytol., 195(1), 97–112. Yu, W., Kan, Q., Zhang, J., Zeng, B., & Chen, Q., (2016). Role of the plasma membrane H+-ATPase in the regulation of organic acid exudation under aluminum toxicity and phosphorus deficiency. Plant Signal. Behav., 11(1), e1106660. Zeng, H., Feng, X., Wang, B., Zhu, Y., Shen, Q., & Xu, G., (2013). Citrate exudation induced by aluminum is independent of plasma membrane H+-ATPase activity and coupled with potassium efflux from cluster roots of phosphorus-deficient white lupin. Plant Soil, 366(1), 389–400. Zhang, F. S., Ma, J., & Cao, Y. P., (1997). Phosphorus deficiency enhances root exudation of low-molecular-weight organic acids and utilization of sparingly soluble inorganic phosphates by radish (Raghanus satiuvs L.) and rape (Brassica napus L.) plants. Plant Soil., 196(2), 261–264. Zhang, F., Yan, X., Han, X., Tang, R., Chu, M., Yang, Y., Yang, Y. H., et al., (2019). A defective vacuolar proton pump enhances aluminum tolerance by reducing vacuole sequestration of organic acids. Plant Physiol., 181(2), 743–761. Zhang, H., Zhao, F. G., Tang, R. J., Yu, Y., Song, J., Wang, Y., Li, L., & Luan, S., (2017). Two tonoplast MATE proteins function as turgor-regulating chloride channels in Arabidopsis. Proc. Nat. Acad. Sci., 114(10), E2036–E2045.

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Zhang, J., Wei, J., Li, D., Kong, X., Rengel, Z., Chen, L., Yang, Y., et al., (2017). The role of the plasma membrane H+-ATPase in plant responses to aluminum toxicity. Front. Plant Sci., 8, 1757. Zhang, L., Yan, C., Guo, Q., Zhang, J., & Ruiz-Menjivar, J., (2018). The impact of agricultural chemical inputs on environment: Global evidence from informetrics analysis and visualization. Int. J. Low-Carbon Technol., 13(4), 338–352. Zhang, W. H., Ryan, P. R., & Tyerman, S. D., (2001). Malate-permeable channels and cation channels activated by aluminum in the apical cells of wheat roots. Plant Physiol., 125(3), 1459–1472. Zhang, Y., Chen, F. S., Wu, X. Q., Luan, F. G., Zhang, L. P., Fang, X. M., Wan, S. Z., et al., (2018). Isolation and characterization of two phosphate-solubilizing fungi from rhizosphere soil of moso bamboo and their functional capacities when exposed to different phosphorus sources and pH environments. PloS One, 13(7), e0199625. Zhang, Y., Zhang, J., Guo, J., Zhou, F., Singh, S., Xu, X., Xie, Q., et al., (2019). F-box protein RAE1 regulates the stability of the aluminum-resistance transcription factor STOP1 in Arabidopsis. Proc. Nat. Acad. Sci., 116(1), 319–327. Zhao, C., Liu, B., Piao, S., Wang, X., Lobell, D. B., Huang, Y., Huang, M., et al., (2017). Temperature increase reduces global yields of major crops in four independent estimates. Proc. Nat. Acad. Sci., 114(35), 9326–9331. Zhou, G., Pereira, J. F., Delhaize, E., Zhou, M., Magalhaes, J. V., & Ryan, P. R., (2014). Enhancing the aluminum tolerance of barley by expressing the citrate transporter genes SbMATE and FRD3. J. Exp. Bot., 65(9), 2381–2390. Zhu, X. F., Zheng, C., Hu, Y. T., Jiang, T. A. O., Liu, Y. U., Dong, N. Y., Yang, J. L., & Zheng, S. J., (2011). Cadmium‐induced oxalate secretion from root apex is associated with cadmium exclusion and resistance in Lycopersicon esulentum. Plant Cell Environment, 34(7), 1055–1064. Zonia, L., Cordeiro, S., Tupý, J., & Feijó, J. A., (2002). Oscillatory chloride efflux at the pollen tube apex has a role in growth and cell volume regulation and is targeted by inositol 3,4,5,6-tetrakisphosphate. Plant Cell, 14(9), 2233–2249.

