Abiotic Stresses in Wheat: Unfolding the Challenges 0323953689, 9780323953689

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Abiotic Stresses in Wheat Unfolding the Challenges

Edited by

Mohd. Kamran Khan Department of Soil Science and Plant Nutrition, Faculty of Agriculture, Selcuk University, Konya, Turkey

Anamika Pandey Department of Soil Science and Plant Nutrition, Faculty of Agriculture, Selcuk University, Konya, Turkey

Mehmet Hamurcu Department of Soil Science and Plant Nutrition, Faculty of Agriculture, Selcuk University, Konya, Turkey

Om Prakash Gupta ICAR-Indian Institute of Wheat and Barley Research, Karnal, Haryana, India

Sait Gezgin Department of Soil Science and Plant Nutrition, Faculty of Agriculture, Selcuk University, Konya, Turkey

Abiotic Stresses in Wheat Unfolding the Challenges

Academic Press is an imprint of Elsevier 125 London Wall, London EC2Y 5AS, United Kingdom 525 B Street, Suite 1650, San Diego, CA 92101, United States 50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, United Kingdom Copyright © 2023 Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. ISBN 978-0-323-95368-9 For information on all Academic Press publications visit our website at https://www.elsevier.com/books-and-journals

Publisher: Nikki Levy Acquisitions Editor: Nancy Maragioglio Editorial Project Manager: Maria Elaine Desamero Production Project Manager: Sruthi Satheesh Cover Designer: Matthew Limbert Typeset by STRAIVE, India

Contributors Numbers in parentheses indicate the pages on which the authors’ contributions begin.

Saju Adhikary (131), Department of Agronomy, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, Nadia, West Bengal, India Nadia Afroz (195), Institute of Biotechnology and Genetic Engineering (IBGE), Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh Disha Agarwal (247), Department of Biosciences, Manipal University Jaipur, Jaipur, Rajasthan, India Yamini Agrawal (247), Department of Biosciences, Manipal University Jaipur, Jaipur, Rajasthan, India Zeeshan Ahmad (393), MOE Key Laboratory of Plant-Soil Interactions, Department of Plant Nutrition, China Agricultural University, Beijing, China Saif Alharbi (233), National Center for Agriculture Technology, Life Science and Environment Research Institute, King Abdulaziz City for Science & Technology, Saudi Arabia

Annu (209), Department of Molecular Biology, Biotechnology and Bioinformatics, CCS Haryana Agricultural University, Hisar, India Most. Waheda Rahman Ansary (195), Institute of Biotechnology and Genetic Engineering (IBGE), Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh Hirdayesh Anuragi (259), Tree Improvement Research, ICAR-Central Agroforestry Research Institute, Jhansi, Uttar Pradesh, India Md. Arifuzzaman (15, 141, 329), Department of Genetics and Plant Breeding, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh Tabinda Athar (273, 329, 393, 413), Faculty of Agriculture, Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan Kousik Atta (1, 95, 131, 357), Department of Plant Physiology, Faculty of Agriculture, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, West Bengal, India

Mohammed Anwar Ali (131), Department of Crop Physiology, Agriculture College (ANGRAU), Bapatla, Andhra Pradesh, India

Ananya Baidya (95, 131), Department of Plant Physiology, Faculty of Agriculture, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, West Bengal, India

Fahad Alotaibi (233), National Center for Agriculture Technology, Life Science and Environment Research Institute, King Abdulaziz City for Science & Technology, Saudi Arabia

Aneesa Batool (393), Proteomics Laboratory, Division of Plant Biotechnology, Sher-e-Kashmir University of Agricultural Sciences and Technology of Kashmir, Shalimar, Srinagar, Jammu and Kashmir, India

Abdullah Alrajhi (233), National Center for Agriculture Technology, Life Science and Environment Research Institute, King Abdulaziz City for Science & Technology, Saudi Arabia

Vijendra S. Baviskar (161), Genetics and Plant Breeding Group, Agharkar Research Institute, Pune, Maharashtra, India

Muhammad Ameen (393), Faculty of Agriculture, Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan

Anurag Bera (339), Department of Agronomy, Dr. Rajendra Prasad Central Agricultural University, Pusa, Bihar, India K.L. Bhutia (339), Department of Agril. Biotechnology and Molecular Biology, Dr. Rajendra Prasad Central Agricultural University, Pusa, Bihar, India

Mst. Anamika Amzad (141), Department of Genetics and Plant Breeding, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh

Cheng Chang (67), College of Life Sciences, Qingdao University, Qingdao, China

Anjali (259), Department of Plant Physiology, G.B. Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India

Shukti Rani Chowdhury (357), Department of Plant Pathology, University of Georgia, Griffin, GA, United States xiii

xiv

Contributors

Sri Sai Subramnyam Dash (95), Research Scholar, Department of Genetics and Plant Breeding, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, West Bengal, India Shreenivas A. Desai (161), Department of Genetics and Plant Breeding, University of Agricultural Sciences, Dharwad, Karnataka, India Kapil Deswal (33, 283), Department of Botany and Plant Physiology, Chaudhary Charan Singh Haryana Agricultural University, Hisar, Haryana, India Yengkhom Linthoingambi Devi (95), Research Scholar, Department of Genetics and Plant Breeding, Indira Gandhi Krishi Vishwavidyalaya, Raipur, Chhattisgarh, India Rajiv Dubey (339), Department of Agronomy, RVSKVVCollege of Horticulture, Mandsaur; Department of Agronomy, RVS Krishi Vishwa Vidyalaya, Gwalior, Madhya Pradesh, India Debjani Dutta (1, 95), Department of Plant Physiology, Faculty of Agriculture, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur; School of Agriculture, Seacom Skills University, Kendradangal, Birbhum, West Bengal, India Mateja Germ (273), Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia Sait Gezgin (273, 329, 393, 413), Department of Soil Science and Plant Nutrition, Faculty of Agriculture, Selcuk University, Konya, Turkey Fatma Gokmen Yilmaz (329), Department of Soil Science and Plant Nutrition, Faculty of Agriculture, Selcuk University, Konya, Turkey K. Gopalareddy (161), ICAR-Indian Institute of Wheat and Barley Research, Karnal, Haryana, India Alisha Goyal (209), Department of Botany and Plant Physiology, Chaudhary Charan Singh Haryana Agricultural University, Hisar, Haryana; Division of Crop Improvement, ICAR—Central Soil Salinity Research Institute, Karnal, India Dinoo Gunasekera (297), Department of Information Technology, Faculty of Computing, General Sir John Kotelawala Defence University, Sewanagala, Sri Lanka Mehmet Hamurcu (141, 273, 329, 393, 413), Department of Soil Science and Plant Nutrition, Faculty of Agriculture, Selcuk University, Konya, Turkey M. Hasanuzzaman (141), Department of Genetics and Plant Breeding, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh

Mst. Hasna Hena (15), Department of Genetics and Plant Breeding, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh Akbar Hossain (1, 95, 131, 357), Division of Agronomy; Division of Soil Science, Bangladesh Wheat and Maize Research Institute, Nashipur, Dinajpur, Bangladesh Huan Hu (375), Microbial Resources and Drug Development Key Laboratory of Guizhou Tertiary Institution, Life Sciences Institute, School of Preclinical Medicine, Zunyi Medical University, Zunyi, Guizhou Province, China Ashal Ilyas (247), Department of Biotechnology, Invertis University, Bareilly, Uttar Pradesh, India Md. Rafiqul Islam (179), Department of Agronomy, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh Tofazzal Islam (15, 141, 179, 195), Institute of Biotechnology and Genetic Engineering (IBGE), Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh Sohana Jui (141), Department of Genetics and Plant Breeding, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh Snehashis Karmakar (1, 95), Department of Plant Physiology, Faculty of Agriculture, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur; School of Agriculture, Seacom Skills University, Kendradangal, Birbhum, West Bengal, India Amit Kesarwani (339), Department of Agronomy, G.B. Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India Ayesha Azad Keya (15), Department of Genetics and Plant Breeding, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh Mohd. Kamran Khan (141, 273, 329, 393, 413), Department of Soil Science and Plant Nutrition, Faculty of Agriculture, Selcuk University, Konya, Turkey Manoj Kumar (259), Department of Plant Breeding and Genetics, Agricultural Research Station, Agriculture University Kota, Kota, Rajasthan, India Mukesh Kumar (339), Department of Agronomy, Dr. Rajendra Prasad Central Agricultural University, Pusa, Bihar, India Pawan Kumar (259), Division of Crop Improvement, ICAR-Central Institute for Arid Horticulture, Bikaner, Rajasthan, India Anita Kumari (209), Department of Botany and Plant Physiology, Chaudhary Charan Singh Haryana Agricultural University, Hisar, Haryana, India

Contributors

xv

Nita Lakra (209), Department of Molecular Biology, Biotechnology and Bioinformatics, CCS Haryana Agricultural University, Hisar, India

Subhasis Mondal (131), Department of Plant Physiology, Faculty of Agriculture, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, West Bengal, India

Haoyu Li (67), College of Life Sciences, Qingdao University, Qingdao, China

Md. Mosfeq-Ul-Hasan (141), Controller Section of Examinations, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh

Xiaolan Li (375), Microbial Resources and Drug Development Key Laboratory of Guizhou Tertiary Institution, Life Sciences Institute, School of Preclinical Medicine, Zunyi Medical University, Zunyi, Guizhou Province, China Chengcheng Liao (375), Microbial Resources and Drug Development Key Laboratory of Guizhou Tertiary Institution, Life Sciences Institute, School of Preclinical Medicine, Zunyi Medical University, Zunyi, Guizhou Province, China Jianguo Liu (375), Microbial Resources and Drug Development Key Laboratory of Guizhou Tertiary Institution, Life Sciences Institute, School of Preclinical Medicine, ZunyiMedicalUniversity,Zunyi,GuizhouProvince,China Sagar Maitra (131, 339, 357), Department of Agronomy and Agroforestry, Centurion University of Technology and Management, Paralakhemundi, Odisha, India Sadia Majeed (393), Department of Agronomy, Faculty of Agriculture, The Islamia University of Bahawalpur, Bahawalpur, Pakistan Hina Ahmed Malik (393), Faculty of Agriculture, Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan Riffat Naseem Malik (313), Department of Environmental Sciences, Faculty of Biological Sciences, Environmental Health and Ecotoxicology Laboratory, Quaid-i-Azam University, Islamabad, Pakistan

Soumik Mukherjee (357), Department of Plant Pathology, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, West Bengal, India Renu Munjal (33, 209, 283), Department of Botany and Plant Physiology, Chaudhary Charan Singh Haryana Agricultural University, Hisar, Haryana, India Zarin Mushrat (15), Department of Genetics and Plant Breeding, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh Aneta Myskova (247), Department of Analytical Chemistry, University of Chemistry & Technology Prague, Prague, Czech Republic Sudhir Navathe (161), Genetics and Plant Breeding Group, Agharkar Research Institute, Pune, Maharashtra, India Manoj D. Oak (51, 161), Genetics and Plant Breeding Group, Agharkar Research Institute, Pune, Maharashtra; Savitribai Phule Pune University, Pune, India Apurba Pal (357), Horticulture College, Khuntpani, Birsa Agriculture University, Ranchi, Jharkhand, India Anamika Pandey (141, 273, 329, 393, 413), Department of Soil Science and Plant Nutrition, Faculty of Agriculture, Selcuk University, Konya, Turkey Himanshu Pandey (259), Department of Biotechnology, Dr. YSP UHF Nauni, Solan, Himachal Pradesh, India

Manorma (209), Department of Molecular Biology, Biotechnology and Bioinformatics, CCS Haryana Agricultural University, Hisar, India

Megha Panwar (259), Department of Plant Physiology, G.B. Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India

Mst. Salma Masuda (15, 329), Department of Genetics and Plant Breeding, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh

Ravindra Patil (51), Genetics and Plant Breeding Group, Agharkar Research Institute, Pune, Maharashtra; Savitribai Phule Pune University, Pune, India

Meenakshi (209), Department of Molecular Biology, Biotechnology and Bioinformatics, CCS Haryana Agricultural University, Hisar, India

Pravin Bhausaheb Pawar (161), Genetics and Plant Breeding Group, Agharkar Research Institute, Pune, Maharashtra, India

M.A. Baset Mia (179), Department of Crop Botany, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh

Nitesh Kumar Poddar (247), Department of Biosciences, Manipal University Jaipur, Jaipur, Rajasthan, India

Udit Nandan Mishra (259), Faculty of Agriculture, Sri University, Cuttack, Odisha, India

Biswajit Pramanick (339), Department of Agronomy, Dr. Rajendra Prasad Central Agricultural University, Pusa, Bihar, India

Saptarshi Mondal (357), Department of Crop and Soil Sciences, University of Georgia, Griffin, GA, United States

Sankar Pramanick (1), Department of Plant Physiology, Faculty of Agriculture, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, West Bengal, India

xvi

Contributors

Most. Maria Haque Prodhan (141), Department of Genetics and Plant Breeding, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh Xiaokang Qian (375), Zunyi City Rural Development Service Center, Zunyi, Guizhou Province, China Umar Masood Quraishi (313), Department of Plant Sciences, Quaid-i-Azam University, Islamabad, Pakistan Hanuman Ram (259), Division of Crop Improvement, ICAR-Central Institute for Arid Horticulture, Bikaner, Rajasthan, India Vineeta Rana (33), Department of Botany and Plant Physiology, Chaudhary Charan Singh Haryana Agricultural University, Hisar, Haryana, India Sudarshana Ranjan (259), Department of Plant Physiology, G.B. Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India Disna Ratnasekera (297), Department of Agricultural Biology, Faculty of Agriculture, University of Ruhuna, Kamburupitiya, Sri Lanka Reena (209), Department of Molecular Biology, Biotechnology and Bioinformatics, CCS Haryana Agricultural University, Hisar, India Mingjian Ren (375), College of Agriculture, College of Life Sciences, Guizhou University, Guiyang, Guizhou Province, China Qunli Ren (375), Microbial Resources and Drug Development Key Laboratory of Guizhou Tertiary Institution, Life Sciences Institute, School of Preclinical Medicine, Zunyi Medical University, Zunyi, Guizhou Province, China Disha Roy (15), Department of Genetics and Plant Breeding, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh Anjana Rustagi (413), Department of Botany, Gargi College, New Delhi, India Rahul Sadhukhan (1), MTTC & VTC, CAU (Imphal), Selesih, Mizoram, India Muhammad Saeed (313), Department of Environmental Sciences, Faculty of Biological Sciences, Environmental Health and Ecotoxicology Laboratory, Quaidi-Azam University, Islamabad, Pakistan Ajanta Sarker (15), Department of Genetics and Plant Breeding, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh Maksud Hasan Shah (95, 131), Department of Agronomy, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, Nadia, West Bengal, India

Shreya Sharma (247), Department of Biotechnology, Invertis University, Bareilly, Uttar Pradesh, India Aditya Pratap Singh (95), Research Scholar, Department of Genetics and Plant Breeding, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, West Bengal, India Sanjay Kumar Singh (161), Division of Genetics, ICARIndian Agricultural Research Institute, Pusa, New Delhi, India Rajesh Kumar Singhal (259, 413), Division of Crop Improvement, ICAR-Indian Grassland and Fodder Research Institute, Jhansi, Uttar Pradesh, India Aarti Soni (209), Department of Botany and Plant Physiology, Chaudhary Charan Singh Haryana Agricultural University, Hisar, Haryana, India Pooja Swami (33, 283), Department of Botany and Plant Physiology, Chaudhary Charan Singh Haryana Agricultural University, Hisar, Haryana, India Neveen B. Talaat (111), Department of Plant Physiology, Faculty of Agriculture, Cairo University, Giza, Egypt Ali Topal (329), Department of Field Crops, Faculty of Agriculture, Selcuk University, Konya, Turkey Mst. Tanjina Shahanaj Turin (15, 329), Department of Genetics and Plant Breeding, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh Suhasini Venkatesan (51), Genetics and Plant Breeding Group, Agharkar Research Institute, Pune, Maharashtra; Savitribai Phule Pune University, Pune, India Miao Wang (375), Microbial Resources and Drug Development Key Laboratory of Guizhou Tertiary Institution, Life Sciences Institute, School of Preclinical Medicine, Zunyi Medical University, Zunyi, Guizhou Province, China Qian Wang (375), Microbial Resources and Drug Development Key Laboratory of Guizhou Tertiary Institution, Life Sciences Institute, School of Preclinical Medicine, Zunyi Medical University, Zunyi, Guizhou Province, China Xiaoyu Wang (67), College of Life Sciences, Qingdao University, Qingdao, China Devvart Yadav (33), Department of Genetics and Plant Breeding, CCS Haryana Agricultural University, Hisar, Haryana, India Shengwei Yang (375), Zunyi Agricultural Science and Technology Research Institute, Zunyi, Guizhou Province, China Zige Yang (67), College of Life Sciences, Qingdao University, Qingdao, China

Contributors

xvii

K.J. Yashavanthakumar (161), Genetics and Plant Breeding Group, Agharkar Research Institute, Pune, Maharashtra, India

University of Agricultural Sciences and Technology of Kashmir, Shalimar, Srinagar, Jammu and Kashmir, India

Hamza Yousaf (413), Faculty of Agriculture, Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan

Mingsheng Zhang (375), College of Agriculture, College of Life Sciences, Guizhou University, Guiyang, Guizhou Province, China

Sajad Majeed Zargar (393), Proteomics Laboratory, Division of Plant Biotechnology, Sher-e-Kashmir

Pengfei Zhi (67), College of Life Sciences, Qingdao University, Qingdao, China

Chapter 1

Wheat and abiotic stress challenges: An overview Debjani Duttaa,b, Snehashis Karmakara,b,⁎, Akbar Hossainc, Rahul Sadhukhand, Kousik Attaa, and Sankar Pramanicka a

Department of Plant Physiology, Faculty of Agriculture, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, West Bengal, India, b School of Agriculture,

Seacom Skills University, Kendradangal, Birbhum, West Bengal, India, c Division of Soil Science, Bangladesh Wheat and Maize Research Institute, Nashipur, Dinajpur, Bangladesh, d MTTC & VTC, CAU (Imphal), Selesih, Mizoram, India *

Corresponding author. e-mail: [email protected]

Introduction Wheat (Triticum aestivum L.), the second most important staple crop in India as well as in the world, delivers nutritional and dietary security to billions of the world population. The global wheat production for the past few years has reached new heights with significant increase in production, area, and productivity. Over the last four decades, the wheat program in India was very energetic, but it lacks satisfaction and the agenda requires to be more reactive toward the new evolving challenges imposed by abiotic stresses. Besides the increasing global population, the challenges imparted by several abiotic stresses have been creating a great havoc for worldwide wheat production and thus causing obstacles to meet the global food demand. The susceptibility of wheat crops to abiotic stresses is obvious from a considerable dip in wheat production to 86.53 M tonnes during 2014–15 owing to uneven rainfall, regarding the higher production of 95.85 M tonnes attained for the duration of the previous 2013–14 crop season. On the other hand, during the period of the next 2015–16 crop year, India produced 93.50 M tonnes of wheat grain (Tiwari et al., 2017). Though during the current years, the speed of genetic improvement in productivity does not show much magnificence like in the past, the under-trial cultivars are being designed to support the demand for greater yield alongside the challenges enforced by a number of abiotic stresses, for instance, water stress, temperature stress, heavy metal stress, and salinity stress. The production of wheat is mostly affected by water stresses. There are mainly two types of water stress, i.e., drought stress and waterlogging stress. Among these, drought stress is most responsible for significant yield loss in wheat and it may occur throughout the crop-growing season. Significant yield loss occurs when wheat is exposed to drought stress during the heading stage, but it shows the highest yield loss when stress exposure occurs during the reproductive stages (Tiwari et al., 2015). Early-season drought at seedling stages in wheat decreases plant numbers/unit area and number of tillers/plants, whereas mid-season (CRI to ear emergence) water-deficit stress reduces total biomass of crop, effective tiller number as well as gain number/spike, and late-season (anthesis to physiological maturity) or terminal water-deficit stress enhances the oxidative damages (Abid et al., 2018; Sattar et al., 2020), thus lessening the current photosynthesis, pollen fertility, and grain yield (Tiwari et al., 2015). If no irrigation has been given to wheat crops, the yield losses due to water stress of some wheat varieties in Central India range from 11.6% to 43.6% (Tiwari et al., 2015). Waterlogging is the condition when the water remains stagnant on the surface of the land for a prolonged period or the fraction of available water in the surface layer of soil is, however, 20% greater than the field capacity (FC) of the soil. The crop production in almost 4.5 M ha cultivated irrigated land in Indo-Gangetic regions is adversely affected by the waterlogged condition (CSSRI, 1997). Mainly where the soil is sodic and groundwater level is high, as a result of increased natural calamities like storms and heavy rainfalls, waterlogging is more prominent, thus causing serious problems in worldwide crop production. Though the optimum temperature for proper growth and development of crops varies with the prevalent agro-climatic zones where the crop is cultivated, the most optimum temperature considered for wheat crops is 21–24°C. In India, more or less total wheat cultivated area experiences heat stress. Though throughout the crop season, the peninsular and central parts experience heat stress, major parts of the northeastern and northwestern steppes experience terminal heat stress. That is why, the farmers in these regions follow the trend of early sowing of wheat for taking benefit of residual moisture content that helps provide tolerance of wheat cultivars to both terminal and early heat stresses (Misra and Varghese, 2012). The rise Abiotic Stresses in Wheat. https://doi.org/10.1016/B978-0-323-95368-9.00006-0 Copyright © 2023 Elsevier Inc. All rights reserved.

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2 Abiotic stresses in wheat

of temperature above 30°C during the crop growth cycle often severely affects grain formation and grain filling stages (Rane et al., 2007). Under controlled condition, above 15°C temperature, a 1°C increase in temperature can reduce grain yield per spike in wheat up to 3%–4% (Wardlaw et al., 1989). Similarly, very high-temperature exposure of 4 days only can cause significant yield reduction of up to 23% (Stone and Nicolas, 1994). In view of the present situations and future forecasts on global warming, the effect of heat exposure is expected to take on much greater proportion. As said by Pachauri et al. (2014) in the 5th evaluation report of the Inter-Governmental Panel on Climate Change, the ocean surface and worldwide average collective land temperature record display a warming of 0.85°C temperature (0.65–1.06) from 1880 to 2012, and temperature is expected to increase over the 21st century. In addition, in northern India and northern hilly zones due to sudden fall in temperature, wheat crop also suffers damage due to chilling and/or freezing injuries. However, in these regions, the yield losses due to these stresses are not that much devastating than that of heat stress. Nowadays, heavy metal (metalloids) toxicity, due to the presence of heavy metals (HMs) in organic fertilizer, became more prominent in agricultural lands, and as a result, it hampers proper growth and development of crops, thus leading to potential yield losses. Likewise, due to excess accumulation of HMs in the edible parts of wheat plants, it causes severe health hazards in human beings through multiple pathways via soil-plant system (Zhang et al., 2018). After being taken up by plant roots, metalloids are transported to the aerial parts of plants through xylem loading (Page et al., 2006), which in turn is aided by different transport pathways and takes place through apoplastic or symplastic pathways (Pourrut et al., 2011). Inhibition of proper growth of plants due to HM accumulation occurs because of the reduced chlorophyll content as well as photosynthetic rate (Sarwar et al., 2015). Several studies have reported that plants grown in HM intoxicated environments exhibit alteration of metabolism (Khan et al., 2016), reduction in growth (Imtiaz et al., 2016; Karmakar and Prakash, 2019), production of lower biomass (Dutta et al., 2021a, 2021b; Dutta and Pal, 2019; Zhang et al., 2013), accumulation of HMs as well as oxidative damages (Dutta et al., 2017, 2021a,b; Karmakar et al., 2021). In addition, higher level of HMs’ exposure in the environment is the cause of serious concern for human health (Leveque et al., 2014) as these could easily enter the food chain and accumulate in our bodies (Niu et al., 2013), thus resulting in weakened immunity, respiratory disorders, and harmful lesions in several organs (Tong et al., 2000). Salinity stress was reported to adversely affect more than 6% (800 M ha) of land worldwide, and it is a serious constraint in wheat cultivation all over the world (Wang and Xia, 2018). In India, there is almost 6.73 M ha of salt-affected land, among which 2.96 M ha and 3.77 M ha lands are covered by saline and sodic soils, respectively. In Indo-Gangetic regions, almost 2.5 M ha of land is composed of sodic soils, whereas 2.2 M ha of land is adversely affected by seepage water from irrigation canals (CSSRI, 1997). The soil affected by either salinity or alkalinity or sodicity can considerably reduce crop yield. Wheat plants when exposed to salt and waterlogged stress in combination have shown significant reductions in yield attributes, for example, number of grains in spike, spike length, number of spikelets, and grain yield, and the severity increased in compacted soil. In extreme salinity, because of the hyperosmotic pressure, loss of water instead of absorption of water occurs in root cells. As a result of water deficit due to salinity, it hampers biological, physiological, as well as biochemical status, gene expression patterns, and cell signaling cascades of plant cells, thus causing inhibition of cell elongation and wilting and ultimately leading to cell death (Machado and Serralheiro, 2017). Saline soil is rich in soluble salt contents (especially NaCl), which causes potential toxicity in plants by significant elevation of Na+, Cl concentrations in cells. These ions are responsible for alteration in many enzymatic activities and many cellular functions like photosynthesis (Cheeseman, 2013; Tavakkoli et al., 2010). Besides, as they show a shared transportation system and their similar physiochemical functions, K+ ions in soils face competition for uptake by Na+ ions (Schachtman and Liu, 1999), and consequently, K+ deficiency occurs in plants (Ball et al., 1987; Botella et al., 1997). Thus, the induced K+ deficiency hinders plant growth since it performs a key role in maintaining enzyme activities, membrane potentials, and cell turgor pressure. Besides these, UV-B exposure is also responsible for creating a harmful impact on wheat cultivation. It interferes in many physio-biochemical processes, reduces photosynthetic rates and stomatal conductance, diverts carbon allocation, and creates oxidative stress in plants. Through this chapter, we are going to highlight the challenging effects that are caused by some abiotic stresses in wheat.

Impact of water stress on wheat Water stress is mainly deciphered as either waterlogging stress or water-deficit (drought) stress. Both of these are responsible for potential yield reduction in wheat.

Impact of waterlogging stress on wheat Wheat cultivars are often exposed to waterlogged condition due to heavy precipitation, level topography, and insufficient soil drainage. Waterlogging condition is one of the growth and production limiting factors of wheat (Collaku and Harrison, 2002).

Wheat and abiotic stress challenges: An overview Chapter

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3

O2 deficiency caused by waterlogged condition decreased root and shoot growth, biomass accumulation, and yield. It can affect water absorption and hormonal relations in root and shoot (Huang et al., 1994) and reduce ion uptake and transport through the root, which causes nutrient deficiency in wheat (Trought and Drew, 1980a,b; Huang et al., 1995). Huang et al. (1994) reported that waterlogging stress causes nitrogen deficiency in wheat by triggering denitrification and leaching. It also promotes the accumulation of toxic elements in soil and plant body. Musgrave (1994) stated that waterlogging stress reduces winter wheat grain yield by 20%–50% (Belford, 1981; Musgrave and Ding, 1998). Collaku and Harrison (2002) reported that under waterlogging situation, wheat kernels per ear and tiller number were decreased by 20% and 41%, respectively. Waterlogging stress during the first months of growth reduces the yield of wheat cultivars (Musgrave, 1994). Luxomore et al. (1973) found that waterlogging stress decreases leaf elongation, number of kernels, and finally grain yield. Waterlogged condition may reduce the yield of wheat cultivars by reducing the rate of photosynthesis (Huang et al., 1994). Musgrave (1994) found that waterlogging reduces wheat kernel weight and number. It also decreases flag leaf conductance and photosynthesis.

Impact of drought stress on wheat Water deficit is a worldwide environmental problem toward crop production, and climate change is making this condition more crucial (Anjum et al., 2011). Plants generally adopt drought condition by three mechanisms, i.e., drought escape, drought avoidance, and drought tolerance. Wheat crop responses to drought to its growth stages, metabolism and grain yield potential (Ali, 2019). Seed germination, heading, flowering, and grain development stages are critical stages of the drought stage (Waraich and Ahmad, 2010; Hammad and Ali, 2014; Akram et al., 2014). Esfandiari et al. (2008) reported that drought stress causes a reduction in wheat shoot elongation of seedling. The restriction in leaf area, stem elongation, and shoot dry matter in wheat cultivars grown under medium drought stress condition were recorded at 14.50%, 17.35% and 18.54%, respectively, whereas those parameters valued 32.34%, 29.53%, and 43.90% reduction under severe drought condition, respectively, compared with nonstress condition (Hammad and Ali, 2014). Waraich and Ahmad (2010) stated that stunted leaf expansion and internode elongation of stem generally occur in wheat under drought stress condition due to restricted cell expansion. Water scarcity condition lowers tissue water content and reduces cell turgor pressure. In this way, it finally inhibits cell division, cell enlargement, growth, and dry matter production in wheat (Ali, 2019). Under water-deficit condition, stomatal closure occurs and inhibited CO2 uptake. Reduced stomatal conductance and photosynthesis rate comprise some signaling pathways such as ABA accumulation in wheat (Le et al., 2017). Hammad and Ali (2014) found significant reduction in both the chlorophyll and carotenoid content by rising drought stress compared to well-watered condition. Reduction in net photosynthesis under drought stress is related to interruption in various physiological and biochemical processes due to oxidation of lipid molecules present in chloroplast and structural changes in protein and pigment molecules (Fig. 1). Drought-induced reduction in photochemical reaction in chloroplast also reduces chlorophyll accumulation in wheat (Marcinska et al., 2013). Wheat cultivars raised under severe drought stress, followed by medium drought condition, showed highest remarkable values of osmotic pressure and membrane integrity compared to nonstress condition. There was a slight decrease in relative water content with increasing drought stress. Under severe drought condition, relative water content decreased up to 15.15% in wheat (Hammad and Ali, 2014). According to Waraich and Ahmad (2010), relative water content is a principal indicator of leaf water stress and this parameter is directly associated with soil water status. Under drought stress, wheat cultivars can cut down the harmful effects by improving osmotic adjustment through solute accumulation in cells. Cell permeability also

FIG. 1 A diagrammatic representation of abiotic stress-induced physiological responses of wheat with respect to crop yield and productivity (abbreviations: RNS, reactive nitrogen species; ROS, reactive oxygen species; RWC, relative water content; UV-B, ultraviolet B).

4 Abiotic stresses in wheat

increased under drought stress (Iqbal, 2009). Yang et al. (2010) reported that under drought condition, due to upregulation in expressions of many genes, the metabolism of various biomolecules such as hormones, enzymes, carbohydrates, and amino acids is influenced. Drought stress remarkably affected total soluble sugar, total carbohydrate, total amino acid, and total phenolic compounds. In drought-affected wheat plants, the lowest values of total carbohydrate and total amino acids were recorded, whereas the highest values of total phenols and total soluble sugar were noted down in nonstress plants (Hammad and Ali, 2014). Solute loss from stomatal guard cells under drought condition induces stomatal closure in wheat (Zhang et al., 2009). Ahmed et al. (2017) found a gentle rise in proline content in wheat plants under drought condition and proline accumulation promoted drought tolerance. Proline acts as a stabilizer of subcellular molecular structures besides its function as an osmolyte (Rampino et al., 2006; Alaei and Moosavi-Movahedi, 2020). Hammad and Ali (2014) reported that drought stress severely reduced N, P, and K content and their uptake in leaves compared to normal condition. Hammad and Ali (2014) reported that under water-deficit condition, the activity of many enzymes such as nitrate reductase (NR), peroxidase (POD), and catalase (CAT) was suppressed and maximum reduction was observed under severe drought condition during booting and grain development stages of wheat. Drought stress promotes a considerable rise in ABA content, whereas it reduces GA and IAA content in wheat leaves (Baranwal et al., 2017). Delayed irrigation during the crown root initiation stage reduced the yield of wheat cultivars up to 27% (Hunsigi and Krishna, 1998). Drought stress at 3 weeks after pollination cannot affect the number of grains per spike, but it can reduce grain weight. It indicates that water deficit restricts the rate of photosynthesis and translocation of photosynthates in spikes and interrupts the normal growth of wheat grain (Nakhforoosh et al., 2014). Hammad and Ali (2014) reported that increasing water scarcity reduces wheat grain yield that valued 14.63% and 41.37% during medium and severe water deficit, respectively, compared to nonstress condition.

Impact of temperature stress on wheat Both cold stress and high-temperature stress have a serious impact on wheat crops. Here, we are going to discuss the impact of both stresses on wheat.

Impact of cold stress on wheat Chilling temperatures have a serious effect on crop growth, quality, yield, and geographical distribution ( Jin and Kim, 2013). Two major factors that affect the degree of plant tissue injury under chilling stress are cold acclimation (occurs >0°C) and tissue freezing (occurs 500 ppm), maize photosynthesis may be accelerated. Maize growth is unaffected if the minimum temperature is less than 25°C and the maximum temperature is greater than 35°C. Speed breeding’s main goal is to shorten the breeding cycle by encouraging vegetative and flowering stages. Light, day length by extending photoperiod, temperature, and humidity are the primary changing factors. Temperature has a large influence on the rate of plant development, so raising the temperature to accumulate desired growing degree days can shorten the generation time even more (GDD). It may, however, cause stress and impair plant performance. As a result, at appropriate growth stages, a higher temperature can be applied. The maize crop is temperature sensitive, as large yield

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losses were observed whenever the minimum temperature was high at night. As a result, Hickey et al. (2019) proposed that a high temperature be used during vegetative growth and a low temperature be used during reproductive stages to ensure proper grain development. Another crucial component is synchronous flowering across genotypes, which is desirable for cross-breeding.

Pearl millet Pearl millet [Pennisetum glaucum (L.) R. Br.] is an important nutricereal crop of the arid and semiarid regions of the Indian subcontinent and sub-Saharan Africa grown under the most adverse agroclimatic conditions where other crops like sorghum and maize fail to produce economic yields. In India, pearl millet is generally grown as a rainy season (June–October months) crop with the onset of monsoon rains in most of the pearl millet growing regions of India. However, it is grown as a summer (January–April) crop in some parts of India (Gujarat, Maharashtra, Telangana, Karnataka, and Tamil Nadu). As far as research crop is concerned, research institutes located in the northwestern parts of India take only one crop during the rainy season but in peninsular India, locations like Hyderabad and other places of South India, 3–4 crops can be easily taken. Therefore, there is a distinct natural advantage of undertaking research in these places where rapid generation advances can be achieved in natural field conditions. In pearl millet, this is the shuttle breeding as also done in the case of wheat in Mexico by CIMMYT. Research institutes in North India such as CCS HAU, Hisar, or those in Rajasthan state take an additional off-season (January–April months) crop in Hyderabad (Telangana state), thereby reducing the time of the breeding cycle by 50%. For example, the seed of hybrids selected during the rainy season in North Indian locations could be multiplied during the off-season and then can be tested in multilocations in northwest India in the ensuing rainy season (June to October months) under the All India Coordinated Research Project trials. Lack of this would lead to a wait of a full 1 year to achieve this step. Another advantage of the off-season crop is that fresh crosses (F1s) made in the rainy season are selfed to produce the F2s during the off-season and these could then be evaluated in the representative growing environments of northwestern India in the ensuing rainy season. The COVID situation for the last couple of years has had a severe impact on global activities including the traditional breeding process. Pearl millet breeding has also seen a setback for those researchers located in North India as it was not possible to take the off-season crop in South India due to the corona situation as only one crop could be taken in a year instead of two crops. Although enormous progress has been made in the genetic improvement of pearl millet in India during the last several decades, this new challenge requires a new approach. To mitigate such COVID-like situations, it is desirable to have rapid generation advance or speed breeding facility in a hybrid crop-like pearl millet. As we know speed breeding protocols have been developed now for many crops, a lot of information is available in pearl millet that can help in standardizing the rapid generation advance protocols in this crop as well. Some of the important points that merit attention are discussed here, particularly temperature and photoperiod requirements.

Temperature For rapid growth, pearl millet necessitates a high temperature. Thermal requirements range from 10°C to 45°C, with an optimum temperature of 33–34°C (Arnold, 1959). The effects of temperature on pearl millet growth and development are well documented (Ong and Monteith, 1985; Squire et al., 1984). According to Ong and Monteith (1985), the growth rate is proportional to the solar radiation intercepted per day, while the developmental rate is proportional to the accumulation of degree days above a base temperature of 10°C. In northeast Mexico, Maiti and Soto (1990) found significant genetic variation in growth stages (GS1, GS2, and GS3), thermal time in the respective growth stages, days to flowering, and yield components under different conditions (sowing dates).

Photoperiod The pearl millet plant is primarily a quantitative short-day plant (Burton, 1965; Begg and Burton, 1971). Under a 12-h photoperiod, the plant flowers early, but a longer photoperiod (14–16 h) may affect phenology and delay flowering. One class of materials, known as maiwa and sanio, will always remain vegetative in the presence of longer days. These are known as obligate photoperiod-sensitive types. Flowering is greatly delayed (10–30 days) under long days in other groups of materials, known as gero and souna in West African countries. These are known as facultative photoperiodsensitive species. The oasis pearl millets (Djanet, Faya, and Ligui) from West and North Africa, as well as desert types from Rajasthan and Gujarat, are the least sensitive to longer photoperiods and can be referred to as day-neutral types

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TABLE 1 Speed breeding protocol in major crops summarized. Photoperiodic response

Generation time in field and greenhouse (days)

Generation time under speed breeding (days)

Wheat (Triticum aestivum)

Long day

113

60

Early seed harvest, 22-h light cycle, 22°C day/17°C night, and high-intensity PAR (Watson et al., 2018; Ghosh et al., 2018)

Maize (Zea mays)

Short day

–

–

–

Rice (Oryza sativa)

Short day

113

95–105

Rapid generation in the field with 40 cm3 soil/plant (Collard et al., 2017)

Barley (Hordeum vulgare)

Long day

110

63

22 h of light, 22°C day/17°C night, high-intensity PAR, 22°C day/17°C night, early seed harvest. Watson et al. (2018) and Ghosh et al. (2018) are two examples of this

Pearl millet (Pennisetum glaucum)

Facultative or obligate short day

85–90

–

Pearl millet has a faster growth rate at 38°C than at 31°C (Ashraf and Hafeez, 2004)

Crop

Protocol

(Kumar and Rao, 1987). The genetic stocks (Hanna and Burton, 1985) and an extra-early maturing photoperiod-insensitive B-composite are the only sources of photoperiod-insensitive types (Rai et al., 1998). Temperature and photoperiod can be used to manipulate the time required for flowering and inflorescence growth. High day and night temperatures, long photoperiods (16 h), and high light intensity promote growth and delay flowering (Burton, 1965). Carberry and Campbell (1985) discovered that the grain yield of pearl millet plants was less affected by the photoperiod when the plant population was high. When the photoperiod was extended at a low population, the yield was reduced by up to 35% due to a lower contribution from tillers. The photoperiod had no effect on the total number of tillers, but it reduced the number of productive tillers by 38% when the photoperiod was extended. Under a long photoperiod, grain number/tiller decreases, but this is partially offset by a positive effect on seed weight. McCloud and Alexander (1959) estimated net photosynthesis in a potted millet plant in a growth chamber under 5000 foot candles of light. They found that the net photosynthetic rates rose rapidly as plant density increased from ¾ to 2 plants per 900 cm2, but above that density, the net photosynthetic rate fell sharply to less than that for the lowest density, probably due to the lowered effective leaf area (Table 1).

Speed breeding capsules Plant research typically necessitates the use of controlled environment cabinets and glasshouses. In many crop breeding applications, this can be a considerable impediment to using speed breeding. Containers suitable for commercial-scale agricultural production are manufactured by a few indoor farming enterprises. The main goal of these efforts is to grow crops in any location, at any time of year, closer to the point of consumption, while utilizing 99% less land and other resources than traditional crops. Capsules may be sent to any location on the planet as long as there is enough water and electricity. Speed breeding capsules, meanwhile, can be made from reused refrigerated shipping containers that have been installed with temperature and light control mechanisms, watering systems, and greenhouse benches. Because refrigerated bins are protected and have inserted surfaces with drainage openings on both sides, tall plants that may be grown directly on the floor do not require greenhouse benches. The capsule’s adaptability is increased by the use of adjustable height LED lights, which allow it to fit plants of various heights while adjusting light intensity at the canopy level. The heat from the lights can be vented straight through the container’s walls in warm areas, but the heat produced by the lights can be kept in cooler climes to help with heating. The majority of the electricity generation would ideally come from a connected solar power system. A capsule like this would be significantly less expensive than the hydroponic system mentioned earlier, and it could be made to specs anywhere in the world and distributed to local breeding program. Local breeders will be able to apply and customize the

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procedures, thanks to the deployment of speed breeding capsules, giving them a stake in the infrastructure and their speed breeding applications, which is crucial for long-term sustainability and development.

Centers for speed breeding Establishing regional or crop group-focused centers, engaging with existing partners with speed breeding facilities to simply provide access to the speed breeding approach, would be an alternative way of introducing speed breeding programs. The main objective of the speed breeding centers would be to train scientists for speed breeding and provide services like trait integration and other breeding protocols. Trait integration, in combination with other cutting-edge breeding methods, would hasten trait transmission or stack into desired crop genetics. Large-scale breeding facilities (greenhouses and controlled environment rooms) would be built with low-cost components (such as LED lighting and solar electricity) and could handle a wide range of crops. Institutions that provide genotyping services, do ongoing crop breeding and research, and are equipped, co-located, or collaborate closely with them would be good hosting partners for the centers. This would help with phytosanitary issues including plant quarantine and other seed and plant material transport challenges.

Speed breeding limitations When plants are subjected to extended photoperiods, their responses can vary greatly. Because the critical day length is frequently exceeded in long-day plants, the days to flowering are frequently accelerated under a longer photoperiod. This is also true for photoperiod-independent day-neutral plants. Short-day (SD) plants, on the other hand, require a photoperiod that is less than the critical day length in order to flower, which may be incompatible with speed breeding conditions. Some crops, such as winter wheat, require vernalization, which results in a condition similar to the one described earlier. To start flowering, young plants must be chilled for a few weeks. After the vernalization criterion has been met, exposing winter wheat plants to extended photoperiod is likely to accelerate growth. Overall, the “speed breeding formula” is more straightforward and easier to implement for long-day and day-neutral species that do not require vernalization. The speed breeding operations are carried out in a controlled, artificial environment that is vastly different from the field where agricultural production will be carried out in the future. Although this is appropriate for many actions, such as crossing, SSD, and screening for a few simple traits, other activities, such as adaptation selection in the target environment, must still be carried out in the field.

Challenges One of the major challenges with speed breeding is maintaining precise control parameters such as temperature, light, and humidity, as well as disease or insect infestations in the crops developed through speed breeding. Second, when compared to conventional breeding, speed breeding is much more costly, and the size and cost of running a suitable facility frequently restrict the number of crossings and population sizes under consideration. The barrier can be overcome by concentrating on the plant which is most likely to contribute to the goal of breeding and combining speed breeding with the current breeding approaches such as genomic selection, transgenic development, and CRISPR-based genome editing (Li et al., 2018). Speed breeding necessitates infrastructure to maintain the controlled environment as well as specialized equipment to perform precise trait selection, both of which are costly. Furthermore, institutional support is scarce in public plant breeding and many developing countries, limiting the speed with which breeding can adapt (Byerlee and Fischer, 2002). Collaborations between national and regional groups may be able to help with the problem’s resolution. Using energy-efficient light sources such as LED and air conditioners, as well as solar power panel, to supplement the national grid’s electricity and gas (Ghosh et al., 2018), as well as new innovative and local equipment outfitted with solar-powered temperature and humidity control panels, could help reduce the cost of speed breeding. Water and electricity supply reliability is also a major issue in the majority of developing countries. Using existing technologies, a compact speed breeding equipped kit with fixed temperature and LED light control panels powered by a solar system with battery backup could be built. One alternative would be to adapt speed breeding concepts to semicontrolled field-based setups, in which high-density planting can be maintained while vast populations can be produced at a cheaper cost. If these facilities are not already in place, the cost of building a glasshouse or purchasing a growth chamber with enough supplemental lighting and temperature control is significant. However, depending on the study’s or breeding program’s funding, the benefits may exceed the disadvantages.

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Conclusion In addition, combining speed breeding with traditional, marker-assisted selection, and genetic engineering breeding procedures can help improve the choice of elite genotypes and lines with pioneering features, like improved yield and nutritional quality, as well as biotic and abiotic stress tolerance. However, in many developing countries, the adoption of speed breeding is hampered by a scarcity of trained crop breeders and technicians, as well as a shortage of essential infrastructure and consistent electricity and water supply. Plant breeding has resulted in high-yielding crops, allowing human population growth to continue for the past 100 years. The development of next-generation types through speed breeding will meet the demand for population expansion in the next decades. Global food security has become a major concern as the world’s population grows and the climate changes. Several major crops are currently improving at a rate that is insufficient to meet the demand of the future. This steady progress could be attributed in part to crop plants’ long generation times, which have been reduced by speed breeding. Speed breeding can speed up the production of cultivars with good performance based on market features by minimizing the usage of space, resources, and time spent on crop variety selection and advancement. Plant breeders can now offer improved crop types more quickly, thanks to this technology. The use of speed breeding in conjunction with traditional, marker-assisted selection, and genetic engineering breeding procedures can help in the selection of elite genotypes and lines with characteristics such as enhanced yield and nutritional quality, as well as biotic and abiotic stress tolerance. However, the adoption of speed breeding is hampered in many developing countries due to the lack of trained crop breeders and technicians, as well as a lack of essential infrastructure and a consistent supply of electricity and water. Plant breeding has produced high-yielding crops, allowing human population growth to continue for the past century. In the coming decades, the development of next-generation types through speed breeding will meet the demand for population expansion.

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Richard, C.A., Hickey, L.T., Fletcher, S., Jennings, R., Chenu, K., Christopher, J.T., 2015. High-throughput phenotyping of seminal root traits in wheat. Plant Methods 11 (1), 1–11. Samineni, S., Sen, M., Sajja, S.B., Gaur, P.M., 2020. Rapid generation advance (RGA) in chickpea to produce up to seven generations per year and enable speed breeding. Crop J. 8 (1), 164–169. Singh, V., Nguyen, C.T., van Oosterom, E.J., Chapman, S.C., Jordan, D.R., Hammer, G.L., 2015. Sorghum genotypes differ in high temperature responses for seed set. Field Crop Res. 171, 32–40.

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Squire, G.R., Marshall, B., Terry, A.C., Monteith, J.L., 1984. Response to temperature in a stand of pearl millet: VI. Light interception and dry matter production. J. Exp. Bot. 35 (4), 599–610. Steuernagel, B., Periyannan, S.K., Herna´ndez-Pinzo´n, I., Witek, K., Rouse, M.N., Yu, G., et al., 2016. Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. Nat. Biotechnol. 34 (6), 652–655. Stutte, G.W., 2015. Commercial transition to LEDs: a pathway to high-value products. HortScience 50 (9), 1297–1300. Vince-Prue, D., Kendrick, R.E., Kronenberg, G.H.M., 1994. Photomorphogenesis in Plants. Kluwer Academic Publishers, Dordrecht. Watson, A., Ghosh, S., Williams, M.J., Cuddy, W.S., Simmonds, J., Rey, M.D., et al., 2018. Speed breeding is a powerful tool to accelerate crop research and breeding. Nat. Plants 4 (1), 23–29. Wiebbecke, C.E., Graham, M.A., Cianzio, S.R., Palmer, R.G., 2012. Day temperature influences the male-sterile locus ms9 in soybean. Crop Sci. 52 (4), 1503–1510. Yan, L., Loukoianov, A., Blechl, A., Tranquilli, G., Ramakrishna, W., SanMiguel, P., Dubcovsky, J., 2004. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303 (5664), 1640–1644. Yang, L., Wang, D., Xu, Y., Zhao, H., Wang, L., Cao, X., et al., 2017. A new resistance gene against potato late blight originating from Solanum pinnatisectum located on potato chromosome 7. Front. Plant Sci. 8, 1729. Zhang, Z., Mao, Y., Ha, S., Liu, W., Botella, J.R., Zhu, J.K., 2016. A multiplex CRISPR/Cas9 platform for fast and efficient editing of multiple genes in Arabidopsis. Plant Cell Rep. 35 (7), 1519–1533. Zheng, Z., Wang, H.B., Chen, G.D., Yan, G.J., Liu, C.J., 2013. A procedure allowing up to eight generations of wheat and nine generations of barley per annum. Euphytica 191 (2), 311–316.

Further reading Dinglasan, E., Godwin, I.D., Mortlock, M.Y., Hickey, L.T., 2016. Resistance to yellow spot in wheat grown under accelerated growth conditions. Euphytica 209 (3), 693–707. Fischer, R.A., Rebetzke, G.J., 2018. Indirect selection for potential yield in early-generation, spaced plantings of wheat and other small-grain cereals: a review. Crop Pasture Sci. 69 (5), 439–459. Hickey, L.T., Dieters, M.J., DeLacy, I.H., Kravchuk, O.Y., Mares, D.J., Banks, P.M., 2009. Grain dormancy in fixed lines of white-grained wheat (Triticum aestivum L.) grown under controlled environmental conditions. Euphytica 168 (3), 303–310. Peters, G.P., Andrew, R.M., Boden, T., Canadell, J.G., Ciais, P., Le Quere, C., Wilson, C., 2013. The challenge to keep global warming below 2 C. Nat. Clim. Chang. 3 (1), 4–6.

Chapter 4

Marker-assisted breeding for abiotic stress tolerance in wheat crop Suhasini Venkatesana,b, Ravindra Patila,b, and Manoj D. Oaka,b,⁎ a *

Genetics and Plant Breeding Group, Agharkar Research Institute, Pune, Maharashtra, India, b Savitribai Phule Pune University, Pune, India Corresponding author. e-mail: [email protected]

Introduction About 40% of the world’s population depends on wheat (Triticum spp.) as the primary source of nutrients. Wheat was domesticated about 8000 years back and has been the staple food for civilizations in Europe, West Asia, and North Africa. Wheat occupies a central place in human nutrition, providing 20% of the daily protein and food calories. It is the second most important crop in terms of food security. Presently, wheat production estimates for the year 2020–21 is
775.1 million tonnes, and annual consumption is
757 million tonnes (https://www.fao.org/worldfoodsituation/csdb/en/ Accessed on September 15, 2021). Wheat production needs to achieve the target of
858 million tonnes in the next three decades to feed the global human population, which will reach
9.7 billion in 2050. Enhanced production systems with higher yield potential have resulted in a 1%–2% increase in the average yield on a global scale over the last 50 years. (https://www.wheatinitiative.org/accessed on September 15, 2021). Breeding approaches to increase wheat production need to address two main things; first, the impact of climate change, and second, shrinkage of arable land due to urbanization. International organizations such as International Maize and Wheat Improvement Centre (CIMMYT)-International Centre for Agricultural Research in Dry Areas (ICARDA), and The Organization for Economic Cooperation and Development (OECD)-Food and Agriculture Organization (FAO) have forecasted the reduction in wheat yield by 20%–30% due to challenges posed by abiotic stresses such as drought, high temperature, salinity/alkalinity, waterlogging, mineral deficiency, crop lodging, and preharvest sprouting (Hossain et al., 2021). In this chapter, we will discuss about the abiotic stresses, which pose a major threat to wheat production globally, and the strategies to mitigate abiotic stress using genetic resources, phenotyping protocols, markers linked with QTL/genes for abiotic stress tolerance, marker-assisted breeding, and genomic selection.

Wheat and abiotic stresses Stress can be considered a limiting factor that destroys the biomass and productivity of a crop. Abiotic stress can be defined as the influence of nonliving factors on the living organisms of the environment. Their effect on the environment is beyond the normal range which eventually affects the plant population. Physiological and biochemical alterations in the plants due to stress ultimately decrease production (here wheat yield). In wheat, drought, heat, and salinity stresses are more frequent and have led to tremendous yield loss. Severe drought conditions result from inconsistent or low rainfall, which reduces soil water availability to plants causing premature plant death; this causes 19.3%–50.4% of yield loss in wheat-growing regions of the world (Table 1). Intermittent droughts affect plant growth and development but are not usually lethal. Drought is known to affect all stages of crop growth. Drought at the early growth stage of wheat leads to poor seedling establishment and fewer tillers per unit area. However, a drought at the mid-stage of growth causes reduced dry matter production, effective tillers, and grains per plant. In Canada, wheat production has been reduced by 32% for 2021–22 compared to last year and 26% below the 5-year average (Foreign Agricultural Service/USDA August 2, 2021 Global Market Analysis). Climate change and increase in temperatures seriously affect wheat, making them more vulnerable in the near future. An increase in temperature may cause 14.7%–31.3% of yield losses in wheat depending upon the region. This becomes alarming when the rate of increase in global temperatures has accelerated. Exposure to heat reduces the germination percentage and photosynthetic efficiency, leading to yield loss. Abiotic Stresses in Wheat. https://doi.org/10.1016/B978-0-323-95368-9.00012-6 Copyright © 2023 Elsevier Inc. All rights reserved.

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Abiotic stresses in wheat

TABLE 1 Extent of yield losses in wheat due to various abiotic stresses. Abiotic stress

Area affected Million hectare

Yield losses

References

Heat stress

58.7

14.7%–31.3%

Kosina et al. (2007)

Drought

42.6

19.3%–50.4%

Kosina et al. (2007)

Water logging

10–15

22%–50%

Gupta et al. (1999), Mason et al. (2010), Singh et al. (2018)

Salt stress

10–11

10.1%–82.8%

Kosina et al. (2007), Oyiga et al. (2016)

Cold stress

15–16

1%

Kosina et al. (2007)

Thus, abiotic stress is one of the most concerning factors worldwide. Recognizing the importance of wheat and to meet the global target of 2050 wheat production needs to be increased by another 40%–50% (Sharma et al., 2021). The global Wheat Yield Consortium (WYC) is one such initiative that addresses one such issue (Parry et al., 2011). Research in the field of marker-assisted breeding for abiotic stress tolerance has gained significant importance for various crops including wheat.

Available genetic resources for abiotic stress tolerance in wheat Genetic resources provide important gene pools for the development of new varieties with improved characteristics. Repeated cycles of plant breeding, recurrent use of elite wheat lines, and selections of targeted phenotypes have resulted in the elimination of natural genetic variation in elite wheat varieties (van de Wouw et al., 2010). Abiotic constraints such as heat, drought, and salt stress are increasingly difficult to address genetically as insufficient diversity exists in the current gene pool. Due to changing climatic conditions, there is a need to manage genetic diversity in an innovative way to develop new germplasm, being able to cope with increased drought and heat stress. Restoring genetic variation using landraces and wild relatives of wheat is essential to achieve sustainable improvement in yield and abiotic stress tolerance in wheat (Dwivedi et al., 2016; Ullah et al., 2018). To address the challenge of improvement of genetic diversity with enhanced abiotic stress tolerance, synthetic hexaploid wheat derivatives were generated by crossing elite tetraploid durum wheat cultivars (T. turgidum, 2 n ¼ 4x ¼ 28, AABB) with diploid Aegilops tauschii (2 n ¼ 2x ¼ 14, DD). Synthetic wheat and their cross derivatives showed 24% higher yield and 57% more biomass and were 41% or more water-use efficient than their recurrent parents with the ability to maintain seed weight under drought/heat stress (Mujeeb-Kazi et al., 2009; Reynolds et al., 2007; Trethowan et al., 2005). In a combined attempt by CIMMYT Mexico, PBI Sydney, and ARI Pune, to generate novel AB genome diversity, durum- and emmer-based synthetic hexaploids were crossed with common wheat, and about 1000 doubled haploid (DH) lines were generated. These DH lines were tested for heat and drought tolerance at ARI Pune and some promising DH lines carrying heat and drought tolerance have been identified and utilized in the wheatimprovement program. Diploid, tetraploid, and hexaploid wild species were surveyed for tolerance to heat and drought stress, and it was observed that accessions from Ae. speltoides, Ae longissimi, Ae. searsii, T. turgidum ssp. dicoccoides, T. aestivum cv. C306, and T. sphaerococcum carry adaptation mechanism for heat and drought stress (Bansal and Sinha, 1991; Khanna-chopra and Viswanathan, 1999; Ehdaie and Waines, 1992; Villareal, 1994; Waines, 1994). At ARI Pune, the effect of change in temperature on yield was analyzed using 12 Indian wheat cultivars grown over 11 years at three locations in the peninsular zone, viz., Pune, Niphad, and Dharwad. Regression analysis showed that per °C rise in minimum temperature during the heading, anthesis, and dough-to-ripening stage caused a yield loss of 1.45, 1.94, and 2.24 q/ha, respectively, in durum wheat (Table 2). The yield of T. dicoccum was significantly affected by a °C rise in minimum temperature at all the stages studied. The significant yield loss of 2.01 to 3.29 q/ha suggested that T. dicoccum cultivars were more sensitive to a rise in the temperature. Surprisingly, in regression analysis, T. aestivum cultivars did not show any significant yield loss due to the rise in temperature at any given stage. Similar observations were reported earlier (Khanna-chopra and Viswanathan, 1999) and suggested that hexaploidy conferred heat tolerance as it combines higher productivity and stability under heat stress when compared with the tetraploid group. The stress tolerance in hexaploid wheat was again confirmed based on the genome plasticity as a key factor in wheat domestication and its spread all around the world (Dubcovsky and Dvorak, 2007).

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TABLE 2 Yield loss (q/ha) due to rise in 1°C in minimum temperature at various growth stages in durum and dicoccum wheat. T. durum 95% Confidence interval

Average yield loss (q/ha)

Lower bound

Tillering to stem elongation

2.24⁎

Heading

ns

Growth stages

Flowering Milk stage Dough to ripening

⁎

1.94

⁎

1.45 ns

T. dicoccum 95% Confidence interval

Upper bound

Average yield loss (q/ha)

Lower bound

4.07

0.41

3.29⁎

–

–

2.8⁎

3.53 2.82 –

0.35 0.09 –

T. aestivum 95% Confidence interval

Upper bound

Average yield loss (q/ha)

Lower bound

Upper bound

5.08

1.5

Ns

–

–

4.39

1.21

Ns

–

–

⁎

4.15

1.22

Ns

–

–

⁎

4.07

1.94

Ns

–

–

⁎

3.39

0.63

Ns

–

–

2.69 3.01 2.01

⁎

P  0.05; ns: nonsignificant.

Translocation of rye chromosome 1RS to the wheat produced T1BL-1RS derivatives of hexaploid wheat that showed wider adaptability to reduced irrigation conditions. This adaptability to limited moisture stress was attributed to the vigorous and deeper root systems of T1BL-1RS genotypes. These translocation lines generated in the 1980s have been extensively used as a source of abiotic and biotic stress tolerance and dominated wheat cultivation in South Asia and globally (Hussain et al., 2015; Mujeeb-Kazi et al., 2013). Sources for salt tolerance have been identified in several members of Triticum species such as bread wheat (Kingsbury and Epstein, 1984), durum wheat (Munns and James, 2003), einkorn wheat (Datta et al., 1995; Gorham et al., 1991), and wild emmer (Nevo et al., 1992). Besides this, several Aegilops and wheatgrass species have been identified as valuable resources carrying salt tolerance (Colmer et al., 2006; Farooq et al., 1989; Gorham et al., 1990).

Phenotyping for abiotic stress tolerance Therefore, breeding for stress tolerance in wheat needs much attention and their response mechanism can be used as an effective tool for phenotyping. These stresses are complex and affect multigenic traits. Plants generally have three mechanisms when they encounter stress—avoidance, escape, and tolerance. In stress avoidance, plants undergo physiomorphological changes like reduced leaf area, increased pubescence, leaf rolling, and leaf reflectance with epicuticular wax accumulation—glaucousness (Richards et al., 1986). The escape mechanism is when the plants complete their life cycle as soon as they sense the occurrence of stress. In the case of stress tolerance, plants develop mechanisms to fight stress. Thus, the most feasible approach to breed for stress tolerance is the selection of a representative stress environment; this needs understanding and genetic dissection of quantitative traits, especially those related to yield and stress tolerance. Abiotic stresses have been known to affect grain size; grain weight, grain number, and single-grain weight have been studied in greater detail (Bhatta et al., 2018; Bheemanahalli et al., 2019; Foulkes et al., 2002). Various growth-related phenotypic and physiological traits have been studied over the years in different plants. Early seedling establishment helps with water-use efficiency in plants that can utilize residual moisture, as it correlates to the deep root system in plants (Awan et al., 2007). Deeper roots also help in efficient nutrient uptake (Liao et al., 2006). Early growth vigor also helps with radiation-use efficiency (RUE) in plants by producing active tillers, reducing soil water evaporation, and providing a cool plant canopy. These stages can be used for selection as they affect the biomass as compared to conditions when not in stress. Images can be captured by a digital camera at high resolution and saved in either a JPEG or PNG format for analysis. These images can be extracted for RGB pixel values to measure leaf greenness and plant biomass (Golzarian et al., 2011). Spectral reflectance studies have picked up pace in plant phenotyping at heading and grain-filling stages. Normalized differential vegetative index (NDVI) and canopy temperature (CT) measurements are done with the help of a

54

Abiotic stresses in wheat

spectroradiometer using a thermal camera respectively. Such techniques assist with the selection of genotypes with higher heritability (Babar et al., 2006; Kumar et al., 2017). Mechanistic approaches in plant phenotyping for large-scale yield components are possible with the help of X-raycomputed tomographic measurements in less than 7 min per spike in wheat. Here, seed traits—seed weight, seed number, single-seed weight, and seed morphology along with root traits—can be analyzed in detail without any damage to the plant. Root architectural changes in heat in water-deficit conditions compared to stress-free environment, the number of lateral roots, root hairs, and length of the root can be studied by this technique (Manschadi et al., 2008; Schmidt et al., 2020). LiDAR (light detection and ranging) is another above-ground biomass measurement technique compared to the traditional one (Fig. 1). It has an advantage over NDVI which is otherwise affected by saturation of high-ground cover. LiDAR can operate at ambient light conditions and overcome the limitations posed by digital imaging like over- or underexposure, resulting in poor image quality. The buggy or trolly helps accommodate multiple sensors like camera NDVI, laser scanner, etc. (Deery et al., 2014). Precision phenotyping during drought and heat needs special conditions to replicate the stress environment. For drought, rain-out shelter (ROS) is constructed and stress is induced at various stages to study the plant response. To avoid any variation among the trial, seeds are sown at a uniform depth and studied for traits mentioned earlier. The temperaturecontrolled phenotyping facility (TCPF) is a novel way to study heat stress under controlled conditions. This facility has an advantage of bifurcating heat stress-tolerant and -susceptible genotypes compared to the late-sown plants in the field trial. Various high-throughput platforms are being developed to record observations of hundreds of breeding lines per day with a high degree of precision. These platforms include greenhouse/chamber-based (conveyer-type, benchtop), field groundbased (mobile cart-based), and aerial (unmanned aerial vehicle, satellite)-type systems (Li et al., 2021a). Some of the high-throughput platforms having a potential application for the screening of breeding materials for abiotic stress tolerance are listed in Table 3.

FIG. 1 Phenomobile Lite comprising LiDAR laser scanner, digital single-lens reflex (DSLR) camera, GreenSeeker, and touch-screen computer mounted on an aluminum frame with adjustable wheel spacing to accommodate different plot widths (1.75–2.20 m) and ground clearance for canopy heights up to 1.5 m. The height adjustable sensor boom (2.0–2.5 m) enables data capture from crop emergence to maturity. The Phenomobile Lite is powered by an electric wheel and steered by an operator walking behind. Data are captured on a touch-screen computer and processed through a web interface whereby the user processes the plot data in a semiautomated fashion. (Source: Jimenez-Berni, J.A., Deery, D.M., Rozas-Larraondo, P., Condon, A.T.G., Rebetzke, G. J., James, R.A., Bovill, W.D., Furbank, R.T., & Sirault, X.R.R. (2018). High throughput determination of plant height, ground cover, and above-ground biomass in wheat with LiDAR. Front. Plant Sci., 9(February), 1–18. https://doi.org/10.3389/fpls.2018.00237.)

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TABLE 3 High-throughput phenotyping platforms having potential application in screening phenotypes for abiotic stress tolerance in crops. Trait

Equipment

Capacity

Accuracy compared with a manual score

Crop lodging

Unmanned aerial system (UAS)

1320 plots

r ¼ 0.76–0.91

Singh et al. (2019)

Canopy temperature and green NDVI

Aircraft mounted with hyperspectral and thermal cameras

1094

NA

Sun et al. (2019)

Plant height, ground cover, biomass

Light detection and ranging (LiDAR) mounted on a ground-based mobile platform

700 plots/h

r ¼ 0.82–0.98

Jimenez-Berni et al. (2018)

Plant height, ground cover, canopy temperature

Ultrasonic sensor, NDVI sensor, thermal infrared radiometer mounted on a ground-based mobile platform

240 plots/hr

NA

Bai et al. (2016)

Plant height, growth rate

RGB camera mounted on unmanned aerial vehicle (UAV)

1000 plots/hour

R2 ¼ 0.52–0.99

Holman et al. (2016)

Seminal root traits

Ultra-zoom digital camera fixed on a tripod

600 seedlings/ m2 /day

r2 ¼ 0.75–0.85

Richard et al. (2015)

Plant height

RGB camera mounted on UAV

NA

R2 > 0.90

Volpato et al. (2021)

NDVI

Multispectral camera mounted on UAV

NA

R2 ¼ 0.92

Khan et al. (2018)

NDVI

Multispectral camera mounted on UAV; GreenSeeker spectral sensor mounted on tractor

NA

r ¼ 0.42–0.61

Condorelli et al. (2018)

Photosynthetic performance

Light-induced fluores- cence-transient (LIFT) sensor mounted on a cart

504 plots/ day

NA

Zendonadi dos Santos et al. (2021)

Plant and canopy architectural traits

LiDAR, RGB/multispectral camera

NA

NA

Liu et al. (2019)

Reference

NA: not available.

QTL and markers associated with abiotic stress tolerance in wheat The use of molecular marker for the selection of plants carrying genomic regions of interest is refered to as marker-assisted breeding (MAB). Conventional breeding is the selection of superior cultivars through a hybridization technique based on its phenotype without knowing the genes or traits governing them; this leads to linkage drag. Linkage drag involves the selection of unwanted genes along with the genes of interest (Ruane and Sonnino, 2007). Marker-assisted breeding has advantages over conventional breeding with increased efficiency and precision for selection (Babu et al., 2004). These markers are linked to the trait and act as flags for introgression of the gene of interest and do not affect the phenotype themselves (O’Boyle et al., 2007). Marker-assisted breeding has accelerated the selection procedures in breeding programs for various traits such as abiotic and biotic stresses, yield, and end-use quality (Oliveira et al., 2008, see review Hussain et al., 2021). Over the past several decades, research on wheat genomics became a major area of research around the globe. Intensive efforts have been made for the improvement of wheat under diverse agroecologies (Giraldo et al., 2019). Salient features of MAB are the tight linkage between the gene of interest and the selection marker and the presence of highly polymorphic markers among the breeding material. These markers must be reproducible, stable, and easy to assay. In order to face these hardships, there is an utmost need to adopt new technologies, including MAB combined with high throughput and precision phenotyping to enhance wheat production. Molecular breeding technologies will accelerate the progress in selecting stress-tolerant wheat (Devi et al., 2017).

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Abiotic stresses in wheat

Salt stress Soil salinization is one of the most common reasons for land degradation. It is a predominant issue in arid and semiarid regions where the evapotranspiration rates exceed the rainfall. Most of the time excess waterlogging also leads to salinization of the soil. Soil salinity poses a serious threat to world agriculture because it reduces the crop yield primarily by affecting the osmotic balance leading to ionic toxicity. Under normal conditions, plant cells have high osmotic pressure which enables them to take up water and minerals from the soil solution. However, under salt stress, the osmotic pressure in the plant cells is reduced. This limits the uptake of essential minerals like K + whereas Na + and Cl  ions can enter the cells and have direct toxic effects on cell membranes as well as metabolic activities. About 8%–10% of wheat grown in Asia is affected by salinity. In Western Australia, about half of the 13,475 farms, for most of which wheat is the major crop, are affected by salinity (ABS, 2005). Thus, breeding salt-tolerant wheat is an important breeding program. Screening for breeding salt-tolerant wheat cultivar revealed that durum wheat is more sensitive to salt stress compared to T. aestivum. This is because a trait of enhanced K +/Na + discrimination at low salinity was found to be located on chromosome 4DL (Gorham et al., 1987). This locus contributes to low Na + accumulation in the leaves and it is controlled by a single-gene Kna1 (Dubcovsky et al., 1996). MAS has been successfully applied in developing Australian durum wheat. A Na +  exclusion locus has been mapped in the durum wheat population from a cross between a low Na + landrace and wheat cv Tamaroi (Lindsay et al., 2004). Studies revealed the presence of a QTL on chromosome 2AL linked to an SSR marker—Xgwm312. This trait showed a heritability of 0.90 at the F2 generation (Munns et al., 2000), which proves it to be a dominant trait. The marker is found to be in close association with the trait for easy selection of both tolerant and sensitive lines. Another trait Nax2 has been mapped on chromosome 5AL for Na + exclusion. Salt tolerance index and proportions of dead leaves (%DL) are considered key parameters in the mapping studies for the identification of tolerant cultivars at an early vegetative stage. A QTL on chromosome 4B was found to have a close association with %DL (Turki et al., 2015). QTL have also been mapped in a RIL population developed from a cross between Chuan 35,050 and Shannong 483, for shoot K +/Na + concentration on chromosome 5A (Xu et al., 2013).

Metal toxicity and deficiency Various metals are essential plant micronutrients and play a vital role in plant metabolism. However, excess of these metals leads to metal toxicity and hampers their growth. Boron toxicity has been recognized in crop plants under dry conditions in West Asia, North Africa, Australia, and many other parts of the world where irrigation is a problem (Gupta et al., 1995). A population was developed of 161 double haploids from a cross between tolerant wheat cv. Halbred and moderately sensitive cv Cranbrook Loci on chromosome 7B and 7D were shown to be effective in selecting for improved boron tolerance. A region on 7B was found to control boron uptake and reduce boron toxicity on root growth suppression. Introgressing potential region can significantly improve grain yield in soil prone to boron toxicity ( Jefferies et al., 2000). Aluminum also affects crop productivity in regions where acidic soil is more prevalent (pH below 5). Al3 + released in the soil inhibits normal root growth Wheat is more sensitive to aluminum toxicity as compared to other cereals like rice and maize (Famoso et al., 2010). In conventional practices, adding lime to acidic soil was used to increase the pH of the soil. But it was a more expensive and ineffective method to revive deeper layers of the soil. Tolerant wheat lines like Atlas 66 have been developed in Brazilian gene wheat backgrounds where aluminum toxicity is a concern (Boff et al., 2019). Validation studies have been carried out to estimate the net growth rate and staining of root tips with hematoxylin under aluminum stress. This has been carried out in cross between FSW an Al-tolerant Chinese landrace and Wheaton an Al-sensitive US spring wheat, and QTL was identified on chromosome 4DL. Pollution of water and soil is a major environmental problem. With increased industrialization and not having proper disposal methods, dumping of industrial waste in water bodies and the use of these water for irrigation lead to soil pollution. Heavy metals like cadmium are highly soluble in water, and plants easily uptake them. This leads to phytotoxicity and can lead to biomagnification in the food chain. Earlier three promising markers were reported for screening high and low Cd content in durum wheat grains (Zaid et al., 2018). Recently, Ahmad Alsaleh et al. (2022) used these three molecular markers (usw47, Cadd5B, and KASP marker Cadd5B) to differentiate high and low Cd accumulating durum wheat lines. Results showed a high correlation coefficient (r ¼ 0.944*) and successful classification of accessions. Based on molecular markers, 96.2% of the accessions were classified accurately. The KASP assay was highly effective to differentiate high and low Cd content accessions, and these authors proposed that it could be used as a molecular tool in durum wheat breeding programs, with less cost and time, for reduced grain Cd levels.

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Heat stress Crops are sensitive to climate change, including changes in temperature and precipitation, and to rising atmospheric CO2. In the present scenario, the rise in temperature globally is affecting wheat yield negatively. This leads to terminal heat stress, which is a major concern for wheat production worldwide. Wheat-growing ecologies are severely affected due to heat (high temperature) stress during the grain-filling period. The lethal high temperature for wheat is 47.5 °C (Porter and Gawith, 1999). The optimum temperature during the post-anthesis period for wheat is between 22 and 25 °C. Higher temperatures through post anthesis and grain filling can cause pollen sterility, tissue dehydration, lower CO2 assimilation, and increased photorespiration (Farooq et al., 2011). It also causes irreversible damage like a reduction in the grain-filling duration by 2.8 days, grain weight by 5%, and grain numbers by 4% (Bhusal et al., 2017). Approximately 6% reduction in wheat yields is predicted with every 1 °C rise in global mean temperature (Bergkamp et al., 2018; Zhao et al., 2017). Under controlled conditions, thermotolerance can be induced by short periods of moderately high temperatures before subsequent heat stress. In field conditions, thermotolerance occurs naturally, the effect of which is heat tolerance (Fokar et al., 1998). Although it is a natural phenomenon, very little is known about the genes governing it in plants. Certain physiological changes such as thylakoid membrane damage (TMD), plasma membrane damage (PMD), and SPAD chlorophyll content (SCC) are good indicators of heat tolerance and can show a correlation with growth (Blum et al., 2001; Wahid et al., 2007). With the help of molecular markers, many objectives can be fulfilled for breeding programs by targeting traits that are indicative of heat tolerance in crop plants. Talukder et al. (2014) identified 5 QTL in the RIL population developed by crossing Ventnor, a hard white Australian wheat, and Karl 92, a hard red winter wheat from Kansas. Genomic regions on chromosome (1B, 1D,2B, 6A, and 7A) were found to be significantly associated with TMD, SCC, and PMD. With longer exposure time to heat, photosystem-II activity is inhibited which leads to subsequent damage of the thylakoid. SSR markers Xbarc49 and Xbarc121 were found on chromosome 7A for all three traits—TMD, SCC, and PMD. Markers Xgwm18 and Xbarc113 for QTL close to SCC were found on chromosomes 1B and 6A, respectively. Five GBS Bin markers Bin747, Bin 1596, Bin 178, Bin 81, and Bin 1130 were also found strongly associated with all the traits. The heat susceptibility index has also been used as an indicator for identifying heat tolerance in wheat which is indirectly related to flag leaf length, width, and visual wax content (Mason et al., 2010). QTL mapping in the DH population of a cross between the wheat cultivars Berkut and Krichauff led to the identification of seven stable QTL on chromosomes 1D, 6B, 2D, and 7A for HSI traits; of which, one was for grain yield and canopy temperature, two for thousand grain weight, and three for grain filling (Tiwari et al., 2013). Composite interval mapping on RILs developed from a cross HD2808 (heat tolerant) and HUW510 (heat susceptible) identified 9 (HSI of traits) mapped on linkage groups 2A, 2B, and 6D with phenotypic variance ranging from 11.2% to 30.6% (Bhusal et al., 2017). Association mapping studies of 197 spring wheat genotypes from ICARDA suggested that under severe heat stress, genotypes carrying the positive allele of the markers wsnp_Ex_c12812_20324622(4A) and wsnp_Ex_c2526_4715978, (5A) have 15% greater yield on average that can be used in breeding programs (Tadesse et al., 2019). Like drought stress, a number of QTL/SNPs/candidate genes were reported for heat tolerance also (Hussain et al., 2021) and mainly targeted the grain yield, flag leaf cuticular waxes, temperature depression of flag leaf and main spike, maximum quantum efficiency of phtosystem II, chlorophyll content, plasma and thalakoid membrane stability, grain-filling rate and duration, chlorophyll II fluroscence kinetics, proline content, spike ethylene, grain yield stability coefficient, and susceptibility indices.

Drought Water resources play an important role in crop productivity. Agriculture depends on water supplies and different components of the hydrological cycle, like the natural replenishment of surface and groundwater resources (Kang et al., 2009). Drought stress response varies with stages for genotypes (Dhanda et al., 2002). Some genotypes can be sensitive at the seedling stage and others can be at the flowering stage (Sallam et al., 2019). Changing rainfall patterns and climatic conditions may lead to frequent occurrences of droughts in the future. As drought is a complex phenomenon, it affects multiple facets of plant development. Also, crops adopt various mechanisms when they face water deficit. Traits that govern seedling emergence, change in leaf area, osmotic adjustments, water deficit and assimilation, and root formation are affected by drought (Blum, 1996). Thus, a genetic approach for breeding for drought tolerance is attaining global importance. At present, using traditional biparental approaches, QTL for various agronomic and physiological traits responsive to drought stress have been genetically mapped and extensively reviewed (Gupta et al., 2020; Hossain et al., 2021). The most common physiological traits that have been targeted for QTL mapping of wheat drought stress tolerance include canopy

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temperature, carbon isotope discrimination, chlorophyll content, water-soluble carbohydrates, ABA production (Iehisa et al., 2014), relative water content, stay green habit (Shi et al., 2017), photosynthetic capacity/rate, cell membrane thermostability (Shahinnia et al., 2016; Wang et al., 2016; Xu et al., 2017), and various root architectural traits (Soriano and Alvaro, 2019; Li et al., 2021b). Due to the availability of high-density SNP arrays (9 K, 15 K, 90 K, 660 K, and 820 K) and other high-density wheat genotyping platforms (genotyping by sequencing and DArTseq), GWAS became an important approach for the dissection of complex traits (drought) in wheat. In a few studies, haplotype-based GWAS and candidate gene-based association mapping approaches were also used to find QTLs/genes for drought stress in wheat (Gupta et al., 2014, 2020; Hussain et al., 2021).

Frost tolerance Low temperature is another factor that limits the growth of wheat leading to a loss in productivity. Wheat is generally grown in autumn to avoid the drought conditions of summer. This is a limiting factor for wheat-growing regions in North and Eastern Europe, Russia, and North America. Prolonged periods of subzero temperatures lead to a reduction in winter hardiness. Frost tolerance is known to be a polygenic trait affecting multiple physiological processes in plant development by retarding plant metabolism. Lower temperatures lead to the formation of ice crystals inside the plant cells causing leaf or spike injury (Single and Marcellos, 1974). Temperatures below 10 °C are known to cause low yields in wheat as they affect critical phases of gamete formation leading to male sterility (Saulescu and Braun, 2001; Zhao et al., 2013). QTL associated with frost tolerance were identified in the hexaploid wheat population produced from a cross between Mirnovoskaya 808-winter-type-tolerant parent and Pishtaz-spring-type-susceptible parent. They were phenotyped by artificial freeze test and genotyped using SSRs, AFLPs, etc. Three dominant-effect QTL were detected in the winter parent, Mirnovoskaya 808, whereas three partial dominant-effect QTL were detected in the spring parent, Pishtaz (Taleei et al., 2010). Frost tolerance is the ability to survive extremely low temperatures for a prolonged duration, without significant damage to the cell membrane or any of its components. Genes associated with photoperiod and vernalization are known to play a significant role in frost tolerance by increasing the vegetative period, thereby increasing wheat production. Studies supporting this were carried out in homozygous deletion lines and Chinese spring for frost resistance and vernalization. It was found that VRN-1 gene and frost-resistant gene FR1 are linked and they are located on chromosome 5AL, which delays flowering. Another frost-tolerant locus (FR2) has also been identified on chromosome 5D and linked to VRN-3 (Sutka et al., 1999). With the help of IWGSC RefSeq v1.0, reference sequence analysis suggests the role of C-repeat-binding factors (CBFs) in the pathway associated with flowering response. The identified CBFs (CBF-A3, CBF-A5, CBF-A10, CBF-A13, CBF-A14, CBF-A15, and CBF-A18), vernalization (VRN-A1 and VRNdB3), and photoperiod response genes (PPD-B1 and PPD-D1) play an important role in frost tolerance (Babben et al., 2018).

Marker-assisted breeding for abiotic stress tolerance in wheat Although there are several reports that deal with the identification of QTL or marker-trait association for abiotic stress tolerance and the surrogate traits, very few reports are available that have shown the deployment of markers in breeding for abiotic stress tolerance in wheat. QTL for grain yield under drought stress, canopy temperature, NDVI, and chlorophyll content were transferred from HI 1500 to Indian popular cultivars HD 2733 and GW 322 using the marker-assisted backcross breeding approach (Fig. 2). Selected advanced breeding lines showed superior performance against parent genotypes in field trials conducted under drought conditions (Rai et al., 2018a,b; Todkar et al., 2020). Similarly, QTL for yield under heat stress and days to anthesis were transferred from the heat-tolerant genotype WL 730 to HD 2733. The backcrossderived lines showed a significant improvement in yield traits under heat stress (Amasiddha et al., 2016). A major QTL (Qyld.csdh.7AL) for grain yield under drought was introgressed into four Indian wheat cultivars using MAS. The introgressed lines showed up to a 25% higher yield of the recurring parent under drought conditions (Gautam et al., 2021). Babax, a drought-tolerant line from CIMMYT, was used for marker-assisted introgression of drought-tolerant QTL in advanced breeding lines developed at Punjab Agriculture University, Ludhiana. Selected BC2F4 lines introgressed with babax allele showed improved drought tolerance (Mavi et al., 2018). Wild wheat relatives have been used as donors in the marker-assisted improvement of elite wheat for abiotic stress tolerance. Triticum durum—Aegilops speltoides backcross introgression lines were used for transferring seven heattolerant QTL to three different hexaploid backgrounds using a marker-assisted selection (Dhillon et al., 2021). A total of 164 BC2F3 progenies with different combinations of QTL were generated and 40 progenies were evaluated in replicated

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FIG. 2 Outline of marker-assisted breeding for abiotic stress tolerance in wheat.

trials across two years under normal and heat stress environments. Phenotypic evaluation and heat tolerance index analysis over two environments showed that traits such as grain-filling duration, spikelets/spike, tiller number, thousand grain weight, and yield were enhanced in the BC2F3 progenies due to the introgression of heat stress-tolerant QTL. The progenies developed during this study can further be used for developing heat-tolerant wheat varieties. Wild emmer wheat was used as a donor for a drought-related QTL to develop near-isogenic lines with improved yield performance under drought stress (Merchuk-Ovnat et al., 2016). The introgressed near-isogenic lines also showed higher biomass, better photosynthetic capacity, and photochemistry combined with a higher flag leaf area.

Genomic selection QTL mapping studies have extensively been carried out in crop plants in a biparental population and 3-5 QTL were detected in each study. These analyses generally were sufficient to study genetic architecture in several segregating genes and gene interaction in a relatively limited environment. However, the size of mapping populations and other available resources affect the accuracy of QTL (Dekkers and Hospital, 2002; Kearsey and Farquhar, 1998). These reported QTL have accounted for
40%–60% of phenotypic variation. Among the segregating population, the confidence intervals (CI) associated with the QTL are large. Given a particular trait, the heritability of an individual QTL is 50% or less (Darvasi and Weller, 1993; Hyne et al., 1995). Also, as we deal with a biparental breeding population, allelic diversity and genetic background constrain their use in directly applying to different germplasm. This requires multiple mapping populations for QTL validation. Genomic selection (GS) has been proposed to avoid these deficiencies between the mapping population and breeding population. It was first proposed in dairy cattle breeding by Meuwissen et al., 2001. GS is the linkage disequilibrium (LD)based mapping strategy used to predict phenotypes for complex traits across locations and years ( Jannink et al., 2010). With advances in genome sequencing technology and a wide range of markers across the genome, it is an exceptionally useful tool in breeding programs. It is considered a form of MAS that evaluates all the markers on a population to estimate the total genetic variance, and selection of the individuals is based on their marker effects to predict the breeding value also known as genome-estimated breeding values (GEBVs). GS accelerates the breeding cycle for the development of superior genotypes by increasing the accuracy and reliability required for selecting complex traits (Crossa et al., 2017). The central process of genomic selection (GS) is to screen all marker data rather than identifying individual loci significantly associated with a trait; this gives more accurate predictions in selection. It mainly involves development of the training population having both genotypic and phenotypic data that help calculate the GEBVs of the breeding population (Fig. 3) (Heffner et al., 2009).

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FIG. 3 Steps involved in the process of genomic selection useful in wheat-improvement programs.

GS is beginning to be implemented as just a prediction model to get into practice. We must 1) design a training population—representative of the breeding population where GS is being applied, 2) need high-density markers and genomewide linkage disequilibrium, and 3) precisely combine the GEBVs in the prediction model. Presently, GS has been applied in various crops mainly for agronomic traits, and very few studies for GS in abiotic stress management have been carried out (Krishnappa et al., 2021).

Challenges and future perspectives Despite breakthroughs in sequencing technologies, the availability of high-quality reference genomes, the amount of QTL/ markers, and millions of SNPs, there is still a long way to go. The number of QTL and marker-trait association studies of a variety of complex traits, such as drought, have increased exponentially. Hundreds of QTL and marker-trait associations (MTA) with varying degrees of effects have been identified for abiotic stress tolerance in wheat; however, deploying all of them in breeding programs is a major challenge. An alternative approach, QTL meta-analysis, could be helpful to identify a few promising QTL/MTAs by eliminating redundant QTL/MTAs. Recently, this approach was demonstrated by Soriano et al. (2021) and identified 85 meta-QTL in wheat out of 368 QTL for abiotic, biotic, and quality traits; of which, 15 most promising QTL were tested for the candidate gene analysis. Now that we have a lot of transcriptome sequencing data and sequenced mutant data, we can use them to validate candidate genes or find meta-QTL, and they can also be used in the MAS of genomic selection. We now know how to dissect complex traits and how many QTL can be found using highresolution GWAS. The availability of various types of markers, high-standard and precise statistical software, sophisticated advanced technologies in fast precise phenotyping (using drones, for example), and advances in data mining and data analysis (artificial intelligence, cloud computing, and 5th generation mobile networks) will help reduce the present gap between wheat genomics and its breeding. A wheat-improvement program at any given center consists of an evaluation of about thousands of breeding lines in a season. Although the cost of next-generation sequencing and high-throughput genotyping is reduced day by day, the cost to cover thousands of breeding lines is still substantial and beyond reach for most of the resource-poor centers. Despite significant advances in gene discovery and the application of novel genomic technologies, the use of MAS and genomicassisted breeding in public wheat breeding programs is still limited to a few resource-rich institutions. Not every wheat breeding program can afford to hire a geneticist or bioinformatics expert to help them convert their traditional wheat breeding operations to genomic-based wheat breeding programs. As a result, a fully utilized marker-assisted or genomic selection in wheat will be a significant issue in the coming years.

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Chapter 5

Epigenetics and abiotic stress tolerance in wheat crops: Consequences and application Zige Yang, Pengfei Zhi, Haoyu Li, Xiaoyu Wang, and Cheng Chang⁎ College of Life Sciences, Qingdao University, Qingdao, China *

Corresponding author. e-mail: [email protected]

Introduction In eukaryotic cells, genomic DNAs wrap around histone octamers composed of histones H2A, H2B, H3, and H4 to form nucleosomes (Lai and Pugh, 2017; Luger et al., 1997; Nodelman and Bowman, 2021; Richmond and Davey, 2003). In assistance with linker DNA and histone H1, nucleosomes are further assembled into compactly condensed chromatin (Bednar et al., 2016; Fyodorov et al., 2018; Zhou and Bai, 2019). This tightly coiled chromatin structure is essential to the maintenance of plant genome stability and displays dynamics in response to developmental and environmental cues (Kim, 2021; Probst and Mittelsten Scheid, 2015; Vriet et al., 2015). Through governing accessibility of DNA to transcriptional machinery, chromatin dynamics greatly contributes to the regulation of transcriptional reprogramming in plant development and stress response (Asensi-Fabado et al., 2017; Kim et al., 2010; Luo et al., 2012a). In plants, chromatin dynamics is tightly governed by plant epigenetic regulators (Berger and Gaudin, 2003; Fransz and de Jong, 2002; Hsieh and Fischer, 2005; Ramirez-Prado et al., 2018). So far, four groups of epigenetic regulators have been identified from model and crop plants and include DNA (de)methylation enzymes, histone-modifying enzymes, chromatin remodeling factors, and regulatory noncoding RNAs (ncRNAs) (Bartman and Blobel, 2015; Brown et al., 2013; Kim et al., 2015; Kong et al., 2020) (Fig. 1). As typical DNA (de)methylation enzymes, DNA methyltransferase and DNA demethylase mediate the DNA methylation and demethylation, respectively, and govern the DNA methylation profile in the sequence context of CG, CHG, and CHH (where H is A, T, or C) (Meyer, 2011; Simon and Meyers, 2011; To et al., 2015). Histone-modifying enzymes catalyze histone posttranslational modifications (PTMs), including acetylation, methylation, phosphorylation, and ubiquitination, at histone N-terminal tails (Stillman, 2018). For instance, histone acetyltransferases (HATs) and histone deacetylases (HDACs) mediated histone acetylation and deacetylation, respectively (Hu et al., 2019; Liu et al., 2014; Shen et al., 2015b) (Fig. 1). Similarly, histone methylation and demethylation were catalyzed by histone methyltransferases (HMTs) and histone demethylases (HDMs), respectively (Cheng et al., 2020; Liu et al., 2010; Zheng and Chen, 2011) (Fig. 1). As other important epigenetic regulators, chromatin remodeling factors could utilize the energy of ATP hydrolysis to reposition and/or evict nucleosomes, as well as incorporate histone variants like H2A.Z into nucleosomes to reconfigure chromatin structure and regulate plant expression (Reyes et al., 2002; Song et al., 2021; Verbsky and Richards, 2001) (Fig. 1). In addition, regulatory ncRNAs such as microRNAs (miRNAs), small interference RNAs (siRNAs), and long noncoding RNAs (lncRNAs) also get involved in the epigenetic regulation of plant gene expression (Yu et al., 2019b; Song et al., 2019; Waititu et al., 2020). Interestingly, these are cumulative evidence that these epigenetic regulators usually function in concert rather than independently to fine-tune plant genome stability and gene expression (Du et al., 2015; Liu and Chang, 2021; Wang et al., 2016). For instance, Arabidopsis histone deacetylase HDA6 could associate with various epigenetic regulators such as DNA methyltransferase MET1, histone methyltransferases SUVH4/5/6, histone demethylase FLD, and chromatin remodeling factor SWI3B to regulate transposon silencing and plant flowering time (Liu et al., 2012; To et al., 2011; Yang et al., 2020; Yu et al., 2011; Yu et al., 2017). In fluctuating environments, various abiotic stresses such as salinity, water deficit, water logging, extreme temperature, ultraviolet radiation, nutrient deficiency and heavy metal stress seriously threaten plant growth and development as well as crop yield and quality (Gong et al., 2020; Zhang et al., 2021; Zhu, 2016). Therefore, improving crop tolerance Abiotic Stresses in Wheat. https://doi.org/10.1016/B978-0-323-95368-9.00017-5 Copyright © 2023 Elsevier Inc. All rights reserved.

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FIG. 1 Simplified models for the regulation of gene transcription by epigenetic regulators. (A) DNA methylation is deposited by DMTs (DNA methyltransferases) and removed by DDMs (DNA demethylases). Heavy DNA methylation at gene promoters is associated with gene repression. (B) Histone acetylation is catalyzed by HATs (histone acetyltransferases) and erased by HDACs (histone deacetylases). Histone acetylation is generally associated with gene activation, while histone deacetylation usually leads to gene repression. (C) Repressive histone methylation marks like H3K27me3 and H3K9me1/2 are deposited by HMTs (histone methyltransferases) enzymes. Removal of these marks by HDMs (histone demethylases) enzymes is associated with gene activation. (D) Chromatin remodeling factors (CHRs) regulate gene expression by repositioning and/or evicting nucleosomes, as well as incorporating histone variants like H2A.Z into nucleosomes.

to these abiotic stresses is a major target of plant breeding (Bailey-Serres et al., 2019; Hawkesford and Griffiths, 2019; Wang et al., 2021b). To secure crop production in stressful environments, genetic variations have been widely employed in conventional breeding for crop improvement (Bruce, 2012). However, these conventional breeding strategies based on Mendelian genetics are usually labor-intensive and time-consuming (Hartl and Orel, 1992). In addition, environmental stresses usually change at a higher rate than genetic mutation, and intensive artificial selection practices in conventional breeding have eroded plant genetic diversity essential for crop improvement (Bruce, 2012; Hartl and Orel, 1992). Thus, conventional breeding strategies relying on the exploitation of genetic variations have become less effective. For instance, global yields of important crops like bread wheat increased marginally in the past decade even in the presence of sophisticated genetic breeding approaches like marker-assisted selection (MAS), genomic selection, and double haploid (DH) ( Jones, 2011). As an alternative direction, epigenetic mechanisms and regulators could fine-tune abiotic stress response in model and crop plants (Chang et al., 2020; L€amke and B€aurle, 2017). For instance, Arabidopsis histone deacetylase 2C (HD2C) gets involved in the epigenetic repression of cold-responsive gene COLD RESPONSIVE (COR) through mediating histone deacetylation, and thus, regulating plant response to cold stress (Park et al., 2018). Similarly, the SWI2/SNF2-Related 1 (SWR1) chromatin remodeling complex gets involved in the maintenance of phosphate (Pi) homeostasis through mediating H2A.Z deposition at Pi starvation-induced genes such as Phosphate transporter 1 (Pht1) genes Pht1:1, Pht1:2, Pht1:4, and Pht1:9 (Smith et al., 2010). Therefore, epigenetic mechanisms and regulators govern stress-responsive gene expression and contribute to plant phenotypic diversity in stressful environments, and have great potential for improving crop stress tolerance (Hou and Wan, 2021; Springer and Schmitz, 2017; Varotto et al., 2020). In this chapter, we highlighted the important roles of epigenetic mechanisms and regulators in abiotic stress tolerance of wheat crops and discuss the potentials, challenges, as well as strategies in exploiting epigenetic mechanisms and regulators to mitigate abiotic stresses in wheat crops.

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DNA methylation and its roles in plant response to abiotic stresses DNA methylation is a conserved epigenetic modification essential to plant gene regulation and genome stability, and is catalyzed by DNA methyltransferase using S-adenosylmethionine (SAM) as a donor for methyl group (He et al., 2011; Law and Jacobsen, 2010; Liu and He, 2020). In plants, DNA methylation generally refers to the addition of a methyl group to the fifth carbon of cytosine (5-mC) (Tirnaz and Jacqueline, 2019; Zhang et al., 2018a). Plant 5-mC DNA methylation generally occurs in the sequence context of CG, CHG, and CHH (H represents A, C, and T), and could be removed in the DNA demethylation pathways (Cortellino et al., 2011; Lang et al., 2017; Wu and Zhang, 2010; Zhang and Zhu, 2012; Zhu, 2009). Genome-wide DNA methylation profiling revealed that DNA methylation could occur in transposable elements (TEs), gene promoters, and gene bodies (Cokus et al., 2008; Zilberman et al., 2007; Li et al., 2012b; Slotkin and Martienssen, 2007; Zhang et al., 2006). Increasing evidence has revealed that DNA methylation in TEs is associated with TE silencing and genome stability, whereas DNA hypermethylation at gene promoters generally contributes to gene repression (Deniz et al., 2019; Henderson and Jacobsen, 2007). DNA methylation pattern is dynamically determined by three processes: establishment, maintenance, and erasing (Erdmann and Picard, 2020; Gao et al., 2010; Matzke and Mosher, 2014). De novo DNA methylation is established via the RNA-dependent DNA methylation (RdDM) pathway involving small interference RNAs (siRNAs) and the DNA methyltransferase domains rearranged methyltranferase 2 (DRM2) (Zhai et al., 2015; Zhong et al., 2014). In the canonical RdDM pathway in model plant Arabidopsis thaliana, noncoding RNAs (P4 RNAs) are initially transcribed by RNA polymerase IV (Pol IV) from heterochromatin regions and direct the generation of double-stranded RNAs (dsRNAs), which requires the RNA-DEPENDENT RNA POLYMERASE 2 (RDR2) (Singh et al., 2019; Ye et al., 2012). These dsRNAs are then cleaved by RNase III-class endonucleases DICER LIKE 3 (DCL3), DCL2, and DCL4 to generate mainly 24nucleotides siRNAs. Subsequently, these siRNAs are bounded by ARGONAUTE 4 (AGO4) or AGO6 and paired with complementary noncoding RNAs (scaffold RNAs) that are transcribed by RNA polymerase V (Pol V) from transposons and repeats (Kanno et al., 2004, 2008; Law et al., 2010, 2013). DNA methyltransferase DRM2 is then recruited by AGO4 and/or AGO6 to catalyze the de novo DNA methylation in a sequence-independent manner (Smith et al., 2007; Zhang et al., 2013; Zhong et al., 2012). A wide range of other proteins and complexes such as SAWADEE HOMEODOMAIN HOMOLOGUE 1 (SHH1), SNF2 DOMAIN-CONTAINING PROTEIN CLASSY1 (CLSY1), and DRD1-DMS3-RDM1 (DDR) chromatin remodeling complex get involved into the canonical RdDM pathway (He et al., 2011; Law and Jacobsen, 2010; Liu and He, 2020; Tirnaz and Jacqueline, 2019; Zhang et al., 2018a). In addition to the canonical Pol IV-RDR2-DCL3 pathway, other subsidiary RdDM pathways such as the Pol II-DCL3 pathway and RDR6-DCL3 RdDM pathway also contribute to the establishment of DNA methylation (Cuerda-Gil and Slotkin, 2016). Once established, DNA methylation in the sequence context of CG, CHG, and CHH are maintained by different DNA methyltransferases during mitosis and meiosis. Maintenance of CG methylation in Arabidopsis requires METHYLTRANSFERASE 1 (MET1), an orthologue of mammalian DNA methyltransferase 1 (DNMT1) (Kankel et al., 2003). CHG and CHH methylation are maintained by DNA methyltransferases CHROMOMETHYLASE 3 (CMT3)/CMT2 and DRM2/CMT2, respectively (Lindroth et al., 2001; Stroud et al., 2014). In addition, chromatin remodeling factor DECREASE IN DNA METHYLATION 1 (DDM1) could function in concert with CMT2 to maintain CHH methylation (Huettel et al., 2006; Jeddeloh et al., 1999; Zemach et al., 2013). Structural and biochemical analysis revealed that Arabidopsis DNA methyltransferase CMT2/3 as well as maize Zea methyltransferase 2 (ZMET2, maize orthologue of CMT3) could preferentially target the histone modification mark H3K9me2 and catalyze the non-CG DNA methylation (CHG and CHH methylation) in corresponding chromatin regions (Du et al., 2012, 2014, 2015; Johnson et al., 2007). Interestingly, histone H3K9 methyltransferase SUPPRESSOR OF VARIEGATION 3-9 HOMOLOG 4 (SUVH4), SUVH5, and SUVH6 have the binding preference to CHG and CHH DNA methylation and mediate histone H3H9 dimethylation at these DNA methylation regions, thereby establishing the reinforcing loop between the non-CG DNA methylation and histone H3K9 dimethylation (Stroud et al., 2014). Both passive and active demethylation pathways contribute to the erasing of 5-mC marks from plant genomes. During DNA replication, failure in methylation maintenance under shortage of methyl group donor or lack of DNA methyltransferase activity could cause passive demethylation and result in the dilution of 5-mC marks in nascent DNA strands (Groth et al., 2016; Rocha et al., 2005; Zhang et al., 2012; Zhou et al., 2013). In contrast, active demethylation in plants requires DNA glycosylase to directly remove 5-mC marks (Gong et al., 2002; Liu and Lang, 2020). In Arabidopsis, four bifunctional 5-mC DNA glycosylases, including REPRESSOR OF SILENCING 1 (ROS1), DEMETER (DME), DEMETER-LIKE 2 (DML2), and DML3, function to remove 5-mC marks in all sequence contexts (Agius et al., 2006; Gehring et al., 2006; Martı´nez-Macı´as et al., 2012; Ortega-Galisteo et al., 2008). Generally, these DNA glycosylases first cut the glycosylic bond between the 5-mC base and the deoxyribose, and then cleave the DNA backbone to generate a gap, which is subsequently

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filled with an unmethylated cytosine nucleotide under the action of DNA polymerase and ligase (Andreuzza et al., 2010; Huh et al., 2008; Lee et al., 2014; Lei et al., 2015; Penterman et al., 2007; Wu and Zhang, 2017; Zhu et al., 2007). As the first identified DNA glycosylase in active demethylation 20 years ago, ROS1 could sense the DNA methylation levels through a DNA methylation monitoring sequence (MEMS) at its promoters and serves as a DNA methylation rheostat in plants (Li et al., 2015a,b; Williams et al., 2015). With recent advances in genome-wide and gene-specific DNA methylation profiling techniques such as whole-genome bisulfite sequencing (WGBS), methyl-CpG binding domain protein capture sequencing (MBDCap-seq), methylated DNA immunoprecipitation sequencing (MeDIP-seq), methylation-sensitive amplification polymorphism (MSAP) technique, as well as methylation-sensitive restriction enzyme PCR (chop-PCR), patterns and dynamics of DNA methylation in plant response to various abiotic stresses have been extensively studied in model and crop plants (Guevara et al., 2017; Feng and Lou, 2019; Hsu et al., 2020; Tirnaz and Jacqueline, 2019; Li et al., 2018a; Dasgupta and Chaudhuri, 2019). Accumulative evidence revealed that abiotic stresses such as extreme temperatures, water deficit, and salt stress could induce the altered patterns of 5-mC methylation in various plant species. For instance, DNA hypomethylation was induced by heat stress in cotton (Gossypium hirsutum), soybean (Glycine max), and canola (Brassica napus) (Gao et al., 2014; Hossain et al., 2017; Li et al., 2016; Ma et al., 2018; Min et al., 2014). Reduced 5-mC levels were also observed in A. thaliana, rice, Brassica rapa, Nicotiana plumbaginifolia, cucumber, and rubber tree (Hevea brasiliensis) upon exposure to cold stress (Burn et al., 1993; Guo et al., 2019; Lai et al., 2017; Tang et al., 2018; Xie et al., 2019). Similarly, salt stress could induce DNA hypomethylation in soybean and rapeseed (Brassica napus var. oleifera) (Chen et al., 2019; Marconi et al., 2013). In addition, drought-induced DNA hypomethylation was observed in the monocot model Brachypodium distachyon (GagneBourque et al., 2015). Further transcriptional profiling demonstrated that this stress-induced DNA hypomethylation might be contributed by altered expression of DNA methylation enzyme genes in response to abiotic stresses. Indeed, the expression of cotton DNA methyltransferases DRM1, DRM3, and rice OsCMT3 was downregulated by heat stress (Folsom et al., 2014; Min et al., 2014). On another hand, hypermethylation induced by abiotic stresses was also observed in some model and crop plants. For instance, hypermethylation induced by salt stress was observed in the salinity-sensitive rapeseed (B. napus var. oleifera) cultivar Toccata (Marconi et al., 2013). Similarly, drought treatment could significantly increase the 5-mC levels in the sequence context of CG, CHG, and CHH in cotton and Populus trichocarpa (Liang et al., 2014; Lu et al., 2017). Therefore, these studies provided novel insights into the complex responses of plant DNA methylation to multiple abiotic stresses. Global changes of DNA methylation were observed in wheat response to multiple abiotic stresses, including water deficit, osmotic stress, salinity stress, and heavy metals like lead (Pb), cadmium (Cd), and zinc (Zn) (Chwialkowska et al., 2016; Duan et al., 2020; Kapazoglou et al., 2013; Kashino-Fujii et al., 2018; Shafiq et al., 2019; Wang et al., 2021c; Wang et al., 2014). These DNA methylation changes were obvious at promoters of stress-responsive genes such as DEHYDRATION-RESPONSIVE ELEMENT-BINDING PROTEINS 2 (DREB2) and DREB6 under osmotic stress, HEAVY METAL ATPASE 2 (TaHMA2), ATP-BINDING CASSETTE (TaABCC2, TaABCG3, TaABCG4) metal detoxification transporter genes, flavonol synthase gene TaFLS2, and Bowman-Birk-type protease inhibitor gene TaWRSI5, which could be associated with changes in gene expression levels (Chwialkowska et al., 2016; Duan et al., 2020; Wang et al., 2021a; Wang et al., 2014). For instance, osmotic stress-induced CG hypomethylation was observed at the promoter regions of wheat genes DREB2, which is correlated with the enhanced DREB2 expression in response to osmotic stress (Wang et al., 2021a). Notably, these changes in DNA methylation and gene expression generally displayed variation between stresstolerant and susceptible wheat cultivars, implying the potential roles of DNA methylation in wheat stress tolerance (Wang et al., 2021a, 2021b). Indeed, a decrease in 5-mC levels was observed at the promoter regions of TaHMA2, TaABCC2, TaABCG3, and TaABCG4 in the wheat Pb-resistant variety Pirsabak 2004 but not in the Pb sensitive variety Fakhar-e-sarhad under Pb, Cd, and Zn metal stress treatments, which is associated with the upregulation of TaHMA2, TaABCC2, TaABCG3, and TaABCG4 in Pirsabak 2004 in response to these heavy metal stresses (Shafiq et al., 2019). Similarly, changes of DNA methylation and related-gene expression were also observed in barley response to drought, water deficiency, and aluminum (Al) toxicity (Kashino-Fujii et al., 2018). Surprisingly, barley roots and leaves displayed different methylome changes in water-deficiency conditions, implicating the organ specificity of the DNA methylation dynamics in response to water deficiency (Kashino-Fujii et al., 2018). It was recently demonstrated that insertion of a multiretrotransposon-like (MRL) sequence in the promoter region of HvAACT1 (Al-activated citrate transporter1) as well as its degree of DNA methylation influences HvAACT1 expression and Al tolerance in European barley accessions (Kashino-Fujii et al., 2018). Interestingly, expression of the barley DME-family DNA glycosylase gene HvDME was induced by drought treatment in a drought-tolerant barley cultivar, which correlated with the changed DNA methylation in HvDME promoter and gene body (Kapazoglou et al., 2013) (Table 1). These studies elucidated the important roles of

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TABLE 1 Epigenetic processes and regulators involved in the regulation of plant response to abiotic stresses. Epigenetic process category

Modulation of plant response to abiotic stresses by epigenetic regulators

Regulator gene name

Gene product family

Plant species

AtNRPD2

Subunit of the DNAdependent RNA polymerase IV functioning in RdDM pathway

A. thaliana

Arabidopsis nrpd2 mutants exhibited compromised heat tolerance.

Popova et al. (2013)

AtDCL3

Dicer-like endoribonuclease functioning in RdDM pathway

A. thaliana

Arabidopsis dcl3 mutants exhibited compromised heat tolerance.

Popova et al. (2013)

AtRDR2

RNA-dependent RNA polymerase functioning in RdDM pathway

A. thaliana

Arabidopsis rdr2 mutants exhibited compromised heat tolerance.

Popova et al. (2013)

AtAGO4

Argonaute protein functioning in RdDM pathway

A. thaliana

Arabidopsis ago4 mutants exhibited compromised heat tolerance.

Popova et al. (2013)

AtDCL4

Dicer-like endoribonuclease functioning in RdDM pathway

A. thaliana

Arabidopsis dcl4 mutants exhibited compromised heat tolerance.

Popova et al. (2013)

AtDRM2

DNA methyltransferase functioning in de novo DNA methylation

A. thaliana

Arabidopsis drm2 mutant displayed enhanced freezing tolerance.

Xie et al. (2019)

AtRDM4

A transcriptional regulator functioning in RdDM pathway

A. thaliana

Arabidopsis rdm4 mutant showed reduced cold tolerance.

Chan et al. (2016)

AtMET1

DNA methyltransferase

A. thaliana

Loss-of-function of Arabidopsis AtMET1 reduced plant salinitystress tolerance.

Baek et al. (2011)

AtDDM1

A chromatin remodeling factor essential for the maintenance of CHH DNA methylation

A. thaliana

Loss-of-function of Arabidopsis AtDDM1 reduced plant salinitystress tolerance.

Yao et al. (2012)

HvDME

DNA glycosylase

H. vulgare

Expression of HvDME was induced by drought treatment in a drought-tolerant barley cultivar, which correlated with the changed DNA methylation in the HvDME promoter and gene body.

Kapazoglou et al. (2013)

Histone modifications

AtHDA9

Histone deacetylase

A. thaliana

Loss-of-function of Arabidopsis HDA9 could enhance plant tolerance to drought and salinity stress.

Zheng et al. (2016, 2020)

Histone modifications

AtHDA15

Histone deacetylase

A. thaliana

Arabidopsis HDA15 interacts with transcription factor HFR1 to negatively regulate plant response to elevated ambient temperature.

Shen et al. (2019)

DNA (de) methylation

Reference

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TABLE 1 Epigenetic processes and regulators involved in the regulation of plant response to abiotic stresses—cont’d Epigenetic process category

Histone modifications

Modulation of plant response to abiotic stresses by epigenetic regulators

Regulator gene name

Gene product family

Plant species

AtHD6

Histone deacetylase

A. thaliana

Arabidopsis HDA6 interacts with another histone deacetylase HD2C to regulate plant responses to salinity stress by mediating histone deacetylation at ABAresponsive genes.

Luo et al. (2012b)

AtHD2C

Histone deacetylase

A. thaliana

Arabidopsis HD2C interacts with the WD40-repeat protein HOS15 and transcription factors CBFs to fine-tune plant dynamic response to cold stress.

Park et al. (2018)

GhHDT4D

Histone deacetylase

G. hirsutum

GhHDT4D positively contributes to the plant drought tolerance by mediating histone deacetylation at drought tolerance regulator gene WRKY33.

Wang et al. (2019a), Zhang et al. (2020)

ZmHATB

Histone acetyltransferase

Z. mays

ZmHATB activates the expression of cell wall-related ZmEXPB2 and ZmXET1 genes by potentiating histone H3K9 acetylation under salt stress.

Li et al. (2014)

ZmGCN5

Histone acetyltransferase

Z. mays

ZmGCN5 activates the expression of cell wall-related ZmEXPB2 and ZmXET1 genes by potentiating histone H3K9 acetylation under salt stress.

Li et al. (2014)

TaGCN5

Histone acetyltransferase

T. aestivum

Expression of the wheat TaGCN5 gene in Arabidopsis gcn5 mutant plants could rescue their penalty in the heat and salt tolerance.

Zheng et al. (2019)

TaHAG1

Histone acetyltransferase

T. aestivum

TaHAG1 could directly activate the transcription of three respiratory burst oxidase genes TraesCS4D02G324800, TraesCS1D02G284900, and TraesCS3D02G347900 by mediating H3 acetylation under salt stress, and contributes to salt tolerance through modulating reactive oxygen species (ROS) production.

Zheng et al. (2021)

AtCLF

Histone H3K27 methyltransferase

A. thaliana

Arabidopsis AtCLF catalyzes the H3K27me3 deposition at COR genes and regulates plant cold stress response.

Carter et al. (2018)

AtPRMT5

Protein arginine methyltransferase

A. thaliana

Arabidopsis PRMT5 negatively regulates plant iron homeostasis through mediating histone H4R3 dimethylation at Ib subgroup bHLH genes.

Fan et al. (2014)

AtMLK1/2

Ser/Thr protein kinase

A. thaliana

Arabidopsis mlk1 mlk2 double mutant displayed decreased tolerance to osmotic stresses.

Wang et al. (2015)

Reference

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TABLE 1 Epigenetic processes and regulators involved in the regulation of plant response to abiotic stresses—cont’d Epigenetic process category

Chromatin remodeling

Noncoding RNA

Modulation of plant response to abiotic stresses by epigenetic regulators

Regulator gene name

Gene product family

Plant species

OsHUB2

Histone E3 ligase

O. sativa

Rice OsHUB2 mediates histone H2B monoubiquitination (H2Bub1) at drought-responsive genes in response to drought stress.

Ma et al. (2019)

OsOTLD1

Histone deubiquitinase

O. sativa

Rice OsOTLD1 reduces both H2Bub1 levels and expression of drought-responsive genes, and fine-tunes plant drought response.

Ma et al. (2019)

AtPKL

Chromatin remodeling factor

A. thaliana

Arabidopsis AtPKL functions in concert with histone methyltransferase CLF to promote H3K27me3 deposition at COR genes and affects plant cold stress response.

Carter et al. (2018)

AtCHR 11/17

Chromatin remodeling factor

A. thaliana

Arabidopsis AtCHR11 and AtCHR17 interact with AtFGT1 to mediates the heat stress-induced chromatin memory through nucleosome remodeling at heat stress memory-related genes

Charng et al. (2006)

AtBRM

Chromatin remodeling factor

A. thaliana

Arabidopsis AtBRM represses the ABI5 transcription by stabilizing the nucleosome positioning at the ABI5 transcription start site, thereby regulating plant response to drought stress.

Han et al. (2012) Peirats-Llobet et al. (2015) Weiner et al. (2010)

AtMINU1/2

Chromatin remodeling factor

A. thaliana

Arabidopsis MINU1 and MINU2 positively contribute to the growth retardation in plant response to salinity and heat stresses.

Folta et al. (2014, 2016)

AtARP6

An essential component of the SWR1 chromatin remodeling complex

A. thaliana

Arabidopsis arp6 mutants displayed loss of H2A.Z at Phosphate (Pi) starvation response (PSR) genes and multiple Pistarvation-related phenotypes.

Smith et al. (2010)

AtSWI3B

An essential subunit of SWI/SNF chromatinremodeling complex

A. thaliana

Arabidopsis AtSWI3B interacts with HAB1 to regulate drought stress response. In addition, SWI3B associates with histone deacetylase HD2C to regulate plant adaptation to heat stress.

Buszewicz et al. (2016)

ZmCHB101

Chromatin remodeling factor

Z. mays

ZmCHB101 regulates the maize response to osmotic stress and nitrate deficiency through controlling nucleosome density at the stress and nitrate-responsive genes.

Yu et al. (2018, 2019)

At4

LncRNA

A. thaliana

Expression of Arabidopsis lncRNA At4 is regulated by the GCN5mediated histone acetylation in response to phosphate starvation.

Wang et al. (2019b)

Reference

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DNA methylation in the regulation of abiotic stress response in wheat species as well as its great potential in mitigating abiotic stress in these wheat crops. In addition to these DNA methylation and gene expression profiling studies, characterizing plant mutants in DNA methylation also contributes to elucidating the essential regulatory role of DNA methylation in the plant adaption to abiotic stresses. For instance, Arabidopsis mutants deficient in genes involved in small RNA biogenesis essential for the RdDM pathway, including nrpd2, dcl3, rdr2, ago4, and dcl4, exhibited compromised heat tolerance, suggesting the involvement of RdDM pathway in plant basal heat tolerance (Popova et al., 2013) (Table 1). Arabidopsis DNA methyltransferase gene mutant drm2 displayed enhanced freezing tolerance, but mutants deficient in genes essential for RdDM pathways such as RNA-DIRECTED DNA METHYLATION 4 (RDM4) showed reduced cold tolerance (Chan et al., 2016; Xie et al., 2019) (Table 1). In addition, loss-of-function of Arabidopsis DNA methyltransferase gene MET1 and chromatin remodeling enzyme gene DDM1 reduced plant salinity-stress tolerance (Baek et al., 2011; Yao et al., 2012) (Table 1). Functional analysis of wheat DNA (de)methylation genes would certainly shed novel light on the roles of DNA methylation in regulating abiotic stress tolerance in wheat species in future research.