CHAPTER 14

Role of Sulfur in Protection Against Major Environmental Stress in Plants SNEHALATA MAJUMDAR, FALGUNI BARMAN, ALIVIA PAUL, and RITA KUNDU*

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

Corresponding author. E-mail: [email protected]

ABSTRACT Sulfur, an essential macronutrient for plant growth, is a crucial component of several primary and secondary metabolites. Plants are frequently subjected to various environmental stresses, comprising of abiotic stress like salinity, heavy metal, drought, cold or biotic stress like pathogenic invasions. These are marked by the induction of oxidative stress by the generation of reactive oxygen species (ROS), to combat this plethora of sulfur-containing compounds are produced. “Master antioxidant” glutathione (GSH) acts as a redox sensor maintaining cellular homeostasis and preventing oxidative denaturation of proteins by protecting their thiol groups. Null mutation of GSH gene was lethal for plants. Downregulation of GSH1, GSH2 gene, involved in GSH synthesis, led to hypersensitivity towards stress. Overexpression of glutathione reductase (GR1 and GR2) glutathione transferase (GST) and GSH peroxidase (GPX) genes imparted better stress tolerance. GSH also serves as a substrate for detoxifying enzyme glyoxalase-1 during salt stress. Phytochelatins (PCs), oligomers of GSH, play key role during heavy metal stress by chelating, compartmentalizing metal ions and phytochelatin synthase (PCS) gene overexpression was beneficial for both Biology and Biotechnology of Environmental Stress Tolerance in Plants: Trace Elements in Environmental Stress Tolerance, Volume 2. Aryadeep Roychoudhury (Ed.) © 2024 Apple Academic Press, Inc. Co-published with CRC Press (Taylor & Francis)

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metal and salt stress tolerance. Drought exposure induces the production of osmoprotectants such as choline-O-sulfate and polyamines. Elemental sulfur has antifungal activity along with several secondary metabolites like glucosinolates (GSLs), camalexin, etc. Knocking out transcription factors (TFs) MYB28 and MYB29 involved in glucosinolate synthesis pathway made plants 1.8 times more susceptible to pathogen attacks than the single mutants. Benzylated thiosulfinates exhibit broad spectrum antimicrobial properties. We briefly review here the protective role of these sulfur compounds in imparting tolerance against the major abiotic and biotic stress in plants. 14.1 INTRODUCTION Various natural and anthropogenic sources cumulatively contribute to environmental stress. These factors include both abiotic and biotic stress inducers, which lead to alteration in gene expression, changes in metabolism, and altered growth and development. Any environmental stress is mediated by changes in the external conditions of the plants. The severity of the changes determines the degree of toxicity within the plants. The environmental stress can be divided into abiotic and biotic stress. The major abiotic stresses include salinity, drought, heavy metal and cold stress as explained by Majumdar et al. (2020). The major biotic stresses include the toxicity induced by biological agents like microbes, fungi, insects, and weeds. The stressful impact caused by these abiotic and biotic factors negatively affect the plants worldwide and restrict their development and productivity (Anjum et al., 2015). Different plants respond differentially to stress conditions. Mainly the stress exposures lead to toxic shock in the plants which eventually lead to generation of ROS, these in turn affect the functionality of biomolecules like protein, carbohydrate, lipid, and DNA. Many of the biomolecules which act as inducers of important reaction cascades are affected under stressed conditions, leading to alterations in several physiological, biochemical, and molecular mechanisms (Dresselhaus & Huckelhoven, 2018). Homeostasis of plant nutrients play an important role in the improvement of crop yield and conferring resistance to various environmental stresses (Lamers et al., 2020). Sulfur is an important nutrient in agriculture after N, P, and K (Hasanuzzaman et al., 2018) and is being studied for its contribution in plant stress tolerance (Samanta et al., 2020). Sulfur plays key roles in electron transport reactions, and maintenance of cellular structure and metabolic regulations (Capaldi et al., 2015). Optimal sulfur utilization in plants

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improves plant growth and yield (Carciochi et al., 2017). Sulfur being an integral part of several antioxidants, proteins, enzymes, and amino acids, play essential roles in photosynthesis, nitrogen fixation and assimilation (Capaldi et al., 2015). In addition to the significant contribution to plant fundamental processes, it aids plants to develop tolerance to stress conditions (Osman & Rady, 2012). Several defense-related sulfurs containing compounds like cysteine (Cys), methionine, phytochelatin, GSH, thiol containing compounds, elemental sulfur and various S containing metabolites play crucial roles for plant defense strategies against biotic and abiotic stresses. 14.2 INVOLVEMENT OF SULFUR-CONTAINING COMPOUNDS IN STRESS TOLERANCE 14.2.1 METHIONINE Sulfur containing essential amino acids like methionine and Cys improves stress tolerance by altering several biochemical and physiological processes to favor plant growth. Methionine comprises a major part of stress related proteins (Garcia-Garcia et al., 2020). Methionine was able to maintain plant nutrient status by regulating N, P, and K uptake (Ali et al., 2019). Rise in methionine level was noted during various stressed conditions (Ali et al., 2019). Oxidative stress is generated as primary stress response in both abiotic and biotic stress, and it was currently demonstrated by Akram et al. (2020), that methionine regulates synthesis of osmolytes under such oxidative environment. Under oxidative stress, methionine residues are oxidized generally, damaging the proteins (Dann & Pell, 1989), it can be reduced back rapidly with help of peptide MetSO reductase (PMSR) enzyme, restoring their function instantly (Brot et al., 1981; Vieira Dos Santos et al., 2005). Total methionine content of canola and safflower was found to increase under drought stress (DS) depending on the degree of water deficiency. Additionally, an increased concentration of methionine was found to impart salt tolerance in Triticum aestivum and Glycine max (Cornelia et al., 2011; Farhangi-Abriz & Ghassemi-Golezani, 2016). Rise in methionine level was due to increase in rate of biosynthesis of this amino acid as reported by (Marur et al., 1994) in two cotton cultivars IAC 13–1 and IAC 20, under DS. Similar findings were reported under salt stress where methionine biosynthesis was found to be enhanced in Arabidopsis (Ogawa & Mitsuya, 2012). Increase in methionine level could be correlated with enhanced stress tolerance because methionine could regulate stomatal movement in a way to improve water utilization