Histone modifications and their involvements in plant response to abiotic stresses As histone codes to determine chromatin structure and gene transcription, histone posttranslational modifications (PTMs) such as acetylation, methylation, phosphorylation, and ubiquitination mainly occur at histone N-terminal tails (Berger, 2007; Strahl and Allis, 2000; Zhao et al., 2019). Histone acetylation is one of the most studied histone PTMs and occurs by the addition of the acetyl group to the lysine residue at histone N-terminal tails (Chen et al., 2020b; Kumar et al., 2021; Luo et al., 2017). Up to now, several acetylation sites at H2A (K5), H2B (K5, K12, K15, K20), H3 (K4, K9, K14, K18, K23, K27), and H4 (K5, K8, K16, K12, K16) have been identified in model and crop plants (Peterson and Laniel, 2004). As reversible histone modification, histone acetylation is catalyzed by histone acetyltransferase (HAT) and could be removed by histone deacetylase (HDAC) (Aquea et al., 2010; Gao et al., 2021; Hu et al., 2019). 12 HATs have been identified from the model plant A. thaliana and classified into four groups such as GCN5-related acetyltransferases (HAGs), MYST-related acetyltransferases (HAMs), CBP-related acetyltransferases (HACs), and TAFII250-related acetyltransferases (HATs) based on their sequence similarity and domain organization ( Jin et al., 2020; Pandey et al., 2002; Zhao et al., 2015). Similarly, 18 HDACs were identified from A. thaliana and could be classified into three groups, including reduced potassium dependency 3/histone deacetylase 1 (RPD3/HDA1), silent information regulator 2 (SIR2), and a plant-specific histone deacetylase 2 (HD2), according to their sequence similarity and domain organization (Hu et al., 2019; Jin et al., 2020; Zhao et al., 2015). In addition, orthologues of Arabidopsis HATs and HDACs have been identified from crop plants such as rice and bread wheat. Generally, histone acetylation mediated by HATs could neutralize the positive charge of histone and weaken DNA-histone association, thereby facilitating the binding of transcription machinery and contributing to gene transcription. In contrast, histone deacetylation catalyzed by HDACs could enhance the interaction of histones with DNAs, thereby increasing chromatin compactness and contributing to gene repression. Considering that histone (de)acetylation usually interplays with other epigenetic mechanisms such as histone (de)methylation and DNA (de)methylation, the effect of histone (de)acetylation on gene expression should be considered in a comprehensive network of different epigenetic marks (Du et al., 2015; Liu and Chang, 2021; Wang et al., 2016). Increasing evidence revealed that histone (de)acetylation governed by HATs and HDACs play important roles in finetuning plant response to environmental stresses such as salinity, water deficit, and extreme temperatures. For instance, lossof-function of Arabidopsis HDAC gene HDA9 could enhance plant tolerance to drought and salinity stress, which is correlated with hyperacetylation and upregulation of stress-responsive genes, suggesting that HDA9 negatively regulates plant tolerance due to drought and salinity stress by mediating histone deacetylation at stress-responsive genes (Zheng et al., 2016) (Table 1). Notably, the regulation of stress response by RPD3-type HDAC HDA9 could be antagonized by the Arabidopsis transcription factor WRKY53 (Zheng et al., 2020). Another plant RPD3-type HDAC HDA15 could interact with a putative bHLH class transcription factor HFR1 (long Hypocotyl in Far Red1) to negatively regulate plant response to elevated ambient temperature in A. thaliana (Shen et al., 2019) (Table 1). Moreover, a plant HD2-type HDAC HD2C could interact with the WD40-repeat protein HOS15 and transcription factors CBFs to repress expression of cold-responsive COR genes, COR15A and COR47, by maintaining histone hypoacetylation (Park et al., 2018) (Table 1). Notably, cold stress could induce an epigenetic switch from repressive (histone hypoacetylation) to permissive (histone hyperacetylation) chromatin through the proteasomal degradation of HD2C mediated by a HOS15-containing E3 ubiquitin ligase complex (Park et al., 2018). Interestingly, HD2C could also interact with the plant RPD3-type HDAC HDA6 to regulate plant responses to the stress-related phytohormone abscisic acid (ABA) and salinity stress by mediating histone deacetylation at ABAresponsive genes (Luo et al., 2012b) (Table 1). In addition, a cotton HD2-type HDAC HD2C GhHDT4D positively

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contributes to the plant drought tolerance by mediating histone deacetylation at WRKY33, a negative regulator of plant response to drought stress (Zhang et al., 2020; Wang et al., 2019a) (Table 1). In maize, two HATs ZmHATB and ZmGCN5 activate the expression of cell wall-related ZmEXPB2 and ZmXET1 genes by potentiating histone H3K9 acetylation under salt stress (Li et al., 2014) (Table 1). These studies shed novel light on the involvement of histone (de)acetylation mediated by HATs and HDACs in plant stress adaptation in model and crop plants. Transcriptional and functional characterization of HATs and HDACs supported that histone acetylation plays important roles in the regulation of plant response to abiotic stresses in wheat species. For instance, expressions of barley HAT genes HvMYST, HvELP3, and HvGCN5 was induced by the stress-related phytohormone ABA, suggesting a possible regulation of these barley HAT genes by ABA during stress response (Papaefthimiou et al., 2010). Consistent with this, histone acetylation mark H3K9ac was found enriched at barley senescence-associated gene HvS40 at the onset of drought-induced senescence, elucidating the dynamics of barley histone acetylation in response to drought stress (Ay et al., 2015). Consistent with these studies on barley HATs, expression of wheat HAT gene TaGCN5 was induced by heat and salt stress, and TaHAG1 gene was induced by salt stress (Hu et al., 2015b; Zheng et al., 2019). In addition, Arabidopsis AtGCN5 was shown to directly activate the expression of both heat stress-responsive genes HSFA3 and UVH6 under heat stress and cell wall-related genes CTL1, PGX3, and MYB54 under salt stress through mediating acetylation of H3K9 and H3K14, and contributes to the plant tolerance to heat and salt stress (Zheng et al., 2019). Interestingly, expression of the wheat TaGCN5 gene in Arabidopsis gcn5 mutant plants could rescue their penalty in the heat and salt tolerance, suggesting that the regulation of plant tolerance to heat and salt stress by GCN5 might be conserved between Arabidopsis and wheat (Zheng et al., 2019) (Table 1). Similarly, another wheat HAT TaHAG1 could directly activate the transcription of three respiratory burst oxidase genes TraesCS4D02G324800, TraesCS1D02G284900, and TraesCS3D02G347900 by mediating H3 acetylation under salt stress, and contribute to salt tolerance through modulating reactive oxygen species (ROS) production in bread wheat (Zheng et al., 2021) (Table 1). These studies revealed that histone (de)acetylation governs plant response to abiotic stress in wheat species. Histone methylation occurs by the addition of one to three methyl groups (namely, monomethylation, dimethylation, and trimethylation) to the lysine and/or arginine residues at histone N-terminal tails (Cheng et al., 2020; Liu et al., 2010; Zhou et al., 2020). So far, methylation sites have been identified from histones H3 (K4, K9, K27, K36, R2, R8, R17, R26) and H4 (R3) in mammals and plants (He et al., 2021; Xiao et al., 2016; Xu and Jiang, 2020). As reversible histone PTMs, histone methylation at lysine residue is catalyzed by SET domain group (SDG) histone lysine methyltransferases and removed by either jumonji C (JmjC) domain-containing histone demethylases or lysine-specific demethylase 1 (LSD1) like histone demethylases (Duan et al., 2018). In contrast, histone methylation at arginine residue is catalyzed by protein arginine methyltransferases (PRMTs) and could be removed by JmjC domain-containing histone demethylases (Liu et al., 2010; Xiao et al., 2016; Xu and Jiang, 2020; Zhou et al., 2020). As well-characterized epigenetic marks, mono- and dimethylation of histone H3 lysine 9 (H3K9me1 and H3K9me2) are deposited by Arabidopsis histone H3K9 methyltransferase SUPPRESSOR OF VARIEGATION 3-9 HOMOLOG 4 (SUVH4/KRYPTONITE), SUVH5, and SUVH6, and generally localize on transposons and repetitives in heterochromatic regions (Bernatavichute et al., 2008; Ebbs et al., 2005; Jackson et al., 2002; Zhang et al., 2007; Zhang et al., 2009). Structural and biochemical analysis revealed that SUVH4, SUVH5, and SUVH6 could recognize and bind to non-CG DNA methylation (CHG and CHH methylation) and deposit H3K9me1/2 marks at these DNA methylation regions, resulting in the co-occurrence of non-CG DNA methylation and histone H3K9me1/2 marks at heterochromatic regions (Du et al., 2012, 2014, 2015; Johnson et al., 2007; Stroud et al., 2014). Monomethylation of histone H3 lysine 27 (H3K27me1) is deposited by Arabidopsis SDG histone methyltransferases ARABIDOPSIS TRITHORAXRELATED PROTEIN 5 (ATXR5/SDG15) and ATXR6 (SDG34), and also enriched in heterochromatic regions ( Jacob et al., 2009). In contrast, trimethylation of histone H3 lysine 27 (H3K27me3) is deposited by polycomb repressive complex 2 (PRC2), an evolutionarily conserved multisubunit complex, and is enriched in euchromatic regions (Mozgova and Hennig, 2015; Li et al., 2018b). In Arabidopsis, the SDG histone methyltransferases CURLY LEAF (CLF, SDG1), SWINGER (SWN, SDG10), and MEDEA (MEA, SDG5) could be assembled into multiple PRC2 complexes to mediate H3K27me3 deposition during different developmental processes and responses to environments (Mozgova and Hennig, 2015; Li et al., 2018b). Unlike the repressive mark H3K27me3, trimethylation of histone H3 lysine 4 (H3K27me4) is usually associated with actively transcribed genes and deposited by complex proteins associated with Set1 (COMPASS), another evolutionarily conserved multisubunit complex (Li et al., 2008; Zhang et al., 2009). In Arabidopsis, the SDG histone methyltransferases such as SDG2, ARABIDOPSIS TRITHORAX 1 (ATX1/SDG27), and ARABIDOPSIS TRITHORAX-RELATED7 (ATXR7/SDG25) could be assembled into multiple COMPASS-like complexes to mediate H3K4me3 deposition in plant developmental processes and stress response (Berr et al., 2010; Chen et al., 2017; Fromm and Avramova, 2014; Guo et al., 2010; Jiang et al., 2009; Saleh et al., 2008; Tamada et al., 2009).

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Increasing evidence revealed that histone (de)methylation governed by histone methyltransferases and demethylases play key roles in regulating plant response to abiotic stresses such as extreme temperatures and nutrient deficiency. For instance, cold exposure-induced upregulation of cold-responsive genes cold-regulated 15A (COR15A) and galactinol synthase 3 (ATGOLS3) as well as H3K27me3 decreases at COR15A and ATGOLS3 (Kwon et al., 2009). Upon return to normal growth temperature, cold-induced induction of transcription in COR15A and ATGOLS3 is repressed, but a cold-induced decrease in H3K27me3 is maintained (Kwon et al., 2009). Interestingly, chromatin remodeling factor PICKLE (PKL) could function in concert with H3K27 methyltransferase CLF to promote H3K27me3 deposition at C REPEAT BINDING FACTOR (CBF)-COLD RESPONSIVE (COR) genes and affect plant cold stress response (Carter et al., 2018) (Table 1). Recurring heat stress could induce hyperinduction of heat stress memory-related genes such as HSP18.2, HSP22.0, and HSP21, as well as accumulation of H3K4 methylation at these memory-related loci, suggesting that heat stress memory in Arabidopsis is associated with changes in di- and trimethylation of histone H3 lysine 4 (H3K4me2 and H3K4me3) at memory-related loci (L€amke et al., 2016). In addition, Arabidopsis SKB1/PRMT5 (Shk1 binding protein 1/protein arginine methyltransferase 5) could associate with the chromatin of the Ib subgroup bHLH genes (AtbHLH38, AtbHLH39, AtbHLH100, and AtbHLH101) and catalyze the symmetric dimethylation of histone H4R3 (H4R3sme2) at these Ib subgroup bHLH genes, thereby regulating plant iron homeostasis (Fan et al., 2014) (Table 1). Transcriptional and functional characterization of histone methyltransferase and demethylase genes supported the involvements of histone (de)methylation in plant response to abiotic stresses in wheat species. For instance, expression analysis showed that 36 SDG genes involved in histone methylation could respond to drought and heat stress in bread wheat, suggesting a potential involvement of these wheat SDG genes, as well as histone methylation, in the regulation of wheat response to drought and heat stress (Batra et al., 2020). As demonstrated by extensive studies on vernalization, histone methylation plays an important role in plant adaptation to prolonged exposure to low temperatures in wheat species. For instance, vernalization resulted in the enhanced deposition of permissive epigenetic mark H3K4me3 and a loss of repressive mark H3K27me3 at the floral promoter gene VERNALIZATION1 (VRN1) in barley (Oliver et al., 2009). Similarly, upregulation of vernalization genes TaVRN1, TaVRN2, and FLOWERING LOCUS T-like 1 (TaFT1) was associated with an increased level of permissive epigenetic mark H3K4me3 under vernalization in winter wheat (Diallo et al., 2012). Histone phosphorylation at serine, threonine, and/or tyrosine residues is catalyzed by specific protein kinase and plays a vital role in the regulation of gene transcription (Rossetto et al., 2012). For instance, phosphorylation at the serine 95 residue of histone H2A is catalyzed by protein kinase MUT9-LIKE KINASE4 (MLK4), which is associated with gene activation (Su et al., 2017). Interestingly, MLK4 could interact with CIRCADIAN CLOCK ASSOCIATED1 (CCA1), a partner of the Swi2/Snf2-related ATPase (SWR1) and NuA4 complexes co-subunit YAF9a, thereby providing a physical basis for the interplay of histone phosphorylation, histone acetylation, and deposition of the histone variant H2A.Z in the regulation of gene transcription (Su et al., 2017). In addition, monoubiquitylation usually occurs at the C-terminal lysine residues of histones H2A and H2B (Roudier et al., 2011; Weake and Workman, 2008; Vaughan et al., 2021). In Arabidopsis, H2B monoubiquitylation is deposited by the E3 ubiquitin ligase HISTONE MONOUBIQUITINATION1 (HUB1) and HUB2, which is generally associated with gene activation (Cao et al., 2008; Gu et al., 2009; Schmitz et al., 2009; Sridhar et al., 2007; Xu et al., 2009). In contrast, H2A monoubiquitylation usually functions in concert with the repressive epigenetic mark H3K27me3 to suppress gene transcription and is catalyzed by the evolutionarily conserved Polycomb repressive complex 1 (PRC1) (Bratzel et al., 2010; Calonje et al., 2008; Li et al., 2018b; Turck et al., 2007; Wang et al., 2004; Xu and Shen, 2008; Zhang et al., 2007). Increasing evidence revealed that histone phosphorylation and ubiquitylation play key roles in regulating plant response to abiotic stresses. For instance, osmotic stress induce phosphorylation of histone H3 at threonine 3 in pericentromeric/knob regions, which relies on Ser/Thr protein kinases MUT9-LIKE KINASE 1 and 2 (MLK1 and MLK2) in A. thaliana. Compared with the wild type, Arabidopsis mlk1 mlk2 double mutant displayed decreased tolerance to osmotic stresses, shedding light on the importance of histone phosphorylation to osmotic stress response (Wang et al., 2015) (Table 1). Similarly, drought stress stimulates rice histone H2B monoubiquitination (H2Bub1) at drought-responsive genes, which depends on the E3 ligase HISTONE MONOUBIQUITINATION2 (OsHUB2) recruited by the transcription factor OsbZIP46 (Ma et al., 2019) (Table 1). Interestingly, mediator of OsbZIP46 deactivation and degradation (MODD), which could promote deactivation and degradation of OsbZIP46 and negatively regulate ABA signaling and drought resistance, could recruit a putative deubiquitinase OsOTLD1 to reduce both H2Bub1 levels and expression of defense responsive genes, implicating the significance of histone monoubiquitination in fine-tuning plant drought response (Ma et al., 2019) (Table 1). In bread wheat, 60Co-γ radiation caused enhanced phosphorylation of histone H3 at serine 3, suggesting the possible role of histone phosphorylation in wheat response to ionizing radiation (Raut and Sainis, 2012). Characterizing more histone kinase and E3 ligase in wheat species will improve our understanding of histone phosphorylation and ubiquitylation in regulating plant response to abiotic stresses in wheat crops in future research.

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Chromatin remodeling and its roles in plant response to abiotic stresses To store a large amount of genomic DNA in the nucleus, chromatin composed of histones and DNAs is highly compacted and tightly coiled, limiting the access of transcription machinery to their target DNAs (Engelhorn et al., 2014; Li et al., 2007; Wang and Qiao, 2020). To overcome this restriction, chromatin modifiers and remodelers are employed to alter DNA-histone interaction and secure the genome accessibility for transcription machinery (Brkljacic and Grotewold, 2017; Deal and Henikoff, 2011; Zhao et al., 2019). As typical chromatin modifiers, DNA/histone-modifying enzymes such as DNA methyltransferase, DNA demethylase, histone methyltransferase, histone demethylase, histone acetyltransferase, and histone deacetylase could catalyze the deposition and/or removal of special epigenetic marks on DNAs and histones, thereby affecting DNA-histone association as well as the access of genome DNAs to transcriptional regulators (Han and Wagner, 2014; Pikaard and Mittelsten Scheid, 2014; Reyes, 2006). In contrast, chromatin remodelers could utilize the energy of ATP hydrolysis to alter the composition, position, and density of nucleosomes, thereby affecting the genome accessibility for transcription machinery (Aslam et al., 2019; Clapier and Cairns, 2009; Ojolo et al., 2018). Based on the types of their central catalytic ATPase components, plant chromatin remodelers could be classified into four major subfamilies, including the switch/sucrose nonfermentable (SWI/SNF) subfamily, the imitation switch (ISWI) subfamily, the chromodomain helicase DNA-binding (CHD) subfamily, and the inositol requiring 80/SWI2/SNF2-Related 1 (INO80/SWR1) subfamily (Clapier and Cairns, 2012; Hargreaves and Crabtree, 2011; Knizewski et al., 2008; Narlikar et al., 2013). Although other types of chromatin remodelers exist, these four major subfamilies ATPase are evolutionarily conserved and have been identified from diverse eukaryotic organisms including budding yeast, fruit fly, mice, human, and plants (Flaus et al., 2006; Gentry and Hennig, 2014; Kwon and Wagner, 2007; Hu et al., 2013). In Arabidopsis, four SWI/SNF-type chromatin remodeling ATPases including BRAHMA (BRM), SPLAYED (SYD), AtCHR12 (MINU1), and AtCHR23 (MINU2) are characterized, and the MINU2 is demonstrated to have the chromatin remodeling activity (Bezhani et al., 2007; Farrona et al., 2004; Jerzmanowski, 2007). In addition, one SWR1-type ATPase PHOTOPERIOD-INDEPENDENT EARLY FLOWERING1 (PIE1), three CHD3-type ATPases PICKLE (PKL), PICKLE RELATED1 (PKR1) and PKR2, one INO80-type ATPase CHR21/ INO80, and two ISWI-type ATPases CHR11 and CHR17 are identified from Arabidopsis genome (Brzezinka et al., 2016; Carter et al., 2018; Kang et al., 2019; March-Diaz et al., 2008; Rosa et al., 2013; Yang et al., 2017; Zha et al., 2017; Zhang et al., 2015). Increasing evidence revealed that these chromatin remodelers govern a wide range of biological processes such as gene transcription, mRNA splicing, DNA replication, and even DNA damage repair. For instance, the Arabidopsis SWI/SNFtype chromatin remodeler SYD could interact with the transcriptional activator LEAFY (LFY) to repress transcription events essential to plant reproductive development (Wu et al., 2012). Similarly, another chromatin remodeler BRM interacts with the transcription factor MONOPTEROS (MP) to positively regulate gene expression essential to flower primordium initiation (Wu et al., 2015; Yang et al., 2015). In contrast, the maize SWI/SNF-type chromatin remodeling protein ZmCHB101, a maize homologue of Arabidopsis chromatin remodeler SWI3D, could modulate alternative splicing contexts by controlling the histone modification status and the nucleosome distribution on alternative exons, and govern the exon incorporation efficiencies by affecting transcriptional elongation rate of RNA polymerase II in response to osmotic stress (Yu et al., 2018, 2019a). In plants, chromatin remodelers could activate and repress their target genes. For instance, Arabidopsis SWI/SNF-type chromatin remodeler SPLAYED (SYD) directly activates the transcription of its target gene WUSCHEL (WUS), a key regulator gene in the shoot apical meristem (SAM) maintenance (Kwon et al., 2005). Similarly, chromatin remodelers SYD and BRM could antagonize the polycomb-repressive complexes and induce expression of AGAMOUS (AG) and APETALA3 (AP3) genes essential for flower morphogenesis in A. thaliana. In addition, the CHD-type chromatin remodeler CHR5 could destabilize the nucleosome at the transcription start site and activate transcription of seed maturation genes FUSCA3 (FUS3) and ABSCISIC ACIDINSENSITIVE3 (ABI3) (Shen et al., 2015a). In contrast, ISWI-type chromatin remodelers CHR11 and CHR17 negatively regulate the expression of FLOWERING LOCUS T (FT) and SEPALLATA3 (SEP3), two essential genes for flowering and flower development in A. thaliana (Li et al., 2012a; Smaczniak et al., 2012). Through modulating the expression of stress-responsive genes, ATP-dependent chromatin remodelers get involved in the regulation of plant response to abiotic stresses. For instance, chromatin remodelers of the ISWI family, CHROMATIN-REMODELING FACTOR 11 (CHR11) and CHR17, could interact with FORGETTER1, Arabidopsis orthologue of Strawberry notch (Sno), to mediate the heat stress-induced chromatin memory through nucleosome remodeling at heat stress (HS) memory-related genes such as heat shock protein 21 (HSP21), HSP22, and HSP18.2 (Charng et al., 2006) (Table 1). Arabidopsis SWI/SNF subfamily chromatin remodeling complex BRM directly binds to the locus ABA INSENSITIVE5 (ABI5), a key regulator gene in ABA signaling, and represses the ABI5 transcription by stabilizing the nucleosome positioning at the ABI5 transcription start site, thereby regulating plant response to drought stress and

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phytohormone ABA (Han et al., 2012; Peirats-Llobet et al., 2015; Weiner et al., 2010) (Table 1). Overexpression studies support that the Arabidopsis SWI/SNF type chromatin remodeling ATPases MINU1 and MINU2 positively contribute to the growth retardation in plant response to salinity and heat stresses (Folta et al., 2014, 2016) (Table 1). Incorporation of H2A.Z histone variant into nucleosome catalyzed by the SWR1 remodeling complex mediates the thermosensory response through conferring a temperature dependence on transcription of HS response genes like HSP70 in A. thaliana (Kumar and Wigge, 2010). Similarly, deposition of H2A.Z histone variant into chromatin at a set of Phosphate (Pi) starvation response (PSR) genes, which is dependent on SWR1 chromatin remodeling complex, regulates transcription of these PSR genes in A. thaliana (Smith et al., 2010) (Table 1). Notably, direct interaction was detected between SWI3B subunit of SWI/SNF chromatin-remodeling complexes and the negative regulator of ABA signaling, HYPERSENSITIVE TO ABA1 (HAB1), suggesting that the SWI/SNF remodeling complex get involved into the regulation of ABA signaling and stress response through regulating the expression of the ABA-responsive genes such as RAB18 and RD29B in A. thaliana (Table 1). Interestingly, the Arabidopsis HD2-type histone deacetylase HD2C could associate with SWI3B, as well as the BRM-containing SWI/SNF chromatin-remodeling complex, to regulate the expression of heat-responsive genes and plant response to heat stress, suggesting that chromatin remodeler could interplay with other epigenetic modifiers such as histone deacetylase to fine-tune plant adaptation to adverse environments like heat stress (Buszewicz et al., 2016) (Table 1). In maize, the core subunit of the SWI/SNF-type ATP-dependent chromatin remodeling complex ZmCHB101 was shown to regulate the maize response to osmotic stress and nitrate deficiency through controlling nucleosome density at the stress and nitrate-responsive genes (Table 1). Although regulation of biotic stress response by CHD family chromatin remodeler TaCHR729 was recently reported in bread wheat, our understanding of chromosome remodeling in response to abiotic stress is very limited in wheat species (Wang et al., 2019c). Identifying more ATP-dependent chromatin remodelers in wheat crops will contribute to our understanding of chromatin remodeling in the regulation of abiotic stress response in wheat crops.

Noncoding RNAs and their involvements in plant epigenetic response to abiotic stresses Noncoding RNAs (ncRNAs) that lack a protein-encoding function play key roles in the regulation of plant development and stress responses (Meng et al., 2021; Wang et al., 2017; Xue et al., 2020; Yu et al., 2019b). As emerging hotspots in epigenetic research, regulatory ncRNAs, especially microRNAs (miRNAs), small interfering RNAs (siRNAs), and long noncoding RNAs (lncRNAs), could modulate gene transcription (Wang et al., 2017; Xue et al., 2020). Generally, miRNA and siRNA contain 18-24 nucleotides (nt), whereas lncRNAs contain more than 200 nt (Yu et al., 2019b). In eukaryotes, primary miRNAs (pri-miRNAs) were transcribed from miRNA genes by RNA polymerase II (RNAPII) and processed by RNase III-type enzyme Dicer-Like1 (DCL1) into miRNA/miRNA* duplexes precursor miRNAs, which are methylated and exported into the cytoplasm, where miRNAs are assembled with ARGONAUTE (AGO) proteins into RNA-mediated silencing complex (RISC) to silence target genes (Baulcombe, 2004; Bologna et al., 2018; Kurihara and Watanabe, 2004; Park et al., 2005; Yu et al., 2005). In contrast, siRNAs were transcribed mainly from transposons and repetitive regions by RNA polymerase IV (RNAPIV) as long linear double-stranded RNAs (Brant and Budak, 2018). As highly heterogeneous molecules in biogenesis, lncRNAs could be transcribed by RNAPII, RNAPIII, RNAPIV, and even RNAPV (Chen et al., 2020a; Quinn and Chang, 2016; Song and Zhang, 2017; Sun et al., 2018; Wu et al., 2020; Zhang et al., 2019). In plants, miRNAs and siRNAs usually mediate gene silencing through posttranscriptional gene silencing (PTGS) and RNAdependent DNA-methylation (RdDM) (Brant and Budak, 2018). In contrast, lncRNAs could mediate gene epigenetic activation and repression (Song and Zhang, 2017; Sun et al., 2018; Wu et al., 2020; Zhang et al., 2019). Increasing evidence revealed that regulatory ncRNAs like miRNAs, siRNAs, and lncRNAs get involved in the epigenetic regulation of plant response to abiotic stresses. For instance, methylation-sensitive amplification polymorphism (MSAP) and expression analysis in Populussi monii showed that several miRNA genes were relevant to targeting the metabolism of H2O2; malondialdehyde and even catalase were differentially methylated in response to temperature stress (Ci et al., 2015). As revealed by reanalysis of existing methylated DNA immunoprecipitation (MeDIP) sequencing data, siRNA and DNA methylation displayed a positive correlation in the varying extent in maize response to drought stress, suggesting that the dynamics of DNA methylation in response to drought stress might be regulated by siRNA (Wang et al., 2021c). Interestingly, Arabidopsis 24 nt siRNAs suppressed by salt stress could directly target the promoter region of AtMYB74, a stress-upregulated R2R3-MYB gene, and regulate AtMYB74 expression through mediating RdDM in response to salt stress (Xu et al., 2015). In addition, histone acetyltransferase GCN5 could mediate H3K9/14 acetylation of lncRNA At4, thereby determining dynamic At4 expression in response to phosphate starvation in A. thaliana (Wang et al., 2019b) (Table 1). However, the epigenetic regulation of plant response to abiotic stress by these regulatory ncRNAs is scarcely reported in wheat crops.

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Characterizing more regulatory ncRNAs in wheat species and disclosing their regulatory mechanisms will broaden our knowledge in epigenetic regulation of abiotic stress response by regulatory ncRNAs in wheat crops in future research.

Plant epigenetic memory to abiotic stresses As originally observed in the study of plant immunity, prior treatment of plants with the bacterial pathogen Pseudomonas syringae or with chemical elicitor acibenzolar-S-methyl (BTH) could prime plant defense responses against the subsequent pathogen infections (Iwasaki and Paszkowski, 2014; Jaskiewicz et al., 2011; Mauch-Mani et al., 2017; Reimer-Michalski and Conrath, 2016; Slaughter et al., 2012). Similarly, a transient abiotic stress (“priming stress”) cue such as extreme temperatures and water deficit could also lead to a faster and stronger plant defense response upon subsequent re-exposure to the same stresses (Conrath et al., 2015; Crisp et al., 2016; He and Li, 2018; L€amke and B€aurle, 2017; Vriet et al., 2015). In addition, plant defense response to one type of stress could be cross-primed by other types of stress. For instance, treatment of Arabidopsis plants with extreme temperatures and/or salt stress could potentiate plant defense response to a subsequent P. syringae infection (Feng et al., 2016; Singh et al., 2014). It was widely demonstrated that these priming events are usually followed by the establishment of stress memory to store the information on priming stress and prepare the plant to experience subsequent adversity more efficiently (D’Urso and Brickner, 2014; Stief et al., 2014). As revealed by elegant studies in plant vernalization and immunity, stress memory could be stably transmitted by mitosis (somatic/intragenerational stress memory) and even meiosis (intergenerational and transgenerational stress memory) in some cases (Cong et al., 2019; Hilker et al., 2016; Luna et al., 2012; Zheng et al., 2017). Somatic/intragenerational stress memory primed by abiotic stresses could be stored for weeks to months, whereas intergenerational and transgenerational stress memory could extend to their stressfree offspring. Generally, intergenerational stress memory is detectable in the immediate stress-free progeny generation, but transgenerational stress memory could extend for at least two stress-free generations. For instance, the vernalization memory to prolonged exposure to cold temperature could last for months in A. thaliana, whereas Arabidopsis defense priming in response to P. syringae infection was evident in the progeny generation (Bouche et al., 2017; Cong et al., 2019; Hilker et al., 2016; Luna et al., 2012; Zheng et al., 2017). Studies in plant vernalization (the prolonged exposure to cold or winter promotes the plant reproductive transition) shed light on the epigenetic mechanism underlying the somatic/intragenerational stress memory (Hepworth and Dean, 2015). In vernalization, prolonged cold triggers a stable epigenetic silencing of FLOWERING LOCUS C (FLC), a negative regulator of floral development, by promoting the PRC2-mediated deposition of repressive epigenetic mark H3K27me3 at the FLC locus, which is essential for the establishment of vernalization memory (Luo and He, 2020; Menon et al., 2021). Similarly, sustained hypermethylation of H3K4 was observed at some heat memory genes in response to priming heat stress, which relies on the presence of HEAT SHOCK TRANSCRIPTION FACTOR A2 (HSFA2) (Charoensawan et al., 2015; L€amke et al., 2016; Para et al., 2014). In addition to histone methylation, chromatin assembly and remodeling also get involved in the establishment of transcriptional memory to environmental stresses. For instance, the histone chaperone CHROMATIN ASSEMBLY FACTOR-1 (CAF-1) functions in the replication-coupled chromatin assembly. Loss-of-function of FASCIATA 2, an essential CAF-1 gene, displayed spurious activation of defense-priming genes in A. thaliana (Mozgova´ et al., 2015; Mun˜oz-Viana et al., 2017). The Arabidopsis ISWI chromatin remodeler, CHR11 and CHR17, and the SWI/SNF chromatin remodeler BRM were shown to interact with FORGETTER1 (FGT1), an Arabidopsis homologue of the Drosophila melanogaster Sno and human SBNO1/2, and regulate nucleosome dynamics during transcription and heat stress memory (Brzezinka et al., 2016) (Table 2). These studies revealed that chromatin assembly and remodeling, together with histone methylation, contribute to the establishment of plant somatic/intragenerational stress memory. Interestingly, these protein-based somatic/intragenerational stress memories could be erased by protein degradation mechanisms including the ubiquitin-proteasome system and autophagy process (Avin-Wittenberg, 2019). It was demonstrated that DNA methylation contributes to intergenerational stress memory. For instance, hyperosmotic stress memory could initiate a paternal inherited intergenerational stress memory in A. thaliana. Transmission of this intergenerational stress memory through the father is hindered in the wild-type Arabidopsis plants but restored by loss-offunction of the DNA glycosylase gene DEMETER (DME), suggesting that the DNA (de)methylation governs the plant intergenerational memory to hyperosmotic stress (Wibowo et al., 2016) (Table 2). As extensively discussed in prior reviews, plant transgenerational memory to biotic stresses such as P. syringae infection and herbivory infestation is fine-tuned by DNA (de)methylation (Bouche et al., 2017; Cong et al., 2019; Hilker et al., 2016; Luna et al., 2012; Zheng et al., 2017). Therefore, DNA (de)methylation is essential for the establishment of intergenerational and transgenerational stress memory. Increasing evidence revealed that epigenetic processes such as DNA methylation, histone modifications, and even chromatin remodeling play important roles in the establishment of plant stress memory to abiotic stresses. As just mentioned,

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TABLE 2 Epigenetic processes and regulators involved in the regulation of plant abiotic stress memory. Epigenetic process category

Regulator gene name

Gene product family

Plant species

Modulation of plant memory to abiotic stresses by epigenetic regulators

Reference

DNA (de) methylation

AtDME

DNA glycosylase

A. thaliana

Arabidopsis AtDME governs the plant intergenerational memory to hyperosmotic stress.

Wibowo et al. (2016)

Histone modifications

AtATX1

H3K4 methyltransferase

A. thaliana

Arabidopsis salt and drought stress memory were associated with AtATX1-mediated H3K4me3 hypermethylation at memory genes RD29B and RAB18.

Ding et al. (2012)

Chromatin remodeling

AtCHR11/17

Chromatin remodeling factor

A. thaliana

Arabidopsis AtCHR11 and AtCHR17 interact with AtFGT1 to mediate the heat stressinduced chromatin memory through nucleosome remodeling at heat stress memory-related genes.

Brzezinka et al. (2016)

AtBRM

Chromatin remodeling factor

A. thaliana

Arabidopsis AtBRM interacts with AtFGT1 to regulate nucleosome dynamics at heat stress memory-related genes, which is required for the establishment of heat stress memory.

Brzezinka et al. (2016) L€ amke et al. (2016)

hyperosmotic stress memory in Arabidopsis could be passed onto their immediate offspring preferentially through the maternal line due to extensive DNA demethylation activity in male gametes, elucidating the important role of DNA (de)methylation in the establishment of intergenerational memory to hyperosmotic stress (Choi et al., 2002; Stief et al., 2014). In addition, salt and drought stress memory was associated with H3K4me3 hypermethylation at memory genes RD29B and RAB18, which relies on the H3K4 methyltransferase ATX1 (Ding et al., 2012) (Table 2). Similarly, heat stress memory was associated with enhanced methylation of histone H3K4, as well as decreased nucleosome occupancy, at heatinducible memory genes in A. thaliana (Charoensawan et al., 2015; L€amke et al., 2016). Consistent with this, the SWI/SNF family chromatin remodeler BRM was required for heat stress memory (Brzezinka et al., 2016; L€amke et al., 2016) (Table 2). These studies implicated the importance of epigenetic processes like DNA methylation, histone modifications, and chromatin remodeling in the regulation of plant somatic and transgenerational stress memory to abiotic stresses. However, whether and how epigenetic processes get involved in abiotic stress memory remains unknown in wheat species. Characterizing defense priming in wheat species and disclosing their underlying mechanisms will broaden our knowledge in epigenetic control of abiotic stress memory in wheat crops in future research.

Exploiting epigenetic variations for mitigating abiotic stresses in wheat crops Over the past centuries, plant breeding has mainly referred to the exploitation of genetic variations, which leads to the development of almost all modern varieties of wheat species (Gadaleta, 2020; Voss-Fels et al., 2019; Wang et al., 2018). The recent advancement in genomic selection and gene editing approaches such as MAS, genome-wide association studies (GWAS), and the CRISPR-Cas9 system has facilitated capturing, creating, and exploiting valuable genetic variations associated with important agronomic traits and certainly could contribute to the genetic improvement of wheat crops (Crossa et al., 2017; Hua et al., 2019; Lozada and Carter, 2020; Rodrı´guez-Leal et al., 2017; Uauy et al., 2017; Zong et al., 2017). However, conventional crop breeding strategies based on the exploitation of genetic variations have become less effective due to declining genetic diversity caused by intensive artificial selection and increasing environmental stresses under climate change (Lopes et al., 2015; Rasheed et al., 2018; Walkowiak et al., 2020). Increasing evidence revealed that epigenetic variations could contribute to the plant plasticity under environmental stresses and have great potential in

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mitigating abiotic stresses in wheat crops (Agarwal et al., 2020; Dalakouras and Vlachostergios, 2021; Springer, 2013; Zhi and Chang, 2021). Epigenetic variations associated with important agronomic traits such as improved stress tolerance in crop plants could be either identified from natural populations or induced by experiments (Gallusci et al., 2017; Latutrie et al., 2019; Tirnaz and Batley, 2019) (Fig. 2). For instance, natural variations (epialleles) of DNA methylation affecting plant development have been identified in Arabidopsis, apple, rice, and tomato (Chen and Zhou, 2013; Cubas et al., 1999; Liu et al., 2015; Manning et al., 2006; Telias et al., 2011) (Fig. 2). Combining genome-wide DNA methylation profiling techniques such as WGBS, MBDCap-seq, and MeDIP-seq with advanced statistical tools like GWAS might help capture these natural DNA methylation variations associated with abiotic stress tolerance in wheat crops. On another hand, epigenetic variations could be artificially induced by stress conditions, chemical treatments, epigenetic recombinant inbred lines (epiRILs) construction, induced gene-specific DNA methylation, as well as epigenome editings (Fig. 2). As discussed in prior sections, environmental stresses such as extreme temperatures and water deficit could induce epigenetic variations in crop plants (Ma et al., 2018; Rutowicz et al., 2015) (Fig. 2). In strawberry, DNA methylation variations associated with flowering, an important agronomic trait, were artificially induced through treatment with DNA methyltransferase inhibitor 5-azacytidine, which provides a path for the chemical induction of epigenetic variations in wheat crops (Dubin et al., 2015; Xu et al., 2016). Furthermore, as revealed by bisulfite sequencing, high-pressure spraying of double-stranded RNA in Nicotiana benthamiana could trigger a promoter DNA methylation, which provides a novel transgene-free method for epigenome modification in wheat crops (Dalakouras and Ganopoulos, 2021; Dalakouras and Papadopoulou, 2020; Kasai and Kanazawa, 2013). Moreover, through utilizing a zinc finger (ZF) to tether SET DOMAIN-CONTAINING PROTEIN 3 (SDG3, SUVH2) to a specific chromatin region, Johnson et al. successfully performed locus-specific RdDM in A. thaliana ( Johnson et al., 2014). Although establishing a similar locus-specific epigenome editing system in wheat species is hindered by their breeding obstacles such as low transformation and regeneration rates; combining gene-editing system with chromatin-modifying enzymes might represent a promising methodology for locus-specific epigenome editing in wheat crops. Indeed, similar locus-specific epigenome editings have been successfully established in mammalian cells through using an inactive variant of CRISPR associated protein 9 (Cas9) to tether chromatin-modifying enzymes such as DNA methyltransferase 3A (DNMT3A) and histone lysine-specific demethylase 1 (LSD1) to a specific chromatin region (Hilton et al., 2015; Kearns et al., 2015; Vojta et al., 2016). In addition, Li et al. recently performed a heritable genome editing in Cas9-transgenic wheat plants through engineering a Barley stripe mosaic virus-based sgRNA delivery vector (BSMV-sg), thereby establishing a convenient genome editing system in bread wheat through virus infection (Li et al., 2021). Combining this BSMV-sg-based genome editing system with chromatin-modifying enzymes such as SDG3 might contribute to the establishment of a convenient tissue culture-free and locus-specific epigenome editing system in wheat crops in future research. In the model plant A. thaliana, epiRIL populations with the same genetic backgrounds but different DNA methylation patterns were established ( Johannes et al., 2009; Reinders et al., 2009; Zhang et al., 2018a,b). These epiRILs displayed phenotypic variations in plant development and stress responses, further implicating the possibility of exploiting natural and induced epigenetic variations for improving crop plants including wheat species. As discussed in prior sections, DNA FIG. 2 Epigenetic variations suitable for wheat breeding. Epigenetic variations could be either identified from natural populations, or induced by stress conditions, chemicals, dsRNAs, and epigenome editings. Natural variations were shown in the green box, and induced variations were displayed in the orange box.

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methylation is a heritable epigenetic mark and could be transmitted in a Mendelian manner during meiosis, but histone modifications could only be sustained by mitosis (Baulcombe and Dean, 2014; Coustham et al., 2012; Li et al., 2015; Schmitz et al., 2013). Therefore, different transmission features of DNA methylation and histone modifications would contribute to their distinct exploitation strategies in crop improvement. DNA methylation variations such as differentially methylated regions (DMRs) in epialleles could be easily exploited for improving wheat crop plants propagated by seed, and these DMRs could also be used as epigenomic markers for the early characterization of epigenetic status in wheat species. In contrast, variations in histone modifications could not be stably inherited and were only suitable for improving clonally propagated crops. Interestingly, Debernardi et al. recently reported that the expression of a fusion protein containing the wheat GROWTH-REGULATING FACTOR 4 (GRF4) and cofactor GRF-INTERACTING FACTOR 1 (GIF1) could greatly enhance the regeneration efficiency in wheat crops, which might contribute to the exploitation of variations in histone modifications for wheat crops improvement in the future research (Debernardi et al., 2020). In addition, to bridge the gap between epigenetic variations and crop improvement on certain agronomic traits, epigenetic modeling such as statistical model and process-based model has been developed. In Arabidopsis, statistical models were developed to establish the association between DNA methylation variations and plant height differences, whereas a process-based model was employed to link histone modifications and vernalization (Angel et al., 2011; Buck-Sorlin, 2013; Hu et al., 2015a; Richards et al., 2012). Therefore, epigenetic modeling could contribute to filling the gap between epigenetic variations and plant abiotic stress and certainly contribute to the exploitation of epigenetic variations for mitigating abiotic stress in wheat crops.

Conclusion and future perspectives Epigenetic processes and elements such as DNA methylation, histone modifications, chromatin remodeling, and ncRNAs could dynamically respond to environmental stresses and are tightly regulated by stress signaling. The Arabidopsis MAP kinase MPK3, a regulator of plant immune signaling, was demonstrated to directly activate the histone deacetylase HD2B through phosphorylation-dependent recompartmentalization, thereby initiating the defense-related chromatin reprogramming. However, the regulation of epigenetic processes by abiotic stress signaling remains to be explored in model and crop plants including wheat species. Identifying the interacting proteins of chromatin modifiers will shine more light on the epigenetic regulatory mechanism, including the steps from stress signaling to epigenetic control, of the plant stress response. Furthermore, different types of chromatin modifications usually function together to initiate transcription reprogramming in response to environmental stresses in model and crop plants. Characterizing the components of dynamic chromatin modifier complex might shed novel light on the interplays among these different chromatin modifications in future research. In addition, a low transformation/regeneration rate has hindered the application of epigenetic variations in the improvement of wheat crops. Developing convenient transformation/regeneration-free epigenome editing methodology would greatly contribute to the epigenetic improvement of wheat crops in future research.

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Chapter 6

Physiological and biochemical approaches for mitigating the effect of abiotic stresses in wheat Kousik Attaa, Aditya Pratap Singhb, Sri Sai Subramnyam Dashb, Yengkhom Linthoingambi Devic, Ananya Baidyaa, Maksud Hasan Shahd, Snehashis Karmakara,f, Debjani Duttaa,f, and Akbar Hossaine,∗ a

Department of Plant Physiology, Faculty of Agriculture, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, West Bengal, India, b Research Scholar,

Department of Genetics and Plant Breeding, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, West Bengal, India, c Research Scholar, Department of Genetics and Plant Breeding, Indira Gandhi Krishi Vishwavidyalaya, Raipur, Chhattisgarh, India, d Department of Agronomy, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, Nadia, West Bengal, India, e Division of Soil Science, Bangladesh Wheat and Maize Research Institute, Nashipur, Dinajpur, Bangladesh, f School of Agriculture, Seacom Skills University, Kendradangal, Birbhum, West Bengal, India ∗ Corresponding author. e-mail: [email protected]

Introduction Agro-industrialists must produce 70% more food for about 2.3 billion people by 2050 while also fighting hunger and poverty jointly, consuming scarce natural resources in an efficient manner, and adapting to climate change (FAO, 2009). Global warming is well documented for its overall negative effects on plant growth, development, and crop productivity. The major impact of global warming is the increment in surface temperature (Wahid et al., 2007). The global surface temperature if follows the current trends of increment is predicted to reach at  1.5°C in 2052 (IPCC, 2012). Global crop production continues to be adversely affected by climate change, with wheat being one of the major crops (Qin et al., 2002). Wheat contributes nearly 20% and 55% of the global calories and carbohydrates consumption, respectively (Enghiad et al., 2017). It is estimated that doubling global wheat production by 2% will be needed each year to meet population growth-related increases in demand for wheat (Gill et al., 2004). Many countries rely on wheat as an important cereal crop for food production, but its production is a constraint to achieving food security (Curtis and Halford, 2014). Like any other crop, wheat also faces a plethora of abiotic stresses (Fig. 1). Drought, extreme temperatures, and salinity are significant and widely spread (Hussain Wani et al., 2013). Heavy metal toxicity, high ozone levels, and other pollutants are few other stress factors to name. According to Porter and Semenov (2005), wheat is highly sensitive to climate and environmental changes. Among the several abiotic factors affecting wheat productivity, drought is one of the most significant (Hossain et al., 2021; Fathi and Tari, 2016). All phases of crop development are affected by drought stress. A lack of water during the early stages of wheat growth leads to poor survival rates and low tillering. Conversely, drought in the middle of the growth cycle causes lower dry matter output, more grains per plant, and fewer effective tillers (Gall et al., 2015). Drought adversely affects assimilate production, fertility, and grain weight in wheat when it is in its terminal growth stage. Wheat requires a temperature of 14°C to 15°C for ripening, and temperatures over 25°C lower grain weight, whereas 35°C is the critical temperature for grain filling (Tiwari et al., 2015; Singh, 1988; Porter and Gawith, 1988). Diurnal temperature fluctuations induce yield loss in a changing climate (Hossain et al., 2020). The temperature increases above a threshold level and causes losses in wheat development and filling, grain yield per spike, and yield loss (Rane et al., 2007; Mukherjee et al., 2019; Tiwari et al., 2017). Salt affects both the quality and growth of wheat in another abiotic way (Loutfy et al., 2020). It is reported that salt stress negatively affects grain weight, spikelet number, spike length, and grain yield in wheat (Tiwari et al., 2017). Natural disasters, unseasonably wet weather, flooding, and storms are becoming more frequent in recent years and thus pose a threat to crop yields, especially wheat (IPCC, 2012). Aslam (2016) reports that excessive rainfall results in crop lodging and waterlogging, both of which adversely affect the yield and quality of wheat and other crops. Compared to other crops, wheat tends to lodge under high fertility conditions and can be seriously damaged by extreme disasters such as hailstorms and cyclones (Singh et al., 2017a,b). For plant Abiotic Stresses in Wheat. https://doi.org/10.1016/B978-0-323-95368-9.00007-2 Copyright © 2023 Elsevier Inc. All rights reserved.

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Abiotic stresses in wheat

FIG. 1 Consequences of abiotic stress in wheat. Adapted and Modified from Ali, N., Akmal, M., 2020. Morphophysiological traits, biochemical characteristic and productivity of wheat under water and nitrogen-colimitation: pathways to improve water and N uptake. In: Fahad, S., Saud, S., Chen, Y., Wu, C., Wang, D. (Eds.), Abiotic Stress in Plants. IntechOpen. https://doi.org/10.5772/intechopen.94355.

Drought

Reduced water availability

Lower water potential

Loss of turgidity, disrupted cell expansion

Decreased photosynthesis

Drought Stress Generation of ROS& Oxidative Stress

Inhibition of mitosis, limited cell division

Membrane damage

Cell death

Growth reduction, Inhibition of reproductive development Yield reduction

biologists, one of the most important aspects of their research involves identifying the mechanisms through which wheat responds to different types of abiotic stresses. In our discussion, we will focus on the adaptive response of wheat to abiotic stresses and how to mitigate them through physiological and biochemical approaches.

Biochemical responses during stress Abiotic stresses cause plants to produce ROS that manipulate their environment biochemically and enzymatically. Stressrelated responses are not only determined by stress’ degree but also by its duration. Various biochemicals, pigments, antioxidants, and phytohormones produced as a response to various abiotic stresses and their beneficial effects, and possible reasons for this response have been listed in Table 1. In addition to the hormones and antioxidants listed in the table, there are others whose effects are not yet fully understood. In addition to determining the health of photosynthetic machinery, acute chlorophyll and carotenoid levels are also indicators of stress tolerance. The various studies in wheat reflected declining chlorophyll concentration under drought (Tabaeizadeh, 1998; Keyvan, 2010; Farooq et al., 2014; Naveed et al., 2014; Saeidi and Abdoli, 2015), salinity (Sairam et al., 2002; Turan et al., 2007; Datta et al., 2009; Dhyani et al., 2013), waterlogging (Huang et al., 1994), heat (Hasanuzzaman et al., 2012; Tack et al., 2015; Mathur and Jajoo, 2014; Ristic et al., 2007, 2008), and heavy metal stress (Hasanuzzaman and Fujita, 2013). In the same way, proline acts as an ROS scavenger and its acute accumulation aids in the mitigation of stress. Several factors have been implicated in increasing proline accumulation in plants, including drought (Garmendia et al., 2017), waterlogging (Olgun et al., 2008; Marashi and Chinchanikar, 2010), heat stress (Kumar et al., 2013a,b; Sarkar et al., 2018), and heavy metal (Alzahrani et al., 2018). Carbohydrate and sugar accumulation rise with the immediate onset of stress but they tend to decline with prolonged stress period (Zhang et al., 2009). Furthermore, higher levels of glycine betaine synthesis have been reported to provide plants with greater osmotic protection when under salinity stress (Talaat and Shawky, 2013, 2014a) as well as the production of antioxidant enzymes like catalase (CAT), peroxidase (POD), superoxide dismutase (SOD), ascorbic acid peroxidase (APX), guaiacol peroxidase (GPX), glutathione reductase (GR), as well as the presence of nonenzymatic scavengers like glutathione (GSH), ascorbic acid (AA), carotenoids. Table 1 summarizes the activities and responses of some of these antioxidants. Most of GPX’s functions are similar to those of APX. Stress has been shown to increase POD activity, as it does with other antioxidants. Several studies have reported enhanced activity under drought (Simova-Stoilova et al., 2008) and salinity (Al-Whaibi et al., 2012; Abedini, 2016; Mandhania et al., 2006). Malondialdehyde is a highly reactive oxidative stress marker generated by lipid peroxidation of polyunsaturated fatty acids. Singh et al. (2017a,b) and Sarkar et al. (2018) found that it is negatively correlated with plant stress response. Among

TABLE 1 Characteristic features and activities of various pigments, biochemical, antioxidants, and phytohormones in response to various abiotic stresses and possible reasons for such response.

Sl No.

Pigments/ biochemical/ antioxidants/ phytohormones

Features/role

Response to various abiotic stresses

Reasons

References

1.

Chlorophyll content

(i) Photosynthesis in plants is a vital physiologic index (ii) Its concentration determines the degree of disruption in photosynthetic machinery due to oxidative damage

(i) Chlorophyll content of wheat leaves decreased under stress (ii) Cholorophyll b declines more quickly than chlorophyll a (iii) A higher ratio of chlorophyll a/b

(i) Damage to the donor side of PSII (ii) Chlorophyllase activation (iii) Poor 5-aminolevulinic acid (ALA) synthesis (iv) A build-up of ions in chloroplasts diminishes the stability of pigmentprotein complexes

Al-Whaibi et al. (2012); Talaat and Shawky (2014a,b); Mehta et al. (2010); Talaat and Shawky (2012); Chookhampaeng (2011); Abdelkader et al. (2007)

2.

Carotenoids

(i) An antioxidant compound that protects the photosynthetic machinery by modulating the ROS responsive genes (ii) Eliminates the risk of photoinhibitory injury resulting from single oxygen (iii) Chlorophyll pigment quenches its excited triple state (iv) Prevents photodamage by dissipation of excess absorbed energy

(i) Decline in total carotenoid content (ii) As stress increases, there is an early indicator of stress in the reduction of chlorophyll/ carotenoid ratio

(i) Thylakoids are disrupted

Shumbe et al. (2014); Pellegrini et al. (2011); Sairam et al. (2002); Shah et al. (2017)

3.

Proline

(i) Excellent osmolyte and metal chelator (ii) Delivers stability to membranes, proteins, and other macromolecules by protecting them from denaturation (iii) Decreases cytoplasmic acidosis (iv) Safeguards cell redox potential (v) Scavenges hydroxyl radicals (vi) Preserves proper NADP+/ NADPH ratios essential for plant metabolism.

(i) Increase in its concentration signifies stress tolerance (ii) Higher accumulation of proline can have detrimental effect on plants

(i) Enhancement of pyroline-5carboxylate synthetase and pyroline-5-carboxylate reductase enzyme activities (ii) Proline dehydrogenase activity declines (iii) Overexpression of wheat WRKY gene

Kishor et al. (2005); Hare and Cress (1997); Abedini (2016); Al-Whaibi et al. (2012); Kumar et al. (2013a); Sumithra and Reddy (2004)

4.

Carbohydrates

(i) Aids in keeping up the osmotic balance in the cytosol

(i) Soluble carbohydrate decrease in stressed plants (ii) Stress tolerance is correlated with an increase in carbohydrate accumulation

(i) Termination of carbohydrate translocation (ii) Poor replenishment of utilized carbohydrate due to disrupted photosynthetic mechanism (iii) A high respiration rate results in reduced assimilate transport to grains, which results in a lower amount of stored carbohydrates

Zhang et al. (2009); Poustini (2002); Ihsan et al. (2016); Dash et al. (2022)

Continued

TABLE 1 Characteristic features and activities of various pigments, biochemical, antioxidants, and phytohormones in response to various abiotic stresses and possible reasons for such response—cont’d

Sl No.

Pigments/ biochemical/ antioxidants/ phytohormones

Reasons

References

5.

Glycinebetaine

(i) Stabilizes the complex protein structures (ii) Guards transcriptional machinery (iii) Preserves the membrane integrity by mitigating oxidative harm caused by ROS

Stress leads to accumulation of glycinebetaine in wheat leaves

(i) Changes of cell turgor may initiate the signal transduction during osmotic stress (ii) Secondary signals from abscisic acid or jasmonates can initiate its formation (iii) Brassinosteroids under salinity conditions stimulate glycinebetaine formation

Yang et al. (2008); Xu et al. (2018); Talaat and Shawky (2012, 2014a,b)

6.

Catalase

(i) This antioxidant enzyme helps remove harmful hydrogen peroxide (H2O2) produced in peroxisomes by oxidases responsible for photorespiration, fatty acid oxidation, and purine metabolism (ii) Plants use catalases to process their metabolic processes and receive signals

(i) Catalase accumulation increases with the onset of stress (ii) Decline in its concentration with severe stress for prolonged time has also been reported

(i) High concentration of ROS leads to upregulation of TaCAT genes (ii) Jasmonic acids also trigger catalase activity

Talaat and Shawky (2013); Yadav et al. (2019); Hammad and Ali (2014); Simova-Stoilova et al. (2008); Tyagi et al. (2021); Qiu et al. (2014)

7.

Superoxide dismutase (SOD)

(i) In terms of ROS defense, SODs are considered first (ii) They are the only enzymatic antioxidant that detoxifies the superoxide radical

Increased activity in tolerant genotypes than the susceptible ones

(i) Accumulation of superoxide ions during stress triggers its formation (ii) Salicylic acids also promote its synthesis

Ashraf (2009); Sairam et al. (2005); Kumar et al. (2013b); Singh and Usha (2003)

8.

Ascorbate peroxidase (APX)

A form of antioxidant that annihilates H2O2 in the symplast

Enhanced accumulation occurs in case of tolerant cultivars

Higher level of H2O2 and MDA in the cytosol triggers its synthesis

Li et al. (2013); Esfandiari and Gohari (2017)

9.

Glutathione (GSH)

(i) Various ROS detoxifying enzymes require this nonenzymatic antioxidant as a reducing cofactor (ii) Prevents the oxidation of specific proteins by forming conjugates with them

Wheat leaves exhibit increased concentration in response to stress

(i) Excessive ROS accumulation in the cytosol (ii) Nitric oxide enhances GSH synthesis

Rouhier et al. (2004); Talaat and Shawky (2014b); Moellering et al. (1998)

Features/role

Response to various abiotic stresses

10.

Glutathione reductase (GR)

(i) In symplastic defense, it catalyzes the reduction of GSSH (oxidized glutathione) to GSH (reduced glutathione) (ii) Ascorbic acid is restored by GSH/ GSSH

Amplified GR levels in the cytosol act as an indicator of stress tolerance

Oxidized glutathione produced as a result of ROS detoxification in the cytosol induces GR synthesis

Noctor and Foyer (1998); Foyer and Noctor (2005); Yousuf et al. (2012); Suzuki et al. (2011)

11.

Ascorbic acid (AA)

(i) Activates superoxide and H2O2 so that it can protect macromolecules from oxidative damage (ii) From tocopheroxyl, it generates α-tocopherol (iii) Utilizes AA-GSH to eliminate H2O2

Increased AA activity ceases leaf senescence

Higher H2O2 accumulation promotes its synthesis

Rai and Agrawal (2014); Farooq et al. (2014); Dalmia and Sawhney (2004)

12.

Malondialdehyde (MDA)

(i) Intensity of oxidative stress can be assessed through MDA content (ii) The ability to detect membrane damage in plants is based on this indicator

(i) Transient MDA accumulation result in defense signaling, while its sustained accumulation trigger cell death (ii) Its accumulation increases with the increasing intensity of stress (iii) Its content is higher in susceptible cultivars than tolerant ones

(i) Lipid peroxidation generates MDA (ii) Its formation can be nonenzymatically induced by ROS or enzymatically through lipoxygenase activity

Morales and Munn
e-Bosch (2019); Esfandiari and Gohari (2017); Sairam et al. (2000); Miller et al. (2009)

13.

Abscissic acid (ABA)

(i) Major phytohormone for adaptation in plants under stress environment (ii) Mostly targets guard cells inducing stomatal closure (iii) Adjusts water balance by elevating root hydraulic conductivity and mitigates osmotic stress (iv) ABA regulates the production of dehydrins, LEA proteins, and other protective proteins

Rapid biosynthesis of ABA promotes stress tolerance in wheat

(i) The second domain of signal protein SnRK2s regulates ABA signaling (ii) Synthesis of DELLA proteins interact with XERICO gene, which induces ABA biosynthesis

Li et al. (2010); Sreenivasulu et al. (2012); Bano and Yasmeen (2010); Yoshida et al. (2006); Chantre Nongpiur et al. (2016)

14.

Ethylene

(i) Activates the cascade of defense for stress tolerance by acting as a signal molecule (ii) Ethylene response factors

Multiple environmental stresses can lead to an increase in endogenous ethylene levels

Upregulation of ethylene synthesis occurs through activation of the MAP kinase pathway

Matyssek et al. (2008); Klay et al. (2014); Larkindale et al. (2005)

100 Abiotic stresses in wheat

all the phytohormones, abscissic acid (ABA) and ethylene have an important effect on the ability to withstand abiotic stress (Zhang et al., 2007). Table 1 summarizes the responses of these hormones and some antioxidants. Basu et al., 2016 demonstrated that under drought conditions, root architecture is controlled by the hormonal cross talk between cytokinin (CK), auxin, gibberellic acid (GA), and abscisic acid (ABA). CKs act as antagonists to ABA and serve as a vital regulatory component in ABA-mediated stress signaling. Additionally, Shakirova et al. (2010a,b) found that CKs levels decrease as a consequence of salinity, and CKs act as a way to demonstrate the protective functions of epibrassinolide and methyl jasmonate in wheat. Accordingly, Hassan and Bano (2016) asserted that a saline environment adversely affects wheat growth and productivity due to a decrease in IAA and GA content followed by the accumulation of ABA. Moreover, DELLA protein accumulation inhibits cell growth and induces stress tolerance by downregulating GA signaling, leading to ROS detoxification enzyme expression (Harberd et al., 2009). Brassinosteroids are polyhydroxy steroidal biomolecules that plants synthesize together with hormones to help with their growth and development. Brassinosteroid synthesis and initiation have been associated with wheat’s protection against UV radiation (Agati et al., 2013). In a similar way, oxylipins are converted into jasmonates in response to stress. Typically, they tend to act as antimicrobial defense mechanisms. Nevertheless, there are reports that support their role as dynamic signaling molecules in drought situations (Du et al., 2013) and in exposure to ozone and ultraviolet (Overmyer et al., 2000) radiations. Additionally, salicylic acid, an endogenous growth regulator, helps plants adapt to abiotic stress by increasing the production of antioxidant compounds like SOD (Singh and Usha, 2003) and GPX (Abbadi et al., 2015), which is produced under drought stress. Similarly, Sheng et al. (2015) found that salicylic acid application under manganese toxicity caused the synthesis of SOD, APX, CAT, and GR, while cadmium (Cd) stress caused the accumulation of ABA (Shakirova et al., 2015).

Physiological adaptation strategies The adaptation mechanisms of plant toward different abiotic stresses have been done by using different omics approaches (such as physiological, agronomic, genomics, metagenomics, met-transcriptomics, proteomics, met-proteomics, and metabolomics) (Fig. 2).

Water stress condition Wheat is sensitive to drought stress at any point in the growing season as it may occur early, late, or anytime. In India, wheat is mostly irrigated, but withholding irrigation causes moisture stress, which causes the yield of wheat to decline by 11.6%– 43.6% (Tiwari et al., 2015). Depending on when the stress occurs, the severity may differ, but if stressful events occur after anthesis, the results are more severe. The physiology of a plant will react as soon as it is exposed to stress to counteract its effects. In response to drought stress, wheat plants show a number of physiological responses (Tiwari et al., 2017). The first one is the closure of the stomata of the plant. For plants, photosynthesis, the process that gives them life, relies heavily on the pigment chlorophyll. Leaf chlorophyll content decreases when water stress is increased (Prasad et al., 2011). In the presence of drought stress and heat stress, chlorophyll production can be reduced by 49% (Pradhan et al., 2012; Awasthi et al., 2014). Compared to chlorophyll a, chlorophyll b exhibited a greater sensitivity to drought stress conditions (Nikolaeva et al., 2010). The drought-tolerant genotypes are therefore better at retaining chlorophyll content under drought

FIG. 2 Various biotechnological approaches for the survival of wheat against abiotic stresses (Hossain et al., 2021).

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stress conditions (Keyvan, 2010). The electron transport of photosystem II is reduced or removed in drought stress. Rolling the leaf when under water stress is an indication of maintaining turgor as part of avoiding dehydration. According to Hasanuzzaman et al. (2013), wheat flag leaf rolling improves the efficiency of water metabolism in response to drought stress. Furthermore, as the roots of the plants extend, those genotypes that have deeply rooted plants are considered drought-tolerant. Plants with low canopy temperatures are better able to maintain plant water status and better absorb soil moisture. Wheat plants with low canopy temperatures are drought-tolerant. Under drought stress conditions, the water potential of the wheat plant also decreases (Nayyar and Gupta, 2006). Water scarcity may also reduce the number of grains during the microspore formation stage during meiosis, resulting in pollen sterility ( Ji et al., 2010).

Heat stress Abiotic stresses like heat stress affect wheat growth and development throughout all stages, from germination to growth and emergence of leaves, roots, and reproductive stages, and even the production of seeds (Fleitas et al., 2020; Buttar et al., 2020). Under extreme heat stress, plants lose their photosynthesis enzymes, such as Rubisco, invertase, and PEP carboxylase, causing them to die. Additionally, heat stress causes leaf shedding, floral abortion, and organ injury and death (Kumar et al., 2019). Thylakoid membrane integrity is also disrupted by high temperatures (Sehgal et al., 2018). After heat wave periods, PSI activity may be reduced due to a decrease in electron transport capacity, as observed by Chovancek et al. (2019). A temperature greater than 34°C inhibits chlorophyll biosynthesis and accelerates leaf senescence (Liu et al., 2017). Flag leaf senescence may also be affected by large diurnal temperature variations (Zhao et al., 2007). According to Mendanha et al. (2018), exposed wheat plants showed increased transpiration due to an increased vapor pressure deficit. Wheat plant development is severely hindered by a high concentration of reactive oxygen species (ROS) caused by heat stress (Caverzan et al., 2016). Temperature increases will decrease photosynthesis. However, the rate of respiration will increase to a certain level to about 50°C, at which point there will be destruction of the respiratory proteins and mechanisms. According to Asthir et al. (2012), an increase in respiration decreases the availability of photoassimilates and their transportation from leaves to grains, causing a decrease in plant growth. The tissues of the plant absorb water to maintain the temperature. Nevertheless, rising temperatures cause less water to be available, resulting in a decline in leaf water potential and leaf relative water content, LRWC (Fahad et al., 2019). Reproduction and grain filling are negatively affected by a decrease in LRWC.

Saline and alkaline stress Plants under saline stress conditions produce osmolytes, alter cellular ionic concentrations, and compartmentalize their cells. Stressed wheat plants suffer from excessive sodium accumulation in the cytoplasm, which results in ionic toxicity (Su et al., 2020). In response to salinity stress, plants’ cytosols and cell vacuoles prevent Na+ ions from entering their roots. Approximately 98% of Na+ ions can be excluded by limiting Na+ ion uptake at the root-soil interface and xylem loading in roots (Tester and Davenport, 2003). H+-ATPase activity in the plasma membrane and SOS1 homologs are responsible for this process. Genc et al., 2019 reported the importance and difference between NaCl osmotic potential and Na+ toxicity. However, osmoregulation is a more important mechanism for salinity tolerance than Na+ exclusion from the leaf. A second nutrient which helps wheat plants maintain stability under salinity stress is potassium (Wu et al., 2015). Plants are typically screened for tolerance using the K+/Na+ ratio (Genc et al., 2016, and Oyiga et al., 2018). As plants lose less water in the rhizosphere, they overcome the lower osmotic potential (Hedrich and Shabala, 2018). In addition to oxidative damage, salt stress produces reactive oxygen species (ROS). Similar to alkali stress, high pH and Na+ toxicity have an adverse impact on plants (Zhang et al., 2020). A breakdown of the proton gradient across root membrane leads to high soil pH and damage to plants (Wang et al., 2015).

Abiotic stress mitigation strategies Plant hormones Hormones influence plants’ ability to adjust to stressful conditions, such as heat, frost, and drought. In addition to auxin, cytokinin (CK), ethylene, gibberellic acid (GA), abscisic acid (ABA), other major hormones are strigolactones, brassinosteroids, and jasmonic acid. Stress hormones help maintain physiological processes in plants during stressful times, which is why ABA is known as “stress hormone.” The major processes interceded by ABA are stress-induced senescence and abscission.

102 Abiotic stresses in wheat

In times of drought, ABA-altered root architecture increases soil water uptake. Additionally, it enhances the development of deeper root systems in plants as well as improving hydraulic conductivity and cell turgor in order to ameliorate desiccation resistance. ABA levels increase in plant parts exposed to salinity stress. Stress causes stomata to close, resulting in diminished photosynthetic rate, transpirational water loss, and stomatal conductance due to oversynthesis of ABA under stress (Wei et al., 2017). In addition, accumulation of endogenous ABA in anther tissue has also been suggested to impact male fertility ( Ji et al., 2010). Autin, ethylene, and cytokinins (CKs) are other hormones that could influence ABA biosynthesis and effects. According to one hypothesis, grains have higher ABA concentrations because of autosynthesis inside the grains as well as translocation from leaves and roots during drying. Drought increases proline production when ABA is present. The activity of expansin protein is positively correlated with auxin and negatively correlated with ABA under oxidative stress. It results in decreased cell division and elongation under stress conditions (Tromas et al., 2013; Kosova´ et al., 2012), leading to reduced pollen viability (Sakata et al., 2010). The growth regulators (IAA and GA) have the ability to inhibit the effects of salinity on wheat seeds prior to sowing. The effects of salinity have been mitigated through the use of a number of plant growth stimulators. Gibberellic acid, zeatin, and ethephon are all known to do so (Afzal et al., 2005). Conversely, it inhibits the germination of seeds and the lengthening of stems (Fleet and Sun, 2005). Khobra et al. (2020) conducted a study that showed seedling vigor and drought tolerance of wheat to be improved by exogenous administration of melatonin (N-acetyl-5-m
ethoxytryptamine). When water-deficit conditions are present, cytokinins (CKs) are responsible for stimulating osmotic adjustment while downregulating the development of the endosperm, photosynthetic reserve, and apical shoot meristem. Researchers hypothesized that plant hormones such as auxins and ABAs could enhance salt tolerance in wheat plants by interacting with CKs. Wheat seedlings grow more rapidly with kinetin exogenously applied. A unique feature of ethylene is that it is produced within the body as a gas from an amino acid called S-adenosyl methionine (SAM). The chemical is mainly responsible for negatively regulating growth hormone activity (Kosova´ et al., 2012; Yang et al., 2017). As a component of plant growth and development, ethylene is important for senescence, abscission, ripening of fruit, maturation of seeds, drying, and dispersal (Wilkinson and Davies, 2010). It has been found that ethylene release inhibits root and leaf growth in addition to reducing embryo absorption as well as reducing grain filling (Wilkinson et al., 2012). In addition to imparting resistance to abiotic stresses, brassinosteroids are thought to display pleiotropy by affecting multiple developmental processes, including seed germination, seed growth, rhizogenesis, flowering, and pollination. A plant hormone called salicylic acid (SA) regulates various processes including germination, photosynthesis, and antioxidant activity (Fardus et al., 2018). When wheat plants were treated with SA, they produced more antioxidants, which meant they were less susceptible to oxidative damage in heat, drought, and saline conditions (Noreen et al., 2017). Through a NADPH-oxidase-dependent increase in H2O2 production, exogenous applications of SA mitigated damage caused by abiotic stresses (Agarwal et al., 2005a,b). Stress tolerance may be bridged by jasmonic acid (JA) signaling. Wheat seedlings treated with 2 mM JA were more salttolerant. As a result, superoxide dismutase, peroxidase, catalase, and ascorbate peroxidase are expressed and enzymatic activity is increased (Qiu et al., 2014). Therefore, minimal H2O2 and other ROS were produced, which would otherwise pose a threat to cellular viability.

Agronomic interventions Crop management under abiotic stresses can also benefit from some agronomical practices.

Heat stress Conservation agriculture has proven effective under heat stress conditions. The strategy calls for reducing tillage practices and adopting diversified, economically viable crop rotations. Zero tillage (ZT) is a resource-conserving practice that allows wheat to be sown after rice harvest so that the grain can be filled before heat stress is experienced (Mehla et al., 2000). Plants can be saved from heat stress through sprinkler irrigation when temperatures exceed 30°C (Shankar et al., 2015). Light irrigation can help reduce heat stress in seedlings at the beginning of their growth process, like when they are tillering or booting. As a conservation agriculture practice, soil moisture conservation, soil organic matter improvement, and modulating temperature fluctuations are all practices that mitigate temperature stress in soil. By sowing wheat with zero tillage immediately following harvesting of a previous crop, a lot of water can be saved as it is possible to sow very early in a wheat crop and it makes use of residual moisture in the soil. As a consequence, terminal heat stress can be avoided and water can be saved from pre-sowing irrigation (Rane et al., 2007).

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Drought stress Water resources can be efficiently managed using methods like furrow irrigation, sprinklers, and drip irrigation. The biomass of plants can be increased when drought stress is present by using PGPR-based biofertilizers coupled with salicylic acid (SA). A simultaneous increase in photosynthetic pigments, relative water content, osmolytes, and defensive system activity leads to this result. A combination of SA and BF significantly enhanced leaf water status, chlorophyll a, chlorophyll b, and carotenoids synthesis under drought stress. Additionally, SA and BF made the plants more tolerant to drought stress because of the enhanced CAT, APX, POD, and SOD activities (Azmat et al., 2020).

Salt stress Salty soils can be reclaimed via mechanical scraping of salts, flushing with good quality water works well in crusted or low permeability soils and leaching works well in saline soils with fine structure and internal drainage. The calcareous subsurface is incorporated after leaching and deep ploughing alkali/sodic soils with acidifying minerals like pyrite and gypsum. According to Astolfi and Zuchi (2013), sulfur absorption plays a critical role in salt stress related metabolic changes. Plants are associated with salinity stress resistance through polyamines (PAs), which come from S-adenosyl methionine (Chen et al., 2014).

Waterlogging As a result of applying organic manure to the soil, physical factors are improved, crusting at the surface of the soil is reduced, plant rooting is enhanced, and pan formation is alleviated, thus producing higher yields. A higher infiltration rate causes a problem of water logging. By increasing soil organic content, the problem can be solved. Water logging can be reduced by using either a drop irrigation system or a ridge and furrow system. The ridges keep the plants’ roots away from flood-prone areas while the furrows keep the soil properly drained. In addition to conservation farming and furrow-irrigated raised-bed planting, crop lodging can also be reduced by using raised-bed planting systems.

PHS PHS is caused mainly by grain wetting after maturity due to rain. Wheat can be harvested and dried when the moisture content is at least 20%; therefore, PHS and test-weight losses can be reduced. All of the equipment, including the combine and hauling capacity, must be ready to work as soon as possible.

Conclusion Crop productivity is directly or indirectly affected by abiotic stresses in one or more ways. It is true, however, that crop yield loss from stress is affected by the stage of the crop and the time during which it is stressed. There may also be differences between gene expression patterns when it comes to tolerance to stress depending on the weather. In order to understand the complex mechanisms involved with these stresses that can be influenced by a variety of genetic factors, physiology, biology, genomics, and genetic engineering need to be studied together. By analyzing wheat genome sequence information, we can identify candidate genes that are involved in complex agronomic traits. Understanding the signaling pathways activated by abiotic stress is essential for developing new technologies that reduce yield losses caused by abiotic stress. The application of plant hormones or preseeding applications of plant hormones is another option.

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Modern Techniques of Raising Field Crops, fourth ed. Oxford and IBH Publishing Co., Pvt. Ltd., New Delhi, India, p. 46. Singh, R.P., Jha, P., Jha, P.N., 2017a. Bio-inoculation of plant growth-promoting rhizobacterium Enterobacter cloacae ZNP-3 increased resistance against salt and temperature stresses in wheat plant (Triticum aestivum L.). J. Plant Growth Regul. 36 (3), 783–798. Singh, S.K., Saxena, R., Porwal, A.N., Ray, S.S., 2017b. Assessment of hailstorm damage in wheat crop using remote sensing. Curr. Sci. 112, 2095–2100. Singh, B., Usha, K., 2003. Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regul. 39 (2), 137–141. Sreenivasulu, N., Harshavardhan, V.T., Govind, G., Seiler, C., Kohli, A., 2012. Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long-term drought stress? Gene 506 (2), 265–273. Su, T., Li, X., Yang, M., Shao, Q., Zhao, Y., Ma, C., Wang, P., 2020. Autophagy: an intracellular degradation pathway regulating plant survival and stress response. Front. Plant Sci. 11, 164. https://doi.org/10.3389/fpls.2020.00164. Sumithra, K., Reddy, A.R., 2004. Changes in proline metabolism of cowpea seedlings under water deficit. J. Plant Biol. 31, 201–204. Suzuki, N., Miller, G., Morales, J., Shulaev, V., Torres, M.A., Mittler, R., 2011. Respiratory burst oxidases: the engines of ROS signaling. Curr. Opin. Plant Biol. 14 (6), 691–699. Tabaeizadeh, Z., 1998. Drought-induced responses in plant cells. Int. Rev. Cytol. 182, 193–247. Tack, J., Barkley, A., Nalley, L.L., 2015. Effect of warming temperatures on US wheat yields. Proc. Natl. Acad. Sci. 112 (22), 6931–6936. Talaat, N.B., Shawky, B.T., 2012. 24-Epibrassinolide ameliorates the saline stress and improves the productivity of wheat (Triticum aestivum L.). Environ. Exp. Bot. 82, 80–88. Talaat, N.B., Shawky, B.T., 2013. 24-Epibrassinolide alleviates salt-induced inhibition of productivity by increasing nutrients and compatible solutes accumulation and enhancing antioxidant system in wheat (Triticum aestivum L.). Acta Physiol. Plant. 35 (3), 729–740. Talaat, N.B., Shawky, B.T., 2014a. Modulation of the ROS-scavenging system in salt-stressed wheat plants inoculated with arbuscular mycorrhizal fungi. J. Plant Nutr. Soil Sci. 177 (2), 199–207.

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Talaat, N.B., Shawky, B.T., 2014b. Protective effects of arbuscular mycorrhizal fungi on wheat (Triticum aestivum L.) plants exposed to salinity. Environ. Exp. Bot. 98, 20–31. Tester, M., Davenport, R., 2003. Na+ tolerance and Na+ transport in higher plants. Ann. Bot. 91 (5), 503–527. Tiwari, V., Mamrutha, H.M., Sareen, S., Sheoran, S., Tiwari, R., Sharma, P., Singh, C., Singh, G., Rane, J., 2017. Managing abiotic stresses in wheat. In: Minhas, P.S. (Ed.), Abiotic Stress Management for Resilient Agriculture. Springer Nature Singapore Pte Ltd., Singapore, pp. 313–337. Tiwari, R., Sheoran, S., Rane, J., 2015. Wheat improvement for drought and heat tolerance. In: Shukla, R.S., Mishra, P.C., Chatrath, R., Gupta, R.K., Tomar, S.S., Sharma, I. (Eds.), Recent Trends on Production Strategies of Wheat in India. Directorate of Wheat Research, Karnal, Haryana, India, pp. 39–58. Tromas, A., Paque, S., Stierl
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Further reading Abebe, T., Guenzi, A.C., Martin, B., Cushman, J.C., 2003. Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity. Plant Physiol. 131 (4), 1748–1755. Al-Quraan, N.A., Sartawe, F.A.B., Qaryouti, M.M., 2013. Characterization of γ-aminobutyric acid metabolism and oxidative damage in wheat (Triticum aestivum L.) seedlings under salt and osmotic stress. J. Plant Physiol. 170 (11), 1003–1009. Ashraf, M.A., Ali, Q., 2010. Response of two genetically diverse wheat cultivars to salt stress at different growth stages: leaf lipid peroxidation and phenolic contents. Pak. J. Bot. 42 (1), 559–565. Barta, C., Dunkle, A.M., Wachter, R.M., Salvucci, M.E., 2010. Structural changes associated with the acute thermal instability of Rubiscoactivase. Arch. Biochem. Biophys. 499 (1-2), 17–25. https://doi.org/10.1016/j.abb.2010.04.022. Chen, D., Wang, X., Wang, X., Feng, K., Su, J., Dong, J., 2020. The mechanism of cadmium sorption by sulphur-modified wheat straw biochar and its application cadmium-contaminated soil. Sci. Total Environ. 714, 136550.

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Chinnusamy, V., Zhu, J., Zhu, J.K., 2006. Salt stress signaling and mechanisms of plant salt tolerance. Genet. Eng., 141–177. Fougere, F., Le Rudulier, D., Streeter, J.G., 1991. Effects of salt stress on amino acid, organic acid, and carbohydrate composition of roots, bacteroids, and cytosol of alfalfa (Medicago sativa L.). Plant Physiol. 96 (4), 1228–1236. Gull, A., Lone, A.A., Wani, N.U.I., 2019. Biotic and abiotic stresses in plants. In: De Oliveira, A.B. (Ed.), Abiotic and Biotic Stress in Plants. IntechOpen, London, UK. Kaushal, M., Wani, S.P., 2016. Plant-growth-promoting rhizobacteria: drought stress alleviators to ameliorate crop production in drylands. Ann. Microbiol. 66 (1), 35–42. https://doi.org/10.1007/s13213-015-1112-3. Mastrandrea, M.D., Mach, K.J., Plattner, G.K., Allen, S.K., et al. (Eds.), 2012. Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation. Cambridge University Press, Cambridge, UK; New York, NY, USA, p. 582. Nishiyama, R., Le, D.T., Watanabe, Y., Matsui, A., Tanaka, M., Seki, M., Tran, L.S.P., 2012. Transcriptome analyses of a salt-tolerant cytokinin-deficient mutant reveal differential regulation of salt stress response by cytokinin deficiency. PLoS One 7 (2), e32124. Petrusa, L.M., Winicov, I., 1997. Proline status in salt-tolerant and salt-sensitive alfalfa cell lines and plants in response to NaCl. In: Plant Physiology and Biochemistry (France). Raza, A., Razzaq, A., Mehmood, S.S., Zou, X., Zhang, X., Lv, Y., Xu, J., 2019. Impact of climate change on crops adaptation and strategies to tackle its outcome: a review. Plants 8 (34), 21. Shinozaki, K., Yamaguchi-Shinozaki, K., 2007. Gene networks involved in drought stress response and tolerance. J. Exp. Bot. 58 (2), 221–227. Takahashi, S., Murata, N., 2008. How do environmental stresses accelerate photoinhibition? Trends Plant Sci. 13 (4), 178–182. https://doi.org/10.1016/j. tplants.2008.01.005. Tarczynski, M.C., Jensen, R.G., Bohnert, H.J., 1993. Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259 (5094), 508–510. Thomas, J.C., Sepahi, M., Arendall, B., Bohnert, H.J., 1995. Enhancement of seed germination in high salinity by engineering mannitol expression in Arabidopsis thaliana. Plant Cell Environ. 18 (7), 801–806. Triantaphylide`s, C., Havaux, M., 2009. Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci. 14 (4), 219–228. Wang, C., Deng, P., Chen, L., Wang, X., Ma, H., Hu, W., He, G., 2013. A wheat WRKY transcription factor TaWRKY10 confers tolerance to multiple abiotic stresses in transgenic tobacco. PLoS One 8 (6), e65120. https://doi.org/10.1371/journal.pone.0065120. Zeeshan, M., Lu, M., Sehar, S., Holford, P., Wu, F., 2020. Comparison of biochemical, anatomical, morphological, and physiological responses to salinity stress in wheat and barley genotypes deferring in salinity tolerance. Agronomy 10 (1), 127. Zlatev, Z., Lidon, F.C., 2012. An overview on drought induced changes in plant growth, water relationsand photosynthesis. Emirates J. Food Agric., 57– 72. https://doi.org/10.9755/ejfa.v24i1.10599.

Chapter 7

Role of phytohormones in regulating abiotic stresses in wheat Neveen B. Talaat⁎ Department of Plant Physiology, Faculty of Agriculture, Cairo University, Giza, Egypt *

Corresponding author. e-mail: [email protected]

Introduction Unfavorable environmental conditions have a direct effect on plant production. They have significant effects on modern agriculture. As a result of the changing environment, recent climate change models forecast large losses in agricultural productivity worldwide, with losses of up to 42 Mt/°C in wheat (Carraro et al., 2015). Even though wheat has the largest overall harvested area (38.8%), its total productivity is the lowest among the other cereal crops (Abhinandan et al., 2018). As a result of climate change, multiple abiotic stresses such as salinity, drought, heat, cold, nutrient deficiency, oxidative stress, and heavy-metal toxicity have emerged, posing a threat to agricultural output and resulting in a 70% average yield loss of major staple crops, raising serious food security concerns (Talaat, 2019a; Lamers et al., 2020). Abiotic stresses that wheat plants are exposed to throughout development can have a negative impact on their growth and productivity (Hussain et al., 2019; Nasharty et al., 2019; Talaat, 2021a,b). Significant decreases in wheat grain yield and plant biomass can result from these harsh conditions (Talaat and Shawky, 2012a; Aldesuquy et al., 2014a,b; Zhang et al., 2019). When wheat plants are exposed to abiotic challenges, reactive oxygen species (ROS) are formed in their tissues, causing damage to the plants’ physiobiochemical processes, obstructing their normal growth and development (Sun et al., 2018; Seleiman et al., 2020; Talaat and Shawky, 2022; Talaat and Todorova, 2022). ROS are largely produced during abiotic stresses and trigger the synthesis of stress-responsive transcription factors (TFs), mitogen-activated protein kinases (MAPKs), and antioxidant enzymes to aid wheat plant survival in extreme conditions (Moghaieb et al., 2011; Cui et al., 2017; Talaat, 2019b; Buttar et al., 2020). Abiotic stresses can also disrupt physiological, biochemical, and molecular homeostasis in wheat plants, such as membranes integrity, enzyme and photosynthetic activities, nutrient and water uptake, as well as hormonal balance (Abhinandan et al., 2018; Zhang et al., 2019; Tofighi et al., 2021). The production and distribution of endogenous hormones are linked to the changes that occur in plants as a result of various stresses (Talaat, 2019c; Sabagh et al., 2021). Hence, understanding the effects of these abiotic stresses becomes critical. Even though several policies aimed at ensuring food security have been implemented, increasing agricultural productivity under adverse environmental conditions remains one of the most difficult issues. Thus, crop production is currently a major problem in agricultural policy, and mitigation strategies must focus on improving plant productivity while dealing with limited resources. Wheat (Triticum aestivum L.) is one of the world’s most significant cereal crops. It is considered an important global food security commodity. The global wheat production in 2016 was 749 million tons (Shin et al., 2017). Wheat serves 4.5 billion people worldwide with 20% of their daily protein and calorie needs (Setter et al., 2016; Cosgrove, 2021). Modern agriculture faces a big issue in improving wheat stress tolerance. Exogenous applications have been demonstrated to increase wheat plants development under environmental stresses. Plant growth regulators (PGRs) are crucial chemical messengers that regulate plant responses to a wide range of environmental stresses, allowing plants to adapt to harsh conditions (Todorova et al., 2016; Wani et al., 2017; Murch and Erland, 2021). Abiotic stress major effects are on wheat growth and production, and both of them can be promoted by PGRs (Li et al., 2020a,b; Talaat, 2021a,b). Auxins, cytokinins, gibberellins, abscisic acid, ethylene, jasmonic acid, brassinosteroids, salicylic acid, polyamines, melatonin, nitric oxide, and strigolactone are all PGRs that play a role in stress adaptation by modulating different plant processes as well as upregulating the transcription factors, metabolic genes, and stress proteins (Sabagh et al., 2021). Photosynthesis, protein synthesis, respiration, nutrient and water uptake, source/sink transition, osmotic adjustment, and antioxidant activity are all regulated by PGRs during stress circumstances (Todorova et al., Abiotic Stresses in Wheat. https://doi.org/10.1016/B978-0-323-95368-9.00019-9 Copyright © 2023 Elsevier Inc. All rights reserved.

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2016; Talaat and Shawky, 2022). PGRs also have an impact on ROS detoxification (Xia et al., 2015; Shopova et al., 2021a, b). They interact with complex signaling networks to overcome damage induced by stressful environmental conditions (Iqbal et al., 2019). Signal reception on the cell surface, production of secondary messengers, and protein phosphorylation all contribute to the activation of stress-responsive genes in phytohormonal signaling (Xia et al., 2018). Plants have evolved complicated mechanisms for detecting environmental signals and can respond optimally to stress situations with the help of PGRs, which primarily control plant defense responses through signaling cross talk (EL Sabagh et al., 2021). This chapter provides an overview of the physiological changes that occur in wheat as a result of different abiotic stresses. Furthermore, it gives an understanding of the recent progress made by new PGRs such as melatonin (MT), salicylic acid (SA), brassinosteroids (BRs), and polyamines (PAs) in improving wheat tolerance to abiotic stresses such as salinity, drought, heat, cold, nutrient deficiency, and heavy-metal toxicity. It also draws attention to research gaps in understanding the underlying processes of these PGRs’ potential functions in conferring tolerance to the negative impacts of unfavorable environmental growth conditions.

Effects of abiotic stresses on physiological, biochemical, and molecular mechanisms of the wheat plant Abiotic stresses such as salt, drought, high temperature, low temperature, waterlogging, nutrients deficiency, and heavymetal toxicity cause alteration in wheat plants’ morphological, physiological, biochemical, and molecular processes (Fig. 1). Harmful effects of these environmental stresses start from seeds germination to the plants maturity. These harsh environmental conditions have a negative impact on wheat growth and development, resulting in larger economic losses at the expense of global food security (Abhinandan et al., 2018; Talaat, 2019a; Lamers et al., 2020). As a result, environmental stresses have a significant impact on global wheat productivity.

Influence of salinity One of the key environmental constraints that restrict plant growth and result in considerable yield losses is salt stress (Talaat, 2014, 2015; Liang et al., 2018; Rady et al., 2019; Talaat et al., 2022). Increasing salinization in semiarid and arid regions is threatening global food security by decreasing crop productivity. Salty soils are rapidly spreading, with 50% of arable agriculture anticipated to be affected by 2050 (Shrivastava and Kumar, 2015; Yang et al., 2021). Every year, salinity damages 2 million hectares (about 1% of the world’s agricultural areas), resulting in reduced or no plant yield (Abhinandan et al., 2018). Salinity has a deleterious impact on plant physiology through a variety of processes. Increased sodium ion accumulation damages cellular organelles, affects protein synthesis, photosynthesis, and respiration, as well as inhibits enzymes activity. Salinity also reduces nutrient uptake and transportation to the shoot; moreover, it lowers soil osmotic potentials and inhibits root water uptake (Ruiz-Lozano et al., 2012; Talaat, 2019c). Wheat (T. aestivum L.) is affected by soil salinization in its growing region. High salt levels cause ion toxicity. Saltstressed wheat plants accumulate sodium (Na+), which causes a decrease in potassium (K+) absorption, resulting in a severe deficit of K+ level, and disturbance in K+/Na+ ratio (Talaat and Shawky, 2011, 2014; Shah et al., 2021). The macronutrient K+ is required for osmotic correction, turgor pressure generation, and enzymes activity. However, Na+ induces hypertension, lowers turgor pressure, and deactivates the enzymes. As a result, K+/Na+ homeostasis is critical for plant health (Almeida et al., 2017). High sodium and chloride concentrations in plant cells disrupt ion homeostasis and cause membrane dysfunction, as well as a reduction in metabolic activity and development (Al Hinai et al., 2022). Excessive salt concentration causes osmotic stress, which prevents important nutrient ions from being taken in and used, resulting in moisture loss and electrolytic leaching owing to cell membrane damage (Zhang et al., 2022). Wheat plants can also activate an osmoregulatory mechanism under saline environments by accumulating low-molecular-weight osmolytes including soluble sugars, glycinebetaine, and proline (Talaat, 2021a; Al Hinai et al., 2022). Photosynthesis is an important physico-chemical process for energy production in higher plants (Talaat, 2013). Salt stress can also affect wheat growth and production by hampering photosynthetic activity. It inhibits the photosynthetic electron transport causing an overabundance of toxic ROS, which promote chlorophyll degradation, reduce consumption of NADPH by the Calvin cycle, lower photochemical efficiency of photosystem II, decrease gas exchange, impair chlorophyll fluorescence, destroy photosynthetic organs, and decrease photosynthetic enzymes activity (Talaat, 2021a; Al Hinai et al., 2022). Furthermore, salt stress causes an overproduction of ROS such as superoxide radical (O2  ), singlet oxygen (1O2), hydroxyl radical (OH ), and hydrogen peroxide (H2O2) in wheat tissues. ROS can impair cell membranes via lipid peroxidation and protein denaturation; moreover, they can inactivate a variety of important enzymes (Talaat and Shawky,

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FIG. 1 A model showing harmful effects of the environmental stresses on various morphological, physiological, biochemical, and molecular processes of wheat plants.

2012a; Zhang et al., 2022). Wheat plants have developed powerful defense responses that include nonenzymatic antioxidants like alkaloids, carotenoids, α-tocopherol, ascorbic acid (AsA), and glutathione (GSH) as well as enzymatic antioxidants like catalase (CAT), superoxide dismutase (SOD), peroxidase (POD), ascorbate peroxidase (APX), glutathione reductase (GR), glutathione peroxidase (GPX), glutathione S-transferase (GST), monodehydroascorbate reductase (MDHAR), and dehydroascorbate (DHAR) (Tofighi et al., 2017; Talaat and Shawky, 2013, 2022).

Influence of drought Drought is a global issue that can create significant osmotic stress in practically any wheat-producing zone. Drought is growing more often and more persistent as a result of global warming, posing a greater risk to crop production (Sarto

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et al., 2017). It has a significant impact on global wheat output. It is one of the most serious problems that wheat plants face when it comes to development (Avalbaev et al., 2020; Li et al., 2020a,b). Drought has an impact on 60% of wheat production in high-income nations and 30% of wheat production in low-income countries. It is responsible for up to 70% of yield losses (Zampieri et al., 2017). Water shortage can lower wheat seed germination potential, reduce shoot and root growth, decrease dry matter accumulation, impair photosynthetic rate, damage the enzymatic system, cause stomatal closure, as well as reduce relative water content (Abid et al., 2016; Cui et al., 2018; Li et al., 2020a,b). It can also reduce the grains number by disrupted floret abortion and pollen sterility (Dong et al., 2017). Drought can alter wheat metabolic activities, such as photosynthesis, impairing sugar synthesis, which is essential to drive wheat yield (Cui et al., 2017; Li et al., 2017). Moreover, it alters osmolyte buildup and raises MDA level in wheat tissues (Maghsoudi et al., 2019; Azmat et al., 2020). Drought stress also reduces carbon assimilation, resulting in an imbalance between electron excitation and utilization through photosynthesis, resulting in the production of ROS, notably H2O2 and O2  , which cause oxidative stress by damaging cell membranes, proteins, and nucleic acids. Water-stressed wheat plants have both enzymatic and nonenzymatic activities to eliminate ROS (Pa´l et al., 2018; Li et al., 2020a,b). Osmotic stress can affect wheat crops at any stage of development, resulting in cellular damage. The amount of cellular damage created during wheat development can be affected by the degree and duration of osmotic stress, impacting growth and developmental processes and resulting in substantial yield losses (Sarto et al., 2017). Germination is a particularly sensitive stage because it influences crop density, which in turn influences productivity. A shortage of water in the soil may hinder seeds’ ability to absorb moisture, which is necessary for proper germination (Almansouri et al., 2001). Crops may be exposed to heat stress at the end of the growing season if germination is delayed, or crop maturation may be uneven (Rauf et al., 2007). Drought conditions during tillering have a substantial impact on wheat yield by reducing kernel number (Abid et al., 2018). Water shortage before or during anthesis has been shown to reduce grains number; additionally, the occurrence of a water deficit during anthesis and grain-filling might result in significant yield loss by altering a variety of developmental processes (Verbeke et al., 2022). Wheat plants suffer from lower height, tillering, leaf area, biomass, yield, and water-use efficiency as a result of preanthesis drought (Abid et al., 2016; Lou et al., 2021).

Influence of temperature changes Heat stress is one of the most harmful abiotic stresses ( Jha et al., 2021). Pseudo-seed setting issues in wheat are caused by high temperatures interfering with pollen development, viability, and fertilization (Kumar et al., 2013). High temperatures during the reproductive phase of wheat plants can have a negative influence on grain number and filling (Farooq et al., 2011). High temperatures during the kernel filling stage might affect seed size due to higher respiration rates, which can lead to a reduction in the flour quality (Abhinandan et al., 2018). Heat stress denatures the key enzymes that involves in numerous metabolic pathways, signaling, and defense systems in wheat plants (Farooq et al., 2011). As a wheat stress-tolerance approach, changes in gene expression and transcript accumulation occur immediately after exposure to high temperatures, leading in the production of stress-associated proteins (SAPs) (Kumar et al., 2012, 2015). SAPs such as heat-responsive transcription factors (TFs), heat shock proteins (HSPs), antioxidant enzymes, signaling molecules, and others are recognized to have a critical role in regulating wheat’s defense mechanisms in response to heat stress, and their expression is a key adaptive strategy (Kumar et al., 2013; Buttar et al., 2020). Heat stress has also been linked to an increase in antioxidants, osmolytes, and metabolites in wheat (Kumar et al., 2015; Afzal et al., 2020; Iqbal et al., 2021). Heat stress changes membrane fluidity, leading in rapid ROS generation and an increase in Ca2+ influx (Kurusu et al., 2012). The heat shock transcription factor, HsfA1, is the master regulator of plant heat responses and can be activated by ROS and Ca2+ (Ohama et al., 2017). When plants subjected to heat stress, the HSP levels in the cytoplasmic pool are significantly elevated (Driedonks et al., 2015). Furthermore, if plants are subjected to nonfreezing temperatures below 12°C for an extended period, they will acquire a physiological malfunction known as “low-temperature damage” (Seydpour and Sayyari, 2015). Indeed, there are two types of cold stress: (a) chilling stress, which happens when temperatures are above freezing but below optimal growing temperatures, and (b) freezing stress, which occurs when temperatures drop below freezing (Abhinandan et al., 2018). Lowtemperature stress alters plant metabolic processes, slowing plant development and inhibiting photosynthesis (Zhuang et al., 2019). Leaf necrosis, irregular plant maturation, lipid cell membrane breakdown, and reduced thylakoid electron transfer are all symptoms of low-temperature stress (Turk et al., 2014; Sun et al., 2018; Wang et al., 2021a). Under this unfavorable condition, ROS will also be produced in large quantities, disrupting the equilibrium and accumulating to dangerous levels, causing serious damage to plant development (Wang et al., 2018; Zhang et al., 2019). Cold stress results in

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the synthesis of antioxidants, the generation of ROS, the release of calcium ions, and the activation of multiple transcriptional cascades (Turk et al., 2014; Ignatenko et al., 2019).

Influence of heavy-metal toxicity Bioaccumulation of heavy metals such as boron (B), chromium (Cr), Cadmium (Cd), copper (Cu), lead (Pb), arsenic (As), zinc (Zn), mercury (Hg), and aluminum (Al) is a key abiotic constraint that restricts crop yield, especially in arid and semiarid regions (Seneviratne et al., 2019). They disrupt the natural ecological balance by accumulating in high quantities in the soil and remaining in the environment for longer periods (Adithya et al., 2021). Heavy-metal pollution has increased in many developed and developing countries as a result of rapid industrialization, long-term irrigation with low-quality water, and intensive agricultural (Khan et al., 2018). Heavy-metal toxicity can affect nutrient homeostasis, gas exchange characteristics, enzymes activity, antioxidants production, protein mobilization, and photosynthesis in plants (Seleiman et al., 2020; Al-Huqail et al., 2020). By accumulating MDA and forming ROS, it promotes osmotic imbalance and increases electrolyte leakage and membrane damage (Kaya et al., 2019; Lei et al., 2021). These heavy metals, as redoxactive metals, can stimulate the generation of hazardous ROS such as H2O2, O2  , and OH . Lipid peroxidation, membrane degradation, and enzyme inactivation are all caused by ROS reacting with lipids, proteins, and nucleic acids. In heavy-metals-stressed plants, oxidative stress has been implicated as one of the key factors causing cellular damage (Yusuf et al., 2017; Filek et al., 2018; Yu et al., 2019). Plants have been shown to regulate the production of various metabolites, chelating compounds, root exudates, or an increase in endodermis thickness to limit heavy-metal uptake and transport (Khan et al., 2021). Toxicity from heavy metals varies with species, dose, heavy-metal exposure, and plant type (Khan et al., 2018, 2021).

Potential roles of plant growth regulators in challenging the deleterious effects of abiotic stresses on wheat plants PGRs, both exogenously applied and endogenously produced, can reduce the detrimental effects of the unfavorable environmental conditions. They are important for controlling stress adaption by modulating physiological, biochemical, and molecular processes (Table 1 and Fig. 2), allowing plants to adapt to these stressful conditions.

Role of melatonin in the alleviation of abiotic stresses Melatonin (MT, N-acetyl-5-methoxy-tryptamine) is a mammalian neurohormone, antioxidant, and signaling molecule. In 1995, it was discovered in plants (Dubbels et al., 1995; Hattori et al., 1995); moreover, it is now recognized as a ubiquitous biomolecule synthesized in all kingdoms (Arnao and Herna´ndez-Ruiz, 2014). It is a small-molecule indole hormone that plays a role in the control of various biological activities as well as abiotic stress resistance. Previous reports have demonstrated that via influencing several physiological regulatory systems, it plays a crucial role in promoting normal plant TABLE 1 Summary of wheat plants hormonal responses following exposure to abiotic stresses such as salt, drought, high temperature, low temperature, and heavy-metals toxicity. Hormone response

Salinity

Drought

High and low temperatures

Ke et al. (2018) Zafar et al. (2019) Talaat (2021a) Talaat (2021b) Zhang et al. (2022) Talaat and Shawky (2022) Talaat and Todorova (2022)

Cui et al. (2017) Li et al. (2017) Cui et al. (2018) Li et al. (2020a,b)

Turk et al. (2014) Sun et al. (2018) Buttar et al. (2020) Iqbal et al. (2021)

Heavy metals

Melatonin Induce hormonal responses Regulate stress-responsive gene expression Enhance photosynthetic ability Stimulate protein synthesis Regulate polyamine metabolism Enhance osmotic adjustment Maintain high water content Maintain ion absorption Scavenge free radicals Reduce oxidative damage Induce membrane stability Maintain source/sink transition

Kaya et al. (2019) Al-Huqail et al. (2020) Seleiman et al. (2020) Lei et al. (2021)

Continued

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TABLE 1 Summary of wheat plants hormonal responses following exposure to abiotic stresses such as salt, drought, high temperature, low temperature, and heavy-metals toxicity—cont’d

Hormone response

High and low temperatures

Salinity

Drought

Heavy metals

Suhaib et al. (2018) Mohammadi et al. (2019) Nasharty et al. (2019) Yadav et al. (2020) Pirasteh-Anosheh et al. (2021) Talaat (2021a) Talaat (2021b) Talaat and Shawky (2022) Talaat and Todorova (2022)

Ilyas et al. (2017) Rihan et al. (2017) Sharma et al. (2017) Maghsoudi et al. (2019) Azmat et al. (2020) Sedaghat et al. (2020) Ahmad et al. (2021) Khalvandi et al. (2021) Maswada et al. (2021) Munsif et al. (2021) Shemi et al. (2021)

Kumar et al. (2015) Wang et al. (2018) Ignatenko et al. (2019) Zhang et al. (2019) Afzal et al. (2020) Wang et al. (2021a) Wang et al. (2021b)

Agami and Mohamed (2013) Kova´cs et al. (2014) Shakirova et al. (2016a)

Talaat and Shawky (2012b) Talaat and Shawky (2013) Abdellatif (2017) Dong et al. (2017) Tofighi et al. (2017) Tofighi et al. (2021)

Shakirova et al. (2016b) Zhao et al. (2017) Avalbaev et al. (2020)

Zhao et al. (2017) Hussain et al. (2019) Zhang et al. (2019)

Kroutil et al. (2010) Hayat et al. (2014) Yusuf et al. (2017) Filek et al. (2018) Bezrukova et al. (2021)

Aldesuquy et al. (2014a)

Yang et al. (2014) Liu et al. (2016) Pa´l et al. (2018) Li et al. (2020a,b)

Gu et al. (2019)

Aldesuquy et al. (2014b) Rady and Hemida (2015) Yu et al. (2015) Agami (2016) Tajti et al. (2018)

Salicylic acid Preserve cellular redox homeostasis Increase photosynthetic activity Improve secondary metabolites production Link to the buildup of organic solutes Enhance osmotic adjustment Alleviate cellular oxidative damage Maintain membrane stability Moderate antioxidative system capacity Induce protein synthesis Maintain ionic homeostasis Activate stress-responsive gene expression Induce hormonal balance Enhance source-to-sink transport

Brassinosteroids Improve osmotic adjustment Enhance water uptake Improve photosynthetic performance Improve protein synthesis Maintain source/sink balance Improve nutrient acquisition Enhance ROS-scavenging capacity Protect cell membrane integrity Maintain intracellular redox potential Alter hormonal state Induce transcription of stressresponsive gene Polyamines Enhance photosynthetic efficiency Induce protein synthesis Contribute to ROS detoxification Regulate mineral uptake Elevate source and sink activities Target genes and activate their expression Improve organic solutes buildup Regulate water relations Alter hormonal balance Improve antioxidant defense systems

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FIG. 2 A model showing potential mechanisms of plant growth regulators induced alleviation of abiotic stresses-caused inhibition in wheat growth and productivity.

development under stressful conditions (Murch and Erland, 2021). By reacting with hydroxyl and peroxy radicals, it possesses an effective ROS-scavenging capability (Khan et al., 2020; Pardo-Herna´ndez et al., 2020). Abiotic antistressor, biological rhythm regulator, and plant hormone are just few of the functions of MT in plants (Bose and Howlader, 2020). Because of its multiple functions, MT is regarded as a master regulator and an antioxidant. Exogenous MT can improve wheat production and salt tolerance by inducing stress-related cellular changes such as inducing the hormonal responses, regulating the stress-responsive gene expression, enhancing the photosynthetic machinery, and scavenging the free radicals. A study of Ke et al. (2018) showed that exogenously applied 1 μM MT enhanced wheat tolerance to saline conditions by mitigating the deleterious effects of salt stress on plant development via improving shoot dry weight, photosynthetic ability, as well as PAs and IAA production. Reduced H2O2 buildup was also reported as a result of the mitigation. By examining the level of TaSNAT transcript, which encodes a crucial regulatory enzyme in the MT biosynthesis pathway, exogenous MT also enhanced its level, resulting in an increase in endogenous MT content. Moreover, in a different study, foliar application of 500 μM MT improved growth, yield, and biomass production of salt-stressed wheat plants, and this was accomplished by reducing oxidative damage through improving SOD, CAT, and POD activities and decreasing MDA content (Zafar et al., 2019). Exogenous application of MT was also used to mitigate damage caused by soil salinization via inducing photosynthetic capability and the carbohydrates translocation to the sink. Exogenously applied 70 μM MT considerably reduced salt-induced reductions in wheat growth and development, and this was linked to an increase in chlorophyll a, chlorophyll b, carotenoids, and total pigments content, photochemical reactions of photosynthesis, gas exchange parameters, chlorophyll fluorescence attributes, Rubisco activity, NADPH content, organic solutes production, and grains carbohydrate content, as well as a decrease in the activity of glycolate oxidase and the content of MDA, NADP+, and H2O2 in salt-stressed wheat plants (Talaat, 2021a). It is also important to note that foliar application of MT appears to regulate the PAs and nitrogen metabolism as well as stimulate protein synthesis in wheat plants subjected to salt stress. Exogenous 70 μM MT treatment improved salt-stress-damage mitigation by increasing PAs content through decreasing the contents of arginine and methionine, upregulating the activities of arginine decarboxylase, ornithine decarboxylase, and s-adenosylmethionine decarboxylase, as well as downregulating the activities of diamine oxidase and polyamine

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oxidase. MT also enhanced nitrogen metabolism in salt-stressed plants by boosting the activity of N uptake and metabolism-related enzymes (nitrate reductase, nitrite reductase, glutamine synthetase, glutamate synthase), as well as increasing nitrogen, nitrate, and protein content. Wheat-stressed plants also showed decreases in the contents of MDA, H2O2, and carbonyl by MT treatment (Talaat, 2021b). Additionally, other reports postulated that MT application significantly ameliorates the deleterious effects of salinity via enhancing osmoprotectant accumulation in the cytosol for intracellular osmotic homeostasis. Under salt stress, adding 300 mM MT to the cultivation solution increased the germination rate of wheat grains and lateral root formation. To maintain high water content, low H2O2 content, and low K+/Na+ ratio, the MT application increased enzymes activity as well as proline, soluble protein, soluble sugar, Ca2+, and amino acids accumulation in salt-stressed wheat plants (Zhang et al., 2022). Besides contributing to osmotic adjustment, MT also helps to maintain ion absorption and transportation to shoots by controlling the H+-pump activity in wheat roots and decreasing the ROS burst. This is confirmed by the observation of Talaat and Shawky (2022), who found that spraying salt-stressed wheat plants with 70 μM MT greatly boosted N, P, K+, Fe, Zn, and Cu accumulation, while it decreased Na+ uptake. It also improved the roots’ ATP content and H+-pump activity. Reduced ROS content, electrolyte leakage, and lipoxygenase activity, as well as increased SOD, CAT, POX, and PPO activities; K+/Na+, Ca2+/Na+, and Mg2+/Na+ ratios; membrane stability index; and osmotic regulation in treated plants were all indicators of the mitigation. As in the case under salinity, wheat water stress tolerance is aided by the presence of MT. Drought tolerance was first linked to MT’s antioxidant ability, which was demonstrated by its direct interaction with ROS. Secondly, in the presence of high amounts of ROS molecules, MT can regulate the activity of antioxidant enzymes and antioxidants. Evidence suggests that a 500 μM MT treatment improved wheat drought tolerance (60% and 40% of field capacity) by reducing membrane damage as well as improving photosynthetic rate, maximum efficiency of photosystem II, cell turgor, and water holding capacity. Besides, MT significantly reduced H2O2 and O2  content in stressed seedlings, which can be linked to improved GSH and AsA levels, as well as APX, MDHAR, DHAR, GPX, and GST activities. Under drought conditions, the expression of GSH-AsA-associated genes such as APX, MDHAR, and DHAR was upregulated by MT treatment, implying that the expression of these genes was responsible for the rise in GSH and AsA content (Cui et al., 2017). There is also a report that exogenous application of 1 μM and 10 μM MT seems to improve wheat drought tolerance by increasing net photosynthetic rate and water-use efficiency. This was possibly related to increasing root auxin and zeatin riboside content as well as inhibiting abscisic acid, hydrogen peroxide, and aminocyclopropane-1-carboxylic acid production in the leaf (Li et al., 2017). Furthermore, under PEG stress, it is evident that seeding priming with 500 μM MT improved wheat seeds germination rate, coleoptile length, primary root number, fresh and dry weights, as well as water content by enhancing photosynthetic ability and water-use efficiency. MT treatment also lowered H2O2, O2  , and MDA content in stressed plants via upregulating the expression of antioxidant enzymes. Besides, MT improved energy production in PEG-stressed plants by affecting the expression of glycolytic proteins; moreover, it modulated electron transport in the respiratory chain (Cui et al., 2018). Further investigation in wheat found that applying 300 μmol L 1 MT to wheat grains reduced the detrimental effects of water stress on germination rate; additionally, the content of amino acids especially lysine was changed significantly during germination. During seedling growth, the soluble protein content and the SOD activity were elevated to alleviate damage in the leaf cytomembrane (Li et al., 2020a,b). MT foliar treatment effectively reduces the negative impacts of heat stress by regulating a myriad of cellular processes, resulting in improved plant performance under this challenging environmental condition. MT overcomes the harmful effects of high-temperature stress by enhancing the activity of the ROS-scavenging system as well as lowering ROS production and MDA content. MT also improves plant heat stress tolerance by modulating stress-responsive genes, increasing photosynthetic efficiency, and increasing the accumulation of osmoprotectants. A study by Buttar et al. (2020) reported that a 100 μM MT treatment to heat-stressed wheat plants was found to considerably reduce oxidative damage by preventing the H2O2 overproduction, enhancing the antioxidant enzymes activity, activating the AsA-GSH cycle, inducing the expression of ROS-related genes and antistress-responsive genes, improving the photosynthetic efficiency, enhancing the endogenous MT content, lowering the lipid peroxidation, as well as increasing the proline biosynthesis. They concluded that increasing the level and activity of antioxidant enzymes to promote the ROS detoxification is critical for wheat heat stress tolerance. Another study demonstrated that applying 100 μM MT to wheat-stressed plants reduced oxidative stress induced by heat stress through lowering TBARS and H2O2 content as well as improving antioxidative enzymes activity. MT treatment also enhanced photosynthetic efficiency and carbohydrate metabolism, both of which are required to provide energy and a carbon skeleton to the developing stressed plants (Iqbal et al., 2021). MT has also a regulatory role in protecting wheat plants from cold stress. It can improve plant resistance to cold stress by directly scavenging ROS and modulating redox balance. Application of mmol L 1 MT significantly increased leaf surface area, water content, photosynthetic pigment content, activation of antioxidant enzymes, contents of antioxidant molecules, as well as levels of total soluble protein, carbohydrate, and proline in cold-stressed wheat plants. However, the

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accumulation of ROS and lipid peroxidation was decreased by MT in stressed plants (Turk et al., 2014). Moreover, in a different study, foliar application of 1 mM MT enhanced the photosynthetic ability, induced membrane stability, boosted antioxidant enzyme activities, and modified the associated gene expressions in cold-stressed wheat plants (Sun et al., 2018). Plant growth and productivity can be improved by MT application under nutrient deficiency conditions. MT enhances N uptake and assimilation, which in turn increases plant development under N-deficient conditions, by improving the N uptake and metabolism-related enzymes activity. Moreover, under N-deficient conditions, the use of 1 μM MT in hydroponic solution dramatically improved wheat seedling growth by increasing N contents, nitrate-nitrogen levels, as well as nitrate reductase and glutamine synthetase activities (Qiao et al., 2019). Under Cd, B, and Cr stresses, the effect of MT as a protective agent was also investigated. In heavy-metals-stressed wheat plants, MT moderated antioxidative system capacity, reduced MDA, O2  , and H2O2 content, maintained membrane stability, improved nutrient uptake, enhanced osmotic adjustment by osmoprotectant solute accumulation, and increased photosynthetic activity. Exogenously applied MT (50 or 100 mM) improved plant growth, total chlorophyll, PSII maximum efficiency, leaf water potential, potassium and calcium content, as well as antioxidant enzymes activity in Cd-stressed wheat plants. MT application to stressed plants also reduced leaf MDA, H2O2, electron leakage, and Cd levels (Kaya et al., 2019). This was also shown by the study of Al-Huqail et al. (2020), who showed that foliar application of 100 μM MT significantly induced wheat plant defense mechanisms by enhancing the content of N and P, the biosynthesis of photosynthetic pigments (Chl a, b), the activation of carbonic anhydrase and ribulose-1,5-bisphosphate carboxylase/oxygenase, net photosynthetic rate, and stomatal conductance under B toxicity condition. MT also suppressed the adverse effects of excess B by alleviating cellular oxidative damage through enhancing ROS-scavenging capacity. Similarly, foliar application of 1 and 2 mM MT increased root and shoot growth as well as grain weight of wheat plants by alleviating the oxidative stress caused by Cr stress through increasing the enzymatic (SOD, POD, CAT, APX) and nonenzymatic (total phenolics, total soluble protein, ascorbic acid) antioxidant activities as well as reducing the electrolyte leakage and production of H2O2 and MDA. It also improved photosynthetic ability by improving chlorophyll a and chlorophyll b content, gas exchange attributes, and water content in wheat plants grown under Cr stress (Seleiman et al., 2020). Furthermore, wheat seeds soaking in 100 μM MT significantly reduced Cr content, while it increased the activity of α-amylase and the content of soluble sugar and free amino acid in Cr-stressed plants’ seeds. Under Cr toxicity, MT pretreatment increased ROS scavenging ability by reducing H2O2 and O2  content as well as upregulating the activities and encoding gene expression levels of antioxidant enzymes (Lei et al., 2021).

Role of salicylic acid in the alleviation of abiotic stresses Salicylic acid (SA, 2-hydroxybenzoic acid) is a phenolic plant growth regulator that plays an important role in plant development, growth, biomass accumulation, flowering, photosynthesis, respiration, stomata movement, gas exchange, protein synthesis, pigment formation, ion uptake and transport, and nutrient metabolism (Wani et al., 2017; Pokotylo et al., 2019; Talaat and Shawky, 2022). Moreover, it prevents the representation of ethylene gas and is incompatible with the work of ABA, which causes leaf fall (Li et al., 2019). It also helps to conserve energy by raising metabolic rates, which is accompanied by a change in nucleic and amino acid levels (Khan et al., 2015). Previous studies have revealed that SA can act as a cell’s stimulant or transmitter, allowing plants to survive under environmental stress conditions like salinity, drought, heavy metals, heat, cold, and conditions of ammonia tension by regulating the antioxidant defense system, transpiration rates, stomatal movement, photosynthetic activity, and abiotic stress-responsive gene expression (Khalvandi et al., 2021; Shemi et al., 2021; Shopova et al., 2021a; Talaat, 2021a,b; Wang et al., 2021a,b). SA may also bond conjugate with some amino acids, such as proline and arginine, improving the plant’s resistance to environmental stresses (Pokotylo et al., 2019). It was discovered that there may be a link between SA supplementation and plant stress tolerance. Photosynthetic and growth rates, membrane permeability and mineral uptake, redox potential and cell homeostasis, as well as secondary metabolites accumulation have all been found to be influenced by exogenous application of SA in salt-stressed wheat plants. Application of 0.25 mM SA dramatically enhanced shoot length, root length, number of tillers, chlorophyll content, and K+/Na+ ratio in salt-stressed wheat plants (Suhaib et al., 2018). Similarly, foliar application of 1 mM SA reduced the negative effects of salinity on wheat growth and production in terms of plant height, spike length, as well as grains number and weight by enhancing the contents of water, chlorophyll, and proline (Mohammadi et al., 2019). SA also enhances salt tolerance of wheat plants and increases their survival by playing a protective role against ROS leading to a delay in the process of senescence. By increasing antioxidants like ascorbic acid and protecting both protein and chlorophyll from free radical breakdown, foliar application of SA (at 100, 200, 400 mg L 1) during tillering and booting initiation stages reduced the damage impacts of salinity stress on wheat development and productivity. SA also increased the grain and straw yields, as well as the potassium content (Nasharty et al., 2019). Besides contributing to ROS detoxification, SA also plays a role in

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maintaining intracellular redox potential and ionic homeostasis. The application of 1 mM SA as seed priming and foliar sprays alleviated adverse impacts of both salinity and drought on wheat plants and significantly enhanced plant height and grain yield by improving relative water content, chlorophyll content, and proline accumulation as well as decreasing the content of MDA, and the ratios of Na+/K+ and Na+/Ca2+ (Yadav et al., 2020). Likewise, exogenously SA application at 0.7–1.05 mM under saline conditions significantly improved wheat salt tolerance and increased yield components, especially grain number of plants mainly via enhancing K+ concentration as well as reducing Na+ uptake and Na+/K+ ratio (Pirasteh-Anosheh et al., 2021). Additionally, other reports postulated that exogenous application of SA protects plants from salinity-induced damage and aids in the development of tolerance to this harsh environmental condition by boosting photosynthetic machinery. Exogenous 75 mg L 1 SA application ameliorated the negative effects of salt on wheat yield by reducing photosynthetic inhibition and enhancing the photosynthetic carbon assimilation, as well as reducing oxidative damage caused by saline conditions (Talaat, 2021a). Furthermore, the regulation of endogenous PA production along with the enhancement of nitrogen metabolism has been observed by SA treatment under saline conditions. Foliar treatment of 75 mg L 1 SA helped wheat plants in dealing with salt stress by raising PAs content via speeding up the metabolic flow from the precursor amino acids arginine and methionine to PAs, improving PAs biosynthesis, and reducing PAs degradation. SA also altered nitrogen metabolism by increasing nitrogen, nitrate, and total protein content in grains, upregulating N uptake and metabolism-related enzymes (nitrate reductase, nitrite reductase, glutamine synthetase, glutamate synthase), as well as reducing MDA, H2O2, and carbonyl contents in salt-stressed plants (Talaat, 2021b). There is also a report that exogenous applications of 75 mg L 1 SA mitigated salt-induced wheat yield losses via controlling ions intake, increasing inorganic ions preferred accumulation or exclusion, modifying cell membrane structure, lowering oxidative damage, suppressing ROS generation, and improving antioxidant enzymes activity (Talaat and Shawky, 2022). Wheat drought tolerance is also induced by SA, which is a critical feature for boosting and stabilizing plant productivity. Exogenous SA has been found to have morphological and physiological impacts on stressed-wheat plants. They have been linked to the buildup of organic solutes that are part of the defensive response and play a key role in osmotic adjustment to keep the activity of the metabolic processes in the plant tissues. Drought impacts on wheat plants were minimized by applying 10 Mm SA, which increased germination rate, shoot length, and water potential by 21%, 20%, and 47%, respectively. Furthermore, a rise in the levels of organic solutes like proline (14%) and soluble sugar (25%) was detected (Ilyas et al., 2017). SA also protects wheat from water-deficit damages and enhances its productivity by improving the photosynthesis process. Application of 1.44 mM SA improved the performance of wheat plants under both well-watered and drought conditions. It significantly increased shoot dry weight, a number of spikes, as well as spikes and grains dry weights by enhancing stomatal conductance and chlorophyll a fluorescence (Rihan et al., 2017). Furthermore, in another study, exogenously applied SA under water stress conditions alleviated wheat yield reduction not only by improving the photosynthesis process but also by boosting the antioxidative enzymes activity and the osmoprotectant solutes accumulation (Sharma et al., 2017). Further investigations in wheat revealed that water-stress alleviation and yield improvement by SA application can be attributed to the enhancement in osmotic adjustment and ROS-scavenging capacity as well as to more relative water content under stressful conditions. A study by Maghsoudi et al. (2019) revealed that the application of 1 mM SA effectively improved wheat yield and its components under water-shortage conditions by promoting the SOD, POD, CAT, and APX activities, increasing the soluble sugars, K+, Mg2+, and Ca2+ accumulation in leaf tissues, enhancing the leaf water potential, as well as decreasing the levels of H2O2 and MDA. Likewise, spraying 1 mM SA on wheat plants increased drought tolerance by improving Chl a, Chl b, and carotenoids synthesis, relative water content, osmolytes, as well as SOD, POD, APX, and CAT activities, while it decreased MDA content (Azmat et al., 2020). Additionally, another report postulated that by boosting proline and soluble sugar production, improving photosynthetic activity, and diminishing H₂O₂ content, exogenous application of SA can promote osmotic adjustment and reduce adverse effects of drought stress on wheat plants (Sedaghat et al., 2020). Some other studies prove that SA foliar application significantly ameliorates the deleterious effects of drought stress via regulating the mineral uptake, ROS production, and photosynthetic efficiency. Application of 100 mM SA significantly increased the plant growth in terms of its height, as well as its fresh and dry weights via enhancing membrane stability index, antioxidant enzymatic activities, contents of water, nutrients (N, P, and K), and chlorophyl, as well as photosynthetic capacity in water-stressed wheat plants (Ahmad et al., 2021). Similar observation was also detected by Khalvandi et al. (2021), who showed that the application of 0.5 mM SA increased wheat drought tolerance through improving the photosynthetic performance, ROS-scavenging system, cell membrane integrity, and numbers of protein bands as well as lowering the membrane electrolyte leakage and lipid peroxidation. In the same line, seed presowing treatment with 50 μM SA significantly improved yield, yield components, and water-use efficiency under water-stress conditions, and these increases could be attributed to SA effect on improving relative water content, osmotic adjustment, and photosynthetic performance with reducing membrane permeability, and ROS accumulation in wheat-treated plants (Maswada et al., 2021). Recently, Munsif et al. (2021) assessed the effect of SA seed priming or foliar spray (0.7 and

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1.1 mM SA) on wheat yield and nutrient acquisition during the tillering stage under water-shortage conditions. SA application had improved the number of spikes, 1000-grain weight, grains per spike, grain and biomass yield, nutrients content, potassium usage efficiency, chlorophyll index, proline content, and antioxidant enzymes (POD, APX, CAT) activity in water-stressed plants. Likewise, exogenously applied SA at 140 mg L 1 significantly improved the plant height, plant fresh and dry weights, leaf area, number of tillers, spikes, and grains, grain weight, 1000-grain weight, biological yield, and harvest index under water-deficit conditions. The Chl a, Chl b, total Chl contents, relative water content, net photosynthesis rate, transpiration rate, stomatal conductance, proline content, and soluble sugar content were also enhanced by SA spraying treatment in stressed wheat plants. Results also revealed that antioxidant enzymes activity was increased; however, H2O2, O2  , and MDA content were decreased by SA application under water-deficit conditions (Shemi et al., 2021). Wheat plants’ thermotolerance has been shown to be modulated by SA. SA activates the expression of stress-responsive genes, protects the transcriptional machinery, and preserves membrane integrity from the harmful effects of heat stress. Foliar application of 100 mM SA on heat-stressed wheat plants enhanced plant fresh weight, total soluble protein content, total RNA content, total antioxidant capacity, proline accumulation, and the expression of numerous heat-responsive proteins. In heat-stressed plants, SA treatment elevated transcript profile of heat shock transcription factors 4 and 7 as well as dehydration response element binding (Kumar et al., 2015). Besides contributing to osmotic adjustment, SA also plays a role in inhibiting the generation of ROS. Exogenously applied 0.01% SA reduced the impact of heat stress on wheat and increased its productivity in terms of spike length, number of grains per spike, 1000-grain weight, and biological yield through improving the accumulation of metabolites, enhancing the water uptake, as well as diminishing the oxidative damage (Afzal et al., 2020). SA has been linked to plant cold-stress tolerance in a variety of ways. SA acts as an antioxidant and preserves cellular redox homeostasis in response to low-temperature stress by suppressing the production of ROS. It also stimulates the photosynthetic and growth rates in stressed plants, as well as the generation and accumulation of organic solutes and the protection of the transcriptional machinery. Evidence indicates that exogenous 100 μM SA pretreatment significantly induced freezing tolerance of wheat via improving photosynthetic activity, inhibiting the increase in MDA and H2O2 contents, as well as decreasing the electrolyte leakage (Wang et al., 2018). Moreover, foliar application of 100 μM SA promoted wheat cold tolerance by preventing the MDA and H2O2 accumulation, promoting antioxidant enzymes activity, inducing organic solutes accumulation, and increasing TaMnSOD, TaFeSOD, and TaCAT gene transcript levels (Ignatenko et al., 2019). Likewise, application of 210 mg L 1 SA effectively alleviated the damage caused to photosynthetic performance by low temperature. It significantly enhanced the productivity of stressed wheat plants by increasing gas exchange attributes, enhancing SOD and POD activities, as well as decreasing MDA content in stressed-wheat plants (Zhang et al., 2019). Similar observation was also detected by Wang et al. (2021a), who postulated that applying 100 μM SA to wheat plants under low-temperature stress enhanced plant height, biomass production, and grain yield via improving leaf net photosynthetic rate, photochemical efficiency of photosystem II, osmoprotectant solutes accumulation, antioxidant enzymes activity, and antioxidant substances level. Recently, Wang et al. (2021b) reported that treated wheat grains with 100 μM SA raised sucrose and free proline concentrations by coordinating carbon and nitrogen metabolism, resulting in higher water content and freezing tolerance. SA has also a regulatory role in protecting wheat plants from heavy-metal toxicity. It can improve plant resistance by alleviating heavy-metal stress-induced oxidative damage and modulating hormonal balance. Application of 500 μM SA as seed soaking alleviated the stress generated by Cd and considerably improved the plant growth, pigment and water content, as well as activities of antioxidant enzymes (Agami and Mohamed, 2013). A direct correlation was detected between SA content and the wheat plants Cd tolerance (Kova´cs et al., 2014). Furthermore, application of 50 μM SA improved the growth of Cd-stressed wheat plants by decreasing the ABA accumulation as well as increasing the IAA and CK levels (Shakirova et al., 2016a). Additionally, exogenous 2 mg L 1 of SA protected wheat plants from contamination by the insecticide chlorpyrifos and increased root and shoot lengths through improving chlorophyll content, inducing antioxidant enzymes activity, and decreasing MDA content (Wang and Zhang, 2017).