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efficiency of the plants. Thus, by balancing the water potentials, methionine could efficiently maintain chlorophyll content and the photosynthetic apparatus hence, improving plant growth and yield (Ali et al., 2019). Neto et al. (2009) reported that methionine played a role in osmotic adjustment and helps improving the total protein content by preventing protein breakdown under salt stress. It was also reported that exogenous application of 6.4 mg/g methionine and S-adenosyl methionine (SAM) imparted tolerance against salt stress. Using methionine alone externally was equally efficient as that of application of a cocktail of amino acids. Methionine serves as a precursor molecule for several stress related compounds. SAM derived from methionine induces the synthesis of stress related compounds like flavonoids, phenolics, and polyamines. Some reports showed that polyamines are degraded back to methionine to combat stressed conditions (Zafari & Ebadi, 2016). Methionine improves growth, and net yield. ROS is produced in abundance in both abiotic and biotic stress and methionine is not only extremely sensitive towards ROS but also capable of detoxifying lipid peroxides, hydroperoxides, etc., efficiently. Methionine itself gets converted to two stereoisomers of methionine sulfoxide (MetSO) (MetO-S and MetO-R). Further, these are reduced back to methionine by thioredoxins (Trx) with help of MetSO reductase (MsrA and MsrB) (Figure 14.1). Thus, methionine forms an effective antioxidant system where ROS is scavenged and methionine gets itself revived through this oxidationreduction cycle, preventing oxidative damage (Bin et al., 2017).

FIGURE 14.1

Protective role of methionine to combat plant environmental stress.

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SAM is a source of 5’-deoxyadenosine radicals and serves as methyl, amino, ribosyl, and aminoalkyl groups. Methyltransferases donates methyl group to modify DNA, RNA or proteins, regulating gene expression, several physiological and metabolical pathways including DNA repair system. SAM exerts antioxidative effects by increasing cystathionine γ-synthase, which is primarily required for transsulfuration during Cys biosynthesis, maintaining activity of glutathione peroxidase (GPX), GSH transferase, superoxide dismutase (SOD) to scavenge ROS. SAM also helps in maintaining the GSH:GSSG ratio of the cells (Bin et al., 2017). SAM is also the precursor molecule of phytohormone ethylene and polyamines, nicotinamine, phytosiderophores (PSs), etc., which are extremely important in combating stress (Ravanel et al., 1998). Sulfur availability modulates ethylene signaling, which is important during several stressed conditions. Ethelene signaling and sulfur metabolism could be coupled closely. Sulfur limitation 1 transcription factor (SLIM1) transcription factor, the only transcription factor that is affected during sulfur deficiency, act in association with EIN3 and was reported to tune up iron homeostasis during times of deficiency by regulating FIT, the central regulator of iron assimilation pathway. Under metal stressed conditions, GSH accumulation was dependent on ethylene signaling pathway (Wawrzynska et al., 2015). 14.2.2 CYSTEINE (CYS) The sulfur containing amino acid Cys plays many structural, catalytic, regulatory, and metabolic functions in plants (Brosnan & Brosnan, 2006; Krishnan & Jez, 2018). Chemical properties due to the presence of reduced sulfur in Cys, makes it an important amino acid with essential biological roles (Toohey & Cooper, 2014). As primary producer plants carry out assimilatory sulfate reduction and synthesize Cys that helps in methionine production. Cys desulfhydrases (CDes) are key enzymes involved in H2S generation (Fang et al., 2016). In plants, Cys is the first organosulfur compound and the precursor for various biomolecules, such as GSH, phytochelatins (PCs), and metallothioneins (MTs) these participate in metal binding and detoxification in plants (Takahashi et al., 2011). 14.2.3 GSH GSH is a sulfur containing tripeptide (γ-glutamyl-cysteine-glycine), which acts as a reducing compound in sulfur metabolism of plants. It protects

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plants from environmental stress, cellular oxidative damage and help in ROS elimination (Tausz et al., 2003) by the regulation of ascorbate GSH cycle (Roychoudhury & Basu, 2012). Features such as high-water solubility, reactivity, and stability of GSH play vital role in metalloid stress management (Cobbett & Goldsbrough, 2002). 14.2.4 PROTEIN THIOLS Protein thiols include mainly thioredoxins (Trx) and glutaredoxins (Grx). All Grx contains a Trx fold (Begas et al., 2017). This protein-based thiol oxidoreductase function to maintain the viable ratio in the cell. Both contains a pair of Cys residue which gets oxidized by donating electrons and allows enzymes like peroxidases, reductases, etc., to reduce and detoxify reactive oxygen species (ROS). They may also function as oxidoreductase acting on specific protein targets. While TRXs are dependent on various site-specific reductases, GRXs are able to convert GSH to GSSG directly. Overexpression of TRX genes was observed along with accumulation of proteins under several biotic and abiotic stresses. GrxS13 was reported to play an antioxidative role protecting Arabidopsis seedlings from photooxidative stress (Laporte et al., 2012). GRXS13/ROXY18 transcription is also induced by the virulent strain of necrotrophic pathogen, Botrytis cinerea. GRXC9/ ROXY19 and GRXS13/ROXY18 played a major role in crosstalk between jasmonic acid (JA) and SA during pathogen attack (Li, 2015). Trx h5 and Trx h8 are two genes expressed preferentially in the chloroplast to deal with oxidative stress induced by biotic and abiotic stress; especially ROS induced from photosynthetic electron transport chain. During pathogen interaction Trx h5 transcripts of the host plant, were found in abundance. Trx h5 was thought to nullify the oxidative burst due to pathogen attack (Laloi et al., 2004). Trx h expression is primarily required during root nodule formation to detoxify the ROS formed and establish the bacterial colony (Lee et al., 2005). Chloroplastic drought-induced stress protein (CDSP 32) was noted to be upregulated under methyl viologen (MV) exposure along with Trx h in potato and rice seedlings. In rice it was observed that, Trx h, Grx, and sodCc1 genes share a novel 28 bp sequence, acting as cis-element (designated as CORE, coordinate regulatory element for antioxidant defense) responds to oxidative stress (MV), indicated a common role in nullifying oxidative stress (Tsukamoto et al., 2005). Proteomic study of Oryza sativa revealed that TRX and GRX genes were upregulated under copper stress and level of expression was more in case of tolerant varieties. A similar observation was

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reported in salt stressed barley. In Arabidopsis, tetratricopeptide thioredoxinlike (TTL) proteins have a role in root growth, organization of root meristem and vascular bundle formation. TTL genes respond differentially in coping salt and osmotic stress in Arabidopsis, ttl1, ttl3 and ttl4 showed hypersensitivity towards osmotic stress, ttl4 showed tolerance to salt stress, while ttl2 remained insensitive to such abiotic stress (Lakhssassi et al., 2012). Apart from acting as reductases, TRX, and GRX act as chaperones as observed in the case of tobacco. Many Trx dependent peroxides play potent role as molecular chaperones too. Such molecular chaperones impart heat tolerance in Saccharomyces cerevisiae. In catalytically inactive mutant GmTRX transgenic plants (Du et al., 2015) found that ROS scavenging activity could be executed even in the absence of oxidoreductase activity at per wild plants. Several peroxisomal enzyme activities could be maintained efficiently under heat stressed conditions owing to the chaperone activity of these Trx. These were found to interact with catalase 3 (CAT) protein, nodulin 5 proteins and maintaining their function at an identical rate with wild type (WT) plants (Table 14.1). TABLE 14.1

Role of Trx in Maintenance of Target Protein Function

Target Proteins Catalase Methionine sulfoxide reductase (A&B) Glutathione peroxidase A 2-Cys peroxiredoxin A Peroxiredoxin Q (atypical 2-Cys Prx) A Peroxiredoxin II (atypical 2-Cys Prx) A

Role of Trx Trx-regulated activity Trx-dependent reductase Trx-dependent reductase Trx-dependent reductase Interaction with Trx in vivo Trx-dependent reductase Interaction with Trx in vivo Trx-dependent reductase

14.3 ATP SULFURYLASE MEDIATED STRESS TOLERANCE The main sources of sulfur in plants are sulfate (SO42˗), which is taken up by plants from soil. The sulfate is activated by the catalyzing activity of ATP-sulfurylase, and adenosine-5’-phosphosulfate is formed as a product, which is eventually reduced to sulfide and forms a part of Cys, Cys having thiol groups have high nucleophilic activity which takes part in significant metabolic reactions and stabilize redox homeostasis (Hell & Wirtz, 2011). Not only in plants, ATP sulfurylase is responsible for sulfate reduction