Role of brassinosteroids in the alleviation of abiotic stresses Brassinosteroids (BRs) are one of the most important plant hormones, capable of boosting plant growth and development, crop yield and quality, as well as crop stress tolerance (Talaat and Abdallah, 2010; Abdellatif, 2017; Talaat, 2020; Li et al., 2021). Cell division, cell elongation, seed germination, photosynthetic activity, photomorphogenesis, flower development, nutrient uptake, as well as antioxidant defense are all improved by BRs (Todorova et al., 2016; Talaat, 2020). To date, more

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than 70 phytohormones have been identified in more than 100 plant species (Zullo and Adam, 2002). Both free and conjugated forms of these steroidal chemicals were discovered (Bajguz and Hayat, 2009). They have a structure that is similar to that of animal and insect steroids (Sasse, 2003). They collaborate with other hormones to regulate tolerance to abiotic stresses such as salt, drought, hot and cold temperatures, and heavy-metal toxicity (Talaat et al., 2015; Talaat and Shawky, 2016). Many extensive investigations on the role of BRs on plant metabolic processes under abiotic stress conditions have been done (Yusuf et al., 2017; Hussain et al., 2019; Avalbaev et al., 2020; Talaat, 2020; Shopova et al., 2021b; Tofighi et al., 2021). Amelioration of the deleterious effects of salt stress has been shown in several reports by using BRs such as EBL (24-epibrassinolide) and HBL (28-homobrassinolide). EBL protects wheat plants from salt damage by adjusting a lot of plant physiological processes such as photosynthesis, protein synthesis, water uptake, nutrient acquisition, source/sink transition, osmotic adjustment, and ROS metabolism. A study conducted by Talaat and Shawky (2012b) reported that by improving membrane integrity, photosynthetic photochemical reactions, contents of water, chlorophyll, nitrate, activities of nitrate reductase, carbonic anhydrase, as well as levels of carbohydrate, and protein, application of 0.1 mg L 1 EBL mitigated the stress caused by salt and significantly enhanced the wheat productivity. It also increased glycinebetaine, Spm, and Spd concentrations as well as decreased diamine oxidase and polyamine oxidase activities in salt-stressed plants. Additionally, another report by Talaat and Shawky (2013) postulated that exogenously applied 0.1 mg L 1 EBL ameliorated the toxic effects of salinity on wheat plants by improving the nutrient (N, P, K) uptake, the osmoregulator solutes accumulation, the activities of SOD, POD, CAT, and GR, as well as the contents of glutathione and ascorbate. However, Na+ uptake, H2O2, MDA contents, as well as electrolyte leakage were decreased in salt-stressed plants when EBL was sprayed. This is confirmed by the observation of Abdellatif (2017), who showed that exogenous treatment of 0.2 mg L 1 EBL to wheat plants reduced the detrimental effects of salinity by increasing the plant fresh and dry weights, plant height, number of tillers, number of spikes, the weight of 1000 grains, relative water content, proline content, and antioxidant enzymes activity. Similarly, in a different study, exogenous 10 nM EBL application enhanced wheat salt stress tolerance by increasing free proline and soluble protein content, SOD, POD, and CAT activities, chlorophyll content, root H+-ATPase activity, as well as K, Ca, Mg, Fe, and Zn uptake. It also decreased ROS content, lipid peroxidation, and electrolyte leakage in wheat plants grown under saline conditions (Dong et al., 2017). Likewise, the deleterious effects of salinity were alleviated by enhancing relative growth rate, shoot fresh weight, phosphorous content, leaf water content, as well as the activities of CAT and APX when salt-stressed wheat plants were sprayed by 5 μM EBL. However, EBL decreased H2O2 and MDA content and membrane electrolyte leakage in the stressed plants (Tofighi et al., 2017). It is also worth noting that foliar EBL application may help to alleviate salt stress by preserving ion homeostasis in cells and modifying Na+/H+ antiporters. Tofighi et al. (2021) found that foliar spraying with 5 μM EBL significantly improved protein biosynthesis, K+ accumulation, and K+/Na+ ratio in shoots as well as reduced Na+ levels in shoots and roots of wheat plants growing in saline environments. Furthermore, when plants were exposed to salt, the expression of the NHX gene was upregulated in EBL-treated plants compared to control ones. Drought is a severe form of environmental stress that lowers wheat production, particularly in semiarid and dry areas. It was established in a study with wheat plants that 0.4 M EBL treatment enhances drought tolerance by reducing the detrimental effects of drought on hormonal state (Shakirova et al., 2016b). Furthermore, Zhao et al. (2017) found that 0.1 mg L 1 EBL significantly ameliorated the deleterious effects of a combination of water stress and heat stress on wheat plants by improving the photosynthetic capability, the Rubisco activase gene expression, as well as SOD, POD, and CAT activities. There is also a report that drought-induced cell division decreases in the root apical meristem which was prevented by using exogenous EBL application at 0.4 mM. It also induced the accumulation of wheat germ agglutinin in the roots of wheatstressed plants. Lower electrolyte leakage was also detected in stress-treated plants (Avalbaev et al., 2020). High and low temperatures are considered as a handicap for wheat growth and productivity. However, improved wheat growth parameters in terms of plant height as well as root and shoot fresh and dry masses, photosynthetic efficacy, activities of antioxidant enzymes (CAT, POX, SOD), and proline content are all evidences of EBL (0.01 μM) treatment-induced better tolerance to high-temperature stress (Hussain et al., 2019). Similarly, low-temperature-induced decreases in wheat production were substantially relieved by 0.1 mg L 1 BR application. It alleviated the damage induced in chilling wheat seedlings by improving the activity of antioxidants, eliminating the ROS production, and enhancing the photosynthetic performance (Zhang et al., 2019). Heavy-metal toxicity is one of the key abiotic stress factors that has a stronger impact on wheat plant growth and development. Interestingly, BRs treatments can help plants become more resistant to heavy metals. When wheat plants were cultivated on soil contaminated with heavy metals (Cu, Cd, Pb, and Zn), Kroutil et al. (2010) found that EBL not only increased the plant development but also reduced the plants content of these heavy metals. It is important to note that exogenous application of BRs has been shown to affect a variety of physiological processes in heavy-metals-stressed plants,

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such as photosynthetic efficiency, antioxidant enzyme activity, membranes integrity, water relations, osmotic management, nutrient uptake and assimilation, as well as hormonal balancing. This is confirmed by the results of Hayat et al. (2014), who showed that applying 10 8 M HBL to wheat plants reduced the toxic effects of Cd and salt stresses and increased plant growth parameters including plant height, fresh and dry weights of shoots and roots, as well as leaf area, by improving photosynthetic attributes (SPAD chlorophyll content, net photosynthetic rate, stomatal conductance, transpiration rate, and internal carbon dioxide concentration), chlorophyll fluorescence, as well as CAT, POX, and SOD activities. It also increased endogenous proline content, carbonic anhydrase and nitrate reductase activities, as well as leaf water potential in stressed plants, while lowering H2O2 and MDA levels. Similarly, in a different study, wheat plants treated with 10 8 M EBL showed significant increases in the shoot and root lengths, plant dry weight, leaf proline and sugar content, net photosynthetic rate, maximum quantum yield of PSII, as well as CAT, POX, and SOD activities after being exposed to combined stress of Al and salt application (Yusuf et al., 2017). Additionally, according to another study, BRs can interact with other plant hormones under heavy-metal toxicity conditions, resulting in a reduction in their level. Seed pretreatment with EBR (0.4 μM) decreased Cd-induced accumulation of ABA and wheat germ agglutinin (WGA) in wheat roots (Bezrukova et al., 2021). In vitro cultures of wheat cells derived from immature embryos were used in an investigation. The stress condition was generated by adding 30 μM of the mycotoxin zearalenone to the media. The application of 0.1 μM EBL to stressed media encouraged the synthesis of casta- and homocastasterone, which are endogenous BRs exist in wheat cells. EBL supplementation also upregulated SOD, CAT, APOX, DHAR, GR, GST, GPOX, and PPO activities, while it reduced MDA content and percentage of total ion leakage from cells (Filek et al., 2018).

Role of polyamines in the alleviation of abiotic stresses Polyamines are biostimulants that consist of low-molecular-weight aliphatic nitrogenous bases with two or more amino groups that are involved in a range of biological activities (Pang et al., 2007; Yu et al., 2019; Todorova et al., 2016). The principal PAs found in plants are the diamine putrescine (Put), triamine spermidine (Spd), and tetraamine spermine (Spm). Put is made up by decarboxylation of ornithine, which is catalyzed by ornithine decarboxylase, or by decarboxylation of arginine, which is catalyzed by arginine decarboxylase. Spd and Spm are made up by adding aminopropyl moieties to the Put skeleton in a series of enzymatic processes catalyzed by the spermidine and spermine synthases (Liu et al., 2015; Talaat and Shawky, 2016; Todorova et al., 2016). PAs can be found in the vacuole, cytoplasm, plastids, mitochondria, and cell wall of plant cells, but Spm can also be detected in the nucleus (Alcazar et al., 2010). They are found in cells not only in free form, but also they can form links with phenolic acids, nucleic acids, and proteins. PAs in their free form are easily translocated within the cells due to their water-soluble features (Takahashi and Kakehi, 2009; Gill and Tuteja, 2010). PAs can create electrostatic connections with negatively charged molecules, producing conformational stabilization/destabilization of DNA, RNA, chromatin, and proteins (Alcazar et al., 2010). They play regulatory functions in cell elongation, cell division, root growth, flower formation, embryogenesis, and DNA replication in plants, all of which are important in the regulation of plant growth and development (Hussain et al., 2011). They are also implicated in abiotic stress responses such as salinity (Aldesuquy et al., 2014a), drought (Yang et al., 2014; Talaat et al., 2015; Pa´l et al., 2018; Talaat, 2020), low temperature (Gu et al., 2019), and heavy metals (Aldesuquy et al., 2014b; Agami, 2016). Under normal and stressed conditions, PAs can improve the ion balance, slow the aging process, protect the photosynthetic tissues, promote the plant growth, regulate the antioxidant system, and reduce the ROS accumulation (Yu et al., 2015; Tajti et al., 2018; Li et al., 2020a,b; Talaat, 2020). A link between PAs treatment and abiotic stress tolerance was detected. Wheat tolerance to unfavorable environmental conditions was improved by exogenous PAs, which improved photosynthetic ability, ROS-scavenging capacity, mineral uptake, organic solutes buildup, water relations, and hormonal balance. A study by Aldesuquy et al. (2014a) reported that by positively affecting pigment (Chl a, Chl b, carotenoids, total pigments) content, Hill reaction activity, flag leaf chloroplast quantities and frequency in mesophyll cells, as well as photosynthetic efficiency, soaking wheat grains in 0.3 mM Spm alleviated the toxic impacts of salt stress and improved plant growth. Additionally, an another report revealed that application of 1 mmol L 1 Spd ameliorated the detrimental effects of water-deficit condition on wheat productivity by reducing the concentrations of 1-aminocyclopropane-1-carboxylic acid and ethylene as well as by increasing the Spd concentration and the total starch and amylopectin contents (Yang et al., 2014). Moreover, seed soaking in Spd and Spm mitigated the deleterious impacts of water-shortage conditions on wheat seeds germination by improving the accumulation of IAA, ABA, GA, and soluble sugars in seeds (Liu et al., 2016). Further investigation in wheat showed that exogenously applied 0.5 mM Put alleviated osmotic stress by inducing the expression of various general stress-related genes. Put treatment under osmotic stress altered the fatty acid content in particular lipid fractions as well as the antioxidant enzyme

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activity (Pa´l et al., 2018). In an another investigation, exogenous Spd applied at anthesis dramatically relieved the inhibitory effect of water shortage on grain-filling by significantly promoting the synthesis of cytokinin and starch, while it decreased ethylene synthesis in wheat grains. Moreover, Spd treatment increased SOD, POD, and CAT activity while lowering MDA level in the grains of drought-stressed plants (Li et al., 2020a,b). An another study found that using BRs considerably reduces the negative impacts of stressful conditions via altering the hormonal balance inside the wheat plants. In this context, the application of 1 mmol L 1 Spd could relieve the chilling stress inhibitory effect on wheat seed germination, whereas 1 mmol L 1 Put had the opposite effect that was related to abscisic acid and gibberellins content. Spd stimulated starch breakdown in seeds by considerably increasing gibberellin and abscisic acid levels. However, Put resulted in excessively abscisic acid concentration in the wheat seeds (Gu et al., 2019). BRs are also helpful in ameliorating the detrimental impacts of the toxicity of heavy metals on wheat plants. Grain presoaking in Spd (0.3 mM), Spm (0.15 mM), as well as their interaction under heavy-metal-polluted wastewater mitigated the harmful disordered of heavy metals on wheat productivity and water-use efficiency through enhancing the concentration of soluble sugars, the content of polysaccharides, total carbohydrates, protein, and phosphorus (inorganic, organic, total phosphorus) as well as through decreasing the content of heavy metals in the developed grains of wheat. In addition, in grains of wheat-stressed plants, Spm, Spd, as well as their interaction boosted growth stimulators (IAA, GA3, total cytokinins) content, while they diminished the inhibitors (ABA) content. With the Spm + Spd application, the effect was more evident. Furthermore, Spd treatment resulted in the development of novel proteins in produced grains (Aldesuquy et al., 2014b). Under Cd stress, presoaking wheat seeds with Spm or Spd increased the plant growth by improving the membrane integrity, water uptake, protein, starch, AsA, and GSH concentrations as well as by decreasing the electrolyte leakage, proline, total soluble sugars, H2O2, and MDA, and Cd2+ concentrations (Rady and Hemida, 2015). Another investigation revealed that exogenous Put application mitigated the damage caused by Al stress. It considerably reduced Al-induced root inhibition and Al buildup in wheat seedling root tips. Moreover, increased Put synthesis improves Al stress tolerance, most likely by lowering cell wall polysaccharides and, as a result, lowering cell wall Al binding capability (Yu et al., 2015). In the same line, Agami (2016) found that by enhancing the water uptake, the soluble proteins and total soluble sugar levels, the antioxidant enzymes (APOX, GPOX, and SOD) activity, and the stem tissues structure, as well as by reducing the electrolyte leakage, soaking wheat grains in 1000 μM Spd ameliorated the deleterious impacts of Cu stress and enhanced the growth of wheat plants. Additionally, an another report postulated that by enhancing the content of chlorophyll, salicylic acid, and proline, the optimal and effective quantum yield of PSII, as well as by decreasing the activity of diamine oxidase and polyamine oxidase, seed soaking or hydroponically added 0.5 mM Spd and Put under Cd stress reduced the toxic effect of Cd on the growth of wheat plants. The gene-producing phytochelatin synthase, on the other hand, was solely impacted by hydroponically applied Spd, which lowered it under Cd stress (Tajti et al., 2018).

Limitations and conclusion Abiotic stressors like salt, drought, heat, cold, waterlogging, nutrient deficiency, heavy-metals toxicity are the primary causes of wheat production losses around the world, and they will become more worse as desertification covers more and more of the planet’s land. They produce changes in wheat plants’ morphological, physiological, biochemical, and molecular activities. Harmful effects of these environmental stresses begin with seed germination and continue until the plants reach maturity. These harsh environmental conditions impede wheat plant growth and development, resulting in greater economic losses at the expense of world food security. Because numerous abiotic stresses diminish crop output around the world, developing biological ways to deal with these stresses is critical. PGRs, exogenously applied as seed priming or foliar treatments as well as endogenously produced, have the ability to mitigate the negative effects of abiotic stressors. They manage stress adaptation by altering the physiological, biochemical, and molecular activities, activating the antioxidant defense systems, as well as elevating the transcript levels, transcription factors, metabolic genes, and stress proteins, allowing plants to adapt to harsh conditions. Wheat plants in nature are exposed to a number of stressful conditions or combinations of these stresses. One of the most difficult challenges that still has to be addressed is conducting trials that focused on a mixture of stress conditions like those in field contexts. Because many stresses can occur at the same time in the field, examining the impacts of a combination of stress variables rather than a single stress component may be advantageous. Although the individual impacts of PGRs have been widely investigated, the coordinated functions of plant hormones, as well as numerous stress-induced plant responses, have not been fully investigated. More molecular and biochemical studies in plants under environmental stress conditions are needed to understand the underlying signaling mechanism of PGRs-mediated stress tolerance. Future studies should concentrate on the interaction of PGRs with other signaling

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molecules during environmental challenges. Combining PGRs with other signaling pathways in a challenging environment would present a big opportunity for improving food security.

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Chapter 8

Abiotic stress-induced ROS production in wheat: Consequences, survival mechanisms, and mitigation strategies Ananya Baidyaa, Kousik Attaa,⁎, Mohammed Anwar Alib, Maksud Hasan Shahc, Saju Adhikaryc, Subhasis Mondala, Sagar Maitrad, and Akbar Hossaine,⁎ a

Department of Plant Physiology, Faculty of Agriculture, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, West Bengal, India, b Department of Crop

Physiology, Agriculture College (ANGRAU), Bapatla, Andhra Pradesh, India, c Department of Agronomy, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, Nadia, West Bengal, India, d Department of Agronomy and Agroforestry, Centurion University of Technology and Management, Paralakhemundi, Odisha, India, e Division of Agronomy, Bangladesh Wheat and Maize Research Institute, Nashipur, Dinajpur, Bangladesh *

Corresponding authors. e-mail: [email protected] (Kousik Atta); [email protected] (Akbar Hossain)

Introduction Besides accounting for around 30% of the global food grain trade and 50% of global production, wheat is one of the world’s most important cereal crops within the Poaceae family (Akter and Islam, 2017). It is cultivated globally. By 2050, it is expected that demand for wheat would have increased by 60% (Aprile et al., 2009). In this changing climate, chasing demand is critical. The impact of global climate change on plant growth and development is making environmental pressure a critical element of modern agriculture. Wheat production has been hampered by salinity, heat, and drought stress globally (Da Costa et al., 2011). As a result of abiotic stress, transformations in the cells limit growth and development, reducing wheat yield. As a result, several novel techniques to wheat production in a changing environment are required to assure the nutritional and food security of the world’s exploding population (Hossain et al., 2021). Drought is a key abiotic stressor that contributes to significant yield reductions around the world. Drought stress can harm crops at any stage of their development. Drought in the early stages inhibits germination and tiller start. Drought in the latter stages reduces dry matter accumulation, grains/plant, and effective tillers count (Gull et al., 2019). Terminal drought stress on wheat is also fatal for pollen germination and seed yield. Heat stress has a diverse effect on plants, which includes alteration in physiological activity, changes in development, growth and reduction in yield and grain production (Mondal et al., 2013). The effects of heat stress are also seen in other aspects of plant growth such as changes in plant water relations (Hasanuzzaman et al., 2012, 2013), metabolic alterations (Farooq et al., 2011), hormonal imbalance (Krasensky and Jonak, 2012), and also a reduction in the activity photosynthesis (Almeselmani et al., 2012; Ashraf and Harris, 2013). Changing climatic conditions may cause high-temperature effects. Optimum temperature required for wheat during ripening stage is 14–15°C. Temperature above 25°C reduces crop productivity (Hossain et al., 2020). High temperatures also hamper grain filling duration during the reproductive and maturation phases. Abiotic stress such as salinity is another factor that adversely affects wheat quality and productivity (Loutfy et al., 2020). In several parts of the world, wheat productivity has been found to be negatively impacted by abiotic stress during the crop growing season (Mueller et al., 2015; Fontana et al., 2015).

Concept of abiotic stress-induced ROS in plants Plants have long been known to release ROS as a by-product of aerobic metabolism (Das and Roychoudhury, 2014). Photosynthetic organisms introduced molecular oxygen into the early reducing atmosphere 2.7 billion years ago, resulting in ROS. ROS are products of atmospheric oxygen that are partially reduced or achieved (Choudhury et al., 2017). Initially,

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Abiotic stresses in wheat

Dioxygen

3

O2

e–

Superoxide radical ion

Peroxide ion

O2.–

O22–

H+

1

O2

Singlet Oxygen

HO2.

Perhydroxyl radical

e–

Oxene ion

e–

2 H+

H2O2

Hydrogen peroxide

e–

O23–

2 H+

H2O Water

O– 2 H+

OH. Hydroxyl radical

Oxide ion

e–

O2– 2 H+

FIG. 1 Various types of ROS generation. (Adopted and modified from Atta, K., Singh, A. P., Adhikary, S., Mondal, S., Dewanjee, S., 2022. Drought stress: manifestation and mechanisms of alleviation in plants. In Eyvaz, A.P.M., € Albahnasawi, A., Tekbas¸ , M.M., Gurbulak, M.E. (Eds.), Drought. IntechOpen. https://doi.org/10. 5772/intechopen.102780.)

H 2O

Water

Fe+ (Fentons reaction)

OH. (Hydroxyl radical)

ROS are constantly produced under ideal conditions. However, various antioxidant mechanisms scavenge these free radicals, so they cannot cause any harm (Foyer and Noctor, 2005). Reactive oxygen species (ROS) are produced in excess by plants under abiotic stress. ROS are highly reactive and toxic, and they destroy proteins, lipids, carbohydrates, and DNA as part of oxidative stress (Fig. 1). ROS comprises of both free . % % radicals (O.
2 , superoxide radicals; OH , hydroxyl radical; HO2, perhydroxy radical and RO , alkoxy radicals) and non1 radical (molecular) forms (H2O2, hydrogen peroxide and O2, singlet oxygen) (Gill and Tujeja, 2010). . Photosystems I and II (PSI and PSII) in chloroplasts are the main sites of production of 1O2 and O.
2 . O2 is generated at the major sites of the electron transport chain (ETC) such as the ubiquinone, Complex I, and Complex III in mitochondria. Such abiotic stresses can cause damage to the wheat crop in various aspects. Wheat crop may adversely be affected in the stages of wheat morphology, physiology, and biochemistry during the stress condition.

Consequences of stress-induced excessive production of ROS in wheat Effect of ROS on wheat morphology Heat and moisture stresses dramatically diminish stomatal conductance, leaf area, photosynthetic efficiency, and water-use efficiency of cereals (Hussain et al., 2016). Heat and drought stresses negatively influence seed germination and plant establishment (Hossain et al., 2013). High temperatures (45°C) harm embryonic cells, causing incorrect germination and emergence, as well as poor crop stand. High temperatures reduce the productive tiller’s ability to survive, resulting in a reduction in yield. Heat stress causes a 53.57% loss in grain output and a fall in tiller number in wheat (15.38%) (Din et al., 2010). Heat stress induces a reduction in root growth, which has an impact on crop output (Huang et al., 2012). Heat stress effects are highly significant during the reproductive phase (Nawaz et al., 2013). A 1°C increase in average temperature during the reproductive stage can lead to a greater loss in grain yields (Yu et al., 2014; Bennett et al., 2012). During flowering and grain filling, a temperature range of 12–22°C is ideal (Sharma et al., 2019). When heat stress occurs at meiosis, it impacts the early stages of gametogenesis. Floral initiation is negatively impacted by heat stress on microspores and pollen cells (Kaur and Behl, 2010). The duration and rate of grain filling, which is extremely susceptible to heat stress, determine the grain development phenomenon (Gourdji et al., 2013). Wheat’s life cycle is shortened in heat stress compared to normal temperature conditions. An increase of 1–2°C in temperature lowers seed weight due to a decrease in grain filling duration. Grain yield can be reduced by up to 23% when subjected to short-term heat stress during grain filling stage. Heat stress has a negative impact on grain yield and quality. In heat stress conditions, grain number decreases, resulting in a decrease in the harvest index. Grain quality suffers as a result of heat-stress-induced decreases in assimilate production and remobilization. The adverse effect of increased temperature during the crop growth period has a substantial impact on wheat productivity. Grain yield significantly hampered when wheat is exposed to ambient temperatures (less than 35°C) for a short length of time.

Effect of ROS on wheat physiology High temperatures have a significant impact on photosynthesis, which is the most fundamental physiological function in plants. Heat stress affects wheat’s stroma and thylakoid lamellae the most. At high temperatures (40°C), a continual

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alternation of Rubisco activase, RuBisCO, and Photosystem II occurs. It has been reported that RuBisCO enzyme can be deactivated within seven days of heat stress in wheat. The breakdown of Rubisco activase during heat stress lowers photosynthetic potential. Heat stress causes light harvesting Complex II to dissociate from Photosystem II by altering the fluidity of the thylakoid membrane. In order for the plant to grow and develop, photosynthetic products must be transferred to various plant parts. High temperatures cause the membrane integrity to collapse, slowing translocation of assimilate from source to sink. Grain growth and development are aided by the transfer of water-soluble carbohydrate to the reproductive sink. Seed set and seed filling are reduced when the source and/or sink are limited. When heat stress causes a source limitation, the plant must find another way to transfer photoassimilates from source to sink (grain) organ. It is observed that when preanthesis heat stress occurs, carbohydrate remobilization from the stem increases to the developing grain, helping to counteract the effects of postanthesis heat stress on grain starch content. Photorespiration is aided by the availability of high O2 concentrations. During heat stress conditions, the solubility of O2 and CO2 gases changed, resulting in increased photorespiration in wheat flag leaf. Plant senescence is the process by which plants age. Leaf senescence is distinguished by loss of membrane integrity, vacuolar collapse, and disruption of cellular homeostasis. Moderate but prolonged heat stress causes gradual senescence, whereas intense heat stress for a short period of time causes protein denaturation and aggregation, resulting in plant death. Heat stress promotes leaf senescence in plants during maturity. High temperatures (34°C) also hasten leaf senescence due to a decrease in chlorophyll biosynthesis. High temperatures influence the plants–water relationship and water content. Due to a decrease in osmotic potential, heat stress promotes cell dehydration. Relative leaf water content (RLWC), transpiration rate, and stomatal conductance are all affected by canopy temperature. It is the fluorescence of chlorophyll that determines photosynthetic efficiency, which is directly proportional to yield. As a result, heatresistant genotypes can be selected using canopy temperature features and chlorophyll fluorescence. The canopy temperature is linked to deeper roots during times of drought and high temperatures. Heat-tolerant and heat-susceptible genotypes of wheat were cultivated under normal and late planted conditions, and heat-sensitive genotypes had significantly lower chlorophyll content and leaf area index, but heat-tolerant genotypes had significantly higher proline content. When plants are exposed to heat stress, they release a large amount of ROS. ROS interfere with cell activity by negatively affecting lipids, proteins, and DNA. Heat stress causes oxidative damage to membranes, which reduces their thermostability by 54%. Protein denaturation and the production of unsaturated fatty acids are caused by heat stress, which enhances cell membrane permeability.

Effect of ROS on wheat biochemistry Starch is the main component of wheat, and this is composed of amylopectin and amylose. The amount of amylose in a starch is an important criterion for determining its quality. The amount of amylose in a starch has an effect on its characteristics. A rise in amylose concentration and the ratio of amylose to amylopectin is linked to a rise in temperature. The enzymes starch synthase and ADP-GlucosePyrophosphorylase (AGPase) are important in starch production. Granulated starch synthase is a type of starch synthase, and soluble starch synthase is another type. Due to decreased effectiveness of enzymes involved in starch biosynthesis, high temperatures cause a decrease in grain starch content, up to one-third of total endosperm starch. At high temperatures of about 40°C, soluble starch synthase activity is reduced, resulting in smaller grain size and less starch deposition. However, Sharma et al. (2019) reported that reduction in starch synthase activity up to 30°C has no effect on starch deposition, but it does affect starch composition. Heat stress has a minimal effect on the granule-bound starch synthase activity of wheat. According to Asthir and Bhatia, wheat grain produced less starch under heat stress, but more soluble sugar and protein. Protein level and composition have a big impact on wheat grain quality. Under heat stress circumstances, grain protein concentration rises along with critical amino acid fractions, sedimentation index, and leaf nitrogen content.

Water/moisture/drought stress-induced ROS production in wheat Desiccation causes stomata to close under moisture stress circumstances, resulting in an accumulation of NADPH due to a reduction in CO2 concentration in mesophyll tissue of leaf. In the absence of NADP, oxygen acts as an alternative electron .
acceptor, leading to the generation of (O.
2 ) superoxide radicals (Egneus et al., 1975; Cadenas, 1989). O2 and the product of its reduction H2O2 is a potentially harmful chemical and generate extremely poisonous OH% via the Haber–Weiss reaction % (Elstner, 1987). Lipid peroxidation (LPO) is caused by ROS such as H2O2, O.
2 and OH which can result in membrane damage, protein degradation, enzyme deactivation, pigment bleaching, and DNA strand disruption (Fridovich, 1986; Davies, 1987; Liebler et al., 1986; Imlay and Linn, 1988). As a result, any defensive system must prioritize the

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detoxification of O.
2 and H2O2. Plants activate enzymatic mechanisms such as the production of GR, CAT, APX, SOD, and metabolic approaches such as the formation of ascorbic acid, tocopherol glutathione, and carotenoids, to defend their subcellular and cellular systems from the harmful effects of ROS (Liebler et al., 1986; Elstner, 1987; Larsen, 1988). In a study conducted by Sairam et al. (1998) on wheat and moisture stress, observed significant reduction in RLWC of wheat genotypes under water stress, accumulation of H2O2, SOD, APX, CAT increased under moisture stress situations in all developmental stages and LPO estimated as MDA content showed a marked increase in water stress conditions. Genotype C-306 exhibited higher RWC, and concentrations of H2O2 and LPO under water stress conditions. H2O2 is a hazardous chemical created by the scavenging of superoxide radicals, and it is poisonous to cells and plants at greater quantities, resulting in membrane injury (MI) and LPO (Menconi et al., 1995; Baisak et al., 1994). H2O2 scavenging is linked to ascorbic acid content via APX. C-306 has a greater tolerance mechanism for H2O2 scavenging due to its higher ascorbate concentration and APX activity. The catalase enzyme is also linked to H2O2 scavenging, and increased enzyme activity correlates with a higher level of stress tolerance (Olmos et al., 1994; Upadhyaya et al., 1990).

UV-B radiation-induced ROS production in wheat In the event of ozone layer depletion, UV-B radiation (wavelength of 280–320 nm can be referred to as UV-B) could become a problem for wheat farming. UV-B radiation reduces the number and weight of wheat grains, thus negatively affecting wheat production (Calderini et al., 2008). UV-B radiation can cause irreversible and reversible changes in plants’ physiological and biochemical processes. According to studies, UV-B can adversely affect biomass accumulation (Mazza et al., 2000) as well as leaf and stem elongation (Ballare et al., 1996; Li et al., 2000). The level of UV-B radiation alters nitrogen content, leaf thickness, and number of leaves (Hatcher and Paul, 1994). Adding 12%–25% of stratospheric ozone to an environment that has UV-B radiation will reduce wheat grain yields by 18%–57%. UV-B radiation is associated with a substantial reduction of 1000 grain weight (up to 30%) and grain number/ m2 (up to 50%) during the three-leaf stage and ripening. Radiation from UV-B is primarily measured in the northern hemisphere and the southern hemisphere, mostly at mid-/ high latitudes. UV-B radiation is still poorly understood as to how it affects crops in latitudes where the ozone layer is the thinnest.

ROS scavenging to survive against abiotic stresses in wheat Oxidative stress in wheat plant can be prevented by the defense mechanisms regulated by different enzymatic and nonenzymatic pathways, i.e., enzymatic [guaiacol peroxidase (GPOX), superoxide dismutase (SOD), dehydroascorbate reductase (DHAR), glutathione peroxidase (GPX), ascorbate peroxidase (APX), catalase (CAT), glutathione-S-transferase (GST), glutathione reductase (GR), monodehydroascorbate reductase (MDHAR)] and nonenzymatic [ascorbic acid (ASH), alkaloids, glutathione (GSH), phenolic compounds, α-tocopherols, and nonprotein amino acids] which control the cascading effects of unregulated oxidation and defend oxidative degradation to cells through ROS scavenging. Furthermore, ROS affect many genes’ expression, which controls a variety of activities including growth, cell cycle, abiotic stress response, pathogen defense, programmed cell death (PCD), systemic signaling, and development. O2 :
+ Fe3+ ! 1 O2 + Fe2+ : SOD

2O2 :
+ 2H+ ! O2 + H2 O2 :
Fe2+ + H2 O2 !Fe3+ + OH
+ OH  Fenton’ s reaction : Protecting the plants by lowering/checking the levels of ROS so that it could not cause harmful effects, by external application of various molecules, is an interesting approach. Salicylic acid (1.0 mM) and abscisic acid (0.5 mM) were applied to the wheat leaves cultivars Hira and C-306 at 20 and 40 DAS (days after sowing) under medium drought stress (
0.8 MPa), respectively, and increased the antioxidative enzyme activities (catalase, APX, SOD, and GR) while decreasing the H2O2 contents and thiobarbituric acid-reactive substances (TBARSs), which is a measure of LPO. Chlorophyll content, relative leaf water content (RLWC), carotenoid content, membrane stability index (MSI), leaf area, and total biomass all improved when oxidative stress and antioxidant enzyme activity were increased (Agarwal et al., 2005).

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Stress-induced production of ROS in wheat: Physiological mechanisms Plant growth at different developmental stages must be studied as well as wheat physiology under changing climatic conditions and plant development under different environmental conditions. Under a number of stress circumstances, ROS production is thought to be a primary event (Noctor and Foyer, 1998). Oxidative cell death is caused by ROS, which are highly reactive and poisonous. The implications of ROS generation are determined by the severity of the stress and the cell’s physiochemical circumstances. Flag leaf is an essential part of wheat grain production. ROS produced at excessive levels could impair flag leaf growth and development. The wheat physiology undergoes some changes that are related to accumulation of osmolytes, the photosynthetic pigments, water relations, and the antioxidative defense mechanisms against excessive ROS generation during abiotic stresses.

High temperature stress/heat stress Environmental changes have been caused by climate change, including rising temperatures and increased heat stress. Wheat yield is greatly impacted by heat stress in different parts of the world, mainly during reproductive phases, which affects grain number as well as dry weight. Heat stress affects wheat yield by 3%–5% for every 1°C increase in temperature. Heat stress causes pollen sterility, reduces CO2 absorption, and increases photorespiration in wheat, according to previous studies. The photosynthetic process is significantly harmed by high temperatures, which has an adverse impact on wheat growth and productivity. Increased temperature causes chloroplast structure to be disrupted, chlorophyll content to be reduced, and chloroplast enzymes to be inactivated, potentially resulting in reduced photosynthesis (Farooq et al., 2011). Heat stress causes the thylakoid lamellae and chloroplasts of wheat to degrade ultrastructurally. Heat stress in wheat plants recently reduced photosynthetic nitrogen usage efficiency (NUE), net photosynthesis, and RuBisCO activity. The photosynthetic machinery in wheat has been shown to be hampered by high temperatures, which impede Photosystem II. Furthermore, high temperatures limit grain quantity and size, which has a significant impact on wheat production, with a significant drop in grain size and number, in heat-susceptible wheat cultivars exposed to heat stress at the time of flowering. Heat stress may have lowered assimilate availability, photosynthate translocation to grain, and starch accumulation in developing grain, resulting in lower grain production. Heat stress has also been linked to reduced wheat yields in previous research. Anthesis (flowering) at temperatures above 27°C resulted in a large number of sterile grains, resulting in a decrease in wheat production. Wheat cultivars yielded fewer grains and had lower grain numbers when the temperature exceeded 30°C before anthesis (Figs. 2 and 3).

FIG. 2 ROS generation by abiotic stress and its effect on wheat.

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FIG. 3 ROS generation induced by abiotic stress in plants.

Abiotic-stress-induced ROS production and its molecular mechanisms The ability to withstand abiotic stresses is a complex quantitative characteristic of several plant species, including wheat. GWAS are being used by scientists all over the world as a tool to investigate the biological mechanism behind these complex attributes (GWAS). It usually entails a large panel of diverse germplasm to give high-resolution gene mapping based on recombination events. Various genes that code for proteins are expressed by plants during abiotic stress response through a large number of signaling cascades. Regulation of these tightly controlled genes is crucial to the synthesis and regulation of ROS. Functional genomics has classified these stress-responsive genes in plants into many types, including functional proteins, enzymes, transcription factors, protein kinases and phosphatases, and molecular chaperones. Plants have been identified and categorized as possessing many genes that help maintain ROS homeostasis and respond to abiotic stresses (Fig. 4, Table 1).

Conclusion ROS are produced as a by-product of cellular metabolism. Many metabolic pathways, located in different organelles of the cell, lead to ROS production through electron transport activities of plasma membranes, mitochondria, and chloroplasts. ROS serves as a signaling molecule in low quantities and as a destructive molecule in high concentrations. Wheat plants activate antioxidant defense systems to counter-balance abiotic stress, which aid in the structural integrity of cell compartments and presumably prevent oxidative damage.

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FIG. 4 Abiotic stress tolerance genes and factors in plants.

TABLE 1 Wheat abiotic stress tolerance traits based on molecular approaches. Abiotic stress

Wheat types

Mapping approach

QTL locations on chromosomes

Trait of stress tolerance

References

Drought

Emmer

QTL mapping

7AS

Root development

Merchuk-Ovnat et al. (2017)

Bread

QTL mapping

3A, 1A, 7A

TKW, seeds/spike, the grain yield, number of spikes/plant

Xu et al. (2017)

4A, 2D

Stem water-soluble carbohydrates

Nadia et al. (2017)

4B, 7A, 5A, 1B,5B, 2B, 6B, 2D, 6B

Length of plant, length of spike, spikes/ plant, days taking to heading and seeds/ spike

Mwadzingeni et al. (2017)

5D, 6D, 7D

Photosynthesis, the 1000-kernel weight (TKW), ultimate grain yield

Saeed et al. (2017)

Bread

Rainfed

PEG stress

Association mapping

Triticale

QTL mapping

4B, 6R

Cell-wall-bound phenolics

Hura et al. (2017)

Bread

QTL mapping

6A

Early ground cover

Mondal et al. (2017)

5A, 7A

Anthesis timing, the grain filling timing, and the 1000-kernel weight (TKW)

Gahlaut et al. (2017)

Durum

Association mapping

6B, 1B, 5B, 2B, 4B, 7B, 3B,

Grain yield, the 1000-kernel weight (TKW), height of the plant, spike length, days to heading

Soriano et al. (2017)

Durum

Association mapping

6B, 1B, 1A, 4B

Yield, root morphology

Lucas et al. (2017)

Source: Modified from Kulkarni, M., Soolanayakanahally, R., Ogawa, S., Uga, Y., Selvaraj, M.G and Kagale, S. 2017. Drought response in wheat: key genes and regulatory mechanisms controlling root system architecture and transpiration efficiency. Front. Chem. 5, 106.

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Ancestral QTL alleles from wild emmer wheat enhance root development under drought in modern wheat. Front. Plant Sci. 8, 703. Mondal, S., Singh, R.P., Crossa, J., Huerta-Espino, J., Sharma, I., Chatrath, R., Singh, G.P., Sohu, V.S., Mavi, G.S., Sukaru, V.S.P., Kalappanavarg, I.K., Mishra, V.K., Hussain, M., Gautam, N.R., Uddin, J., Barma, N.C.D., Hakim, A., Joshi, A.K., 2013. Earliness in wheat: a key to adaptation under terminal and continual high temperature stress in South Asia. Field Crop Res 151, 19–26. Mondal, B., Singh, A., Yadav, A., Tomar, R.S.S., Vinod, G.P.S., Prabhu, K.V., 2017. QTL mapping for early ground cover in wheat (Triticum aestivum L.) under drought stress. Curr. Sci. 112, 1266–1271. Mueller, B., Hauser, M., Iles, C., Rimi, R.H., Zwiers, F.W., Wan, H., 2015. Lengthening of the growing season in wheat and maize producing regions. Weather Clim. Extremes 9, 47–56. Mwadzingeni, L., Shimelis, H., Rees, D.J.G., Tsilo, T.J., 2017. Genome-wide association analysis of agronomic traits in wheat under drought-stressed and non-stressed conditions. PLoS One 12, e0171692. Nadia, K., Chang, X., Jing, R., 2017. Genetic dissection of stem water-soluble carbohydrates and agronomic traits in wheat under different water regimes. J. Agric. Sci. 9, 42. Nawaz, A., Farooq, M., Cheema, S.A., Wahid, A., 2013. Differential response of wheat cultivars to terminal heat stress. Int. J. Agric. Biol. 15, 1354–1358. Noctor, G., Foyer, C.H., 1998. Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 49, 249–279. Olmos, E., Harnandez, J.A., Sevilla, F., Hellin, E., 1994. Induction of several antioxidant enzymes in the selection of salt tolerant cell line of Pisum sativum. J. Plant Physiol. 144, 594–598. Saeed, I., Chen, X., Bachir, D.G., Chen, L., Hu, Y.G., 2017. Association mapping for photosynthesis and yield traits under two moisture conditions and their drought indices in winter bread wheat (Triticum aestivum L.) using SSR markers. Aust. J. Crop. Sci. 11, 248. Sairam, R.K., Deshmukh, P.S., Saxena, D.C., 1998. Role of antioxidant systems in wheat genotypes tolerance to water stress. Biol. Plant. 41 (3), 387–394. Sharma, A., Rawat, R.S., Verma, J.S., Jaiswal, J.P., 2019. Correlation and heat susceptibility index analysis for terminal heat tolerance in bread wheat. J. Cent. Eur. Agric. 14, 57–66. Soriano, J.M., Malosetti, M., Rosello´, M., Sorrells, M.E., Royo, C., 2017. Dissecting the old Mediterranean durum wheat genetic architecture for phenology, biomass and yield formation by association mapping and QTL meta-analysis. PLoS One 12, e0178290. Upadhyaya, A., Davis, T.D., Larsen, M.H., Walser, R.H., Sankhla, N., 1990. Uniconazole induced thermotolerance in soybean seedling root tissue. Physiol. Plant. 79, 78–84. Xu, Y.F., Li, S.S., Li, L.H., Ma, F.F., Fu, X.Y., Shi, Z.L., 2017. QTL mapping for yield and photosynthetic related traits under different water regimes in wheat. Mol. Breed. 37, 34. Yu, Q., Li, L., Luo, Q., Eamus, D., Xu, S., Chen, C., Wang, E., Liu, J., Nielsen, D.C., 2014. Year patterns of climate impact on wheat yields. Int. J. Climatol. 34, 518–528.

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Further reading Atta, K., Singh, A.P., Adhikary, S., Mondal, S., Dewanjee, S., 2022. Drought stress: Manifestation and mechanisms of alleviation in plants. In: Eyvaz, A.P. M., Albahnasawi, A., Tekbas¸ , M.M., G€urbulak, M.E. (Eds.), Drought. IntechOpen, https://doi.org/10.5772/intechopen.102780. Ayalew, H., Liu, H., Yan, G., 2017. Identification and validation of root length QTLs for water stress resistance in hexaploid wheat (Titicum aestivum L.). Euphytica 213 (126). Dhyani, K., Ansari, M.W., Rao, Y.R., Verma, R.S., Shukla, A., Tuteja, N., 2013. Comparative physiological response of wheat genotypes under terminal heat stress. Plant Signal. Behav. 8 (6), 1–6. Foyer, C.H., Noctor, G., 2009. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid. Redox Signal. 11, 861–905. Iannucci, A., Marone, D., Russo, M.A., De Vita, P., Miullo, V., Ferragonio, P., 2017. Mapping QTL for root and shoot morphological traits in a durum wheat  T. dicoccum segregating population at seedling stage. Int. J. Genom. 2017, 1–17. https://doi.org/10.1155/2017/6876393. Article ID 6876393. Ji, X., Shiran, B., Wan, J., Lewis, D.C., Jenkins, C.L.D., Condon, A.G., 2010. Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat. Plant Cell Environ. 33, 926–942. Kratus, T.E., Mc Kersie, B.D., Fletcher, R.A., 1995. Paclobutrazol induced tolerance of wheat leaves to paraquat may involve antioxidant enzyme activity. J. Plant Physiol. 145, 570–576. Kulkarni, M., Soolanayakanahally, R., Ogawa, S., Uga, Y., Selvaraj, M.G., Kagale, S., 2017. Drought response in wheat: key genes and regulatory mechanisms controlling root system architecture and transpiration efficiency. Front. Chem. 5, 106. Lizana, X.C., Calderini, D.F., 2013. Yield and grain quality of wheat in response to increased temperatures at key periods for grain number and grain weight determination: considerations for the climatic change scenarios of Chile. J. Agric. Sci. 151, 209–221. Loutfy, N., El-Tayeb, M.A., Hassanen, M., Moustafa, M.F., Sakuma, Y., Inouhe, M., 2012. Changes in the water status and osmotic solute contents in response to drought and salicylic acid treatments in four different cultivars of wheat (Triticum aestivum L.). J. Plant Res. 125, 173–184. Ma, J., Luo, W., Zhang, H., Zhou, X.H., Qin, N.-N., Wei, Y.-M., 2017. Identification of quantitative trait loci for seedling root traits from Tibetan semi-wild wheat (Triticum aestivum ssp. tibetanum). Genome 25, 18. Ovenden, B., Milgate, A., Wade, L.J., Rebetzke, G.J., Holland, J.B., 2017. Genome-wide associations for water-soluble carbohydrate concentration and relative maturity in wheat using SNP and DArT marker arrays. Genes Genomes Genet. 7, 2821–2830. Pastouri, G.M., Trippi, V.S., 1992. Oxidative stress induces high rate of glutathione reductase synthesis in a drought resistant maize strain. Plant Cell Physiol. 33 (7), 957–961. https://doi.org/10.1093/oxfordjournals.pcp.a078347. Tiwari, R., Sheoran, S., Rane, J., 2015. Wheat improvement for drought and heat tolerance. In: Shukla, R.S., Mishra, P.C., Chatrath, R., Gupta, R.K., Tomar, S.S., Sharma, I. (Eds.), Recent Trends on Production Strategies of Wheat in India. Directorate of Wheat Research, Karnal, Haryana, India, pp. 39–58.

Chapter 9

Regulation of circadian for enhancing abiotic stress tolerance in wheat Mst. Anamika Amzada, Mohd. Kamran Khanb, Most. Maria Haque Prodhana, Anamika Pandeyb, Sohana Juia, M. Hasanuzzamana, Md. Mosfeq-Ul-Hasanc, Mehmet Hamurcub, Md. Arifuzzamana,⁎, and Tofazzal Islamd,⁎ a

Department of Genetics and Plant Breeding, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh, b Department of Soil

Science and Plant Nutrition, Faculty of Agriculture, Selcuk University, Konya, Turkey, c Controller Section of Examinations, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh, d Institute of Biotechnology and Genetic Engineering (IBGE), Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh *

Corresponding authors. e-mail: [email protected] (Md. Arifuzzaman); [email protected] (Tofazzal Islam)

Introduction The second most important commercially produced grain crop in the world is bread wheat (Triticum aestivum L., 2n ¼ 6  ¼ 42, AABBDD). It is a great source of nutrition for 40% of the world’s people (Giraldo et al., 2019). Wheat provides 70% carbohydrate, 12% protein, 22% crude fiber, 2% fat, and micronutrients like zinc and iron (Lemmens et al., 2018; Alomari et al., 2019). By 2050, global wheat production must be increased by 60%, from 3.5 t per hectare to 5 t per hectare, to nourish about of 9 billion people (Langridge, 2013; Borisjuk et al., 2019). With an expansion of 5.35 million hectares of land, worldwide wheat production increased from 762.20 million tons (2019/20) to 775.87 million tons (2020/ 21), but the yield dropped from 3.54 to 3.51 metric tons per hectare (USDA, 2021). The main factors limiting wheat production decline are current climatic change and abiotic stresses (Lobell et al., 2011; Banerjee et al., 2021). Abiotic stresses in agriculture have shown to be a significant danger to food security, and the consequences of global warming and climate change are exacerbating. Abiotic stressors like heat, drought, salt, mineral toxicity, cold, and others affect crops at various phases from germination through harvest. These stresses affect plants on their morphology, biochemistry, and physiology. After all, growth and yield of plants become retarded (Yadav et al., 2020). Heat and drought are two major abiotic stressors of wheat where heat stress affects metabolic pathways, changing the grain’s starch and protein composition. It is predicted that if global temperatures rise by 10 degrees Celsius, global wheat yields would decline by around 6% (Asseng et al., 2013). Drought stress occurs when there is insufficient precipitation throughout the season, and it has a variety of morphological, physiological, and biochemical impacts on wheat. A significant decrease of yield and quality in wheat is happened owing to continuous exposure to cold stress that causes leaf chlorosis, lowered root-shoot surface area, stunted growth, and troubled water and nutrient relations (Hassan et al., 2021). Salinity causes a decline in plant development and agricultural production by delaying seedling germination, reducing seedling growth and seedling metabolism (El Sabagh et al., 2020). Overall, wheat morphology (root and shoot length, number of leaves, flowering period, growth rate during vegetative stage), physiology (photosynthetic activity, lowering of leaf osmotic potential, water potential and relative water content, creation of nutritional imbalance), and biochemical changes (accumulation of glycine betaine, proline, MDA, abscisic acid) are all critical processes for biomass production and are all regulated by a clock under abiotic stress conditions (Chow and Kay, 2013; Dodd et al., 2005; Ni et al., 2009). The clock that regulates all of the mechanisms mentioned above is known as circadian clock. The circadian clock is a self-contained oscillator that produces 24-h endogenous biological rhythms. This clock enables organisms to regulate their metabolism and development in response to changes in their external environment on a daily and seasonal basis (Faure et al., 2012). “Zeitgeber” is a German word that means “time-giver,” and it refers to an internal timekeeping mechanism that works well and precisely when external stimuli give a time cue (Gamble et al., 2014; Gill et al., 2015; Greenham and McClung, 2015; Nohales and Kay, 2016; Xu et al., 2022)The clock functions as a molecular switch, turning genes on or off, usually by directing their transcription, when conditions are better or worse, or when something needs to be done right immediately (Espinoza et al., 2010).

Abiotic Stresses in Wheat. https://doi.org/10.1016/B978-0-323-95368-9.00024-2 Copyright © 2023 Elsevier Inc. All rights reserved.

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Circadian clocks have been discovered in fungi, insects, cyanobacteria, and mammals, among other creatures (Young and Kay, 2001). We now know a lot more about the structure of the plant’s circadian clock by extensive research on the model organism Arabidopsis thaliana. In plants, a clock system is composed of three components: a central oscillator, input and output pathways. Interlocking transcription and translation feedback loops a central oscillator, which allows Arabidopsis to grow and flower at the right times. Here, two pathways involved: (i) input pathways which allow the oscillator to think about what’s going on outside; and (ii) output pathways, which control things like growth, stress responses, and flowering time (Greenham and McClung, 2015; Hsu and Harmer, 2014). A circadian rhythm is a clock that helps plants to stay healthy by regulating their physiological activities with changes in the environment. Both natural and man-made choices looked at the circadian clock as a way to make crops healthier, and to make more biomass for people to use. We still don’t know much about the crop circadian clock, even though we’ve learned a lot in Arabidopsis, preventing it from being rationally improved for improved fitness. Nothing is known about how these genes impact the circadian clock, good thing is that several crucial agronomic features are connected (Bendix et al., 2015; Kim et al., 2012; Preuss et al., 2012). Again, we can’t make more exact choices for certain circadian features in plants. We could figure out how modifying the clock’s functions might help plants develop more biomass if we understood more about the clock’s involvement in these physiological processes. Furthermore, it was unclear if the critical physiological systems in wheat, flowering time control, and stress responses to cold, drought, and salt, interacted. In this chapter, we’ll review and discuss about how circadian clock works in plants with special emphasis to wheat. The molecular and physiological mechanisms of circadian clock in monocots and wheat in response to abiotic stress are also elaborately discussed in relation to the improvement of the abiotic stress tolerance in wheat.

General mechanism of the circadian clock The general mechanism of the circadian clock in plants has been studied under this category. Arabidopsis is a model plant in which the circadian clock regulates more than 30% of transcriptomes (Michael et al., 2008). In monocot, such as in rice, this similar kind of transcriptomes is presented as well (Marcolino-Gomes et al., 2014; Filichkin et al., 2011; Khan et al., 2010). The circadian clock regulates a number of vital physiological functions in plants (Fig. 1). For example, the clock controls flowering time, phytohormone and signaling generation, growth regulation, metabolic activities, and more (Covington et al., 2008). Many genes in our circadian clock cooperate through transcriptional and posttranscriptional series feedback loops to verify genes that are turned on and off at the optimal times throughout the day (Fogelmark and Troein, 2014; McClung, 2014). Even though the core circadian clock genes are produced all day, there are three different transcriptional stages in the morning, day, and evening, each of which shows the activity of several fundamental circadian clock proteins (Fig. 1).

FIG. 1 General mechanism of circadian clock. The central area shows how the core circadian clock regulates itself, based on the model modified from Fogelmark and Troein (2014). The blackish gray area represents nighttime, whereas the yellow highlighted area represents daytime. Lines with blunt arrows denote something that isn’t working, while lines with pointed arrows denote something that is working. Green-colored solid circles are used to stop giving feedback.

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Fig. 1 shows two transcription factors LATE ELONGATED HYPOCOTYL (LHY) and CIRCADIAN CLOCK ASSOCIATED1 (CCA1), both are express and active around dawn (Wang and Tobin, 1998). REVEILLE (RVE) gene family such as RE1, RE4, RE6, and RE8 is MYB (myeloblastosis)-like transcription factors, which shows redundancy with main clockactivating genes LHY and CCA1 (Rawat et al., 2009, 2011; Zhang et al., 2007; Kuno et al., 2003;). Inside the promoters of target genes, LHY and CCA1 find two similar cis-regulatory regions named the evening element (EE) and the CCA1binding site (CBS) (Harmer et al., 2000; Wang et al., 1997). LHY and CCA1 suppress evening-expressed genes TIMING OF CAB EXPRESSION1 (TOC1), EARLY FLOWERING 3 (ELF3), EARLY FLOWERING 4 (ELF4), and LUX ARRHYTHMO (Kikis et al., 2005; Hazen et al., 2005; Alabadı´ et al., 2001), while increasing the expression in the morning (Farr
e et al., 2005). The sequential expression of PRR genes throughout the day promotes transcriptional suppression of other PRR family members and extra core clock genes (Farr
e and Liu, 2013). PRR9 expression increases in the morning after LHY and CCA1 activation, while PRR7 expression rises in the afternoon (Matsushika et al., 2000). In the late morning, PRR7 and PRR9 act together to suppress LHY and CCA1 activity in a feedback loop (Nakamichi et al., 2010; Farr
e and Kay, 2007). The evening buildup of TOC1 maintains its control of LHY, CCA1, and previously expressed PRRs; moreover, TOC1 action feeds back to decrease its expression (Huang et al., 2012; Gendron et al., 2012). Despite the evidence that PRR3 interacts to and regulates the TOC1 protein in the vasculature (Para et al., 2007), it is uncertain what role PRR3 plays within the clock. LUX, ELF3, and ELF4 are the three proteins that make up the evening complex (EC) (Nusinow et al., 2011). However, ELF3 and ELF4 are plant-specific proteins with no conserved functional domains (Hazen et al., 2005; Onai and Ishiura, 2005). In the late evening, the EC inhibits GIGANTEA (GI), PRR7, PRR9, and NIGHT LIGHT-INDUCIBLE AND CLOCK-REGULATED1 (LNK1) (Chow et al., 2012; Herrero et al., 2012; Helfer et al., 2011; Kolmos et al., 2009). The EC downregulates itself by suppressing LUX at dawn, allowing the clock-regulating cycle to resume the next day (Helfer et al., 2011). Unlike CCA1 and LHY, RVE8 increases evening-expressed genes (Rawat et al., 2011). RVE8 protein rises in the afternoon, despite the fact that its transcript has a dawn-phased expression. By binding EE sequences, RVE8 activates TOC1, PRR5, PRR9, GI, LUX, and ELF4 (Rawat et al., 2011). The action of RVE8 is comparable to RVE4 and RVE6 (Hsu et al., 2013). LNK1 and LNK2 are similarly expressed early in the morning, although their protein expression is perhaps a little afterward. Physically binding to RVE transcription factors, both LNK1 and LNK2 proteins operate as coactivators for RVE8 and RVE4 in the increase of PRR5 and TOC1 transcription (Xie et al., 2014). ZEITLUPE (ZTL) and GIGANTEA (GI) function together to regulate the accumulation of TOC1 and PRR5 proteins, which is a significant posttranscriptional process (Ito et al., 2012; Demarsy and Fankhauser, 2009). ZTL is an F-box protein that functions as a clock in blue-light photoreceptors (Somers et al., 2000). GI is a major plant-specific protein that serves as a scaffold for a number of different protein complexes (Park et al., 1999; Fowler et al., 1999; Huq et al., 2000). When light activates ZTL, it strengthens its link with GI, preventing the 26S proteasome from destroying both of them (Kim et al., 2007). When the ZTL-GI complex binds to PRR5 or TOC1, the 26S proteasome degrades the PRR protein (Fujiwara et al., 2008; Kiba et al., 2007; Ma´s et al., 2003). The formation of a complex with ELF3, which causes GI breakdown by the 26S proteasome, also controls the accumulation of GI proteins (Yu et al., 2008). To keep circadian rhythms, gene expression timing and regulatory interactions inside the core oscillator are essential. When clock genes act together, they establish a complex regulatory network that affects a variety of plant signaling and metabolic pathways (Fogelmark and Troein, 2014; Hsu et al., 2013; Pokhilko et al., 2012).

Clock-mediated abiotic stress response Genetic regulation of the circadian clock is controlled by several biotic stress responses. Under abiotic stress conditions, it is involved in a complex signaling network which coordinates many physiological and metabolic processes of the plant. However, coordination of abiotic stress and circadian clock provides a control mechanism over the amount of energy on a daily basis (Markham and Greenham, 2021). In abiotic stress response pathways, individual genes are expressed in a wide variety of phases, but peaks of expression are grouped around specific times of day. This is true for reactions to diurnal environmental changes, such as cold or heat, as well as longer-term changes, such as drought, or persistent changes, such as high osmoticum, etc. When these genes are turned on and off at different times on each day, this raises how the clock is also responsible for the stress-response gene’s rhythmic and basal expression. It also functions by controlling their amplitude responses to external inputs through a process known as gating, which is how it works (Grundy et al., 2015) (Fig. 2). According to Fig. 2, a large number of cold-inducible genes are at their peak in the afternoon, just before it starts to become cold at night, while genes that are turned off by cold are at their peak around dawn. These include cold-responsive transcription factors CRE/DRE-BINDING FACTORs 1, 2, 3, and the circadian and cold-regulated genes CCR1, CCR2, and

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FIG. 2 Abiotic stress reactions during different times of the day and night. Abiotic stress is depicted on the map in red. In the case of every stress, most stress-responsive genes are expressed at their peak at a specific period. For every form of stress, the time of maximum basal expression is represented in blue, while the peak responsiveness time to various environmental signals is given in green.

RD29A (Dodd et al., 2005; Harmer et al., 2000). This suggests that the rhythmic fluctuations in freezing tolerance may produce transcription of these cold-responsive genes. Plants respond to heat stress during the day, and many heat-sensitive genes are expressed. In contrast, these heatrepressed genes showed its expression during night. For example, the peaks revealed for ROS-scavenging enzymes in Arabidopsis and heat shock proteins (HSP70s) in spinach were found to be upregulated in the middle of the day (Lai et al., 2012; Li and Guy, 2001). During the day, plants lose water by stomatal opening ( Jarvis, 1976), and rhythmic activation of drought-inducible genes may help plants to conserve water. Many drought-repressible genes rise during the day, whereas they should have expected to peak at night. Again, most of the drought-inducing genes reveal their peak at dawn (Grundy et al., 2015). Overall, it can be postulated that the genes involved in tolerance to one type of abiotic stress may also contribute to other pathways, putting them under more selective pressure for optimal expression timing than other genes. The clock can ensure that the stress responses endure after the first exposure in several ways. The following Fig. 3 shows some of these ways: Because LHY and CCA1 are both expressed more in cold temperatures, this would then make coldresponsive genes such as CBFs and CORs more active over a long period of time, like a whole year or more. Cold treatments at various times of the day induce CBF1,2,3 transcription differently, with the morning being the most effective (Fowler et al., 2005; Thomashow, 2010). Heat stress, on the other hand, keeps the circadian period shorter (Kusakina et al., 2014) and suppresses the expression of the LHY and CCA1 genes while boosting the expression of the TOC1 gene. CBF gene peak expression should be reduced as a result of this. Drought stress stops the expression of TOC1, which makes the stomata close more tightly. Salinity inhibits the production of GI, which improves the function of the Na +/H + transporter SOS1 (Kim et al., 2013). Because plants are frequently exposed to numerous forms of abiotic stress at the same time in their natural environment, the frequency and expression pattern of clock genes are more likely to reveal how these signals are coupled. Drought and heat stress, for example, have conflicting effects on TOC1 and LUX transcription, but work together to increase PRR7 activity through increasing HSFB2b activity (Kolmos et al., 2014). On the other hand, CBF1 binding to the LUX promoter maintains vigorous transcriptional oscillations at low temperatures (Chow and Kay, 2013). So, the combined effect would be that PRR7 would be more likely to be expressed, and TOC1 and LUX transcription would be at the same level as before. Because cold has an unknown effect on TOC1, LUX and CCA1 should be the same. As a result, cold and drought have a combined effect that would cause LUX expression to fall to intermediate levels. Minimum levels of TOC1 and maximum levels of CCA1 expression would, however, be associated with this. As a result, different combinations of environmental stressors may produce different clock gene expression profiles and, as a result, diverse

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FIG. 3 Regulating the plant’s circadian clock when under stress. The components of the oscillator are shown in these boxes based on when they are expressed, and the circadian cycle that represents day and light intervals is depicted in white and ash, respectively. The top part of the diagram depicts how various types of abiotic stress influence the expression of several clock genes. The bottom portion demonstrates how clock components affect how abiotic stress is communicated. Arrows indicate transcription activation and repression, respectively. Genes are given in rectangle boxes of different colors, and star-shaped boxes show hormones, which are also rectangle boxes. The dashed lines depict how alternative splicing is triggered, whereas the dotted lines depict how the dashed lines influence hormone pathways. These lines don’t have signs on them because opposite sign regulation can happen at many points in the hormone biosynthesis and signal transduction process, but it’s not clear what the overall effect of this regulation will be. PRR stands for “regulator of pseudo-response.” LHY stands for “late elongated hypocotyl.” CCA1 stands for “circadian clock associated 1,” and GI stands for “gigantea.” Abscisic acid, ABAR, CBF, CORS, SOS, and ERDs are all words that refer to the same thing: abscisic acid, ABA, CBF, CORS, and SOS. Salic acid, jasmonic acid, ZEITLUPE, LKP2, LKP2, and CDF are all words that mean “cycling of factors,” but they’re not the same thing.

effects on how the body responds to stress in the future. In order to find out if the clock does integrate abiotic stress signals and if it helps plants stay alive or produce more, more research work will be needed in upcoming days.

Circadian clock response in various monocot crop species To meet up the cereal crop demand by maintaining food security around the globe is crucial to know the circadian clock genes present in the plants. Here, some gene functions are clear and some of them are unclear. In this subhead, we will discuss different circadian clock genes that are present in Table 1.

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TABLE 1 List of some important QTL/genes associated with circadian clocks in different cereal crops.

Crop species Rice (O. sativa)

Barley (H. vulgare)

Gene in crop species

Arabidopsis homolog(s)

Locus/QTL/ chromosome

Functions

References

OsELF3-1

ELF3

ef7/hd17

Light-dependent circadian clock regulation

Yang et al., 2013; Zhao et al., 2012

OsELF3-2

ELF3

–

Light-dependent circadian clock regulation

Yang et al., 2013; Zhao et al., 2012

OsELF3a

ELF3

Photoperiodic flowering

Cai et al., 2022

OsELF3a

ELF3

Photoperiodic flowering

Cai et al., 2022

OsLux

Lux

Photoperiodic flowering

Cai et al., 2022

OsGI-1

GI

–

Flowering and circadian clock regulation

Hayama et al., 2003; Izawa et al., 2011

OsGI-2

GI

–

Flowering and circadian clock regulation

Hayama et al., 2003; Izawa et al., 2011

OsPRR1

TOC1

–

OsPRR37

PRR3/PRR7

Hd2

Flowering time control

Koo et al., 2013; Murakami et al., 2003

OsPRR73

PRR7/PRR3

–

–

Koo et al., 2013; Murakami et al., 2003

OsPRR59

PRR5/PRR9

–

–

Koo et al., 2013; Murakami et al., 2003

OsPRR95

PRR9/PRR5

–

–

Koo et al., 2013; Murakami et al., 2003

OsCCA1

CCA1

–

Chilling stress reduction

Nagel et al., 2015; Zhang et al., 2017

Hd6

CK2α

Chromosome-3

Light and circadian rhythm regulates gene expression

Kato et al., 2002

–

–

M€ uller et al., 2020

EAM7

Koo et al., 2013; Murakami et al., 2003

EAM8

ELF3

eam8/mat-a

Flowering time and circadian clock regulation

Faure et al., 2012

EAM10

LUX

eam10

Growth, flowering time, and circadian clock regulation

Campoli et al., 2013

HvELF3

ELF3

–

Photoperiodic flowering

Dixon et al., 2011; Chow et al., 2012

HvGI

GI

–

Limit flowering time

Pasam et al., 2012; Wang et al., 2010; Dunford et al., 2005

–

–

M€ uller et al., 2020

HvLUX1

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TABLE 1 List of some important QTL/genes associated with circadian clocks in different cereal crops—cont’d

Crop species

Gene in crop species

Arabidopsis homolog(s)

CO HvPpd-H

PRR3/PRR7

FT

Locus/QTL/ chromosome

Functions

References

–

Early flowering

Imaizumi and Kay, 2006

2H

Flowering time regulation

Laurie et al., 1995

–

Early flowering

Imaizumi and Kay, 2006

HvPRR37

PRR3/PRR7

Ppd-H1

Early flowering

Turner et al., 2005; Campoli et al., 2013

Sorghum (S. bicolor)

SbPRR37

PRR3/PRR7

Ma1

Flowering time regulation

Murphy et al., 2011

Maize (Zea mays)

ZmGI1

GI

–

To regulate growth and time of the flowering

Bendix et al., 2013; Mendoza et al., 2012; Miller et al., 2008

ZmGI2

GI

–

–

Bendix et al., 2013; Mendoza et al., 2012; Miller et al., 2008

Ppd-A1

PRR3/PRR7

2A

Flowering time regulation

Shaw et al., 2012, 2013; Seki et al., 2011

Ppd-B1

PRR3/PRR7

2B

Flowering time regulation

Shaw et al., 2012, 2013; Seki et al., 2011

Ppd-D1

PRR3/PRR7

2D

Flowering time regulation

Shaw et al., 2012, 2013; Seki et al., 2011

WAP1/ TaVRN-1

AP1/FUL

–

Act as a flowering promoter

Shimada et al., 2009; Murai et al., 2003; Trevaskis et al., 2003; Danyluk et al., 2003

TaVrn-A1

FT

5A

Flowering time regulation

Worland and Snape, 2001

TaVrn-B1

FT

5B

Flowering time regulation

Worland and Snape, 2001

TaVrnD1

FT

5D

Flowering time regulation

Worland and Snape, 2001

TaVRN-2

FT

5A, 4B

Flowering time, cold stress

Diallo et al., 2010; Kane et al., 2005

TaVRN-3

FT

7B

Act as a flowering promoter

Yan et al., 2006

CO/ TaHd1

–

group-6

Early flowering

Imaizumi and Kay, 2006

TaFT

–

–

Early flowering

Imaizumi and Kay, 2006

TaFDL2

FT

–

Flowering promoter

Li and Dubcovsky, 2008

Rht-B1b

–

–

Yield increase

B€ orner et al., 1996; McVittie et al., 1978

Rht-D1b

–

–

Yield increase

B€ orner et al., 1996; McVittie et al., 1978

WCO1

–

–

Early flowering

Mizuno et al., 2012

RCA-A

–

–

Responding to heat stress

Wan et al., 2008

Wheat (Triticum aestivum)

Continued

148

Abiotic stresses in wheat

TABLE 1 List of some important QTL/genes associated with circadian clocks in different cereal crops—cont’d

Crop species

Wheat (Triticum monococcum)

Gene in crop species

Arabidopsis homolog(s)

Locus/QTL/ chromosome

HSFa-6a

–

HSP17.8

–

TaPRR1

6A, 6B, 6D

TaPRR37

PRR3/PRR7

TaCRY1a

Functions

References

–

Responding to heat stress

Wan et al., 2008

–

Responding to heat stress

Wan et al., 2008

Yield-related traits

Sun et al., 2020

Ppd-H1

Early flowering

Beales et al., 2007

–

–

–

Xu et al., 2010

TaCRY1b

–

–

–

Xu et al., 2010

TaCRY2

–

–

ABA signaling

Xu et al., 2009

TaCAT

–

–

–

Zhang et al., 2022

Eps-D1

ELF3/LUX

1D

Early flowering

Ochagavı´a Orbegozo et al., 2019

tck2a

CK2

Chromosome 5A (Vrn-A1)

Light and circadian rhythm regulation

Kato et al., 2002

WPCL1

LUX

Eps-3Am

Growth, flowering time, and circadian clock regulation

Gawron´ ski et al., 2014; Mizuno et al., 2012

Vrn-Am1

TOC1

–

Flowering time regulation and vernalization response

Dubcovsky et al., 1998; Yan et al., 2006

Vrn-Am2

TOC1

–

Flowering time regulation and vernalization response

Dubcovsky et al., 1998

TmFT

–

–

Early flowering

Mizuno et al., 2012

–

–

Early flowering

Mizuno et al., 2012

Early flowering

Gawron´ ski et al., 2014

TmHd1 m

Wheat (Triticum durum)

Eps-3A

ELF3/LUX

7H8

7H8

–

–

Mastrangelo et al., 2005

6G2

6G2

–

–

Mastrangelo et al., 2005

Rice In rice, circadian clock genes, viz. ELF, Lux, PRR, GI, TOC, and CCA are discovered till date (Table 1). Arabidopsis ELF3 homologs OsELF3-1/OsELF3a, OsELF3-2/OsELF3b, OsELF4a, OsELF4b, and OsELF4c are reported till date in the rice genome (Murakami et al., 2007; Cai et al., 2022). There are multiple independent alleles that modify OsELF3-1 activity, including two QTLs, early flowering 7 (ef7) and heading date 17 (hd17), and the T-DNA insertion allele oself3-1 and the transposon insertion allele oself3 (Matsushika et al., 2000; Saito et al., 2012; Yang et al., 2013; Zhao et al., 2012) Regardless of photoperiod, the strong alleles ef7 and oself3 both produce late flowering (Yuan et al., 2009; Yang et al., 2013). The OsELF3-1 is late to flower in both long days (> 14 h per day) and short days ( 0.254 mm

Bai et al. (2013)

Support plants in soil, constitute root system architecture, control depth of root system and enhances plant’s ability to grow in compact soil

Gupta et al. (2012) and Henry et al. (2011)

Number of seminal roots was negatively correlated with water use efficiency

Manschadi et al. (2008)

The number of roots originating from the first node

Fradgley et al. (2020)

Harvest late season precipitation

Suzuki et al. (2003)

Nitrogen uptake

Herrera et al. (2007)

The uptake of nutrients is 2–6 times more for nodal roots than seminal roots, and thus growing such genotypes in rain-fed areas would be desirable

Kuhlmann and Barraclough (2007)

Regulates root length, surface area, increase water uptake under drought

Fitter (2002), Wasson et al. (2012), and Uga et al. (2015)

Large xylem vessels with increased resource uptake and are well organized in searching deep soil layers to extract water

Clark et al. (2008)

Root hairs

Assist in root contact with soil particles for uptake of water and nutrients as soil dries.

Wasson et al. (2012)

Root angle

The angle between two lines originating at the base of the plant at ground level which fits the angle of the majority of the crown roots in a 2D image of the whole plant

Rueden et al. (2017)

Helps in deeper root growth and affects the area from which roots capture water and nutrients

Rostamza et al. (2013), Comas et al. (2012), Henry et al. (2011), Fitter et al. (2002), Wasson et al. (2012), Uga et al. (2015), and Wasson et al. (2012)

Root dry mass to root voulme

Nakhforoosh et al. (2014)

Controls specific root length and specific surface area which increases plant’s performance and carbon economy under water stress

Lilley and Kirkegaard (2011) and Clark et al. (2011)

Phosphorus uptake

Manske and Vlek (2002)

Root density has been reported to be positively correlated with total root length, root diameter and water use efficiency

Atta et al. (2013)

Root length per unit of soil volume

Nakhforoosh et al. (2014)

Involved in efficient extraction of subsoil water

Pfeifer et al. (2015)

It marks the spreading of roots in the soil and affects the resource uptake

Manschadi et al. (2006)

Maximum root length

Evolved to capture deeper water from the soil under drought stress

Manske and Vlek (2002)

Specific root length

Total root length divided by the total root biomass

Nakhforoosh et al. (2014)

Is an indirect measure of root thickness

Nakhforoosh et al. (2014)

Coarse roots

Nodal roots

Root diameter

Root tissue density

Root length density at depth

(Modified from Wasaya, A., Zhang, X., Fang, Q., Yan, Z., 2018. Root phenotyping for drought tolerance: a review. Agronomy 8 (11), 241.)

164

Abiotic stresses in wheat

evolved through the many diploid and tetraploid ancestors. There are limited studies about root behavior and adaptation to drought among different wheat species. Wang et al. (2016) studied root behavior in the accessions of Aegilops tauschii Coss. (2n), T. monococcum L. (2n), T. dicoccum Schrank ex Sch€ubl. (4n), and domesticated T. aestivum L. (6n) different water regimes under drought stress, diploid species allocated more biomass to roots, whereas tetraploid and hexaploid domesticated species allocated less biomass to roots. Again, with drought, increased biomass was allocated to roots in Ae. tauschii but not in the domesticated species. Wheat acquired a number of adaption mechanisms both before and after domestication to deal with temporary or terminal water deficits in order to ensure survival and reproductive potential. Plants, on the other hand, can change their phenotypes and dry matter partitioning in response to drought stress (Passioura, 2012). Richards et al. (2010) found that smaller plants, lower leaf area, higher root biomass, or less green leaf area ensured reduced harm under drought stress. Root density investigations on underused wheat species such as T. monococcum and T. timopheevi suggested a significant potential for rooting density (Nakhforoosh et al., 2014). In all soil depths, these species demonstrated maximum root length density in full moistened circumstances and limited moisture conditions (see Table 2). In response to reduced rainfall, Durum cultivars Floradur and Matt and Kamut wheat exhibited a significant rise in SRL, but T. monococcum and T. timopheevi appeared to be more stable in this root feature. The observations on these species hypothesized that the enhanced tillering potential leads to a more intensive shoot-borne root system originating from lower stem nodes (Klepper et al., 1984; Zobel and Waisel, 2010). We tried to summarize the important findings from original studies of Nakhforoosh et al. (2014) (Table 2). Greater root diameter was found in T. timopheevii followed by T. monococcum, T. carthlicum, T. turanicum, T. durum, and T. aestivum. Maximum root length density and high specific root length were observed in T. monococcum and T. timopheevii compared to the rest of the species. The concluding point from the studies of Nakhforoosh et al. (2014) is that T. monococcum and T. timopheevii are important sources for root traits like root diameter, root length density, tissue mass density, specific root length for the improvement of bread wheat, and durum wheat under moisture stress condition. In the soil-plant-atmosphere continuum, the root system is a crucial component of resistance to water transport in a drying environment (Blum, 2011). The economic response of the root system to environmental changes is assumed to be indicated by specific root length (SRL) (Ostonen et al., 2007). A higher SRL suggests that there is a greater proportion of fine roots (Ryser, 2006). Oyanagi (1994) asserts that genotypes adapted to drier environments have a deeper root system owing to a lower seminal root angle, whereas genotypes adapted to wetter conditions have more horizontal seminal root growth and shallow root systems. Previous research indicated a wide range of variation and a number of seminal roots ranging from 3.6 for einkorn wheat to 6 for Kamut wheat (T. durum) (Gregory et al., 1978; Manschadi et al., 2008). The significant and positive relationship between seminal root number and RLD at 50–60 cm soil depth demonstrates the functional importance of seminal roots for deeper soil exploration. This research backs up Watt et al. (2008)‘s claim that seminal roots are primarily responsible for root growth. Zhang et al. (2002) studied the influence of root system development on WUE in wheat evolution, focusing on wheat species with various ploidy chromosomes. An important finding revealed that soil drought increased WUE and reduced root growth of wheat markedly at the whole plant level. Under the drought condition, greater WUE was observed in Oct. triticales French. S. cereals followed by Hex. Triticales, T. aestivum, T. dicoccum, T. dicoccoides, Ae. Squarrosa, T. monococcum, T. boeoticum, and T. spelta. The root growth variation was very much evident from wheat evolution. The root weight of T. spelta is the biggest under the drought condition, followed by T. monococcum, T. boeoticum, Oct. triticales, T. aestivum, T. dicoccum, T. dicoccoides, French. S. Cereals, Hex. Triticales, and Ae. squarrosa. Increased WUE was observed at the whole plant level of chromosome ploidy in the evolution from 2n to 6n under both water conditions but decreased root weight and root length.

Root behavior in wheat under heat stresses and its improvement Heat stress is often caused by increased canopy temperature, which is determined by air and soil temperature, soil and canopy parameters, and soil moisture loss (Ugarte et al., 2007). Crops are affected by high temperatures in a variety of ways, including poor germination and plant establishment, reduced photosynthesis, leaf senescence, decreased pollen viability, and lower grain production with smaller grain size (Asseng et al., 2011). While most plant study focuses on aboveground organs, the radicular system accounts for a significant amount of the plant’s bulk and energy requirements. Nonetheless, a thorough knowledge of root systems involved in, for example, drought and heat response is critical to boosting crop adaptability to harsher settings due to climate change (Pinto and Reynolds, 2015). Anchorage, mechanical support, nutrition and water intake, and signaling are all functions of roots. Roots are similarly vulnerable to water deficiency and extreme temperatures; for example, compared to other organs, they have a small range of optimum development temperature (Porter and Gawith, 1999). Root growth was inhibited in high-temperature field experiments due to poor carbon partitioning below ground. During the reproductive stage, heat has a significant influence on the quantity, length, and diameter of roots (Batts et al., 1998).

TABLE 2 Wheat species and average fixed effect of root traits (modified from Nakhforoosh et al., 2014).

Sr.

Botanical name

1

T. monococcum L.

2

Common name

Root diameter

Root length density

Tissue mass density

Specific root length

Soil water Depletion

Origin

Ploidy

Genome

Genotypes

Einkorn wheat

Turkey

2

Am

PI428154, PI428165

0.41

6.36

42.98

190.65

9.05

T. timopheevii (Zhuk.) Zhuk.

Zanduri wheat

Georgia

4

GAm

W9

0.45

4.93

43.85

168.50

9.55

3

T. carthlicum Nevski in Kom.

Persian wheat

Georgia

4

BAu

W13

0.22

1.72

16.55

104.65

2.40

4

T. turanicum Jakubz.

Khorasan wheat

US

4

BAu

QK-77 (Kamut), TRI5254

0.34

3.35

45.35

96.55

6.60

5

T. durum Desf.

Durum

Austria, US, France, Mexico

4

BAu

Floradur, SZD3146, Matt, Clovis,7060, 7063, 7604

0.29

2.79

42.54

81.16

5.02

6

T. aestivum L.

Common wheat

Iran, Germany

6

BAuD

Tabasi, Taifun

0.23

1.97

17.80

85.53

1.85

166

Abiotic stresses in wheat

Well-watered plants increase their transpiration rate in response to a substantial vapor pressure deficit for evaporative canopy cooling under heat stress. To fulfill evaporative demand, increased stomatal conductance (Amani et al., 1996) and sufficient vascular capacity, including roots, are necessary. Some characteristics, such as canopy temperature, can be utilized as surrogates to study root growth. Cool canopy temperatures have enhanced plant water availability due to deeper roots (Lopes and Reynolds, 2010). Researchers observed that genotypes with cooler canopy temperatures generated 30% more yield, which was associated with a 40% increase in root dry weight at 60–120 cm. QTL controlling canopy temperature has been shown to be co-located with genetic regions regulating other drought adaptation traits like as kernel number, grain yield, and chlorophyll content (Pinto et al., 2010; Diab et al., 2008; Olivares-Villegas et al., 2007). In previous study, Pinto et al. (2010) revealed 15 QTL for canopy temperature (CT) in the Seri/Babax bread wheat population grown under drought, hot-irrigated, and nonstressed conditions. The researchers discovered five consistent QTL (1B-a, 2B-a, 3B-b, 4A-a, and 7A-a) associated with cooler canopies under drought and heat conditions. Three QTL were exclusively found in drought and heat stress environments, whereas the other two were also seen in nonstressed conditions. The five QTL for canopy temperature explained an average of 7% and 14% of variance under drought and heat, respectively, with a maximal of 27.6% variation under heat in the 4A-a linkage group. A QTL explained a maximum of 27.4% and 17.1% of yield variation under drought and heat, respectively, on the same linkage group. Cooler canopies result from greater transpiration rates, which demand an adequate water supply; hence, root involvement was inferred. Water-soluble carbohydrates (WSC), kernel number, yield, and plant greenness are among the five QTL that overlap with QTL previously associated with drought and heat tolerance (Kuchel et al., 2007; Marza et al., 2006; Rebetzke et al., 2008). Several studies have discussed the importance of root growth as a critical feature for drought resistance, but there is little evidence on its significance under heat stress. Deep root growth at high temperatures has been linked to increased leaf transpiration rates. Plants with a strong radicular system can meet the high evaporative requirement by increasing transpiration rates in hot irrigated circumstances, resulting in cooler canopies (Amani et al., 1996; Bonos and Murphy, 1999). Because soil temperatures at deep are insulated from changes in air temperatures, the global temperature rise may have a more minimal direct effect on roots than on shoots (K€atterer and Andren, 2009). However, some study indicates that RSA is susceptible to temperature changes in the soil (Luo et al., 2020). Many temperature-responsive genes influence shoot and root traits in a pleiotropic manner (e.g., Voss-Fels et al., 2017). Heat stress effects on shoots can be alleviated in part by maintaining evaporative cooling of the plant through transpiration, and root systems are critical in this regard (Lopes and Reynolds, 2010). When compared to controls at 25°C/20°C, 21-day-old wheat plants subjected to a 36°C/28°C (day/night) regime showed a significant decrease in a series of root metrics (e.g., root biomass, shoot-to-root ratio, primary root length, root surface area, and root volume) (Rehman et al., 2019). Carbon transfer from shoots to roots, on the other hand, has been reported to be impeded at high soil temperatures. Wheat root development is reduced in high-temperature field settings due to a carbon reduction partitioned belowground, and the quantity, length, and diameter of roots are considerably impacted (Batts et al., 1998). According to an analysis, significant progress has been made in CIMMYT worldwide nurseries aimed for warmer, irrigated areas. Many lines that perform well in the warmest locations also have high yield potential in more moderate climates (Lillemo et al., 2005). Given the average year-to-year temperature volatility, this is an essential factor. CT assessed at the breeding location was demonstrated to be an excellent predictor of performance across a range of heat-stressed target conditions in hot, low RH situations (Reynolds et al., 1994). More recent attempts have concentrated on breeding for early maturing cultivars that withstand terminal heat stress and illnesses linked with warm, humid conditions ( Joshi et al., 2007). The genotypes exhibited genetic variation for canopy temperature under heat-stressed growth conditions, according to findings from a previous study that used these lines. For example, the QTL for CT on chromosome 2B has been identified as the key QTL responsible for defining root pattern in wheat, exactly the maximum root length of lateral and primary roots, and as stress-exclusive (drought and heat) (Ren et al., 2010; Sanguineti et al., 2007). GWAS have been commonly utilized in recent years to find loci on tolerance to high temperatures in crops (Hu et al., 2017; Jamil et al., 2019; Jia et al., 2017; Oladzad et al., 2019) or root architecture (Darzi-Ramandi et al., 2017), but research on root response to temperature are still limited. Similarly, QTL mapping has been used to narrow down crop genomic areas associated with root architecture (Gong et al., 2015). Several research have discovered, mapped, and predicted possible gene candidates for QTLs linked with heat or high-temperature tolerance in various crops such as tomato wheat (Sharma et al., 2017), but very few have focused on root related features. Thus, in wheat, QTLs for cooler canopy temperature (QTL-CT) are associated with a higher number of superficial roots than deep roots (Pinto and Reynolds, 2015). QTL analyses also in the wheat show a coincidence of a QTL for heat and drought tolerance, suggesting a common genetic basis for adaptation to both stresses. This QTL seems to be associated with changes in root distribution to increase water availability (Pinto et al., 2010). Likewise, a later analysis in wheat to identify meta-QTL associated with adaptation to drought and heat stress shows that many QTLs are shared to both heat and drought response, and two of them are associated with higher root length (Acun˜a-Galindo et al., 2015).

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Root behavior in wheat under salinity stress and its improvement Salinity, among other abiotic stress, is a serious hazard to agriculture; today, more than 20% of agricultural land is impacted by salinity, which is spreading day by day and already impacts almost 954 million hectares of the world’s total land area (Saddiq et al., 2021). More than 20% of the world’s soils are salt-affected, and the extent of these soils is growing due to human activity (Munns and Tester, 2008, Ding et al., 2021, Seleiman et al., 2022). Germination is critical in the plant life cycle because it determines subsequent growth, development, and yield parameters. Salinity stress lowers seed germination, resulting in a significant loss in the wheat crop’s final yield. Plant seedlings are vulnerable to stress conditions, and salt stress causes seedling mortality (Saddiq et al., 2021; Seleiman et al., 2022). Salinity stress also has a deleterious impact on root and shoot parameters (Ghiyasi et al., 2008; Jamal et al., 2011). Salt stress (100 mM NaCl) has also been shown to reduce root and shoot lengths and dry weight (Zou et al., 2016). Wheat plants employ a number of physiological, biochemical, and molecular mechanisms to adapt to salt stress at the cell, tissue, and whole plant levels in order to enhance growth and output while mitigating the detrimental effects of the saline environment (Sabagh et al., 2021). Osmotic stress induced by root zone salt slows the production of tillers, resulting in a greater loss in grain harvest than later phases under salinity (Mahboob et al., 2017). Salt has an influence on several physiological aspects in seedlings and mature plants, including root and shoot growth, water relation, ion homeostasis, photosynthesis, senescence, and yield components (Hasanuzzaman et al., 2017). Different degrees of salinity, such as 150 mM NaCl (Khan and Ashraf, 2008), 125 mM NaCl (Afzal et al., 2008), 16 dS m1 salinity (Ghiyasi et al., 2008), and 120 mM NaCl ( Jamal et al., 2011), had a detrimental effect on root length, fresh weight (FW), and dry weight (DW) of both (2015). Similarly, Zou et al. (2016) detected decreased shoot length, root length, wet weight, and DW following 10 days of 100 mM NaCl treatment. The percentage of water content dropped in the root but rose in the shoot and spike of the wheat cultivar Banysoif 1. (Tammam et al., 2008). Lv et al. (2016) discovered reduced RWC in T. monococcum seedling leaves subjected to 320 mM NaCl salt stress. Durum (pasta) wheat (Triticum turgidum ssp. durum) is more salt-sensitive than bread wheat (T. aestivum), which limits its cultivation on farms with sodic or saline soils. The genetic study of segregating populations derived from crossings between genotypes with low and high Na + uptake rates revealed two dominant and interacting genes with considerable effects (Munns et al., 2003). One gene is expected to govern sodium ion (Na +) loading in the xylem in the roots, whereas the other controls Na + retrieval from the xylem in the lower portion of the leaves (Davenport et al., 2005). These mechanisms would cooperate to create low Na + concentrations in the leaf blades, and the Mendelian analysis of two interacting genes would fit. Using a QTL technique using AFLP, RFLP, and microsatellite markers, a locus for one gene, Nax1 (Na + exclusion), was localized to the long arm of chromosome 2A (Lindsay et al., 2004). The LOD score for this locus was 7.5, and it accounted for 38% of the phenotypic variance in the mapping population. One microsatellite marker, Xgwm312, was shown to be strongly linked to the low Na + characteristic in various populations with diverse genetic origins and is now being utilized to select low Na + progeny in a durum breeding program (Lindsay et al., 2004). To transfer the trait of Na + exclusion into current durum wheat varieties, the genetic diversity in salt tolerance was studied over a wide variety of ancient durum-related accessions and landraces representing five Triticum turgidum subspecies (Munns et al., 2006). Borrelli et al. (2018) analyzed metabolic and mineral changes in response to salt stress in durum wheat (T. turgidum ssp. durum). The reduced amplitude of salinity reaction identified in the roots verified the shoots’ important involvement in defining durum wheat salt tolerance. Photosynthesis is restricted in the early stages of plant salt stress owing to stomatal closure induced by decreased leaf turgor and hormone secretion in shoots and roots (Chaves et al., 2009). As a result, durum wheat may be subjected to higher salinities during germination and the early stages of plant growth rather than later in development when winter and spring rainfall leaches the salts out of the root zone (Caliandro et al., 1991). Durum wheat has a fairly salt-resistant crop performance (Flagella et al., 2002). Salinity showed a significant detrimental effect on biomass and growth-related indicators at the root level, which was consistent with previous findings (Rewald et al., 2013; Robin et al., 2016). These parameters began to drop even at 100 mM NaCl and became more evident at 200 mM NaCl. Despite the fact that the Na + concentration in the roots was never dangerous (40, 60, and 90 mM NaCl at 50, 100, and 200 mM NaCl on a tissue water basis), growth reduction was seen due to osmotic stress in the roots, which enforced direct contact of the roots with the saline solution (Munns, 2002). However, the significant decrease in 100 and significant increase in root diameter (Rewald et al., 2013) observed under salinity indicate that the roots respond to the increased osmotic pressure of the nutritional solution by accumulating osmolytes and water. Short-term osmotic stress can cause root cell plasmolysis (Munns, 2002). Salinity-induced decrease in root surface area and alterations in the main root and shoot characteristics were investigated at the phytomer level in bread wheat by Robin et al. (2016). The youngest roots at Pr1 and Pr2 showed the largest influence of salinity on root axis elongation. Compared to the control, both the 50 mM and 100 mM salinity levels reduced root hair length by around 25% and root hair density by 40%. On the other hand, root hair accounted for almost 93% of an

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Abiotic stresses in wheat

individual tiller’s estimated total root surface area. At elevated NaCl concentrations, a reduction in new root main axis length, root hair density, and root hair length combined to reduce estimated root surface area by 36%–66%. Salinity stress reduced the number of root tips (lateral roots), total root length, average root diameter, and total root volume (Shafi et al., 2010). The earliest vital organ is the root. Wheat plants with a well-developed root system have an advantage in maintaining plant development throughout early growth phases and extracting water and micronutrients from the soil (Egamberdieva, 2009). Forming a well-developed root system is crucial for above-ground biomass production under stressful conditions (Iqbal et al., 2018). Saboora et al. (2006) found that salt stress caused severe root growth in wheat and decreased root length and area. Many plants, including wheat, have their root growth inhibited by ammonium, whereas NaCl causes ammonium buildup in roots, which reduces root growth. Root tip bioassay was utilized by Nakamura et al., (2021) to investigate the high sensitivity of wheat seedling roots to salt stress. According to Wu et al. (2015), the root meristem acts as a salt stress sensor, and excessive salt content suppresses root development by inhibiting cell division and elongation (Duan et al., 2015). Salinity is a considerable hindrance to primary axis elongation, lowering root axis length, root hair density and length, and root surface area in wheat, according to a thorough investigation of root development at the phytomer level (Robin et al., 2016). Terletskaya et al. (2020) discovered that anatomical root modulations under osmotic stress conditions were species-specific. Under control settings, the rise in absolute values of root diameter was reduced as wheat species ploidy increased. The species T. monococcum showed the greatest drop in RWC and biomass indices during a water deficit. There is also an increase in the root/shoot length ratio in T. monococcum and T. aestivum species. Simultaneously, no significant differences in the number of roots were identified in any of the plant species studied under stress and control conditions (Serraj and Sinclair, 2002). Maintaining root development in water-stressed situations during the early stages of ontogenesis is critical for plant survival because larger roots in drying soil have an added benefit of making water and mobile nutrients more accessible (Lynch and Wojciechowski, 2015). Monitoring water uptake by the root is frequently more critical than managing leaf transpiration in stressful situations for overcoming the traumatic consequences of osmotic stress (Aroca et al., 2011). However, in longterm breeding strategy, plant selection is predominantly based on organ bioproductivity indices, which has resulted in a decrease in root biomass of contemporary varieties when compared to drought-resistant wild species (Waines and Endaie, 2007). The findings back this up: The species studied were ranked as follows: The value of the root length index under situations of induced water shortage identified T. aestivum, T. monococcum, and T. dicoccum from the control. The degree of variability in root shape determines above-ground organ growth and development (Giehl et al., 2014; Paez-Garcia et al., 2015). Data on changes in the root/shoot ratio under stressful conditions on T. dicoccum, in particular, proved this; the value of this indicator remained practically constant during water deficit. Simultaneously, the rise in root/shoot index in T. monococcum and T. aestivum species during induced water deficit demonstrated that this stress had a negative impact on the growth characteristics of these species’ first leaves. Based on percent to control, these species ranked as T. dicoccum followed by T. monococcum and T. aestivum. Although the impact of osmotic stress on root system development has long been investigated, very little researchers have focused on the processes that determine the change in root growth rate underwater deprivation. Plant tissues are dehydrated as a result of osmotic stress. Yang et al. (2016) demonstrated that their osmotic potential and turgor predominantly determined root cell development. A minimal loss of water in the root can increase tensile strength, but a substantial loss of water reduces the root’s ability to stretch. In compared to the control, all studied species showed a proclivity to lower root RWC under situations of artificial water shortage. T. monococcum comes first, followed by T. aestivum and T. dicoccum. When compared to the control and other studied species, the tetraploid species T. dicoccum had the maximum water content of the main roots. As a result, the root’s ability to retain water under osmotic stress is an important factor in determining its growth. When examining biomass increase by primary roots under water deficiency conditions relative to the control, a comparable ranking of researched species was achieved. It seems reasonable to assume that osmotolerant plants have more visible, stronger, and deeper roots than sensitive plants (Wasson et al., 2012). According to the research, roots adopt a variety of morphophysiological developmental techniques. They can, for example, alter tissue development rate, diameter, and density in response to diverse stresses (Nie et al., 2013; Carrillo et al., 2014; Suseela et al., 2017). Simultaneously, the range of variability in root diameter within a specific species’ root system may vary (Wu and Guo, 2014). A too-small root diameter, on the other hand, impedes root penetration into the soil and does not contribute to the formation of internal structures that transport water and nutrients (Clark et al., 2008; Jaramillo et al., 2013). However, there is evidence that these indicators hinder the root’s capacity to stretch (Yang et al., 2016). Genet et al. (2005) discovered negative connections between root diameter and tensile strength and positive correlations between root diameter and tensile resistance. According to Wu et al. (2016), the root’s potential length is determined by its basal diameter. The longest roots, on average, retain (and even increase) their diameters during elongation.

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The relationship between hyperspectral vegetation indices and soil salinity at different depths can aid in diagnosing salt stress in wheat (Zhu et al., 2021). Soil salinity increases will disrupt water potential equilibrium inside and outside crop root cells, reducing crop water absorption. When soil salt accumulates to a particular level outside the root cells, it causes ion toxicity and destroys their interior structure. These will affect crop physiological processes such as root structure, photosynthesis, transpiration, chlorophyll, and cell structure, resulting in a decrease in yield (Zhang et al., 2011; Miller et al., 1991; Kriston-Vizi et al., 2008; Hackl et al., 2013). According to field observations and prior research, the root density of winter wheat at a depth of 30 cm is relatively high during the filling stage. Furthermore, at this level, the root system has a greater capacity for water absorption and is more susceptible to salt stress (Xue et al., 2003; Jha et al., 2017; Guo et al., 2018). Microorganisms are typically colonized in the rhizosphere and improve germination, root and shoot length, mineral absorption, and yield (Ashraf and Foolad, 2013; Chattha et al., 2017a, b, c), as well as tolerance to salt (Ashraf and Foolad, 2013, Chattha et al., 2017a, b, c) (Arora et al., 2008; Lugtenberg and Kamilova, 2009). Many positive benefits of salt-tolerant rhizobacteria were identified under abiotic stress (Adesemoye et al., 2008; Egamberdieva et al., 2011). Salinity has a deleterious impact on plant development, while it has a negative effect on the function and composition of beneficial soil microbes (Ofek et al., 2006). With a decrease in the amount and quality of root exudates, saline soils impair the structure established by the microbial community near the rhizosphere area (Nelson and Mele, 2007). Many PGPR strains (Stenotrophomonas rhizophila e-p10, Pseudomonas fluorescens SPB2145, Pseudomonas chlororaphis TSAU 13, Serratia plymuthica RR2–5–10, Pseudomonas putida TSAU1, Pseudomonas extremorientalis TSAU20, P. fluorescens PCL1751, and Pseudomonas aureofaciens TSAU22) increased salt tolerance (Egamberdieva et al., 2011, Egamberdieva and Kucharova, 2009). As a result of these strains, wheat can survive and perform better in saline stress settings, yielding higher yields (Mayak et al., 2004; Yasmin et al., 2007). PGPR improves germination rate, growth characteristics, thousand-grain weight, and grain output (Nabti et al., 2010; Abbaspoor et al., 2009). Salt-tolerant rhizobacteria isolated from wheat roots were responsible for enhancing root length in saline environments (Egamberdieva et al., 2008). PGPR for seed inoculation enhanced crop root and shoot length as well as dry biomass, fruiting, and grain yield by enhancing salt tolerance (Barassi et al., 2006; Egamberdieva et al., 2013). Furthermore, PGPR promoted osmotic adjustment during saline circumstances, which helped minimize the negative consequences of salinity stress (Creus et al., 2004).

Breeding model roots for the stressed environments Breeders often require three fundamental inputs, including root systems, to introgress a trait in new varieties: (Abbaspoor et al., 2009) favorable alleles for the target trait in donor germplasm, (Acun˜a-Galindo et al., 2015) a method for identifying the trait, either by appearance (phenotypic selection) or the presence of a specific allele (marker-assisted selection), and (Adesemoye et al., 2008) the human and financial resources to carry out the selection and breeding process. The decision on how many resources to commit to a trait is influenced in part by whether the value it contributes to the final product justifies the effort (and compensates for any yield penalties that may come with it). As a result, breeders must have the means and proof in place to get such improvements into the hands of farmers (Fig. 1).

Phenotyping methods for characterization and exploitation of root system architecture Appropriate phenotyping approaches must be employed to thoroughly investigate the possibilities for targeted creation and selection of RSA features. Given the complexity of roots and the difficulty in reaching them when grown in soil, the approach used for phenotyping should consider both the root attribute to be targeted and the growing system under which the roots are to be evaluated (Ober et al., 2021). For example, phenotyping immature plant root systems provide practical benefits. Plants can be screened in controlled environment conditions for short periods of time, ranging from 2 days to a few weeks, allowing for the screening of a more significant number of plants. While seedling root development often correlates well with mature plants or plants produced in the field (Poorter et al., 2016), seedling root growth does not always correlate well with mature plants or plants cultivated in the field (Bai et al., 2019). The underlying genetic determinants, the genetic background of the test materials, phenotyping procedures, and the nature of the test settings all influence the explanatory accuracy of young plant features. As a result, compromises must be established between the complexity of the experimental system and the repeatability of the resulting phenotypes. The stage of the breeding program would also influence the choice of phenotyping approach in a breeding environment (e.g., line development versus yield testing phase). Keeping these factors in mind, we have compiled a list of the most frequent strategies for improving wheat root structure (Ober et al., 2021).

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FIG. 1 Brief outline indicating the breeding wheat species for root ideotype under abiotic stresses.

Field-based root phenotyping Root phenotyping in the field is sometimes more difficult, time-consuming, and labor-intensive than seedling techniques. Many root crowns are dug with a shovel or manually, depending on the soil conditions, in the procedure known as “shovelomics.” This method is remarkably rapid, with a throughput of up to 50 shovel excavations per hour per worker. It is, however, an intrusive procedure that only provides access to roots growing in the top 20 cm of soil. Nonetheless, when paired with picture analysis, shovel-omics can give valuable insights about field-grown agricultural attributes such as nodal root number or growth angle, including wheat (Maccaferri et al., 2016; York et al., 2018; Fradgley et al., 2020). Using “minirhizotrons,” it is also feasible to observe field-grown roots throughout time in a nondestructive manner. Before planting, transparent cylinders are placed in the appropriate position in the field, either with an installed camera for continuous imaging or an opening, such as an endoscope, enabling root imaging at a given time point. Minirhizotrons provide information about root number and length over time, but they are limited to specific sites (Crocker et al., 2003). Soil coring, often employing a tractor-mounted hydraulic system, can assess root structure in the field at deeper soil depths (Wasson et al., 2016), followed by core breaking washing and root measuring. Core breaking and counting roots at the core face without washing is a novel way to phenotyping soil cores. Image analysis and UV (365 nm) LED illumination was used to develop a system for automatically detecting roots at the core break interface that enhances the contrast between the roots and the soil to increase throughput (Wasson et al., 2016). Drought and heat stress signs above ground are quite easy to notice, such as smaller organs and tissue chlorosis. Nonetheless, some researchers have looked at the function roots play in stress response, owing to the difficulty of doing precise, well-controlled field experiments. As a result, many researchers choose to conduct research in controlled circumstances where rooting volume and temperatures are often unrepresentative of field growth conditions (Anderson, 1986). While conventional plant breeding has made significant progress in stress breeding, three approaches to broaden gene pools can be used: (i) introgression of traits from genetic resources with compatible genomes, such as landraces, wild relatives, and germplasm resources; (ii) wide crosses involving interspecific or intergeneric hybridization; and (iii) genetic transformation. Currently, genetic resources are mostly exploited to strengthen resilience to biotic challenges (Dwivedi et al., 2008), with just a few wild crop relatives being used for abiotic stress adaptation (Hajjar and Hodgkin, 2007).

Challenges and future perspectives for breeding better root systems In terms of their ability to enhance yield under abiotic stress, most of the accessions in germplasm collections are uncharacterized. Identifying elite trait sources among genetic resources, calculating possible yield improvements associated with

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trait expression in excellent agronomic environments, and defining possibly complementary characteristics are still difficult. Introgressions into a common genetic background might result in a cascade of gene activation that boosts yield (Reynolds et al., 2009). QTL providing resistance to heat and drought stress gives the important potential for wheat adaptation to climate change, which is projected to exacerbate both stressors. Because heat and drought are both difficult targets on their own and are likely to occur simultaneously, if one or more of the QTL can be exploited to generate near markers, they will be valuable in molecular breeding (Sanderson et al., 2011). It is noteworthy that considerably more study effort has been put toward shoots/leaves rather than roots even though roots are the first tissues directly exposed to salt stress and function as its sensor. Root development assessment is complex since it generally necessitates extensive and damaging procedures to extract root tissue. However, canopy temperature, which is considerably easier to detect, is linked to the plant’s ability to extract deep water through robust roots (Reynolds et al., 2007; Lopes and Reynolds, 2010) and is easily quantified using infrared technology (Pinto and Reynolds, 2015). We believe that (Abbaspoor et al., 2009) the establishment and routine use of high-throughput, high-precision, field-based/field-relevant phenotyping approaches (Acun˜a-Galindo et al., 2015); the development of molecular tools to track and combine beneficial alleles controlling RSA, and, perhaps most importantly (Adesemoye et al., 2008); detailed knowledge of which RSA is best suited to a given agricultural environment will underpin future direct selection of root traits for improved crop performance. In the coming years, we expect the molecular characterization of an increasing number of wheat RSA genes, providing the research community with multiple entry points into the wheat RSA genetic networks and rapid approaches for integrating this knowledge into the targeted design of RSA ideotypes. These include comprehensive modeling and simulation techniques for identifying potential RSA component trait combinations for breeding programs. Once available, such technologies will analyze certain RSA ideotypes in various environments, providing a knowledge base on which future breeding programs may be performed with confidence. We predict that over the next several years, the goal of high-precision in-field root phenotyping will be attained by continuing to develop systems that integrate numerous layers of phenotypic data from direct and indirect root performance measurements with high-power computation and AI technologies. However, further study is needed in several areas, including the physiological basis of absorbing partitioning from sources to sinks. Furthermore, additional research is needed into the response of roots to salinity stress, including root–shoot signaling and the resulting effects on nutrient and water uptake. To increase salinity tolerance in wheat crops, genetic modification of salt-tolerant characteristics is also required. Of course, these specific goals are the product of a series of research and invention improvements. Crop breeders will benefit from the measures since they will give quick practical applications. Advanced research in functional genomics, system biology, modeling, and computing will enable a more detailed evaluation of genotypic and phenotypic data to anticipate the result of various RSA allelic combinations. As the precision of these stochastic models develops at the field and farming system level, breeders will be able to run hundreds of alternative simulated gene combinations before the chosen crosses are developed and put out for field assessment (Ober et al., 2021). Furthermore, little is known about the molecular mechanisms that govern root thermomorphogenesis and the process of warm temperature-mediated regulation of root gravitropism. Under drought stress in natural soils, roots must modify their architecture and respond to drought, heat, and even soil compaction pressures all at the same time. Further research into the connections and molecular interactions between these soil stressors is required.

Acknowledgments The authors are thankful to MACS-Agharkar Research Institute and Indian Council of Agricultural Research (ICAR), New Delhi for support.

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Further reading Wasaya, A., Zhang, X., Fang, Q., Yan, Z., 2018. Root phenotyping for drought tolerance: a review. Agronomy 8 (11), 241.

Chapter 11

Role of abiotic stresses on photosynthesis and yield of crop plants, with special reference to wheat Md. Rafiqul Islama,⁎, M.A. Baset Miab, and Tofazzal Islamc a

Department of Agronomy, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh, b Department of Crop Botany,

Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh, c Institute of Biotechnology and Genetic Engineering (IBGE), Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh *

Corresponding author. e-mail: [email protected]

Introduction Abiotic and biotic stresses are the major factors limiting crop production in the changing global climate (Islam et al., 2016; Hossain et al., 2021). Among the abiotic stresses, drought, salinity, waterlogging, and extreme temperatures pose a significant threat to plant growth and productivity, resulting in huge crop losses each year. Such stresses have a negative impact on many of the photosynthetic components and significantly reduce crop yield. Wheat is the world’s second most important crop, with an estimated area of more than 200 million hectares in 2020. The area of cultivation of wheat is expected to remain fairly constant in 2030 (Erenstein et al., 2021). Each year, approximately 200 million tons of wheat are produced (FAO, 2021). Drought alone is causing yield losses in 161 million hectares (75% cropped area) harvested wheat area globally, with an average yield loss of 8% (Kim et al., 2019). Around the world, more than 833 million ha of land are salt-affected, and more than 1.5 billion people face significant challenges in growing food (FAO, 2021). Wheat is sensitive to soil salinity, with moderate soil salinity causing a 28% yield loss (Satir and Berberoglu, 2016). A frequent waterlogging situation exists in 12% of the world’s cultivable land, resulting in a 33% yield loss when compared to no waterlogging (Tian et al., 2021). It is predicted that by the 2030s, 11% of the world’s wheat-producing areas will be exposed to physiologically critical temperatures during the reproductive stage. As a result, global wheat production may fall by 6% for every degree of warming (Asseng et al., 2015). Therefore, abiotic stresses have the potential to result in significant yield losses in wheat around the world. These stresses have an impact on photosynthesis, the most complex and sole physiological process in plants for harvesting solar energy. Although the impacts of abiotic stresses on photosynthesis in plants, especially wheat crop, are not precisely understood, a large body of literature is available on how these factors influence this essential process of plants. Considerable genetic and agronomic crop management has been practiced to mitigate the detrimental effects of abiotic stresses on plant photosynthesis and yield. The revolutionary clustered regularly interspaced short palindromic repeats (CRISPR)-CRISPR associated (Cas) technology has shown high promise in the improvement of wheat and other crops for abiotic stress tolerance and high yield (Haque et al., 2018; Islam, 2019; Hossain et al., 2021). In this chapter, we critically reviewed and discussed the effects of four major abiotic stresses, namely drought, heat, salinity, and waterlogging, on photosynthetic machineries, stomatal and mesophyll, as well as biochemical and metabolic limitations on photosynthesis. Photosynthesis regulatory mechanisms and the roles of phytohormones, transcription factors, and enzymes in improving photosynthesis under abiotic stresses are also discussed. Finally, we shared our thoughts on future research for improving photosynthesis in wheat to minimize the impacts of abiotic stresses on crop plants, with a special reference to wheat.

Impacts of abiotic stresses on photosynthesis of plants Photosynthesis is a central physiological process that occurs in green leaves and shoots and energizes a variety of metabolic processes by activating the conversion of light energy into chemical energy (Taiz and Zeiger, 2010; Pan et al., 2012; Chen Abiotic Stresses in Wheat. https://doi.org/10.1016/B978-0-323-95368-9.00015-1 Copyright © 2023 Elsevier Inc. All rights reserved.

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(A)

(B)

(D)

(C)

(E)

FIG. 1 Abiotic stresses effect on wheat. Drought stress on wheat—(A) control and (B) drought; (C) drought and heat stress conditions; (D) plant drying in salt affected coastal area of Bangladesh; and (E) instantaneous maximum rainfall and wind speed on the severity of lodging in wheat (Niu et al., 2016).

et al., 2018; Demmig-Adams et al., 2018). The chloroplast is an important photosynthetic house that undergoes both light and dark reactions, which are extremely sensitive to abiotic stresses. Drought, heat, salinity, and water-logging are the most common abiotic stresses that have negative impacts on photosynthesis, crop productivity, including wheat (Fig. 1). Abiotic stress has an impact on stomatal activity, photosynthetic apparatus, and biochemical processes. Abiotic stress also has a negative impact on photosystem I (PSI) and PS II, as well as the electron transport chain (ETC) (Xia et al., 2006; Efeoglu and Terzioglu, 2009; Kalaji et al., 2016; Sharma et al., 2016). The decrease in photosynthesis is directly related to the decrease in yield. A list of the significant effects of key abiotic stresses on the changes in grain yield and photosynthesis-related characteristics in wheat is given in Table 1.

Drought stress on photosynthesis Drought is a prolonged period of low rainfall that causes extensive crop damage and yield loss. It is one of the most important abiotic stresses that hinders crop productivity drastically. Drought directly reduces wheat productivity by lowering the rate of photosynthesis (Taiz and Zeiger, 2010), and it may reduce grain yield by an average of 45% (Ahmadi-Lahijani and Emam, 2016). Grain yield reduction is attributed to the drought-induced influences on the morphology, physiology, and biochemical attributes of plants. The grain quality of wheat is seriously affected when drought is imposed at flowering and grain-filling stages. Drought stress had a significant effect on the number of tillers, root volume, dry matter of root and shoot, and grain yield (Pouri et al., 2019). It also affects wheat by decreasing leaf area index, net assimilation rate, and can disrupt metabolic activity, including photosynthesis (Ihsan et al., 2016). The drought-induced osmotic stress during anthesis and grain-filling can cause substantial yield loss in wheat. Drought disrupts physiological functions such as leaf photosynthesis, carbohydrate accumulation in the ear, pollen development, and grain production, resulting in a reduction in the number of grains per ear (Liu et al., 2015; Dong et al., 2017). This stress causes a reduction in grain number for a variety of reasons, including disrupted meristem development, floret abortion, and pollen sterility ( Ji et al., 2010; Dong et al., 2017). Plants exposed to drought led to a significant decrease in net photosynthesis rate (Pn), stomatal conductance (gs), and reduced mesophyll conductance by forcing stomatal closure and thylakoid membrane alteration. Water stress not only results in the decrease of photosynthesis and transpiration rates but also affects the efficiency of PSII. In fact, the latter may be one of the causes of changes in photosynthesis (Wang et al., 2016a,b). However, there are genotypic differences in Pn and gs reduction depending on the level of drought tolerance. Under drought stress conditions,

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TABLE 1 Effects of abiotic stresses on the changes in grain yield- and photosynthesis-related traits in wheat. Abiotic stresses

Changes in grain yield-related traits

Changes in photosynthesisrelated traits

Drought

Reduced plant height, panicle length, panicle number per unit area, spikelets per spike, grains per spike, filled grain percentage, and 1000-grain weight, grain and biomass yield, reduced RWC

Reduction of gs, E, gm, RWC, Ψ, increase in Ci, proline, inhibition of carboxylation efficiency (Vcmax), decline in leaf water relations, membrane stability, increased reactive oxygen species (ROS) generation, lipid peroxidation and membrane injury, reduction in Chl a & b, chlorophyll a/b ratio chlorophyll fluorescence, decrease in qP, Fv/Fm, (ΦPSII, ETR), increase in abscisic acid, soluble protein content

Saeidi et al. (2017), Khakwani et al. (2013), Wang et al. (2016a, b), Olsovska et al. (2016), del Pozo et al. (2020), Abid et al. (2018), Zhao et al. (2020), Wang et al. (2017), Dorostkar et al. (2015), Zhang et al. (2018), Mirbahar et al. (2009), and Saeidi and Abdoli (2015)

Heat stress

Decrease in total above-ground biomass, affects anthesis, grainfilling, size, number and maturity of wheat grains, higher ear number per plant lower the kernel number per ear, decreased kernel weight, lower GW and grain yield

Decreased Pn, generation of ROS and damage of thylakoid membrane, chloroplast and plasma membrane, increase/decrease unsaturated lipid species, alteration of mesophyll cell ultrastructure, reduced gs, E, iWUE, WUE, Fv/Fm ratio, increased Ci, decrease of sucrose content, while fructose and glucose content increased or unchanged, decrease WUE

Djanaguiraman et al. (2020), Feng et al. (2014), Mahdavi et al. (2021), Mirosavljevi
c et al. (2021), and H€ utsch et al. (2018)

Salinity

Decreased germination percentage, reduced root length (RL), shoot length (SL), RGR-RL, RGR-SL, DW and FW of root and shoot, RGR, reduced shoot biomass, grain yield

Disrupted photosynthesis, hormonal imbalance, oxidative stress, reduced photosynthetic proteins in chloroplasts, reduced gs, E, Fv/Fm, Ft, reduced chl a, b, carotenoids, and total pigments, and RWC, but increase in ABA, stomatal aperture

Elhakem (2020), Saddiq et al. (2021), Ibrahimova et al. (2021), Rahnama et al. (2010), Hasanuzzaman et al. (2017), Kalhoro et al. (2016), and Seleiman et al. (2022)

Waterlogging

Reduced floret formation, number of kernel and kernel weight, grain yield, DW of root and shoot, root length, root length, root mass, root/ shoot ratio, total dry mass, and leaf area index, reduced straw and grain yield

Reduction in gas exchange parameters (Pn, gs, Ci, E), WUE, chlorophyll a + b content, lower Fv/ Fm, Fv/F0 ratio, ETR, ΦPSII and qP, accumulate sugar in leaf, oxidative injury in root

Ding et al. (2020), Wu et al. (2015), Ghobadi et al. (2017), Arduini et al. (2016), Todorova et al. (2022), Herzog et al. (2016), Shao et al. (2013), and Cotrozzi et al. (2021)

References

Saeidi et al. (2017) discovered higher Pn rates in drought-tolerant wheat genotypes. As a result, drought has a different impact on wheat growth at different growth stages. Drought has a greater impact on plant height, biomass, and yield of winter wheat due to its ability to restrict photosynthesis (Zhao et al., 2020).