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in bacteria, fungi, and algae also. Studies revealed that ATP sulfurylase in plants is highly similar to that found in humans (Patron et al., 2008). Adenosine-5’-phosphosulfate undergoes phosphorylation by adenosine5’-phosphosulfate kinase to produce 3’-phosphoadenosine 5’-phosphosulfate. 3’-phosphoadenosine 5’-phosphosulfate is reported to be associated with the production of various methionine or tryptophan derived S-containing metabolites like GSLs (Anjum et al., 2015) (Figure 14.2). Specifically, the indolic type GSLs are reported to confer tolerance to plants against various abiotic stress factors like heavy metal, temperature, salinity, drought (Variyar et al., 2014; Martínez-Ballesta et al., 2015; Salehin et al., 2019) and several biotic stress factors like pathogenic and herbivory induced stress (Frerigmann & Gigolashvili, 2014). The reduced-S transportation and storage is mediated by GSH, a non-protein thiol group containing tripeptide. Several reports of heightened GSH associated defense response and maintenance of redox homeostasis have been made against various abiotic stresses in plants (Anjum et al., 2015). Major Cys containing peptides like MTs and phytochelatins (PCs) are reported to play important roles in ROS detoxification and alleviation of stress induced deleterious effects (Anjum et al., 2014a). ATP-sulfurylase also provides tolerance to several biotic stresses via several sulfur containing compounds like Cys, GSLs, and GSH, which can induce pathogenic defense responses in plants (Alvarez et al., 2012). Suppression of virus-related symptoms and reduced viral role were reported when GSH and

FIGURE 14.2 ATP sulfurylase mediated production of important sulfur containing compounds for stress tolerance (PPi: inorganic phosphate; APS: adenosine 5’-phosphosulfate; PAPS: 3’phosphoadenosine 5’-phosphosulfate; Cys: cysteine; GSH: reduced glutathione; PCs: phytochelatins; MTs: metallothioneins). Source: Anjum et al. (2015).

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Cys were produced in increased amounts in Cucurbita pepo infected with Zucchini yellow mosaic virus (Kiraly et al., 2012). Increased transcription of ATP-sulfurylase was associated with optimized sulfur requirements in Phytophthora infestans infected plants (Matthewman, 2010). 14.4 INTERACTION OF SULFUR WITH PHYTOHORMONES The biosynthesis of several phytohormones is aided by sulfur and its derivatives. Reports suggest the significant association of methionine metabolism and ethylene biosynthesis (Sauter et al., 2013). 1-aminocyclopropane (ACC), formed from S-adenosylmethionine (SAM) via activated methionine, acts as substrate in the process of ethylene biosynthesis, while methylthioadenosine (co-product of ACC biosynthesis) is reversed back to form methionine (Sauter et al., 2004). Association of sulfate deficiency and poor stress tolerance have been reported, as inadequacy of sulfate is related to lowered levels of SAM, Cys, and abscisic acid (ABA) (Cao et al., 2014). Association of sulfur metabolism with biosynthesis of auxins have also been reported, lowered GSH production is reported to be associated with disturbed auxin gradient and compromised lateral root growth (Passaia et al., 2014). In addition to sulfide formation, JA aid in the biosynthesis of GSH and GSLs while maintaining the steady state of Cys or GSH (Frerigmann et al., 2014). The precursors of JA like cyclophilin and 12-oxo-phytodienoic acid are reported to have sulfur association in JA signaling, several sulfur metabolites are also important for cytokinin biosynthesis (Park et al., 2013). SO42˗ assimilation and sulfite reductase (SiR) are induced in case of oxidative stress along with several sulfate transporters (Koprivova et al., 2016). During stress conditions sulfate is associated with ABA signaling and stomatal closure (Ernst et al., 2010). Hydrogen sulfide (H2S) is reported to be associated with ABA downstream pathway and regulate stomatal closure (Scuffi et al., 2014). Sulfur is also reported to be associated with SA mediated signaling pathway which eventually regulate the plant defense response, elevated levels of GSH in exogenously SA applied plants indicating the association of sulfur with SA metabolism. SA metabolism is regulated by sulfation (Nazar et al., 2015; Baek et al., 2010). Gibberellic acid (GA) is reported to be associated with regulation of several enzymes involved in sulfur assimilatory pathway, the synergistic action of GA and sulfur is reported to alleviate oxidative stress-inducing ethylene formation, sulfur utilization and GSH production (Masood et al., 2016). Brassinosteroids also play an important role in sulfur