Heat stress on photosynthesis Heat stress is one of the most significant environmental factors influencing crop plant growth, development, and yield. It is one of the most significant abiotic stresses affecting wheat productivity and profitability in many wheat-growing regions around the world (Farooq et al., 2011; Hays et al., 2007). Drought has an effect on cellular activities, resulting in a decrease in the growth and yield of wheat. The decrease in yield is attributed to the severely damaged photosynthetic apparatus caused by heat stress. Heat stress inhibits photosynthesis, causing morphological changes in the productive tillering and reproductive (anthesis) stages in wheat. It also accelerates leaf senescence and reduces photoassimilates, impeding shoot and root growth (Lal et al., 2022; Abdelrahman et al., 2022; Bali and Sidhu, 2019). Heat stress reduced photosynthetic

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rate by 17%–25%, grain yield by 29%–44%, and thylakoid membrane damage by 61%–68% depending on growth stage. Photosynthetic rate and grain yield had a significant positive relationship, but thylakoid membrane damage and photosynthetic rate have a negative relationship (Djanaguiraman et al., 2020). Mathur et al. (2014) also indicated that the stroma and thylakoid lamellae in wheat are the most sensitive to heat stress. Heat stress has a wide range of negative effects on crop plants, including changes in physiological activity, growth, and development, as well as decreased grain formation and yield (Mondal et al., 2013). Furthermore, heat stress alters plant water relations, reduces photosynthesis capacity, reduces metabolic activities, and alters phytohormone synthesis, increases reactive oxygen species (ROS) production, increases ethylene accumulation, and affects microspore and pollen tube development (Ashraf and Harris, 2013; Hasanuzzaman et al., 2012, 2013; Almeselmani et al., 2009; Krasensky and Jonak, 2012; Wang et al., 2011). Temperatures around 40°C cause an incessant alternation of ribulose-1,5-bisphosphate carboxylase/ oxygenase (RuBisCo), rubisco activase, and photosystem II (Mathur et al., 2011). When exposed to heat stress, the RuBisCO enzyme may be deactivated in less than 7 days, and the breakdown of rubisco activase may result in a decrease in photosynthetic capacity (Kumar et al., 2016; Raines, 2011).

Salinity stress effect on photosynthesis Salt injury starts with an oxidative effect, which is followed by ionic toxicity and osmotic effects at the subcellular level (Elshafei et al., 2019). The most toxic components of salinity are Na+ and Cl . In the cell, high concentrations of Na+ and/or Cl 1 ions are toxic, lowering photosynthetic capacity. As a result, the contribution of carbohydrates to young leaves is reduced, and the rate of shoot growth is slowed (Oyiga et al., 2016). Salt stress decreases wheat productivity, which is linked to lower seed germination and seedling growth, lower enzymatic activity and photosynthesis, and lower yield (Seleiman et al., 2022; Kumar et al., 2018; Hasanuzzaman et al., 2017). Excess salts have an immediate effect on water status in wheat, reducing photosynthesis and plant growth. By modulating photosynthetic proteins in chloroplasts, it has the potential to influence photosystem function (Munns and Tester, 2008; Zhao et al., 2013). Salt stress also causes stomatal closure to occur quickly, disrupting all photosynthetic processes by creating an imbalance between light capture and energy utilization (Silveira and Carvalho, 2016). Reduced photosynthesis is caused by stomatal closure and restrictions in photosynthetic electron transport. Stomatal closure can be caused by an increase in levels of Na+ and Cl ions in plant cells near stomatal guard cells, which results in reduced CO2 accumulation and increased ROS production, both of which can lead to cell death (Mohamed et al., 2020; Agami et al., 2017). Salt stress also inhibits photosynthesis by altering organelle ultrastructure, metabolite and pigment concentrations, and suppressing several metabolic and physiological processes (Bacu et al., 2020; Annunziata et al., 2017). In saline conditions, lower Na+ accumulation in photosynthetic tissues and higher stomatal conductance are linked to improved salt tolerance in wheat. However, when the salinity is moderate to high, the osmotic effect of salt is more severe than the Na+-specific effect (Rahnama et al., 2010).

Waterlogging on photosynthesis Waterlogging is an abiotic stress that occurs when soil is flooded as a result of heavy rainfall, nonjudicious irrigation, or a poor soil drainage ecosystem. It has a negative impact on crop plant growth and yield. As a result of climate change, flooding is becoming more common and severe. Flooding can be classified as waterlogging or submergence depending on the height of the water column above the soil surface. Waterlogging occurs when flooding occurs up to a few centimeters above the root system, while submergence occurs when flooding covers the plant’s aerial organs. Oxygen (O2) diffusion is quickly inhibited during waterlogging, and CO2 and ethylene concentrations in the root environment quickly rise, causing root and shoot injury in plants. Waterlogging damage in wheat has been extensively studied around the world, and it has been reported that waterlogging in winter wheat can cause a variety of morphological and physiological changes (Cotrozzi et al., 2021; Wu et al., 2015; Shao et al., 2013). It reduces grain yield by affecting many morphological and yield traits in wheat, such as root and shoot growth, number of tillers, spike and spikelet size, and kernels per spike (Ghobadi et al., 2017; Arduini et al., 2016). Waterlogging reduces photosynthetic rate, stomatal conductance, transpiration, decreased leaf wateruse efficiency, and restricts carbohydrate metabolism in both shoots and roots (Shao et al., 2013; Zheng et al., 2009). As a result, both the accumulation of assimilates and their transformation into grains decrease. Plant biomass production may be reduced as a result of stomatal limitations in net photosynthesis, which reduces carbon assimilation. The negative effects of waterlogging differed depending on the duration and stage of waterlogging stress in wheat. During the tillering stage, the plant is sensitive to waterlogging, which results in a significant decrease in chlorophyll content, photosynthetic capacity, and effective quantum yield of photosystem II (Wu et al., 2015). Plants can tolerate waterlogging in the early stages of crop development, but their photosynthetic capacity declines with prolonged waterlogging (Wang et al., 2012).

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Regulation of photosynthesis in crop plants by abiotic stresses Abiotic stresses have either direct or indirect effects on the photosynthetic machinery due to oxidative damage. This may affect photosynthetic pigments, reaction center complexes, the electron transport system, leaf gas exchange, and water use efficiency (Talaat and Shawky, 2017). Furthermore, these stresses reduce cell physiology activity, such as photosynthetic efficiency and protein synthesis, possibly due to osmotic stress and nutritional imbalance. They can also augment the production and accumulation of various osmolytes and osmoprotectants (Talaat, 2019). Based on recent advances, this section describes the various mechanisms underlying abiotic stresses’ impact on photosynthesis and related physiology of wheat (Fig. 2).

Drought Drought stress restricts the growth and yield of wheat by impacting on photosynthesis. Water scarcity reduces the performance of photosynthetic apparatus, damages the thylakoid membrane, and lowers the level of chlorophyll and other photosynthetic pigments. Many studies have found that stomatal limitation in mild to moderate drought and nonstomatal limitation in severe drought causes a reduction in leaf photosynthesis (Muhammad et al., 2021; del Pozo et al., 2020; Kicheva et al., 1994). Stomatal closure disrupts CO2 intake under mild and moderate drought stress, altering enzymatic activities, causing membrane disruption, and reducing ATP synthesis and ribulose-1,5-bisphophate (RuBP) regeneration, inhibiting rubisco activity and affecting photosynthesis. Under severe drought stress, however, dehydration of mesophyll cells allows the use of available CO2, which significantly restricts photosynthesis metabolic processes, resulting in a reduction in WUE and root hydraulic conductivity (Hajiboland et al., 2017; Olsovska et al., 2016; Damayanthi et al., 2011). Drought stress has an impact on the accumulation and activities of enzymes, amino acids, proteins, phytohormones, antioxidants, and other compounds. Different ROS accumulate in wheat as a result of drought stress, and antioxidant Drought/ Heat stress

Stomata closure

Production of ROS

Lower influx in CO2

Salinity

Reduced enzyme activities

Membrane disruption

Leaf senescence

Reduced Ci

Limited carboxylation

Ethylene production

Inhibits electronic transport Membrane disruption

Inhibition of photosynthesis

Ion toxicity

Inhibit leaf expansion

Leaf abscission

ROS production

Reduced RUE

Decreased growth and yield Root growth inhibition

ACC biosynthesis

Decrease in PS-II

Lower activity of enzymes

Hinder ATP synthesis Elevated photorespiration

Reduction in photosynthetic pigments

Decreased gs

Leaf growth reduction Reduced nutrient uptake

Nutrient deficiency/Toxicity

Hypoxia/ Anoxia

Waterloggin/ Soil flooding FIG. 2 Possible mechanisms by which drought, heat, salinity, and waterlogging stresses reduces photosynthesis in wheat crop.

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accumulations that can scavenge the free radicals reduce the ROS accumulation. In severe drought stress, however, the production of ROS outpaced the accumulation of antioxidants, resulting in a redox homeostasis imbalance (Sharma et al., 2012). ROS will begin to accumulate, eventually leading to plant death due to enzyme inhibition, membrane lipid peroxidation, RNA and DNA damage, and protein degradation (Ishikawa et al., 2010). Wheat plants can withstand and achieve tolerance capacity by producing superoxide dismutase (SOD), catalase (CAT), and peroxidase (POX), enzymes that scavenge reactive oxygen species (ROS), and thus overcome drought (Chen et al., 2012). The concentration of cellular materials, particularly the nonprotoplasmic component, and the viscosity of cellular contents are increased, resulting in an increase in cell toxicity, which is extremely harmful to enzymes when compared to wheat cells. The decreased water flux from the xylem to the parenchyma cell inhibits cell elongation and reduces turgor. Under drought conditions, reduced metabolic activity, particularly photosynthesis in wheat, has been linked to reduced ATP synthesis. Drought affects the membrane permeability of chloroplasts, and as a result, wheat photosynthesis and rubisco activity showed a wide range of responses, either remaining stable or declining. Similarly, Neslihan-Ozturk et al. (2002) found that under drought conditions, proteins involved in photosynthesis were significantly downregulated. Antioxidant content, particularly tocopherol, increased when water was scarce and CO2 was limited. Soluble protein, on the other hand, showed an increasing trend after the severe drought finished. The biochemical or metabolic components that limit photosynthesis in the absence of water are less well understood than diffusion constraints. Drought has been linked to reduced ATP synthesis due to a decrease in electron transport rate (Flexas et al., 1999; Galm
es et al., 2007). The stomatal closure and reduced mesophyll conductance reduce diffusion of CO2 to the site of carboxylation which contributes to a depressed Pn under drought stress conditions (Ashraf and Harris, 2013). The decreases in Pn under water deficit may be due to the closure of stomata caused by osmotic stress or else by the damage of photosynthetic apparatus and other metabolic processes caused by drought. Drought tolerance in Iranian wheat was studied by Farshadfar et al. (2012) who discovered that cell membrane stability, relative water potential, and relative water content have a greater impact on osmotic adjustment.

Heat stress Photosynthesis is the most temperature-sensitive physiological process, and any reduction in photosynthesis affects wheat growth and grain yield (Al-Khatib and Paulsen, 1984). The activity of photosystem II (PSII) can be completely inhibited by heat, and this can lead to a reduction in photosynthesis. Reduced photosynthesis in wheat under heat stress is caused by disruptions in the structure and activity of chloroplasts, as well as a reduction in chlorophyll content and inactivation of chloroplast enzymes (Farooq et al., 2014). Heat stress accelerates leaf senescence in wheat by lowering photosynthetic pigment levels and decreasing photosynthetic activity. Chloroplasts, nuclei, and mitochondria are all affected. As a result of these changes, Rubisco’s functions change. Ribulose-1,5-biphosphate (RuBP) activity decreases photosynthetic CO2 assimilation capacity. PSII is downregulated in response to heat stress due to the closure of the PSII action center and advanced inhibition of electron transport. Heat stress initially causes the thylakoid membrane to breakdown, allowing electrolytes to leak out and disruption of photochemical reactions like photosystem II (PS II) resulting in a drastic reduction in photosynthesis rate. The rapid decline in rubisco activity is the primary cause of Pn decline after short-term waterlogging rather than a decrease in PSII function. Photosystem II plays a key role in photosynthetic responses to high temperatures. Photosystem II is more sensitive to heat than photosystem I (Sharkova, 2001). High temperatures in wheat cause significant damage to various PS II sites. Being a cool season crop, PS II of wheat is more sensitive to high temperature stress than warm-season crops like rice and pearl millet. High temperature stress also causes cessation of photophosphorylation due to thylakoid membrane damage. Cultivar differences, on the other hand, affect photosynthetic efficiency (Feng et al., 2014). The formation of reactive oxygen species as a result of membrane and protein damage results in heat-induced oxidative stress. Heat can also trigger preprogrammed cell death. Overall, these damages may impair photosynthetic rate, impede assimilate translocation, and reduce carbon gain, all of which can lead to distorted growth and abnormal reproduction (Vacca et al., 2004; Larkindale and Knight, 2002).

Salinity stress Drought and salinity both have varying degrees of physiological water-deficit symptoms. In addition to dehydration, prolonged salt stressed, plants showed hyperionic and hyperosmotic stresses. Salt stress results in an accumulation of Na+ and Cl ions in the chloroplast, as well as a decrease in plant water potential, which reduces photosynthesis. Photosynthetic characteristics such as transpiration rate (TR), leaf water potential (LWP), and photosynthetic pigments are all altered in plants exposed to salinity. However, stomata limitation disrupts photosynthesis regulation, lowering TR and LWP (Azeem

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et al., 2017). Stomatal closure is caused by salt stress, resulting in less CO2 absorption and a slower rate of transpiration (Guo et al., 2015; Flexas et al., 2004). Chlorosis is a common symptom of salinity stress in plants, which causes photosynthesis to be inhibited ( Jha and Subramanian, 2016). Salinity has an effect on photosynthetic pigments in the chloroplast. As a result, the photosynthetic efficiency of the plant is reduced, resulting in a significant decrease in plant growth in wheat. It is possible that the reduced growth is due to the negative effect of salt on photosynthetic rate and growth-promoting enzyme activities. Increased Na+ ions cause stomata to close quickly, preventing leaf expansion. However, excessive Na+ ion accumulation can lead to premature leaf senescence and reduced grain yield (Negrao et al., 2017; Qados, 2011). Photosynthetic pigments, particularly chlorophyll, are well-known for allowing plants to absorb energy from light and for being an important determinant of photosynthetic capacity. The cause of decreasing chlorophyll content could be accumulation of a large quantity of Na+ in the leaf tissues, resulting in a change in chlorophyll pigments and/or a restriction in its biosynthesis (Yadav et al., 2020). The increased H2O2 content, which causes extensive cell death in plants, is responsible for the reduced chlorophyll content (Nxele et al., 2017). Wheat genotypes that maintained higher chlorophyll content performed better under salt stress conditions in terms of photosynthesis (Soni et al., 2021). The metabolic activity, particularly photosynthesis in mesophyll tissue, is reduced due to altered enzymatic activity, ionic imbalance, and membrane disruption. The high K+, low Na+, and the resulting high K+: Na+ in the cytoplasm of wheat mesophyll cells maintained photosynthetic capacity. The decreased fluorescence parameter Fv/Fm resulted in declining chlorophyll content in wheat under salt stress conditions. The most important physiological mechanisms of salt tolerance in wheat are the exclusion of Na+ and Cl from the transpiration stream and the sequestration of Na+ and Cl ions in vacuoles of mesophyll tissue (Munns et al., 2006). The photosynthetic machinery is affected by salinity-induced excess Na+ in the cytosol and stomatal closure, resulting in the formation of reactive oxygen species (ROS) in plant green tissues (Shabala and Munns, 2012). Salt stress affects the state between ROS and antioxidant species, resulting in ROS accumulation and oxidative stress in wheat. Under salinity stress, an excess of ROS damages membrane lipids, proteins, and nucleic acids (AbdElgawad et al., 2016). Furthermore, salinity stress can cause ion toxicity, which can lead to reduced leaf growth and abscission, limiting carboxylation and resulting in reduced photosynthesis (Seleiman et al., 2022). Salt has different effects on different species. Some plants can inhibit salt from entering the cytoplasm or minimize its accumulation in the cytoplasm, avoiding toxic effects on photosynthesis and other key metabolic processes. Many enzymes, including photosynthetic ones, are severely inhibited by Na+ at concentrations above 100 mM when those processes do not exist or are insufficient (Munns et al., 2006).

Waterlogging stress Waterlogging occurs when the soil becomes saturated with water, restricting the normal supply of air in the soil, causing oxygen levels to drop and carbon dioxide and ethylene levels to rise. Other gases that accumulate in the root zone, such as carbon dioxide and ethylene, have an effect on the plants. As a result, when O2-deficient tissues switch from aerobic respiration to low-ATP-yielding fermentation, they experience an energy crisis, which inhibits root growth and function in transporting nutrients and water to the shoot, and some roots eventually die. Waterlogging reduces root hydraulic conductivity, which leads to decreased leaf turgor and stomatal conductance, as well as CO2 deficiency in the leaves (Aroca et al., 2012; Vandeleur et al., 2005). Because stomatal limitations in net photosynthesis reduce carbon assimilation, plant biomass production may be reduced. A reduction in photosynthetic activity has been linked to the closure of stomata, a decrease in leaf chlorophyll content, and disruption of photosynthetic translocation. Waterlogging adversely affects photosynthesis of wheat plant by reducing chlorophyll content, lowering Fv/Fm ratio, thus have a negative effects on effective quantum yield of photosystem II (PSII) and photochemical quenching (Wu et al., 2015). Waterlogging reduces net photosynthesis in wheat, but the degree of suppression varies depending on the length of the waterlogging period. Pn decreases at the start of waterlogging due to stomata closure, which limits intercellular CO2 concentration (Ci). Pn is also affected by a decrease in carbohydrate accumulation. Long-term waterlogging also lowers Pn due to nitrogen deficiency. Wheat shows a wide range of short- and long-term photosynthetic responses to soil waterlogging. The initial decline in Pn during the early stages of waterlogging could be due to stomatal closure and limiting Ci. Sugars accumulate in plant components when wheat is waterlogged, indicating that Pn reductions during short-term waterlogging are unlikely to be the cause of wheat shoot growth reductions because tissue sugars remain high. For long-term waterlogging, Herzog et al. (2016) found a comparatively weak correlation between Pn and stomatal conductance (gs), indicating that gs is not the limiting factor of reduced Pn. In most cases, decreases in Pn in waterlogged soil are not due to a decrease in Ci. As a result, decreases in gs were most likely a response to increased Ci. Reduced Pn could be caused by factors such as decreased chlorophyll or other components of the photosynthetic apparatus as a result of N deficiency and/or negative feedback from carbohydrate accumulation during long-term waterlogging, though in some cases, possible damage to leaves from ROS or phytotoxins (Fe2+ or Mn2+) could also play a role.

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Approaches for the improvement of photosynthesis in wheat under abiotic stresses Wheat plants are extremely sensitive to various biotic and abiotic stresses, with abiotic stress causing drastic reductions in growth, development, and yield. The harshness of photosynthesis caused by abiotic stress can be alleviated in two ways: first, by removing abiotic stress, and second, by manipulating the environment. Plants show certain changes in their growth and physiological processes to combat the negative effects of abiotic stress. The photosynthetic activities of wheat are significantly improved by the exogenous application of various chemicals, including phytohormone.

Improvement of photosynthesis under drought stress Drought is a devastating abiotic stress that damages the mesophyll cell and reduces plant photosynthesis, resulting in a reduction in plant growth and yield (Rizwan et al., 2015; Fahad et al., 2017). Its management practices, such as irrigation, mulching, and the use of various chemicals could help to mitigate the negative effects of the drought. Artificial hormones, also known as plant growth regulators (PGR), are effective chemicals for reducing drought stress and increasing photosynthetic activity in wheat. Plant growth regulators are biochemical substances that are produced in small amounts inside plants and perform specific physiological functions. They have the ability to control the growth and development of plants. Plant hormones influence cell division, gene expression, and transcription levels, as well as acting as biochemical messengers for various metabolic activities in crop plants. They also play an important role in responding to biotic and abiotic stresses. Phytohormones have a wide range of applications in different crop plants, particularly wheat. Despite crop enhancement, abiotic stress mitigation has also been documented. The negative effects of abiotic stress can be mitigated by using a variety of growth regulators (Khan et al., 2013; Masood et al., 2012). Under normal and stressful conditions, phytohormones play an important role in photosynthesis in flowering plants (M€uller and Munn
e-Bosch, 2021). Growthstimulating phytohormones, such as auxin, gibberellin, cytokinin, and strigolactones, and growth-retarding phytohormones, such as ethylene, abscisic acid, jasmonic acid, and brassinosteroids, are the most common. Other hormones, such as salicylic acid, play an important role in scavenging ROS produced during photosynthesis. Gibberellic acid (GA) is a growth-stimulating hormone that promotes cell elongation and division (Colebrook et al., 2014). The activity of rubisco has been reported to be stimulated by GAs (Nath and Mishra, 1990; Yuan and Xu, 2001). The use of exogenous GA in wheat increased photosynthetic activity while lowering ROS. Wheat photosynthetic activity is improved by cytokinin, which plays an important role in stress mitigation. It is a crucial plant juvenile hormone that affects plant growth and development. It was first discovered as a substance that increased cell division in the presence of auxin (Davies, 2010). This hormone has the potential to repair the damaged photosynthetic apparatus. It has been reported to play a key role in the synthesis, development, and function of chloroplasts, as well as controlling over 100 photosynthesis-related genes (Cortleven and Schm€ulling, 2015; Brenner and Schm€ulling, 2012). It influences the activation of photosynthesis proteins and genes at various levels of plant and cellular organization, promoting photosynthesis through the development of leaves and plastids. The use of cytokinin on wheat can help to stimulate and mitigate abiotic stress as well as improve crop plant photosynthetic activity. This hormone can slow down a variety of developmental processes, including senescence, which is linked to chlorophyll breakdown, photosynthetic apparatus disintegration, and oxidative damage (H€onig et al., 2018). According to various researchers, its concentration declines during the onset of senescence under abiotic stress conditions, and regreening of leaves can be achieved by exogenous application of cytokinin. External application of BAP increased the activity of CAT and APX enzymes and reduced the level of H2O2 during the dark senescence of wheat leaves under stress, especially in drought conditions. Furthermore, ROS damage to the cell membrane and photosynthesis system can be avoided (Mik et al., 2011; Zavaleta-Mancera et al., 2007).

Improvement of photosynthesis under heat stress Excessive ambient temperature negatively affects wheat plants, preventing growth and development and, ultimately, grain yield. Heat stress hampered the photosynthesis related physiological activities. Dry matter production and yield loss are carried out by photosynthetic activity at a lower level. Various approaches, such as management practices and exogenous application of various types of chemicals, can be used to prevent and mitigate the negative effects of wheat under heat stress. Antitranspirant application can reduce heat shock to a certain extent, and exogenous application of plant growth regulators (PGRs) can prevent harmful effects and improve physiological activities, particularly photosynthesis. Auxin

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is a type of PGR that includes several species, such as IAA (indole-3-acetic acid), IBA (indole-3-butyric acid), and IAA (indole-3-acetic acid), the most common of which is IAA. Plant physiologists have conducted extensive research on this hormone (Simon and Petra´sˇek, 2011). IBA is an auxin-like plant hormone that is found in many commercial horticultural plant rooting products (Ludwig-M€ uller, 2000). The synthetic plant hormones 1-naphthaleneacetic acid (NAA) and 2,4-dichlorophenoxyacetic acid (2,4-D) are also used in plant tissue culture. NAA is a rooting agent that is used to propagate plants vegetatively from stem and leaf cuttings (Naduvilpurakkal et al., 2014). Auxin is a crop-stimulating hormone that promotes apical dominance, shoot elongation, and root formation. It regulates cell elongation and vascular tissue development. It has been reported as a driver of plant development of various physiological processes (Teale et al., 2006; Zhao, 2010), and it plays an important role in the development of chloroplast (Salazar-Iribe and De-la-Pen˜a, 2020). It can indirectly influence photosynthesis by controlling leaf stomata formation and leaf venation. Elanchezhian and Panwar (2008) found that inoculating wheat with plant growth-promoting rhizobacteria, an auxin-synthesizing biofertilizer, increased photosynthetic activity, chlorophyll content, and grain yield. Auxins have been identified as a key regulator of root and shoot architecture, root and shoot meristem maintenance, apical dominance establishment, lateral and adventitious root formation, leaf morphogenesis, flowering, and senescence in wheat (Went and Thimann, 1937; Aloni et al., 2003; Okushima et al., 2005). Ribba et al. (2020) found that exogenous application of auxin in wheat under salt stress reduced stress and increased photosynthetic capacity.

Improvement photosynthesis under salinity stress The use of GA improves wheat seed germination and reduces abiotic stresses, particularly salinity. GA is well known for promoting plant growth and the production of secondary metabolites. Exogenous application of GA increased plant growth and alleviated abiotic stresses. According to Arabshahi et al. (2017), gibberellin increased plant height, grain size, and harvest index in wheat under drought conditions. Proline is an important amino acid that accumulates to high concentrations in plant cells and improves stress tolerance. Although the precise effects on stress tolerance are not fully understood, different functions may interact or act in parallel. Because of the highly soluble zwitterionic molecule, this amino acid could help to limit water loss. Furthermore, its synthesis may improve plant stress tolerance by altering the NADP+/NADPH ratio in the cytosol, resulting in crosstalk with other stress-related pathways such as the oxidative pentose phosphate pathway (Esposito, 2016). Endogenous osmolytes accumulated and recovered stress in wheat under various abiotic stress conditions. Proline, when used as an exogenous compound in crops, can improve salt tolerance (Heuer, 2010). It was discovered that foliar application of proline increased maize growth and yield under salinity stress. Glycine betaine (GB) is one of the most important nitrogenous compound osmoprotectants compatible osmolyte that can be found in a variety of crop plants. In addition to being a well-matched solute, it protects cell structures from stresses and stabilizes the quaternary structures of complex proteins (Demiral and T€urkan, 2004; Yang et al., 2007). It protects plants from osmotic stress and is found in abiotically stressed crop plants. Stress tolerance and hardening are both aided by the biosynthesis of GB via jasmonic acid signal transduction. It can be accumulated in plants to help them maintain osmotic homeostasis in the face of abiotic stresses like salinity, drought, heat, and cold (Kishitani et al., 1994). Under normal conditions, the wheat plant can only accumulate a small amount of GB, which is insufficient to successfully protect the photosynthetic apparatus under stress. The lipid composition of the thylakoid structure can be stabilized by GB, which may be involved in the protection of the thylakoid structure, thereby protecting the plant from stress injury. The application of GB under drought conditions resulted in increased antioxidant enzyme activities and a reduction in MDA and H2O2 accumulation (Ahmed et al., 2019). Because of overexcitation of photosystem II and electron leakage under abiotic stress, the synthesis of stress hormones such as salicylic acid and abscisic acid takes precedence over the biosynthesis of GB.

Improvement photosynthesis under waterlogging stress Waterlogging is an anoxic condition that causes the plant to die due to a lack of oxygen. The wheat plant is extremely sensitive to waterlogging, which reduces the plant’s photosynthetic capacity. Wheat photosynthetic activity under waterlogging can be improved by manipulating the environment and using various chemicals. The use of phytohormones can help to prevent or even repair chloroplast damage caused by waterlogging. Overexpressing transcription factors in the cytokinin (CK) signaling network, which affect chloroplast volume, has recently been used to make a significant technological breakthrough in the photosynthesis system by incorporating the C4 pathway into C3 plants (Ermakova et al., 2020).

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Abiotic stresses in wheat

The interaction between light and phytohormones influences the development of chloroplasts in flowering plants, particularly organelle size modulation, such as the organization of the thylakoid membrane, pigment accumulation, organelle division, and chloroplast genome (Stern et al., 2004). Several phytohormones are synthesized in part in chloroplasts and play an important role in photosynthesis, either directly or indirectly. Phytohormones such as ABA have a significant impact on stomatal development and regulation (Chater et al., 2014); auxin has a significant impact on chloroplast development (Salazar-Iribe and De-la-Pen˜a, 2020); cytokinin and ethylene have a significant impact on leaf senescence and photosynthesis (Cortleven and Schm€ ulling, 2015; Ceusters and Van de Poel, 2018). Other hormones each play a role in protecting photosystem II (PSII) from damage (Gururani et al., 2015). Similarly, salicylic acid and brassinosteroids played a role in overall photosynthesis ( Janda et al., 2014; Siddiqui et al., 2018). Brassinosteroid is a hormone that regulates cell division and elongation to control plant growth and development. It also helps with photomorphogenesis, senescence, and responses to biotic and abiotic stresses (Chen et al., 2017).

Concluding remarks and future prospects Abiotic stresses are increasing due to global climate changes that are posing serious threats to global food and nutritional security. Among the abiotic stresses, drought, heat, salinity, and waterlogging are major limiting factors for growth and development of plants, including wheat. Importantly, these abiotic stresses impact on photosynthesis and other physiological and biochemical processes of wheat and ultimately reduce the yield. Although a large body of literature is reviewed in this chapter, understanding of the underlying molecular mechanisms of the impact of abiotic stressors on photosynthesis is not fully understood, which is essential for improvement of wheat to be tolerant to the stressful environment. Wheat is a hexaploid plant that has a very complex and large genome (17 Gbp). However, the whole genome of wheat is recently being sequenced, which offers an opportunity for elucidating the molecular mechanism of the detrimental effects of abiotic stresses on the photosynthetic machineries of wheat and also for identifying the genes involved in abiotic stress tolerance. Although genetic engineers have abandoned wheat due to genomic complexity, recently developed CRISPR-Cas technology opens a new opportunity for the improvement of abiotic stress tolerance in wheat by genome editing.

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Chapter 12

CRISPR-Cas genome editing for the development of abiotic stress-tolerant wheat Nadia Afroz, Most. Waheda Rahman Ansary, and Tofazzal Islam⁎ Institute of Biotechnology and Genetic Engineering (IBGE), Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh *

Corresponding author. e-mail: [email protected]

Introduction Economic downturn due to COVID-19 pandemic coupled with the global climate change is the biggest challenge to achieve the Sustainable Development Goals (SDGs), which have an ultimate objective of ending hunger by the year 2030. The everincreasing population, limited land and water resources, presence of variety of stresses, and the inadequate supply of domestic food systems are the key variables impacting food security. World Food Program (www.wfp.org) reported that more than 135 million people suffer from acute hunger, and this figure is anticipated to increase 840 million by 2030. To eradicate poverty, we must expand food production in a sustainable manner while also ensuring that food is distributed evenly. Simultaneously, all stakeholders and researchers should work together through open science and open data sharing policy to create a strict program that improves the absorption of agricultural and food security research into policy and practice. Wheat (Triticum aestivum L.) is one of the world’s most widely cultivated cereal grains. It is nutritious, and regarded as the primary source of food for billions worldwide, making a considerable contribution to global trade (42.5%) and cereal production (28%) (Prospects, 2020). Wheat belongs to the family Gramineae and mostly grown for its seeds. It supplies >25% protein and 20% calories to human (FAO, 2015) and is a good source of dietary fibers and other nutrients (Kayim et al., 2022). It is very important to increase wheat production by >60% to fulfill the demand for the growing population of 9.8 million in the world predicted for 2050 (Langridge, 2013; Akter and Islam, 2017; Yadav et al., 2020). Despite having the highest total harvested area (38.8%), wheat has the lowest total productivity among cereals, including rice and maize (Abhinandan et al., 2018). Unfortunately, wheat production was insufficient to fulfill future demand over the last few decades (Borisjuk et al., 2019). Different types of biotic and abiotic stresses are responsible for the major production losses in wheat, hampering physiological and biochemical activities in the cell which ultimately reduce agricultural yields (Porter and Semenov, 2005; Islam et al., 2016, 2019, 2020b; Hossain et al., 2021). Therefore, increased productivity and long-term sustainability of wheat are greatly threatened by various abiotic stresses including salinity, heat, drought, and cold stresses (Mohi-Ud-Din et al., 2022). Salinity is the key abiotic stress negatively affect wheat quality and yield. It has an impact on all stages of plant growth and development, such as, germination, vegetative and reproductive growth of wheat plant (Foolad, 2004). Yieldcontributing parameters of wheat such as, weight of grain, length of spike, spikelet number, and total yield of grain reduce significantly due the salinity stress (Tiwari et al., 2017; Loutfy et al., 2020). Drought also severely affect the productivity of wheat (Fathi and Tari, 2016). It damages crops at all phases of wheat growth and development. Drought during the early stages of wheat growth causes poor seedling stand and a lower number of tillers per square meter of land. In addition, drought in the mid-growth stages results in lower dry matter output, effective tillers, and grains per plant (Gull et al., 2019). Drought has a deadly impact on wheat during the grain development stage, since it affects productivity, grain weight, and assimilate production (Tiwari et al., 2014). High temperature or heat stress is another major environmental factor that frequently occurs as a result of climate change that reduce plant growth and productivity (Mohi-Ud-Din et al., 2021). Grain development and filling (Rane et al., 2007), grain yield per spike (Wardlaw et al., 1989), and yield loss (Tiwari et al., 2017) of wheat are all negatively Abiotic Stresses in Wheat. https://doi.org/10.1016/B978-0-323-95368-9.00014-X Copyright © 2023 Elsevier Inc. All rights reserved.

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affect by temperature increases over the threshold level. Similarly, cold stress or low-temperature stress adversely affects several aspects of wheat plants namely, photosynthesis, water transport, growth, cell division, and ultimately crop yield (Li et al., 2015). One of the most limiting elements for wheat development and production is cold temperature (0–15°C), which has a substantial impact on the early growth of winter wheat (Ruelland et al., 2009). Germination reduces drastically at temperature below 8–10-degree centigrade (Zabihi-e-Mahmoodabad et al., 2011). Cold stress inhibits the activity of Calvin Benson cycle and creates an imbalance between light absorption and light use, also caused the oxidative stress (Hu et al., 2008). To achieve the production goal by 2050 without expanding the amount of available farmed land, the focus must be given on the improvement of plant productivity and adaptability to major environmental stressors through molecular-based breeding and genetic engineering approaches. A shortage of this vital staple crop might represent a serious danger to global food security in the near future (Nazir et al., 2022). It is now time demanding to design wheat cultivars that are resistant or tolerable to their respective abiotic constraints in order to reduce yield loss. In many plant species, transformation protocols aren’t optimized, and desired cultivars may be recalcitrant to genetic transformation, forcing the use of inferior cultivars and time-consuming backcrossing to the chosen variety. The development of abiotic stress tolerant wheat crop will be substantially aided if these constraints are overcome. To attain zero hunger, new technologies are needed, and CRISPR-Cas9-based gene editing being the most promising, and attractive technology to induce specific advantageous mutations is one such route for quick crop improvement (Haque et al., 2018; Islam, 2019; Molla et al., 2020; Abdallah et al., 2021). Many researchers have claimed the successful application of CRISPR-Cas technology in a variety of plant species, including wheat (Zhang et al., 2016a; Liang et al., 2017; Haque et al., 2018; Kim et al., 2018; Arndell et al., 2019; Paixa˜o et al., 2019; Alfatih et al., 2020; Liu et al., 2020). It ensures anticipated particular control of gene mutation that’s why modern plant biologists prefer it. But it is challenging because of the limited knowledge of the molecular basis of stress tolerance in plants precisely. Diversified researches are essential for the widespread use of this technology to improve environmental stress-tolerance ability in major crops. Due to hexaploidy, gene editing using CRISPR technology of wheat seems complicated compared to the diploid species of the members of Graminae. However, there are a good number of reports on successful application of CRISPR-Cas technology in wheat (Bhowmik et al., 2019). This book chapter reviews and updates our knowledge of the applications of CRISPR-Cas technology for improving abiotic stress-tolerance in wheat to elevate their capability to deal with hostile environmental conditions. The challenges and opportunities of using CRISPR-Cas technology to develop climate-resilient wheat variety development are also discussed.

CRISPR-Cas system and its uses in improving abiotic stress-tolerance in plants Breaking of DNA double-strand by the discovery of programmable nucleases has developed molecular biology since it allowed for precise genome editing. Zinc finger nucleases (ZFNs), the first genome editing tool, was an innovation in genome engineering used in programmable nucleases. After that, bacterial TALEs-based tool transcription activator-like effector nucleases (TALENS) further increased the ability of genome editing. For genome modification, these methods were quickly adopted to around 40 different species (Chandrasegaran and Carroll, 2016). Nevertheless, the discovery of “Clustered Regularly Interspaced Short Palindromic Repeat [(CRISPR)/CRISPR-associated protein, the Cas]” achieved tremendous attention of researchers all over the world as it is easier to handle over ZFNs and TALENs ( Jinek et al., 2012; Mao et al., 2013). Protein motifs are utilized by ZFNs and TALENs to target identification that are cumbersome. But, CRISPR-Cas relies on RNA-DNA recognition to generate the double-strand break (Haque et al., 2018; Islam, 2019). Various kinds of genome modification using CRISPR-Cas9 technology have been depicted and elaborately discussed by Islam (2019) and Islam and Molla (2021). The principle of genome editing in plants by CRISPR-Cas method is illustrated in Fig. 1 (Islam, 2019). CRISPR-Cas method is advantageous over TALENs and ZFNs because of the (i) ease of multiplexing, (ii) simplicity of the target design and inducing targeted mutations in multiple genes in a single event, and (iii) effectiveness of introducing mutations by injecting the RNAs encoding Cas protein and gRNA directly (Ma et al., 2015; Malzahn et al., 2017; Molla et al., 2021). As designing of CRISPR-Cas9 vector is relatively less tricky, it is efficient, rapid, easier, and flexible compared to the former techniques such as TALENs and ZFNs. This is due to the easy accessibility of the upgraded bioinformatics tools that could be applied to design the guide RNAs by identifying the most suitable sequences. Further screening libraries are not necessary in order to choose the most effective target. Recently, the CRISPR/Cas toolbox has been improved and modified remarkably. It enabled researchers to modify any organism precisely using “nucleotide-level” precision in an extremely swift manner. The protocols of CRISPR technology for genetic modification of plants are the fast evolving area of research (Islam and Molla, 2021). These advancements have significantly aided in the broadening of the adaptability of this method in eukaryotes (Molla et al., 2021).

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FIG. 1 Variety of genome modification and editing by CRISPR-Cas systems (adapted and redrawn from Chen et al., 2019 and Islam, 2019). (A) Editing plant genome by two CRISPR-Cas9 systems: Cas9 and Cpf1; (B) Probable outcomes depending on the double strand break repair pathways by genome editing using CRISPR-Cas9 systems: (1), (2), and (3) are outcomes of the dominant NHEJ repair pathways; (4) and (5) are results of the HDR pathway using a donor template DNA (available). Abbreviations: crRNA, CRISPR RNA; DSB, double-strand break; dsDNA, double-strand DNA; HDR, homology-directed repair; NHEJ, nonhomologous end joining; PAM protospacer-adjacent motif; sgRNA, single guide RNA; ssODN, single-strand oligodeoxynucleotide; TET, ten-eleven translocation; HNH, an endonuclease domain named for characteristic histidine and asparagine residues; RuvC, an endonuclease domain named for an E. coli protein involved in DNA repair. (The figure is reproduced by the permission of CABI (Islam, 2019)).

The efficient and powerful genome engineering technique, CRISPR-Cas system has already been used successfully in various kinds of organisms including animals, plants, and bacteria (Sander and Joung, 2014). To improve different crops, it can be used by targeting the traits of interest as it is efficient and precise gene-editing tools. Osakabe and Osakabe (2017) reported the utilization of CRISPR/Cas9 framework in several model plants like Oryza, Arabidopsis, and Nicotiana, and in some other crop plants like potato, maize, wheat, tomato, soybean, and sorghum. For instance, CRISPR/Cas9 genome editing tool was applied through multiplex genome editing to increase the content of lycopene (Li et al., 2018), through targeted genetic substitution and mutagenesis in tomato to improve storage period (Yu et al., 2017), and through modifying miR482b and miR482c simultaneously for raising up resistance to Phytophthora infestans (Hong et al., 2020). Moreover, CRISPR/Cas9 modifying technique was applied effectively in soybean to change plant height, internode length and architecture as well as to modify the time of flowering (Bao et al., 2019; Cheng et al., 2019; Li et al., 2020b). After genetic edition using CRISPR/Cas9 tool, phenotypic appearance of several traits linked to biotic stress response has shown promise in many plants (Mushtaq et al., 2018). Furthermore, many researchers are interested now to apply CRISPR/Cas9 for elevating environmental stress-tolerance in plants. Multiple genes of plants are responsible for the abiotic stress responses regarding metabolism, signaling, and regulatory pathways. Either single or multiple genes can be focused on via CRISPR/Cas9 system to rise the stress adaptation capacity of plants. Through CRISPR/Cas9 system, insertions or deletions, point mutations, transcriptional regulation, or forward genetic screens can be produced for the target-based genome editing ( Jain, 2015). According to Osakabe and Osakabe (2017), there are several crucial things in CRISPR/Cas9 gene-editing systems that need to be considered for the development of abiotic stress resistance in plants. They are suitable for gRNA designing, selection of appropriate promoter for Cas9 expression, generation of the new alleles, and development of appropriate gene delivery system for abiotic stress responsive genes (Osakabe and Osakabe, 2017). ABRE1/ABF2 (abscisic acid responsive element binding protein 1/ABRE binding factor 2) is a key regulator of drought stress response. That’s why, a genetic trait ABRE1 was exploited in Arabidopsis by Paixa˜o et al. (2019) for improving drought stress tolerance. The endogenous ABRE1 promoter was activated using CRISPR/Cas9 genome editing tool. HAT, or histone acetyltransferase, generally correlated with gene expression was used to link catalytically inactive

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Cas9 (dCas9). Paixa˜o et al. (2019) reported enhanced tolerance against drought stress in Arabidopsis thaliana applying CRISPR/dCas9HAT due to the positive regulation of ABRE1. In 2020, Alfatih and colleagues have generated increased resistance to oxidative and salt stresses in rice through PARAQUAT TOLERANCE 3 knockout mutants (OsPQT3) using CRISPR/Cas9 toolkit (Alfatih et al., 2020). Besides, Osakabe et al. (2016) used CRISPR/Cas9 (truncated guide RNA for site-specific modification without off-target effects) to introduce new alleles of OST2 (a gene involved in stomatal movement) into Arabidopsis for improved drought stress tolerance by means of co-expression of GFP and Cas9. Moreover, stomatal response during drought stress was improved in Arabidopsis by targeting OST2/AHA1 gene and the tissue-specific promoter, AtEF1 (Osakabe and Osakabe, 2017). In a study, grain yield of maize was enhanced under drought stress by inducing ARGOS8 variations using CRISPR/Cas9 (Shi et al., 2017). Miao et al. (2018) reported extensive heat stress tolerance by knocking-out PYL1/4/6 genes (subfamilies of abscisic acid receptor genes) by CRISPR/Cas9 in rice. All the above-mentioned studies indicated that the efficacy of CRISPR-Cas9 technology to establish drought-resistance crops probably linked with the production of novel allelic variations. With the application of CRISPR/Cas9 technology, several studies have done by the researchers to mitigate mineral toxicity and significant outcomes are reported. Nieves-Cordones et al. (2017) used CRISPR/Cas9 system and became successful to develop rice plant containing lower cesium by inactivating the K+ transporter gene OsHAK1. Wang et al. (2017a) stated that arsenic tolerance rice plant can be developed using CRISPR/Cas9 system through knocking out OsARM1 gene. CRISPR/Cas9 generated the metal transporter gene OsNramp5 knockout mutant rice plant showed accumulation of low cadmium (Tang et al., 2017). Svitashev et al. (2015) targeted ALS1 and 2 gene through CRISPR/Cas9 method to develop herbicide-resistance in maize plant. Similarly, herbicide-resistant rice (Sun et al., 2016) and watermelon (Tian et al., 2018) can be developed using CRISPR-Cas9 by targeting homologous recombination of ALS gene. Protein level, desirable codon-optimization, promoter, and vector construction affect the efficiencies of genome editing using CRISPR-Cas9 ( Johnson et al., 2015; Li et al., 2015; Ma et al., 2015; Xu et al., 2015; Zhang et al., 2016a, 2016b).

Current status of abiotic stress-tolerant wheat by CRISPR-Cas genome editing It is crucial to increase the total production of agricultural crops significantly to feed the increasing global population. But, plant vulnerability to various abiotic stressors is a key concern in reaching this aim (Dhankher and Foyer, 2018). Earlier, many researchers developed many abiotic stress-resistant crop plants applying conventional marker-assisted breeding. However, there is a significant disadvantage to this strategy. Approximately a decade is needed to successfully develop abiotic stress-tolerant variety by this approach because of intensive screening and backcrossing procedures (Hoang et al., 2016). Commercialization of stress-resistant varieties generated by genetic engineering is hampered by a variety of obstacles although they have demonstrated good results. Since genome editing offers specific modification of gene locus in relatively shorter period, it seems to be a smart way for developing abiotic stress-resistant crops in the upcoming days. Thus, it decreases the cost of crop improvement programs (Schaart et al., 2016). Genome editing has been used successfully by many researchers all over the world for improving various growth contributing characters including plant nutritional value and yield (Sedeek et al., 2019). On the contrary, there are only a few studies where CRISPR-Cas method has been used to develop abiotic stress-tolerant crops. However, not only to developed abiotic stress-resistant varieties, CRISPR-Cas technology can be widely utilized to understand the signaling cascades in developing adaptation under abiotic stress condition ( Jain, 2015). This revolutionary technology has successfully been used to edit the genome of wheat plant (Table 1). Examples of some advances of the utilization of CRISPR-Cas9 technology for developing abiotic stress-resistant varieties of wheat are summarized in Table 2. Literature survey revealed that application of CRISPR technology in abiotic stress tolerance in wheat is limited to a few cases. As the protocols are optimized in hexaploid wheat, future progress in editing other wheat genes is high. Recently, multiplexed gRNAs enabled effective targeted gene editing of the Sal1 gene family in hexaploid wheat has been reported (Mohr et al., 2022). These Sal1 mutant wheat plants will be a resource for further research studying the function of this gene family in wheat for the enhancement of abiotic stress tolerance. Drought stress: Physiological, biochemical, and morphological attributes of plant affected crucially during drought stress (Salehi-Lisar and Bakhshayeshan-Agdam, 2016). It is expected to rise the effect of this stress in the near future due to global climate change (Nelson et al., 2009). Successful application of genome editing for developing several drought-tolerant crops has been reported. Precise modification of OPEN STOMATA 2 (OST2) gene responsible for stomatal closing via CRISPR/Cas9 to confer drought stress-tolerant plants. The gene is involved in creating proton gradients and encodes H + for an ATPase in plant cells (Osakabe et al., 2016). The manipulation of important genes linked with abiotic stress in wheat namely, ethylene responsive factor 3 (TaERF3) and dehydration responsive element binding protein 2 (TaDREB2), has been manipulated in wheat protoplasts by Kim and colleagues via CRISPR-Cas9 genome editing tool. Approximately 70% of protoplasts were transfected effectively and T7

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TABLE 1 Some examples of the applications of CRISPR-Cas method in gene editing of wheat.

Target gene

Trait/gene function

sgRNA promoter

Transformation method

References

TaMLO

Repress resistance pathway to powdery mildew

TaU6

Protoplast

Shan et al. (2013)

PDS, INOX

Phytoene desaturase (pds) and inositol Oxygenase (inox)

CaMV35S

Agrobacterium tumefaciens (GV3101)

Upadhyay et al. (2013)

TaLOX2

Lipoxygenase 2, chloroplastic precursor

TaU6

Protoplast

Shan et al. (2014)

TaMLO-A1

Blumeria graminis f. sp. tritici; repress resistance pathway to powdery mildew

TaU6

Protoplast

Wang et al. (2014)

TaGASR7

Control grain length and weight

TaU6

Particle bombardment (PB)

Zhang et al. (2016b)

TaDEP1

Inflorescence architecture and affects panicle growth and grain yield

TaU6

PB

Zhang et al. (2016b)

TaNAC2

Regulate shoot branching

TaU6

PB

Zhang et al. (2016b)

TaPIN1

Auxin-dependent emergence of adventitious root and tillering

TaU6

PB

Zhang et al. (2016b)

TaLOX2

Development of grain and storability of wheat

TaU6

PB

Zhang et al. (2016b)

TaGW2

In bread wheat, act as a negative regulator of kernel width and weight

TaU6

PB

Zhang et al. (2016b)

TaPinB

Seed softness

CRISPR/Cas9 ribonucleoprotein complexes

PB

Brandt et al. (2017)

TaABCC6

ABC transporter (ABCC6) related with FHB (Fusarium head blight) vulnerability

TaU6

Protoplast

Cui (2017)

TaNFXL1

Nuclear transcription factor X boxbinding- Like 1 (NFXL1), linked with FHB susceptibility

TaU6

Protoplast

Cui (2017)

TansLTP9.4

TansLTP9.4, a nonspecific lipid transfer protein (nsLTP), associated with FHB resistance

TaU6

Protoplast

Cui (2017)

TaDREB2

Drought tolerance

TaU6

Protoplast

Kim et al. (2018)

TaERF3

Root elongation and development of root hair

TaU6

Protoplast

Kim et al. (2018)

TaGW2

Control size and weight of grain

CRISPR/Cas9 ribonucleoprotein complexes

PB

Liang et al. (2017)

TaGASR7

Known as gibberellin-regulated gene that regulate grain length

CRISPR/Cas9 ribonucleoprotein complexes

PB

Liang et al. (2017)

Alpha-gliadin gene

Gluten protein

TaU6

PB

Sa´nchez-Leo´n et al. (2018)

TaEDR1

Resistant against powdery mildew

TaU6

PB

Zhang et al. (2017) Continued

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TABLE 1 Some examples of the applications of CRISPR-Cas method in gene editing of wheat—cont’d

Target gene

Trait/gene function

sgRNA promoter

Transformation method

TaLox2 and TaUbiL1

Lox2; lipoxygenase 2 enzyme involved in the hydrolysis of polyunsaturated fatty acids including arachidonic acid, linoleic acid, and α-linolenic acid

TaU6

Electroporation

Bhowmik et al. (2018)

TaGW2

Adversely affect grain weight and size especially increased kernel width

TaU6

Protoplast transformation (PT)

Wang et al. (2018)

TaMLO

Knockout mutants, resistance to powdery mildew

TaU6

PT

Wang et al. (2018)

TaLpx-1

Encodes 9 lipoxygenase, silencing results in resistance to Fusarium graminearum

TaU6

PT

Wang et al. (2018)

TaMs45

Responsible for male fertility

TaU6

A. tumefaciens mediated transformation

Singh et al. (2018)

TaPDS

Complete loss or reduction of function results in a photobleaching phenotype

TaU6

A. tumefaciens mediated transformation

Howells et al. (2018)

TaPin a & b

Affect hardness of grain and contributes to anti-fungal properties

TaU6 & TaU3

A. tumefaciens mediated transformation

Zhang et al. (2018)

TaWAXY or GBSS

Important enzyme in amylase biosynthesis

TaU6 and TaU3

A. tumefaciens mediated transformation

Zhang et al. (2018)

TaDA1

Restrict the period of cell proliferation and negatively regulates the size of seed and organ

TaU6 and TaU3

A. tumefaciens mediated transformation

Zhang et al. (2018)

TaCKX2-1, TaGLW7, TaGW2, TaGW8

Wheat grain-regulatory genes

TaU6

A. tumefaciens mediated transformation

Zhang et al. (2019b)

TaMs1

Encodes a GPI, which is needed for pollen exine development

TaU6

A. tumefaciens mediated transformation

Okada et al. (2019)

TaALS, TaACCase

The absence of the gene increase tolerance to herbicide

TaU6

Biolistic transformation

Zhang et al. (2019a)

TaQsd1

Regulate seed dormancy

OsU6

A. tumefaciens (EHA101) Mediated transformation

Abe et al. (2019)

EPSPS

Important enzyme involved in the aromatic amino acid metabolism via the shikimate pathway

TaU6

PT

Arndell et al. (2019)

TaABCC6 & TaNFXL1

Fusarium head blight (FHB) susceptible

TaU6

PT

Cui et al. (2019)

TansLTP9.4

Resistance to FHB

TaU6

PT

Cui et al. (2019)

TaQsd1, TraesCS4A02G110300 (IWGSC 2018)

Regulate seed dormancy

TaU6

Biolistic transient expression and A. tumefaciens mediated transformation

Kamiya et al. (2020)

References

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TABLE 1 Some examples of the applications of CRISPR-Cas method in gene editing of wheat—cont’d Transformation method

Target gene

Trait/gene function

sgRNA promoter

TaLOX2

Encodes for lipoxygenase 2; regulates growth and development of grain

TaU6

Biolistic transient expression and A. tumefaciens mediated transformation

References Kamiya et al. (2020)

TaNP-A1, TaNP-B, TaNP-D1

Expression in the tapetum and necessary for male fertility

TaU6 and TaU3

Biolistic and protoplast mediated transformation

Li et al. (2020a)

TaWaxy & TaMTL

Pollen-specific phospholipase

OsU6a, TaU3, and TaU6

A. tumefaciens mediated transformation

Liu et al. (2020)

TaASN

Genes encode for asparagine synthetase enzyme essential for asparagine synthesis

Ubi-1

Biolistic transformation

Raffan et al. (2021)

TABLE 2 The significant advances in the application of CRISPR-Cas9 to increase the abiotic stress-resilience of wheat. Targeted gene

Role of the gene

Transformation method

Stress

References

TaDREB2 TaERF3

Dehydration responsive gene

Wheat protoplast

Drought

Kim et al. (2018)

ACCase

Fatty acid biosynthesis

Wheat protoplast

Herbicide

Zhang et al. (2019a)

endonuclease assay confirmed the expression of newly modified genes. Transgene integration and off target mutations are important concerns about the application of CMGE in crop plants (Kim et al., 2018). Zhang et al. (2017) illustrated an effective way of genome editing via the biolistic transfer of CRISPR-Cas9 ribonucleoproteins (RNPs) to avoid these. In one hand, CRISPR-Cas9 DNA expressed steadily after being combined with the host genome. On the other hand, transient expression and rapid degradation will be provided by the biolistic technique of transporting RNPs by which it extremely diminishes off-targets. Critical drought stress-responsive genes can be identified and characterized using CRISPR-Cas9 in wheat and that can be targeted to improve crop in future utilizing several existing genomics approaches. Herbicide stress: In agriculture, herbicides are usually utilized to control the unwanted growth of weed plants since they pose serious threat to the crop yield. However, the usage of excessive herbicides affects nontarget plants (Varshney et al., 2015). ALS gene catalyzes the biosynthetic pathway of amino acids including leucine, isoleucine, and valine (Chipman et al., 1998; Lee et al., 1988). Researchers have reported several herbicides, like the imidazolinones, sulfonylureas, triazolopyrimidines, sulfonylamino-carbonyl-triazolinones, and pyrimidinylthio (or oxy)-benzoates, which hinder the ALS activity in plant (Mazur et al., 1987; Zhou et al., 2007). In 2009, Townsend and other co-workers precisely modified this gene to made sulfonyl urea herbicides-resistant tobacco plants via the ZFN genome editing tool (Townsend et al., 2009). Later on, the ALS gene was edited in different crops like maize, soybean, watermelon, and potato by CRISPR-Cas9 and TALENs technologies (Butler et al., 2015; Sun et al., 2016; Tian et al., 2018; Zhang et al., 2019a, 2019b). An enzyme, 5-enolpyruvylshikimate-3-phosphate encoded by EPSPS gene, affects the biosynthetic pathway of essential aromatic amino acids (Kishore and Shah, 1988), which is extremely susceptible to commonly used herbicide, glyphosate (Sch€ onbrunn et al., 2001). Besides, changing the Acetyl-CoA carboxylase (ACCase) gene via genome editing tool has been reported as an effective way to develop herbicide-resistant plants (Dong et al., 2021). Although genome editing has addressed successfully the menace of herbicide stress, but resistance has been accomplished largely only for glyphosate herbicides and ALS- and ACCase-inhibiting. Thus, further researches against different classes of herbicides to develop herbicide-resistant plants are much warranted (Dong et al., 2021).

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Challenges and opportunities of CRISPR-Cas9 genome editing for mitigation of abiotic stresses in crop production A major challenge for genome editing using CRISPR-Cas9 technology for enhancing abiotic stress tolerance is the limited availability of potential candidate genes and relevant transformation and plant regeneration protocols (Haque et al., 2018). To address these limitations, the optimization of plant tissue culture methods as well as the discovery of new genes is important. Recently, the knowledge of the genetic mechanisms associated with tolerant ability against abiotic stress has immensely advanced to discover new genes (Mickelbart et al., 2015). The molecular dissection of signaling pathways and characterization of transcription factors linked with environmental stress responses in plants are getting popularity day by day (Licausi et al., 2013). Some heat shock transcription factors (HSFs) that could increase abiotic stress tolerance are discovered through the overexpression studies in rice, Arabidopsis, tomato, and tobacco (Grover et al., 2013). The functional properties of stress/ABA-activated protein kinase 2 (SAPK2) have been characterized using loss-of-function mutants induced via the CRISPR/Cas9 technology (Lou et al., 2017). However, the major obstacle for moderation of the abiotic stresses in crop species is the transfer of CRISPR substances into plant cells and regeneration of edited plants. Over the last several years, a number of methods, like the optimization of promoters for driving and expressing Cas9, as well as the use of  ´ k et al., 2015; Wang et al., 2015; Bhowmik et al., 2018; Kaur various selection markers and fluorescence reporters (Cerma et al., 2018; Yan et al., 2018; Islam et al., 2020a; Islam and Molla, 2021), have been estimated in various crops. A microspore-based genome editing system (Bhowmik et al., 2018) could also provide a new framework for gene functional validation, genetic characterization, and abiotic trait improvement. This technique, in combination with mesophyll protoplasts, may be utilized to screen numerous gRNAs at the same time. As a result, as a substitute of traditional gene editing based on somatic cell transformation, gene editing based on microspore has the possibility to speed up gene identification and increase abiotic stress tolerance. Although CRISPR editing is a revolutionary scientific breakthrough, it has some technical limitations. For example, the off-target editing is one of the biggest challenges. The combination of NGG PAM and specific gRNA make highly specific editing, but there are instances of editing of other unintended genomic sites (Zhang et al., 2015). Although it only has 20% of the binding efficiency of NGG PAM, Cas9 can bind with NAG PAM sequence (Hsu et al., 2013). Another challenge to overcome is that CRISPR cannot cut all sequences of interest due to the restricted PAM requirements by different nucleases. The HDR-mediated precise editing is still not effective enough with CRISPR-Cas method. There is no appropriate method of supplying abundant donor template at the DSB site for the plant system. The global climate change has the great impact to reduce the yield of stable food crops up to 70% through increasing occurrence of various abiotic stresses such as soil salinity, flooding, drought, low level of available nutrients in soils, and very low and very high temperature. For the improvement of nontransgenic genome edited crop plants, the CRISPR-Cas technology is becoming a user-friendly tool to cope with the hazardous climate change conditions and safeguard the world’s future food security. We anticipate that CRISPR-Cas technology will overcome the technical and regulatory barriers linked with its mass adoption, and large-scale utilization for genome editing for the creation of new generation of climate smart, high-yielding, and abiotic stress-tolerant crops. A significant number of abiotic stress responsive genes and their loci have been discovered in wheat that can be focused for manipulation through CRISPR-Cas9 technology (Table 3). Some researchers targeted BEL and ALS genes to elevate sulphonyl urea herbicide tolerance in rice (Xu et al., 2014; Sun et al., 2016), and EPSPS for glyphosate resistance in rice using CRISPR (Li et al., 2016). Likewise, OsAOX1a-c has been focused to improve tolerant ability against various abiotic TABLE 3 Possibility of alteration in wheat gene(s) using CRISPR-Cas9 technology to increase abiotic stress tolerance. Abiotic stresses

Target gene(s) and locus

References

Saline soil

TaHKT1;5

Dubcovsky et al. (1996)

High Al3+

ALMT

Sasaki et al. (2004, 2006) and Zhou et al. (2014)

Low temperature

VRN1 at the FR1 locus and CBFs at the FR2 locus

Dhillon et al. (2012) and Knox et al. (2010)

Herbicide

BEL and ALS

Xu et al. (2014), Sun et al. (2016), and Li et al. (2016)

Drought

MAPK3, MIR169a, OST2 and SAPK2

Osakabe et al. (2016), Wang et al. (2017b), Zhao et al. (2016), Lou et al. (2017), and Shi et al. (2017)

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stresses (Xu et al., 2015), AtMIR169a, SlMAPK3, AtOST2, and OsSAPK2 for drought tolerance (Osakabe et al., 2016; Wang et al., 2017b; Zhao et al., 2016; Lou et al., 2017; Shi et al., 2017), ZmARGOS8, OsMPK2 for increasing grain yield under deficiency of water (Shan et al., 2014; Shi et al., 2017). We can use genome editing to target homologues of these genes in wheat for improvement. Under a changing climatic scenario, these genes might play a critical role in improving wheat output in the near future. Due to hexaploidy and limitation of transformation protocols, wider utilization of CRISPR-Cas9 technology in wheat is still limited (Abe et al., 2019). Therefore, advancement in protocols for genome editing in wheat is needed for greater application of CRISPR technology in the improvement of abiotic stress-tolerant smart-wheat for the mitigation of problems associated with global climate change. Recently, Li et al. (2022) demonstrated that genome edited wheat show powdery mildew disease resistance without any yield reduction. The protocols developed by them could largely be utilized for the development of biotic and abiotic stress tolerant wheat.