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metabolism by sulfation and sulfotransferase activity (Marsolais et al., 2007). 14.5 METALLOID STRESS IN PLANTS Metalloids are defined as the intermediate elements of metals and nonmetals. These metalloids are recognized as Boron (B), Selenium (Se), Silicon (Si), Arsenic (As), Antimony (Sb), Tellurium (Te) and Polonium (Po) in the periodic table (Appenroth, 2010). Except As, metalloids are considered as essential micronutrients which play an important role in plants, animals, and humans for their growth, development, and survival (Abbas et al., 2018). These metalloids are also called trace elements due to their presence in small concentration, i.e., 10 mg/kg in the environment. Only a few metalloids like Boron, Selenium, and Silicon are known as essential metalloids and perform beneficial roles in plants (Deng et al., 2021). Essential metalloids perform several physiological and biochemical functions in plants. At optimum level metalloids regulate various types of cellular, biochemical, and metabolic functions including oxidation-reduction, and forms a central component of many enzymes. However, when metalloid concentrations cross their threshold limit they are reported to exhibit toxicity in plants (Hossain, 2012). 14.5.1 RESPONSES OF METALLOID STRESS IN PLANTS Rapid industrial development, ore mining, refining, etc., release significant amounts of toxic metalloids in the environment, are mainly responsible for increasing soil contaminant (Rizwan et al., 2016). These soil contaminants specially disturb plant growth and development. The effects of metalloid stress may range from alteration of different functional groups to generation of ROS, and induction of cellular and molecular damages (Anjum et al., 2015). Additionally, excess metalloids negatively affect seed germination, plant growth and biomass, photosynthesis, mineral homeostasis and yield (Wagner, 1993; Adrees et al., 2015). Since the past two decades, extensive study has been done across the globe to assess the source, phytoavailability, and impact of metalloid stress on the environment (Nascimento & Xing, 2006; Adrees et al., 2015). Excessive concentration of metalloids is reported as imperative environmental toxic elements because they generate oxidative stress in plants (Gjorgieva et al., 2013). The ultimate result of cellular oxidative stress is the generation of ROS including (hydroxyl radical, singlet oxygen) through the Haber–Weiss and Fenton reactions. Beside these reactions

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metalloids can reduce antioxidant GSH pool, activating calcium-dependent system and iron mediated reactive process (Hasanuzzaman & Fujita, 2012; Oves et al., 2016). Under stressed conditions, some plant species generate Methylglyoxals (MGs), which also enhance the oxidative damage. When both ROS and MG are produced in large concentrations in plants, it leads to a wide range of detrimental cellular responses including lipid peroxidation (LPO), destruction of anti-oxidative mechanism, and denaturation of protein and DNA (Sharma et al., 2012). In this section, we have attempted to discuss how excess concentration of metalloids enhances oxidative stress in plants (Figure 14.3).

FIGURE 14.3 Excessive metalloid stress in plant induces ROS generation, growth inhibition, and yield reduction.

14.5.2 SULFUR UPTAKE AND ASSIMILATION BY PLANTS Sulfur is the 4th important macronutrient in plants and plays a pivotal role in growth, metabolism, and development (Matraszek et al., 2016). In soil sulfur is present in the form of sulfate (SO42˗). Sulfate assimilation pathway is initiated by the conversion of inorganic sulfate to sulfide and finally end up with the formation of Cys or homocysteine (HCys). In plants sulfate is taken up by roots with high affinity and the maximum level reaches up to 0.1 mM (Hawkesford et al., 2003). Root to shoot uptake of sulfate is strictly controlled and is one of the key regulatory sites of sulfur assimilation (Figure 14.4).

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Several sulfate transporter proteins are responsible for sulfate uptake and transport and is an energy dependent process (driven by a proton gradient generated by ATPases; Clarkson, 1993). Shoot chloroplastic cells are the center for sulfate unload, transport, and reduction, whereas rest of the sulfate in plant exists in the cell’s vacuole. Sulfate to sulfide reduction is a threestep process, which occurs in the leaf chloroplast. In the first step, sulfate is converted into APS by the help of enzyme ATP sulfurylase and then APS is converted into sulfite (Davidian & Kopriva, 2010). ATP sulfurylase, helps to activate sulfate because the affinity for sulfate is very low (Km approximately 1 mM) and the in situ chloroplastic sulfate concentration is mainly one of the limiting/regulatory steps in sulfur reduction (Buwalda et al., 1993). Sulfite is reduced by SiR and form sulfide, which is incorporated into Cys. This step is catalyzed by Oacetylserine(thiol)lyase, with O-acetylserine acting as substrate (Mugford et al., 2009).

FIGURE 14.4 Outline of sulfate reduction and assimilation in plants (APS: adenosine-5’ phosphosulfate; Fdred and Fdox: reduced and oxidized ferredoxin; GSH and GSSH: reduced and oxidized glutathione; AMP: adenosine monophosphate).

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14.5.3 ROLE OF SULFUR AND SULFUR COMPONENTS IN ALLEVIATING METALLOID STRESS IN VARIOUS PLANTS After potassium, sulfur is considered as the most important macronutrient in plants and performs several biological activities (Capaldi et al., 2015). The productivity of plants highly depends on sulfur and sulfur containing compounds such as sulfur-containing amino acids (Cys and methionine), antioxidants (GSH), proteins, and sulfolipids (Abdalla et al., 2016). Other compounds like iron-sulfur cluster, polysaccharides, vitamins (thiamine and biotin), cofactor (CoA and S-adenosyl-methionine), PCs are also considered as a component of sulfur. The mitigating mechanism of sulfur-containing compounds against metalloid stress has been discussed in the following text. 14.5.3.1 INVOLVEMENT OF CYSTEINE (CYS) IN METAL STRESS Heavy metal stress negatively affects the seed germination by the inhibition of α-amylases and other hydrolytic enzymes. Cys could overcome this enzyme inhibition by mobilizing the breakdown products of amylase (Genisel et al., 2015). Among the sulfur containing metal binding compounds PCs, and MTs are the best characterized as metal binding ligands present in plants. Moreover, MTs and PCs are Cys-rich polypeptides and family of enzymatically synthesized Cys-rich peptides (CRPs), respectively. During the early stages of seedling establishment involving seed germination, the seedling growth phosphatases, proteases, and α-amylases are the key enzymes associated with mobilization of nutrients in the endosperm (Shereen et al., 2011). In plants, ROS (as singlet oxygen, superoxide, hydroxyl radical, and hydrogen peroxide (H2O2)) generation is induced by metal stress. Cys also works as a ROS scavenger due to its antioxidative property (Banerjee & Roychoudhury, 2018). Although plants have an internal ROS detoxification system, but under stressed conditions, high levels of superoxide (•O−2) generation clearly indicate that plants do not have sufficient resistant capacity. Whereas, Cys application is reported to reduce the superoxide (•O−2) level and helps in mitigation of metal induced toxicity (Gaafar et al., 2020). 14.5.3.2 GLUTATHIONE (GSH) Glutathione (GSH) acts as a key component of metal detoxification due to the presence of thiol (-SH) group and the precursor molecule of PCs (Mittler

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et al., 2004; Cuypers et al., 2010). Besides this, GSH has a Cys residue that confers important anti-oxidative machinery by acting as a substrate for the regeneration of many essential antioxidants (Bashandy et al., 2010). GSH also safeguards the susceptible Cys rice protein from binding free metalloid ions and conserve their role in plants. Therefore, it forms non-toxic complexes in cell and sequestrate them away from the sensitive tissue (Verbruggen et al., 2009). However, in addition to metalloids, GSH also binds with toxic xenobiotics like herbicides, metabolites like anthocyanins and help in sequestration (Jozefczak et al., 2012). Glutathione S-transferases (GSTs) catalyze the conjugation of toxic compounds to GSH and store into vacuoles (Foyer et al., 2001). This has been reported in Arabidopsis after Cu or Cd treatment and result showed enhanced free metal binding capacity (Cobbett & Goldsbrough, 2002). Transporters called tonoplast multidrug resistance-associated protein (MRP), type of ATP-binding cassette (ABC) facilitates these GSH – conjugates through the vacuolar membrane (Verbruggen et al., 2009). 14.5.3.3 THIOREDOXIN (TRX) SYSTEMS Thioredoxin (Trx) is ubiquitous, low molecular weight (12–14 kDa) disulfide reductase which control the oxidation and reduction states of a protein (Jedelská et al., 2020). In plants Trx can be categorized into six types such as Trx f, m, h, o, y, and x on the basis of their abundance in cytosol, mitochondria, and chloroplast and according to their sequence (Gelhaye et al., 2005; Collet & Messens, 2010). It prevents cellular inactivation of endogenous proteins from oxidative damage and combats different environmental stresses (Holmgren, 1995). During the nodal development of soybean roots, Trx h assist to detoxify the cellular ROS level (Lee et al., 2005). Oxidative form of Trx made by a disulfide (-S-S-) bridge is reduced to sulfhydryl state (-SH) through the reduced ferredoxin and ferredoxin dependent Trx reductase or NADPH (Balmer et al., 2006; Jacquot et al., 2009). Vido et al. (2001) demonstrated that under metalloids/metal stress, the expression of some Trx isoforms such as h3 and h4 were increased but mutation showed reduced activity of Trx gene. This reduced activity was also correlated with metalloids stress tolerance in plants. Thus, abiotic stress enhances the Trx at gene and protein level. Song et al. (2013) reported that Trx gene was up-regulated under metal stress condition in rice. Trx also controls the level of cellular GPX (Vivancos et al., 2005). Trx has the ability to detoxify lipid hydroperoxides which prevent oxidative damage of proteins (Santos & Rey, 2006).

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14.5.3.4 OTHER COMPOUNDS Other sulfur containing compounds including Vitamin B1, Sulfolipids, and secondary sulfur compounds such as GSLs and PCs also play significant role in environmental stress condition (De Kok et al., 2002). Vitamin B1 or thiamine included two components like thiazole and a pyrimidine moiety (Nosaka, 2006). Thiamine also helps in ATP synthesis, NADPH, and carbohydrate metabolism and protects plants from osmotic and oxidative stress. 14.5.4 SULFATE TRANSPORTER AND METALLOID STRESS Like other environmental stresses, metalloids also affect plant nutrient transport, assimilation, and metabolism. Under such unfavorable conditions, transporter proteins sometime fail to function properly, which disrupt ion homeostasis or nutrient balance (Hasanuzzaman et al., 2018). GSH, play a diverse role under such condition, which express the primary sulfate uptake transporter-like Sultr1;1 (Takahashi et al., 2000) (Table 14.2). Metalloid stress also enhances the activity of ZmST1;1 transporter which is very similar to high affinity sulfate transporter. According to Nocito et al. (2006), higher sulfate accumulation is correlated with higher production of PC for detoxification of mental stress. Sultr1;2 is another high affinity sulfate transporter associated with arsenic (As) stress tolerance in plants. Nishida et al. (2016) showed that Arabidopsis mutant lacking Sultr1;2 transporter was sensitive to As. TABLE 14.2

Sulfate Transporters in Plants, Their Function and Localization in Cell

Transporter Expression Organs and Tissue Localization SULTR1;1 Localized in root surface hairs, epidermis, and cortical cells, expressed in cell layers. SULTR1;2 Localized in root hairs, epidermis, and cortex, expressed in cell layers. SULTR1;3 Found in companion cells of phloem tissue, expressed in both root and shoot.

Functions

References

Initiate uptake of sulfate from nutrient media. Initiate uptake of sulfate from nutrient media. Transport of sulfur from root to shoot and uptake of sulfur in phloem companion cell at the time of repressed condition of other transporters.

Takahashi et al. (2000) Shibagaki et al. (2002) Yoshimoto et al. (2003); Takahashi et al. (2000)

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14.5.5 MOLECULAR APPROACHES IN REGULATING SULFUR STATUS IN PLANTS The requirement of sulfur is very high in plants for optimum growth and development. However, plants do not get sufficient sulfur due to the dynamic nature of the environment (such as drought, salinity, metal, chemical, and several biotic and abiotic stresses). So, to overcome this adverse situation, plants develop various strategies under diverse conditions, including S deficiency and critical environmental conditions. Plants have several regulatory mechanisms by which they ensure the optimal accumulation of S-containing compounds or organic SO42− in cells for metabolic activity. This regulatory mechanism is controlled by different proteins, enzymes, and phytohormones. Under S deficient conditions, the expression of Sultr1;1 transporter is greatly enhanced and Sultr1;1 is more responsive compared to Sultr1;2 transporter (Yoshimoto et al., 2002). The expression of Sultr1;1 transporter inhibited by Phosphatase inhibitors like okadaic acid (OKA) and calyculin A (CalyA) during low S condition suggest the role of protein phosphatase in regulation of Sultr1;1 expression (Maruyama-Nakashita et al., 2004a). According to Maruyama-Nakashita et al. (2004b), only cytokinin can inhibit the expression of Sultr1;1 and Sultr1;2 transporters in Arabidopsis indicating the negative impact of cytokinin in S homeostasis in the plant. An element called sulfur-responsive element (SURE) has been reported in the 5’ promoter region of Sultr1;1 transporter, which is associated with S deficient condition (Maruyama-Nakashita et al., 2005). Wawryzynska et al. (2010) reported EIL group transcription factors (TFs), characterized from the promoter region of UP9C gene of tobacco plants, also work in S deficient condition. S homeostasis involves two enzyme complex such as SAT and OAS-TL known as cysteine synthase complex (CSC) (Takahashi et al., 2011; Koprivova & Kopriva, 2014). Although, enough evidences are not available there to elucidate the complete mechanism, study of the regulatory mechanisms for S metabolism under metalloid stress condition can explain further. 14.6 COLD STRESS IN PLANTS Like other abiotic stresses, cold stress is a major environmental factor that adversely affects plant’s growth, development, and crop production, especially in hilly regions (Sanghera et al., 2011). Additionally, it also restrains the spatial/geographical distribution of plants (Shi et al., 2018). Cold stress

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can be classified into chilling stress (