Conclusions and future perspectives The global climatic change steadily contributes to the increasing environmental stresses to crop plants and poses a severe threat to ensure food security around the whole world. Increasing food and feed demands can’t be fulfilled through the current trends of improvement of crop plants using conventional plant breeding methods to tolerate various abiotic stresses and other environmental challenges. In contrast, molecular breeding approaches can be used to support the enhancement of abiotic stress resistance in novel crop varieties. The applications of CRISPR-Cas technology have intensely shoot up in last 9 years to modify the genomes of a broad array of organisms from bacteria to plants. This developing handy genome editing toolkits can be applied in improvement of crop plants including hexaploid major food crop, wheat for adaptation to the changing climate. Genome editing using revolutionary CRISPR technology in rice and Arabidopsis has been studied widely. In contrast, wheat is lagging behind in genome editing by CRISPR-Cas method. The major challenges for application of CRISPR in wheat are hexaploidy, bulky genome size, and the recalcitrant nature in terms of tissue culture. However, some recent successes in genome editing of wheat by CRISPR-Cas toolkits facilitate the application of this technology for the development of abiotic stress tolerance in wheat. Open data sharing and open science approaches are needed to accelerate the process of application of CRISPR-Cas toolkits for the development of abiotic stress tolerant wheat for ensuring global food security in the changing climate. Regulatory barriers exist in some countries should be removed for the faster application of CRISPR edited nontransgenic wheat in the practical field.

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Chapter 13

Functional genomics approaches for combating the abiotic stresses in wheat Alisha Goyala,c, Nita Lakrab,⁎, Aarti Sonia, Anita Kumaria, Annub, Manormab, Meenakshib, Reenab, and Renu Munjala a

Department of Botany and Plant Physiology, Chaudhary Charan Singh Haryana Agricultural University, Hisar, Haryana, India, b Department of

Molecular Biology, Biotechnology and Bioinformatics, CCS Haryana Agricultural University, Hisar, India, c Division of Crop Improvement, ICAR—Central Soil Salinity Research Institute, Karnal, India *

Corresponding author. e-mail: [email protected]

Introduction Wheat is the most widely grown food crop among cereals. It is grown in various countries of world due to its broad adaptability to a variety of agroclimatic and soil conditions (Abhinandan et al., 2018). It is consumed in various forms by more than a thousand million people worldwide. Wheat grain has higher protein content (12.6%) and relatively high niacin and thiamine content than other cereals (Tang et al., 2013). Wheat is now farmed in more areas than any other commercial crop and is an important source of nourishment for humans. It is essential in ensuring adequate and affordable calorie and protein intake in diets. India occupies second position in wheat production in the world (FAO, 2014). Wheat-grown area around the world is about 222 million hectares and is a good source of calories and proteins (Mondal et al., 2016). Wheat production has surged from 235 million tons in 1961 to an estimated 733 million tons in 2014 (FAO, 2014), with over 768.9 million metric tons produced in the marketing year 2020-2021 (USDA, 2021). To stay within the planetary boundaries in the face of population growth and changing climatic conditions, there is still a need for significant cereal production enhancement in cereals in the coming decades. Abiotic stresses such as water (insufficient or excessive water), temperature (low or high), high salinity, heavy metal toxicity, and light stress are all affecting wheat growth and constituting a severe threat to agriculture and resulting in great loss in crop yields (Dhakal et al., 2021). Abiotic stresses are incredibly complicated, affecting different plant dynamisms such as flowering, grain filling, and maturation at the physiological, cellular, and transcriptomic levels (Maiti and Satya, 2014). A crop’s ability to withstand abiotic stresses is a critical aspect of yield loss, and crop improvement has become a big and long-term goal for plant breeders (Halford et al., 2015). Previous research has shown that high temperature stress causes pollen sterility, reduced CO2 assimilation, damages the photosynthesis process, photosynthesis nitrogen use efficiency (NUE), disrupts chloroplast structure, inactivation of chloroplastic enzymes, and possibly, results in decreased photosynthesis, all of which have a negative effect on the growth and yield of wheat crop (Almansouri et al., 2001; Wahid et al., 2007; Asseng et al., 2011; Hlava´
cova´ et al., 2018; Nuttall et al., 2017; Djanaguiraman et al., 2020). Drought is another major abiotic stress which is characterized by a shortage of water and results in major changes in morphological, physiological, biochemical, and molecular properties of plants (Fig. 1). Drought stress has detrimental consequences at every stage of growth and development, and the extent of these consequences is determined by observing stage-specific stresses and the other climatic conditions present at that time (Ahmed et al., 2019). Water deficiency is faced by more than half of wheat grown areas all over the world on regular basis and resulting in up to 10% yield loses. It is critical to find wheat genotypes that can withstand drought. High salinity is another major excruciating abiotic stress that is blamed for a significant drop in productivity of agricultural crops ( Jan et al., 2017). High salinity stress reduces germination % and increases the ionic concentration of Na+ and Cl- that causes disturbance in the normal metabolic processes of wheat plants. Plants are affected by salt stress via osmotic and ionic effects resulting in nutritional disorders. It has a significant impact on relative water quality, photosynthesis, and its related attributes such as stomatal conductance, sub stomatal CO2 concentration, chlorophyll, and carotenoids content. All the above parameters cumulatively affect the biomass and yield of plant (Yang et al., 2014).

Abiotic Stresses in Wheat. https://doi.org/10.1016/B978-0-323-95368-9.00001-1 Copyright © 2023 Elsevier Inc. All rights reserved.

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Abiotic stress (Heat, Drought, Salinity, Heavy metal, Water-logging, Low temperature)

Induces Osmotic, Ionic and Oxidative stress

Physiological Responses: • Reduced crop growth and yield • Recognition of root signals • Reduced mineral uptake and assimilation • Decrease in net photosynthesis • Decrease in stomatal conductance to CO2 • Reduced internal CO2 concentration • Loss of turgor and osmotic potential • Reduced leaf water potential • Inhibits biological nitrogen fixation

Biochemical Responses: • Loss of photochemical efficiency • Accumulation of stress induced osmolytes (proline, polyamines, glycinebetaine, (Glybet), MDHA etc) • Increased level of antioxidant enzymes(SOD, CAT, APX, POD, GR and MDHAR) • Enhanced ROS scavenging activity • Decreased Rubisco enzyme activity

Molecular Responses: • Signal transduction by MAP Kinases, Ca2+ ions and phospholipases • Transcriptional regulation by transcriptional factors(NAC, DREB, ABA, ZF-HD etc) • Expression of stress responsive genes(antioxidant enzymes, osmolytes, LEA proteins, aquaporins etc)

FIG. 1 Effects and responses of plants to various abiotic stresses.

As a result, in order to meet the ever increasing food demand, there is a need to reduce yield losses caused by different abiotic stresses under changing climatic conditions along with a check on the excessive use of natural resources. Wheat productivity can be increased further by implementing appropriate agronomic management practices. However, it has been discovered that only frequently shift in varieties will not be sufficient to deal with abiotic stresses due to variability in climate change, further increase in diversity of cropping system, and wheat varieties may necessitate abiotic stress tolerance (Kahiluoto et al., 2019). Plants cannot avoid stress because they are sessile, so they have evolved specific adaptive mechanisms to deal with it. They respond to stresses by activating multiple molecular mechanisms, including signal transduction, expression of stress associated genes, then specific proteins and metabolite production. Tolerance to abiotic stress is a polygenic trait that is influenced by a number of genes, transcription factors (TFs), metabolites, proteins, and hormones. Improving abiotic stress tolerance needs a thorough understanding of the numerous systems involved in response to stress. The adaptability of a crop to the environmental conditions in which it grows is crucial to its establishment, survival, and productivity Many factors, like plant genotype, growth stage, stress severity, stress duration, physiological process of growth, and different patterns of gene expression, can all influence how plants respond to abiotic stress and adapt to it (Chaves et al., 2003). The present classical breeding methods used to enhance stress tolerance are successful to a limited extent. This requires new techniques other than conventional breeding techniques to increase crop production and yield. Crop improvement gains a new incentive to biotechnology (e.g., gene editing and molecular markers). Advance techniques such as next-generation sequencing techniques, the availability of genome sequences, and other advanced biotechnological tools all open up new avenues for improving the crop plant stress tolerance in this era of genomics. The main goal of this chapter is to give a comprehensive overview of the key techniques used in the identification and functional annotation of potential candidate gene that range from traditional mapping to robust functional genomics that developed after sequencing of whole genome with the help of genomics, proteomics, transcriptomics, proteomics, and metabolomics. Understanding of these functional annotation strategies is critical in order to choose the best strategy for achieving the required results. This chapter discusses the several functional genomic techniques such as gene expression profiling with microarrays, genome wide association studies (GWAS) which can accelerate the finding of novel genes related with stress, and various OMICS technologies. Furthermore, suppression subtractive hybridization (SSH) is a useful technique for identification and cloning of genes/ESTs that express differently under specific conditions. This chapter also

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covers novel biotechnological tools such as reverse and forward genetics, as well as how functionally verified genes can be employed in plant breeding, transgenic, and genome editing approaches to improve stress tolerance.

Functional genomics approaches for wheat crop improvement Functional genomics is that branch of science which merges molecular and cell biology studies together and works with the entire structure, function, and control of a gene in contrast to gene-by-gene approach of traditional molecular biology techniques. Its goal is to figure out how many components of a biological system interact to produce a certain phenotype that is related to the phenotype and genotype on the genome level, and it includes processes like transcription, translation, proteinprotein interaction, and epigenetic control. The goal of agriculture is to choose progenies with superior features of interest since crop domestication in the ancient world to the current genomic age. Over time, the methods for identifying superior plants have been improved. Genomic, transcriptomic, and metabolomic investigations are used to identify the main genes/ QTLs linked to the trait of interest. Prior to the advent of techniques for whole genome sequencing, forward genetics, i.e., phenotype to gene/QTL, was the most common method for identifying the molecular basis for the trait of interest. In 2000, Arabidopsis thaliana whole genome sequencing resulted in a big repository sequence data that (Kaul et al., 2000) further gave scope for reverse genetics mode, i.e., genes/QTL to phenotype of functional annotation. The completion of the rice genome sequencing (Goff et al., 2002: Yu et al., 2002) was added to the data repository after a few years. Aside from illuminating research of reverse genetics, the phenomenon of whole genome sequencing has also speed up and given forward genetics research a new dimension (Schneeberger and Weigel, 2011). The transition from traditional cDNA-AFLP to high throughput microarrays and RNA sequencing is accumulating evidence for breakthroughs in transcriptome analysis (Vuylsteke et al., 2007; Rutley and Twell, 2015). Proteomics is the study of all proteins present at a certain time and under specific conditions, which also helps to functionally annotate the desired variables linked with trait of interest. Electrophoresis techniques including two-dimensional PAGE and DIGE were initially used to uncover the proteome but now gel-free platforms are also available for investigating the proteome ( Jorrı´n-Novo et al., 2015). Likewise, new metabolomics methodologies improved the knowledge of total metabolites at certain time and under specific conditions (Sumner et al., 2015). We try to develop a model relating genotype to phenotype using our present knowledge about the function of gene in functional genomics. The following section of the chapter will go through several different functional genomics methodologies that are based on the genome, transcriptome, proteome, metabolomes, and ionomes.

Genome-based functional annotation Reverse and Forward genetics methodologies are used in functional genomics research (Fig. 2). Forward genetics involves the technique of uncovering of molecular basis of an intriguing phenotype. It is the study of phenotype to corresponding gene or QTL ( Jankowicz-Cieslak and Till, 2015). Further advancement of genome sequencing has increased the process of research on forward genetics, such as proteomics and metabolomics (Schneeberger and Weigel, 2011). The approach of reverse genetics is diametrically opposed to that of forward genetics. Reverse genetic research begins with a completely sequenced and structurally annotated genome. The goal of "gene to phenotype" research approach is to

Forward Genetic approach

Transcriptome Phenotype

Proteome

Systems Biology approach

Metabolome

Reverse Genetic approach

FIG. 2 Pipelines for functional genomics study.

Candidate QTL(s)/Gene(s)

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give biological significance to the raw sequence data ( Jankowicz-Cieslak and Till, 2015). Forward and reverse genetics approach employs several techniques, which are covered in the following sections:

RNAi/PTGS RNA interference (RNAi) is a valuable technique in functional genomics as it has been frequently employed to describe gene function and construct novel phenotypes. RNAi also called as posttranscriptional gene silencing (PTGS), in which a sequence specific gene silencing mechanism, reduces the expression of a target gene. This method is still in its early stages in polyploid species, but it has a huge amount of potential as it can silence multiple homoeologous copies with a single RNAi construct. RNA interference construct targets the ideal gene which is first introduced into the host, and after insert integration, dsRNA is produced, which is then processed into 22 nucleotides ds-siRNA by the Dicer enzyme with a doublestranded RNA binding domain at C-terminal, two RNaseIII-like domains, and N-terminal RNA helicase (Bernstein et al., 2001: Pare and Hobman, 2007). Dicer enzyme is a member of the RNaseIII gene family. The siRNA has introduced ribosome-induced silencing complex (RISC), which is triggered by its uncoiling. One strand of it functions as a guide siRNA, allowing the target mRNA to be silenced (Ipsaro and Joshua-Tor, 2015). The sRNA is small RNA then bound to the RNAi system catalytic elements; AGOs (Argonaute family proteins). The AGO/siRNA complexes subsequently join RISC (Lee et al., 2010) which further controls the translation, degradation of mRNA, and modifications of chromatin (Borges and Martienssen, 2015). RNAi method has effectively been used to regulate various responses under abiotic stress in many crops (Shriram et al., 2016; Kumar et al., 2018). Furthermore, polycomponent biostimulants and metabolites of streptomycetes present in diverse soil regulate siRNA and miRNA which can promote RNAi. These small RNAs work in conjunction with cereal cyst nematode mRNA to prevent the nematode from reproducing, providing wheat plants with resistance (Blyuss et al., 2019). RNA interference (RNAi) technique is appearing as a promising strategy for plant protection under abiotic stress, but various challenges must be addressed before it can be used effectively in the field. The main disadvantage of this method is that function of gene is not completely blocked, which allows for off-target effects and misunderstanding of data (Gaj et al., 2013). One of the major problems with RNA to use as biopesticide is its stability, particularly in siRNA and dsRNA spray applications. Naturally present microorganisms can destroy dsRNA before pathogens or pests can consume it. Nucleases in the pest saliva, hemolymph, and/or intestinal lumen may also degrade dsRNA rapidly (Kennedy et al., 2004; Allen and Walker III, 2012; Katoch and Thakur, 2012; Chung et al., 2018; Guan et al., 2018). The activity of gut nucleases is affected by pH fluctuation in the gut lumens of some pests, which can diminish the stability of dsRNA directly or indirectly (Cooper et al., 2019). The traditional dsRNA synthesis process is costly and produces just a small amount of dsRNA, making it unsuitable for application at large-scale needs (Ahn et al., 2019). RNAi technology has been used to target few important diseases in wheat-like Fusarium head blight (Cheng et al., 2015). Many crop species, including wheat, have studied their miRNA expression profiles in response to drought. The miRNA microarray platform was used to understand the expression patterns of miRNA for water stress tolerance in barley (Hordeum vulgare) and wild emmer wheat (Triticum dicoccum). Several miRNAs from different families including miR156, miR166, miR172, and miR393 have been linked to high temperature, low temperature stress, and salinity stress and salt stress in wheat (Ding et al., 2009; Xin et al., 2010; Marı´n-Sanz et al., 2020). The processing of these miRNAs and their targets could increase the overall stress tolerance in crops. Geneediting methods have recently been employed to obtain comparable results, which will be explored in the next section

Genome editing Genome editing is a technique that involves the addition, deletion, or substitution of the DNA bases in a specific segment of the DNA of the genome by using various nucleases. The new technology CRISPER-Cas9 is the most recent and effective approach which is available to date for targeted genome editing (Fig. 3). Cas9 is clustered, short palindromic repeat regularly interspaced, CRISPER-associated nuclease 9. Tools include CRISPR Finder, ZiFIT, CRISPR design tool, CHOPCHOP, CasOT, PROGNOSIS, and E-CRISP, etc., used to forecast potential off-targets to achieve targeted genome editing CRISPR design tool. CRISPR-Cas is a group of hybrid enzymes that are used to modify genomes in a variety of organisms, including plants. This CRISPR-Cas is the most recent development. It is more efficient and time-consuming than TALENs. TALENs are transcription activator-like effector nuclease or ZFNs (zinc-finger nuclease) (Kumar and Jain, 2015). Genome editing differs from genetically modified organisms (GMOs) as it does not require the insertion of transgenes and does not cause widespread concern in public when it comes to edible crop species (Stephens and Barakate, 2016). According to the studies of Sander and Joung (2014) and Bortesi and Fischer (2015), the CRISPR/Cas9 genome editing system uses Cas9, an RNA-guided nuclease that is effective and promising in causing targeted changes in endogenous genes and in the double-strand breaks. CRISPR-Cas9-mediated breaks repair is used by the cellular DNA repair mechanism

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Cas9 nuclease binds to a specific DNA location which is dependent on protospacer adjacent motif (PAM)

RuvC and HNH domains clave the double-strand DNA and form a double-strand break (DSB). HNH cleave the sequence which iscomplementary to sgRNA while RuvC cleave non complementary strand.

Cas9interact with guide RNAand form ribonucleoprotein (RNP) complex perform endonuclease activity at target site/s.

The cell own DNA repair mechanisms repair DSB sbyt wo repair pathways, one is non-homologous end joining (NHEJ) repair and another one is homology-directed repair (HDR).

HDR usually requires a template DNAfor DSBrepair,t hat can be a foreign single- or double strand exogenous DNA, the homologous chromosome, the sister chromatid, or even some sequences that are highly related to the sequences with DSBs. FIG. 3 CRISPR/Cas system working mechanism.

to mediate gene or genome changes. CRISPR systems are part of bacterial defense systems that help to protect themselves against invading nucleic acid like viruses and plasmids (Wei et al., 2013; Yang et al., 2013; Zhang et al., 2014). With the improvement and creation of numerous Cas9 nuclease variations, this technique is becoming an effective tool in developing nontransgenic genome-edited crops plant to combat the detrimental consequences of climate change (Haque et al., 2018). RNA-guided nucleases (RGNs), also known as Cas proteins and CRISPR RNAs, are the two important key component of CRISPR-Cas system. Structurally, Cas9 is a Cas protein with two nuclease domains of RuvC and HNH and one of the most studied RGNs Cas protein. It is an endonuclease that uses CRISPR RNA (crRNA) and trans-encoded CRISPR RNA (tracrRNA) to break DNA at a specific target spot (Ma et al., 2013; Sander and Joung, 2014). These crRNA and tracrRNA are short RNA molecules. The crRNA and tracrRNA produce a double-strand RNA structure that instructs Cas9 to make DSBs in the target DNA. The complementary strand which is complementary to crRNA at genomic location is cleaved by Cas9 HNH nuclease domain while noncomplementary strand is cleaved by RuvC-like domain. Chimeric RNA molecule is produced when these two RNA molecules chemically unite to generate a single-guide RNA (sgRNA). Single-guide RNA (sgRNA) can construct an RNA-guided endonuclease with the Cas9 protein that mediates sequence-specific cleavage. Ma et al. (2013) and Wei et al. (2013) reported that this sgRNA-Cas9 complex is determined by a sequence of merely 20 consecutive nucleotide of sgRNA. The first CRISPR/Cas9-mutagenized wheat plants were obtained by Chinese Academy of Sciences researchers in 2014. In Wang et al. (2014a,b), studies in hexaploid bread wheat, CRISPR-Cas9, and transcription activator-like effector nuclease (TALEN) are used to introduce targeted mutation in three homoeoalleles that encode MLOprotein (MILDEW-RESISTANCE LOCUS). Liang et al. (2017) successfully edited two separate genes, namely, TaGW2 and TaGASR7, in two different varietal backgrounds by using immature embryo cells of bread wheat (Kenong 199 and YZ814). In wheat protoplast, Kim et al. (2018) used the genome editing technology (CRISPR/Cas9) to do targeted editing of two abiotic stress responsive transcription factor genes. These are wheat dehydration response element-binding protein 2 (TaDREB2) and wheat ethylene-responsive factor 3 (TaERF3). According to Ouyang et al. (2016), removing of phosphate-

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2 gene (TaPHO2-A1) increases uptake of phosphorus and then yield in wheat crop under phosphorus deficient conditions. Wang et al. (2018a,b) elevated width and wheat grain length by knocking out the RING-type E3 ligase-encoding gene TaGW2 by using the CRISPR/Cas9system. Zhang et al. (2016) studied the three gibberellin-regulated Ta-GASR7 genes, previously been linked to grain size regulation, and discovered a considerable rise in thousand-kernel weight. Bhowmik et al. (2018) created an efficient haploid mutagenesis method using the CRISPR/Cas9 system and microspore technology for inducing genetic alterations in wheat genome. They have shown that specific alterations can be made to exogenous and endogenous wheat genes; DSRed exogenous while TaLox2 and TaUbiL1 are endogenous genes. They have demonstrated the feasibility of introducing targeted alteration into DsRed, TaLox2, and TaUbiL1 genes. Upadhyay et al. (2013) used wheat cell suspension culture to target the inositol oxygenase (inox) and phytoene desaturase (pds) genes as well as the pds gene in Nicotiana benthamiana leaves. Two genes inox and pds were targeted at four regions for editing in wheat, and 18–22 percent mutations in different wheat protospacers were observed. There were both deletion and insertion mutations found.

TILLING/EcoTILLING Targeting-induced local lesions in genomes (TILLING) is a powerful reverse genetics approach in which chemical mutagenesis combines with sequence variation detection in target genes (McCallum et al., 2000a,b). It is a nontransgenic method that enables the specific mutations in targeted genomic sequences based on PCR technique to generate novel mutant allele novel mutant alleles for crop improvement (Gilliham et al., 2017). It makes the use of classical insertion mutagenesis and the availability of genomic sequences to provide rapid identification of point mutation and functional validation of targeted genes (Akpınar et al., 2013). This method could be used widely in all plant species, including both diploids and allohexaploids (Chen et al., 2014). Under different abiotic stress conditions, plants exhibit different phenotypes that are linked to variation in genome sequence (De Lorenzo et al., 2009). This method of identifying natural variations in individuals is known as ecotype TILLING which is a modified version of TILLING; the only distinction is the starting material, i.e., natural population. Targeting-induced local lesions in genomes approaches were used to screen SNPs and small mutations (Uauy et al., 2009; Bajaj et al., 2016) in an exome-sequenced mutant population (Krasileva et al., 2017) and in a classical TILLING population to identify a collection of de novo alleles (McCallum et al., 2000a,b). It reveals the intricacy of stress tolerance by providing information on allelic variants for a variety of genes. Rice SNPs important in drought and salt tolerance were successfully identified using the EcoTILLING method (Negrao et al., 2011). Chemically mutagenized segregating populations (mainly M2) are used as the starting material, with the mutated area in the homozygous state. First, depending on the ploidy level of the crop, DNA is usually combined 2-8 times. Secondly, using a 50 -labeled dye, PCR is used to increase the target candidate genes in pooled DNA, resulting in heteroduplexes and homoduplexes. After being digested cleavage enzyme CEL1, the heteroduplexes are denatured and resolved on DNA analyzer (LI-COR) to detect the altered area. Finally, using a 2D array method, select the mutant person from pooled DNA (Wang and Shi, 2015). Publically available programs for analysis of the generated data are Burrows-Wheeler Aligner (BWA) and Coverage Aware Mutation calling Using Bayesian Analysis (CAMBa). EcoTILLING discovers single-nucleotide polymorphism (SNPs) within natural population (SNPs) while TILLING technology detects mutation in mutagenized population and correlates these differences with features of breeding concern. The fundamental benefit of using these approaches as a “reverse genetics strategy” is that they could be used on any species, independent of genome size and ploidy level. In cereals using these TILLING by sequencing, a number of space-induced EMS induced population have been exploited to identify mutants with essential features like salinity tolerance, grain size, and recombinant crossovers. The EcoTILLING technique has been used to exploit genes such as TaSSIV, which is involved in the production of starch granule, pin a and pin b linked to wheat kernel hardness (Irshad et al., 2020).

TALENS (transcriptional activator-like effector nucleases): TALEN proteins detect a specific DNA sequence (DNA-binding domain), which was initially found in 2009. TALEs are used by Xanthomonas sp. to affect transcriptional activity in plant species which enhance the establishment (Bogdanove and Voytas, 2011). Further, they are injected into plant tissue, in which they bind to specific promoters and trigger the gene expression. In 2010, TALEN knocked out all three TaMlo homoeologs at the same time, resulting in mutant wheat plants that were extremely tolerant to powdery mildew infection. In TALEN, the restriction endonuclease FokI’s catalytic motifs are fused to a transcription activator-like effector (TALE). TALE proteins are made up of three major regions. The microbial secretion signal and a nonspecific DNA-binding activity are found in the N-terminal region (Szurek et al., 2002; Kay et al., 2007). A plant transcription factor IIA contact

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interface, an acidic activation region, and two functional nuclear localization indicators are all found in the C-terminal domain (Van den Ackerveken et al., 1996; Zhu et al., 1998; Yuan et al., 2016). These TALEs have 34 amino acid duplications that effectively change a single base pair (Zhang et al., 2019). The RVDs (repeat-variable di-residues) that determine a TALE or TALEN’s DNA specificity are found at locations 12 and 13 of each repeat (Boch et al., 2009; Moscou and Bogdanove, 2009). TALEs contain two distinct characteristics: the first is based on the usage of unusually long naturally occurring repeat units, and the second is determined by the ability of some RVDs to discriminate between nucleotides with varying methylation levels (Richter et al., 2014; Tsuji and Imanishi, 2019). TALENs also produce changes by causing double-strand breaks (DSBs), which initiate editing pathways (Gaj et al., 2013). TALENs induce double-strand breaks in specific structures, triggering a DNA reaction cascade that results in genome breakdown. TALEN could be delivered as DNA, RNA, or protein via (1) physical methods like biolistic transition, transfection, or electroporation; (2) bacterial delivery; (3) viral delivery; or (4) chemical methods like transfection reagents, polyethylene glycol (PEG), or liposomes. TALEN technique has been used to change several genes in plants, including Brachypodium, rice, Arabidopsis, Barley, tobacco, soybean, maize, and wheat. Wang et al. (2014a,b) use TALEN technology in Triticum aestivum to incorporate genetic changes in three TaMLO homoeologs that provide powdery mildew resistance, utilizing nonhomologous end-joining (NHEJ) as the repair mechanism. In rice, TALEN was utilized to generate genomic alterations for disease resistance in Xanthomonas oryzae pv. Oryzae (Xoo) through TALEN-based disruption of the rice bacterial blight susceptibility locus OsSWEET14 (also known as Os11N3).

MicroRNAs (miRNAs) MicroRNAs (miRNAs) are noncoding RNA molecules that regulate gene expression after transcription (Budak et al., 2015a; Budak et al., 2015b; Alptekin and Budak, 2017). Plant miRNAs bind to their specific transcripts in a synchronized manner and impede translation by cleaving and/or deteriorating the mRNA molecule (Budak and Akpinar, 2015). This expression controls the stress-responsive genes through miRNA activity which is expected to provide a particular advantage in abiotic stress situations. In the model plant Arabidopsis, the significance of miRNA-based stress response was identified (Lu and Fedoroff, 2000; Gim et al., 2014). Many efforts to investigate wheat miRNAs at the subgenomic level led to the discovery of 58 wheat miRNAs, which are classified into 43 miRNA families, 20 of which are conserved (Yao et al., 2007). The importance of these tiny regulators in plant survival during environmental stress was highlighted by the authors. Many miRNA target genes in the Triticeae family have been connected to stress-responsive transcription families, such as NAC and WRKY (Kantar et al., 2011; Deng et al., 2015). Several behavioral and physiological tests demonstrated the importance of miRNA-based gene expression after the expression of stress-responsive miRNAs and/or their target transcripts was altered (Kantar et al., 2011; Feng et al., 2013). A computational transdisciplinary approach has considerably expanded the number of miRNAs by using an EST-based technique. A search of the NCBI EST (expressed sequence tags) database led to the discovery of miRNAs. To predict miRNA in wheat, Pandey et al. (2013) employed 4677 mature miRNA sequences in 50 different miRNA families from various plant taxa. There are four novel abiotic stress-responsive miRNA such as miR1117, Ta-miR1122, Ta-miR1133, and Ta-miR1134 which were detected in newly identified EST sequences. An ubiquitin-carrier protein, 40S ribosomal protein, BTB/POZ domain-containing protein, transcription factors, serine/threonine-protein kinase, and F-box/kelchrepeat protein are all encoded by the majority of miRNAs. The expression of miR855 in wheat for salt tolerance has also been verified among the predicted miRNAs (Pandey et al., 2013). As a result, the number of miRNAs has risen, which might aid future research into the biological activities and development of miRNAs in wheat and other plant species. The expression profile of selected abiotic stress-responsive miRNAs implicated in drought adaptation was studied to better understand the differential regulation mechanism in wheat genotype C-306. Six miRNAs showed differential expression in the drought-stressed C-306 genotype. When compared to mock-treated plants, the accumulation of miR393, miR1029, and miR172 was significantly larger; however, drought had no significant effect on miR529 expression profiling. These findings suggest that a wide range of miRNAs may be important in reducing stress responses. 30 novel miRNAs have been discovered using NGS, and work is underway to further validate drought-specific miRNAs, 14 managing abiotic stresses in wheat-330, and their targets are being invested in wheat genotypes with varying drought stress responses

Transcriptomics-based functional annotation Transcriptomics (also known as transcriptome) is the analysis of whole transcripts at a particular period and situation. Transcriptomic investigations are critical for deciphering the function of candidate genes and identifying them under controlled conditions. Global transcriptomics analysis started with cDNA AFLP and SSH with the advent of NGS technologies and

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further progressed to RNAseq. Now, it has become an important component of any functional genomic research in order to provide better molecular knowledge of the target phenomenon in recent years. The following section of the chapter will go over the major techniques used in transcriptome analysis.

SSH (suppression subtractive hybridization) SSH is useful for finding the transcripts that are particularly expressed in response to a series of treatments. SSH is a useful tool for discovering and isolating genes with low-level differential expression (Diatchenko et al., 1996). This method is prevalent because of its inexpensive cost, a small amount of starting material, and low chance of mistakes. The combination of normalization and subtraction in SSH allows it to detect numerous differentially expressed genes while also enhancing unique transcripts to assist in the discovery of novel genes (Clement et al., 2008). Furthermore, this technique does not require whole genome-based information as it overcomes the limits of global gene expression analysis (Gulyani and Khurana, 2011). As a result, SSH may be used to examine plants with minimal sequence information. By deep sequencing SSH libraries, Bisaga et al. (2017) produced the first high molecular data associated to white clover in response to water deficit and rehydration targets for the development of tolerant types. SSH evaluation of genes is affected by external ABA in pepper plant leaves under chilling stress (Guo et al., 2013). The two key aspects of SSH are the tester and driver in which the tester is ss cDNA from the treated sample, and the driver is the ss cDNA from the equivalent control, which is hybridized in a 10:1 ratio. This large number of drivers ensures that there is a huge amount of tester-driver fusion and reduces the DS-tester-tester complex. Transcripts found in both treated and control samples form a hybrid tester-driver, whereas transcripts expressed as a result of treatment stay single-stranded testers. In the subtractive phase, the tester-driver hybrid and the tester-tester complex are eliminated, leaving only single-stranded tester molecules, i.e., the enriched collection of transcripts expressed only in the treated sample.

SAGE (serial analysis of gene expression) SAGE provides a complete perspective of the transcriptome in both treated and untreated circumstances. SAGE requires a brief sequence tag (10–14 bp) that contains a unique transcript. A vast number of distinct short sequence tags are joined together to generate lengthy serial molecules that are cloned and sequenced in order to identify the transcript (Matsumura et al., 2003; Chaudhary and Sharma, 2015). According to Han et al. (2016), SAGE proved useful in identifying genes involved in the production of natural substances in medicinal plants as well as possible differentially expressed genes in sea buckthorn under cold and freezing stress. SuperSAGE analyses of potatoes infected with Phytophthora infestans novel twenty-two candidate genes were selected (Muktar et al., 2015). Calsa and Figueira (2007) used SAGE in sugarcane (Saccharum spp.) leaves to detect unique transcribed sequences and transcript information. SAGE transcript profiling in arabidopsis showed 270 differentially expressed genes between roots of plants that received NO3 or NH4NO3 as a nitrogen source (Fizames et al., 2004). SAGE is increasingly being used in additional species, including barley, maize, banana, and pine, in addition to plant model systems (Calsa and Figueira, 2007).

EST (expressed sequence tags) ESTs are small tags from the cDNA library that have been sequenced once. They are 500–800 bp long which can be used to define the corresponding transcripts. Physical mapping methods such as happy mapping, radiation hybrid mapping, fluorescent in situ hybridization, and others could be used to map these partial transcript sequences on their corresponding chromosomes. They are especially valuable for functional genomics research in crops that do not have a complete genome (Edwards and Batley, 2010). Using EST sequencing, researchers were able to identify genes associated in terpene synthesis in the medicinal plant. ESTs are single-passed sequences that could be used to search polypeptides and DNA databases for associated genes, resulting in a 200–700 bp sequence (Adams et al., 1991). It is also a method for detecting differentially expressed genes in plants as a result of different treatments (Vij and Tyagi, 2007). ESTs are utilized to identify corresponding genes rapidly and cost-effectively (Bouchez and H€ ofte, 1998). EST sequencing project is a useful tool for intergenomic (Schlueter et al., 2004) and intragenomic (Fulton et al., 2002) comparisons, gene discovery (Michalek et al., 2002), molecular marker identification (Hughes and Friedman, 2005), microarray advancement (Close et al., 2004), and polyploid species genomic resource development. One of the earliest tools for gene discovery and genome annotation was large-scale EST sequencing. As a result, ESTs have played an important role in functional studies. The wheat genome is one of the largest genomes having a haploid size of 16.7 billion bp (Bennett and Leitch, 1995), which is 40 times and 110 times larger than rice and Arabidopsis, respectively (Sasaki, 2003). The large size of the wheat

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TABLE 1 cDNA libraries from the Wheat EST project containing information on EST productivity and mapping (Lazo et al., 2004). Name

Condition and plant part

Number 30 ESTs

Number 50 ESTs

Number of ESTs mapped

TA054XXX (T. aestivum)

Meiotic, untreated anther

–

9139

0

TA038E1X (T. aestivum)

Salt-stressed seedling

286

943

148

TA016E1X (T. aestivum)

Vernalized, seedling

703

2286

416

TA012XXX (T. aestivum)

ABA-treated mature embryo

–

2,107

3

TM011XXX (T. monococcum)

5-week; accession Dv92, Apex, vegetative, shoot

–

3031

11

TM043E1X (T. monococcum)

7-week vernalized (accession Dv92), Apex, early reproductive, shoot

930

2647

426

TT039E1X (T. turgidum)

Whole mature plant (Langdon-16)

284

1194

157

genome, along with the high frequency of repetitive noncoding DNA (over 80%), makes comprehensive wheat genome sequencing a major challenge. On the other hand, large-scale EST creation and analysis can provide a valuable understanding of the expressed fraction of the wheat genome. Wheat EST research funded by the National Science Foundation in the United States is assessing the structure and function of the expressed region of the wheat genome by creating and sequencing more than 100,000 ESTs (Sorrells et al., 2003). It connects wheat unigenes to distinct chromosome locations (Table 1) and offers a comprehensive description of expressed sequences from various tissue types during normal development or after exposure to abiotic stressors (Francki and Appels, 2002).

Microarray Microarray technology has bridged the gap between functional genomics and sequencing data, as genome sequencing progresses. The expression level of thousands of genes has been measured at a multiplex level using a microarray-based technique (Lockhart and Winzeler, 2000). The microarray expression profile analysis provides a better knowledge of genes involved in regulatory networks and signal transduction in response to numerous abiotic stressors tolerance (Ghorbani et al., 2019; Raza et al., 2021). Microarrays are divided into two categories based on the nature of the immobilized probes: (1) DNA microarrays made from DNA fragments that are generally synthesized using PCR procedures (Raza, 2020) and spotted cDNA-microarrays, and (2) oligonucleotide microarrays constructed with shorter (10 to 40-mer) or longer (up to 120-mer) oligonucleotides corresponding to specific coding targets. These cDNA microarrays provide a number of advantages, including the ability to control gene expression patterns. Oligonucleotide microarrays, on the other hand, are limited to minimal sequence complication array elements. With arrays containing longer DNA pieces than oligonucleotides, the hybridization specificity of a compound probe is improved (Pervaiz et al., 2022). The most popular cDNA microarray procedure comprises creating a cDNA library, sequencing the clones, amplifying them, and robotically printing probes onto slides. It is also called "Reverse Northern" in some cases. RNA extraction from nontreated and treated samples is the initial stage in the process. Fluorescent dyes are applied to the dNTPs utilized in cDNA synthesis (Cy5 dUTP orCy3 dUTP). The fluorescently tagged ss cDNA is hybridized on the microarray slide, the unbound materials are rinsed out, and finally, the image is captured by detecting the fluorescence and fluorescent signal is transformed into a digital output, which is then utilized to analyze data. The normalized data are used to calculate the fold change of a transcript in response to a particular treatment (Duggan et al., 1999). The importance of the microarray in dissecting stress responses in plants, especially powdery mildew sensitive miRNAs in wheat, has been stressed by scientists (Wu et al., 2015; Gul et al., 2016). The ability

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to analyze thousands of transcripts at the same time is the main benefit of microarray. The disadvantage is that convincing findings from microarray analysis require whole-genome sequence information and technological expertise.

RNAseq RNAseq is a global transcriptome analysis method in which RNAs are isolated from different samples for the particular desired trait. The sequencing adaptor labeled cDNA library is then created, and the high-throughput sequencing technologies are used to retrieve its short sequence. The sequencing reads are then assembled using the reference genome or transcriptome as a guide (Wang et al., 2009). One of the most significant disadvantages of this strong technique is the time-consuming and challenging data analysis requirements, which necessitate bioinformatics competence. In wheat, RNA-Seq has mostly been used to find new and conserved stress-responsive genes, notably, those involved in biotic stress tolerance and nutrition responsive regulation (Kugler et al., 2013; Oono et al., 2013). Kumar et al. (2015) used RNA sequencing to investigate the heat-related genes in wheat.

Candidate genes and transcription factors Genes implicated in stress tolerance pathways are candidate genes. In stress-responsive gene mining, understanding molecular processes and improving stress tolerance in agricultural crops are critical requirements (Khan et al., 2018). During times of stress, candidate genes may be involved in the regulation of protein kinases and specific transcription factors (Song et al., 2013; Yamasaki et al., 2013). About 10% of the genes in the plant genome code for transcription factors (Franco-Zorrilla et al., 2014). TFs control gene expression by stimulating or inhibiting RNA polymerase activity; in addition, a single TF can control multiple genes involved in stress tolerance. The regulatory response to abiotic stress in plants is extremely complicated, involving complex interactions between transcription factors and cis-acting elements. According to certain studies, stress-responsive TFs or multiple stress-regulating TF genes could be used in genetic modifications and breeding programs to improve a variety of crop cultivars. In Arabidopsis, overexpression of GsNAC019 (Glycine soja TF) and PbeNAC1 (Pyrus betulifolia TF) resulted in tolerance to alkaline, drought, and chilling stresses (Cao et al., 2017; Jin et al., 2017). Because of QTL regions containing hundreds of genes, identifying candidate genes is difficult; thus, combining GWAS and QTL is effective in identifying candidate genes (Sonah et al., 2015). Natural variation associated with a genetic basis and stress tolerance has been discovered in a variety of plant species, including maize (Gao et al., 2019), wheat (Li et al., 2019), rice (Patishtan et al., 2018), Brassica napus (Rahaman et al., 2018), and sorghum (Patishtan et al., 2018; Chen et al., 2018) by using this method. Candidate gene analysis is used to figure out what is causing phenotypic variation. Using genotyping and phenotyping analysis of multiple pairs of near-isogenic lines, Wang et al. (2019) identified five candidate genes (Table 2) for a large 4BL QTL (NILs).

QTLs and single-nucleotide polymorphisms (SNPs) The first wheat genetic map was successfully created in the early 1990s using RFLP markers (Devos et al., 1993). To create genetic maps, a variety of markers (RAPD, AFLP, RFLP, and SSR) are used; however, SSR is the most extensively used molecular marker. The genetic diversity of these molecular markers is quite low. It takes a very long time and requires a lot of effort, and it cannot match the requirements for creating a genetic map for gene cloning and fine gene mapping. Recent advances in NGS technologies have improved the accuracy and effectiveness of sequencing-based genotyping, making it useful for finding SNPs, especially when the reference genome sequence is available, as well as sequence assembly using bacterial artificial chromosomes in species where the reference genome is not available. The development of additional molecular markers on a genome-wide scale is made possible by NGS. As a result, molecular markers, particularly SNPs, are being used to enhance the power of gene discovery related to stress and to aid genome mapping and germplasm characterization (Akpinar et al., 2017). SNPs are preferred over other markers for investigating stress management in a variety of methods, including cultivar identification, genetic diversity evaluation, genetic maps creation, marker-assisted selection, and genotype vs phenotype association detection, due to their availability and inheritance stability (Ganal et al., 2009). In several crops, several SNPs linked to abiotic stress tolerance have been discovered (Kilasi et al., 2018; Ruggieri et al., 2019). Garg et al. (2012) discovered a single SNP in the heat shock protein sequence among heat-sensitive and tolerant genotypes (HSP16.9). SNPs were used to map TFs that confer salt tolerance and drought tolerance, such as DREB1, WRKY1, HKT-1, and Na1 transporters (Mondini et al., 2012).

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TABLE 2 List of the candidate gene in wheat in different stresses. S. no.

Gene ID

Chromosome

Putative function

References

1.

TRITD1Bv1G120210 TRITD1Bv1G119290

1B

RING U-box superfamily protein Cytochrome P450 family protein

Mangini et al. (2021)

2.

TRITD6Bv1G185080 TRITD6Bv1G189120

6B

E3 ubiquitin-protein ligase thioredoxin

Mangini et al. (2021)

3

TRITD3Av1G011970 TRITD3Av1G012140 TRITD3Av1G012070

3A

Kinase family protein Receptor-like kinase Flavin-containing monooxygenase

Mangini et al. (2021)

4

TraesCS5A02G542600

5A

Major facilitator superfamily

Alomari et al. (2021)

5

TraesCS5B02G403400

5B

Semialdehyde dehydrogenase

Alomari et al. (2021)

6

TraesCS1A02G292100

1A

Serine-threonine/tyrosineprotein kinase

Alomari et al. (2021)

7

TraesCS3A02G167700

3A

RWP-RK transcription

Dabab Nahas et al. (2019)

8

TraesCS3D02G540600

3D

Transcription factor MYB59like

Dabab Nahas et al. (2019)

9

TraesCS2D02G533600

2D

Unknown function woundinduced

Dabab Nahas et al. (2019)

10

TraesCS1D02G102400

1D

REF SRPP-01784

Dabab Nahas et al. (2019)

As a result, SNPs are quickly displacing conventional markers. It is also important in the determination of phenotypic differences in plants, microorganisms, animals, and humans (Moen et al., 2008; De Souza et al., 2010). SNPs are appropriate for creating genetic maps in plant species as they were co-dominant, abundant, and inexpensive. Wang et al. (2014a,b) used eight DH lines to create a wheat integration map with 80277 SNPs and investigated the distribution of SNP loci on the 90 K gene chip’s chromosome. All 21 wheat chromosomes were shown to have a substantial number of QTL for the thousand-grain weight (Yang et al., 2020).

Genome-wide association studies (GWAS) The genome-wide association study (GWAS), which is based on the concept of linkage disequilibrium, is an effective tool for identifying genomic regions linked to phenotypic changes in natural populations. The single-locus GWAS (SL-GWAS) methodology employs a one-dimensional genome scan to test one marker at a time, with multiple testing corrections required to prevent false-positive results (Kaler and Purcell, 2019). Due to the availability of highly effective highthroughput genotyping assays, GWAS is increasingly being used to identify genes/genomic areas responsible for agronomically important traits in wheat and other cereals (Alqudah et al., 2020; Gupta et al., 2019). In a variety of crop plants, GWAS has proven to be an effective method for elucidating the complex genetic pathways influencing abiotic stress tolerance (Long et al., 2013; Turki et al., 2015). Furthermore, numerous GWAS studies for salt tolerance in crop species have been published (Hu et al., 2021; Li et al., 2021; ; Quan et al., 2021; Yu et al., 2020a,b). GWAS revealed 42 QTLs that are significantly correlated with ten salt tolerance-related parameters, including 9, 16, and 17 QTLs linked to physiological, shoot ionic, and biomass traits, respectively (Chaurasia et al., 2020).

220

Abiotic stresses in wheat

Functional genomics using proteomics In 1994, Marc Wilkins introduced the term "proteomics" to describe the genome’s protein supplement. It is the main study of structural, functional, and interactions of proteins during several biological processes present in organisms, cells, and tissue at a given period or a particular event. The vast information generated from other “omics” tools was insufficient to highlight the different biological pathways as proteins are the leading players in a more significant part of the cellular events. Proteomics also plays a crucial part between the transcriptome and metabolome (Wang et al., 2004; Gray and Heath, 2005). Proteins are crucial in the stress response of plants because they are directly involved in the creation of new phenotypes by altering physiological features in response to environmental changes. The research uncovers a number of abiotic stress-responsive proteins, some of which may be downstream effectors of transcription factors discovered at the transcriptional level. Moreover, proteomics based on mass spectrometry allows for the discovery of isoform-specific proteins, enabling the diversification of unique and shared roles within a protein family (Ghosh and Xu, 2014). In transcriptome research, such a high level of detection is not feasible. As a result, proteome-wide identification and analysis of functional proteins yielded more data at the transcriptional level, allowing researchers to better understand abiotic stress response networks in plants. Proteomics exposes the quantitative and qualitative assessments of key proteins accumulated in certain tissues, as well as their differential expression in response to treatment at various phases of development and growth (Kumar et al., 2019). The biological activity of a protein is influenced by posttranscriptional activity, posttranslational modifications (PTMs), cellular localization, and protein interactions with other proteins ( Jorrı´n-Novo et al., 2009; Kosova´ et al., 2011). As a result, its molecular structure has no effect on it; therefore, functional studies of these proteins are needed to determine their role in plant stress response. With advancements in the field of proteomics, there has been a shift from gel-based to gel-free proteomics. The feature of first-generation proteomic research is gel-based proteomics. The most common gel-based technique for protein research is 2D-PAGE (two-dimensional polyacrylamide gel electrophoresis). IEF (isoelectric focusing) resolves proteins in the first dimension based on an isoelectric point, while polyacrylamide gel electrophoresis (PAGE) resolves proteins in the second dimension based on molecular weight. Then the gels are dyed and scanned in a densitometer. The differentially expressed spots on the gel are selected and excised, and the proteins are then trypsin digested. The related proteins are then identified by obtaining their peptide mass fingerprint (PMF) using mass spectrometric techniques such as MALDI-TOF (Issaq and Veenstra, 2008). The application of 2D-PAGE has aided in the development of a comprehensive understanding of the proteome. To address the concerns raised by 2D-PAGE, the fluorescent-based method 2D-DIGE (two-dimensional differential ingel electrophoresis) was developed. Proteins isolated from various samples are combined using a fluorescent dye and resolved on a single gel (Arentz et al., 2015). Proteomic alterations in endosperm and embryo of two different wheat cultivars were discovered in order to improve the quality of wheat bread (Cao et al., 2016). The ultimate benefit of 2D-DIGE is that it eliminates gel-to-gel variation; however, fluorescent dyes may interfere with accurate protein abundance estimation when used. To overcome the limitations of 2D and DIGE techniques, gel-free high-throughput mass spectrometric platforms were developed. Top-down protein analysis, in which proteins are identified and quantified without the use of enzymes, is used on these gel-free platforms. These techniques can be used to investigate posttranslational modifications (PTMs), which have been shown to be important in determining a protein’s function. Gel-free platforms include MudPIT (multidimensional protein identification technology), LTQ Orbitrap (Linear Trap Quadrupole), and protein microarrays. MudPIT is a multidimensional liquid chromatography, SEQUEST, and tandem mass spectrometry-based database mining system (Washburn et al., 2001). Proteomic studies of the cell wall, plasma membrane, nucleus, mitochondria, chloroplast, and endoplasmic reticulum proteomes are done in a variety of plant species, including wheat (Table 3) (Dunkley et al., 2006; Komatsu et al., 2014; Wang and Komatsu, 2016; Zhu et al., 2021). Proteomic analyses have been successfully used in wheat to study various stress responses, such as salt, drought, heat, waterlogging, temperature, and other abiotic stress factors (Table 4), which can provide insights into abiotic stress mechanisms and also serve as a good starting point for further dissection of their functions using genetic and other approaches.

Metabolomics-directed plant functional genomics The metabolome is a cell’s or organism’s entire metabolite profile at a given time and condition. Throughout the years, various mass spectrometric approaches for quantifying metabolites have been developed. Metabolic validation is the most reliable method for determining the importance of differentially expressed genes. As a result, it opens the possibility of

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TABLE 3 Summary of primary stress-responsive proteins found in distinct plant cell compartments (Kosova´ et al., 2018). Mitochondria

Chloroplast

Nucleus

Cell wall

Krebs cycle enzymes: MDH, aconitase Respiratory chain: Cytochrome b6-f complex, ferredoxin, NADPH reductase, AOX ATP metabolism: NDPK Translation: EF-Tu Redox- and stress-related proteins: Trx, Prx- Prxll F SNO, GroES, HSP90 ROS scavenging: Mn-SOD

Photosynthesis electron transport: OEC, F1F0 ATP synthase, CF1α,B,y Carbon assimilation: RubisCO, RubisCO activase isoforms; Calvin cycle: PGK, PRK Amino acid metabolism: aspartate aminotransferase Chlorophyll biosynthesis: protoporphyrinogen oxidase

Signal transduction: Calnexin, calmodulin, serine-threonine kinase, Tyr phosphatase Gene expression: At MYB2, MYB34, bZIP TF, BHLH TF, MYC, AP2/EREBP, homeobox leucine zipper TF, CHP-rich Zn-finger protein, H2A, H2B, H1 Redox- and stress-related proteins: HSP70, HSP90, co-chaperones Dna K type, Hsc 70-1

Signaling: Protein kinase2; receptor-like kinase, inositol phosphatase Carbohydrate metabolism: ALDO, PRK Metabolism: NDPK Protein degradation: 20S proteasome alpha SU Redox- and stressrelated proteins: POXS; APX, Trx m, glyoxalase Cu/Zn-SOD, trx MDAR

TABLE 4 List of proteomic studies in wheat under different abiotic stresses. Abiotic stress

Plant material

Major differentially expressed proteins

References

Drought

Common wheat cv. Nesser (T), Opata M85 (S)–root

1656 identified proteins, 805 ABAresponsive proteins: LEA, protein phosphatases PP2C; genotypic differences: HSP70, HSP90, etc.

Alvarez et al. (2014)

Heat

Common wheat–Fang (T), Wyuna (S)—grain endosperm

Genotypic differences: 7 small HSP (16.9 kD class I HSP) proteins unique to T

Skylas et al. (2002)

Osmotic stress (PEG- 6000)

Common wheat cv. Hanxuan 10(T) and Ningchun 47(t)—seedling leaf

173(T) and 251(t) phosphoproteins identified

Zhang et al. (2014)

Salinity

Common wheat (T. aestivum) cv. Chinese Spring (S), T. aestivum  Lophopyrumelongatum amphiploid (T)—mitochondrial fraction (shoot, root)

15 shoot and 55 root differentially abundant proteins Organ-specific differences: aspartate aminotransferase

Jacoby et al. (2013)

Salinity

Durum wheat cv. Waha—seed embryo and surrounding tissue

697 Identified proteins–proteins involved in energy metabolism, protein metabolism, disease/defense, protein destination,

Fercha et al. (2013, 2014)

Low temperature

Wild wheat (Triticum urartu)—leaf

34 Identified proteins—25 upregulated and 9 downregulated Up: LEA-III, WCOR14, PR4; OEE1, chloroplast ribosomal protein L12 Down: Rubisco SSU

Gharechahi et al. (2014)

Drought or waterlogging and cold

Winter common wheat cv. Yannong 19—leaf

32 Identified proteins Up: DHAR, GR, Hsp70 Down: C metabolism-related proteins, RubisCO activase A, ATP synthase CF1 α,β

Li et al. (2014)

222

Abiotic stresses in wheat

identifying a group of potential crop-improvement genes (Feussner and Polle, 2015). Environmental–gene interactions, phenotyping, mutant characterization, biomarker identification, and drug discovery all benefit from metabolomics. Ultrahigh performance liquid chromatography linked to triple-quadrupole mass spectrometry (UPLC-QqQ-MS) is commonly used for high-throughput quantification of plant metabolites, and the multiple reaction monitoring (MRM) mode is adjusted to achieve the best results (Wei et al., 2010). Sumner et al. (2015) examined the use of metabolomics in plant research and found it to be ineffective. In plants, the metabolite glycerol-3-phosphate (G3P) has been discovered to induce systemic immunity (Chanda et al., 2011). Metlin, PRIme, MassBank, MeltDB, and other online databases make structural data available to the public (Sakurai et al., 2013). For novel metabolites that are not in the databases, computational analysis such as LipidBlast, MetFrag, Metfusion, and the use of MS/MS data for annotation is required (Sumner et al., 2015). Ren et al. (2021) used a liquid chromatography/mass spectrometry (LC/MS) metabolomics approach to investigate changes in the grain metabolomics of Tilletia controversa infected and noninfected samples, and discovered 62 different metabolites in the grains, 34 of which were upregulated and 28 of which were downregulated. Matthews et al. (2012) discovered 935 ions in a variety of wheat lines using ultraperformance liquid chromatography and time-of-flight mass spectrometry using GC/MS-based metabolomics; Zhen et al. (2016) uncover 74 metabolites in bread wheat during the grain growth stage. A more advanced type of association mapping is the metabolome-based genome-wide association study (mGWAS). Genotyping and phenotypic scoring by sequencing (SNPs)/RNAseq is used to map genes. Metabolomics-assisted breeding allows for effective yield and stress tolerance screening at the metabolomic level. Advanced metabolomics analytical tools (Table 5) such as gas chromatography-mass spectrometry (GC-MS), nondestructive nuclear magnetic resonance (NMR), liquid chromatography-mass spectroscopy (LC-MS), direct flow injection (DFI) mass spectrometry, and high-performance liquid chromatography have accelerated metabolomic profiling (HPLC). The combination of metabolomics and postgenomics methods now allows for the efficient dissection of genetic and phenotypic connections in crop plants. The convergence of omics methods such as genomics, transcriptomics, and metabolomics holds enormous promise for deciphering complex metabolic pathways that govern key regulatory processes in plant metabolism. Metabolomics could TABLE 5 Tools with techniques. Stress condition

Analytic platform

Specific tissue

Drought

1.GC-MS 2.GC/MS 3.GC-TOF-MS

Salinity

Key metabolites produced

Data analysis

References

Roots and leaves Flag leaves Shoots

Malic acid, valine, fumaric acid, citric acid, and tryptophan Glutamine, serine, methionine, lysine, and asparagine Malic acid, sucrose mannose, fructose, and proline

KEGG, PLS-DA Metabolome express SIMCA 14.0, PCA, KEGG, MetaboAnalyst

Kang et al. (2019) Yadav et al. (2019) Guo et al. (2018)

GC/MS HPLC GC-TOF/MS

Leaves Roots and shoots Leaves

Proline, lysine, alanine, and GABA Malic acid, proline, fructose, mannose, glycine, Glutamic acid Lysine, proline, sorbitol, lyxose, and sucrose

Metabolome express ANOVA, PCA PCA, OPLS-DA, KEGG and MetaboAnalyst

Che-Othman et al. (2020) Borrelli et al. (2018) Guo et al. (2015)

Waterlogging

GC/MS and LC/MS

Shoot

Lysine, proline, methionine, and tryptophan

ANOVA, PCA

Herzog et al. (2018)

High Temperature

LC-HRMS GC-MS

Flag leaves Leaves

Pipecolate and L-tryptophan Melibiose, serine, lysine, glycine, malic acid, mannitol, xylitol, inositol, fructose, proline, glutamic acid, and alanine

PLS-DA, KEGG LSD

Thomason et al. (2018) Qi et al. (2017)

Nitrogen stress

LC-MS and GC-MS GC-TOF-MS UPLC-TOF

Leaves Leaves Flag leaf

Tyrosine, allo-inositol lysine, and L-ascorbic acid Fucose, ribulose, lyxose, galactinol, and erythritol Methylisoorientin-2”O-rhamnoside, iso-orientin, and iso-vitexin

MS-excel package PCA PCA, OPLS-DA, Markerlunx XSM, SIMCA-P

Khan et al. (2019) Heyneke et al. (2017) Zhang et al. (2017)

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Crop plants under abiotic stress

Metabolomics for crop improvement Targeted metabolic profiling

Non – targeted metabolic profiling

Diagnostic and deciphering novel metabolic pathways for stress regulation, Biosynthesis of secondary metabolites (flavanoids, organic acids and sugars etc.), Metabolic pathways (ABA networks, TCA Cycle, Jasmonate pathways etc.), Revert genetic bottlenecks (reversion of important traits lost during extensive breeding)

Metabolomics-assisted breeding

mGWAS

mQTL

Dissecting genotypic and phenotypic relationship, Linking metabolites with stress– responsive traits, Discovery of metabolic markers, Breeding for stress tolerant elite lines

Integrating with modern breeding platforms

Engineering metabolic pathways CRISPER Cas system

Transgenic technology

Speed breeding FIG. 4 Flowchart illustrating the key mechanisms in plant metabolomics for crop development (Razzaq et al., 2019).

be used to find metabolic markers to study plant metabolism and predict the type and magnitude of future biotic/abiotic stress. Crop improvement projects will employ techniques such as metabolomics-assisted breeding to create high-yielding, stress-tolerant cultivars and implement climate-smart crop production. Metabolomics techniques were also used to characterize the metabolic properties of genome-edited crops using the CRISPR/Cas9 system. Speed breeding is another exciting area where metabolomics has the potential to increase agricultural yield (Fig. 4).

Ionomics In the current period of omics, ionomics is one of the crucial technologies for studying genomics. With the development in genomic study, the regulation of genomic ions in the plant system will concrete the path for finding out the novel gene with its function (Sowmya et al., 2018). As a result, the development of ionomics has aided the study of natural variation in nutrient metabolism based on genetics. Ionomics is the study of inorganic element composition changes in response to physiological stimuli, developmental state, and genetic changes. It is a high-throughput method for representing the mineral nutrient and trace element composition of living organisms (Michaletti et al., 2018). Combining ionomics with other omics technologies such as transcriptomics, proteomics, and metabolomics can help bridge the gap between genotypic and phenotypic information (Salt et al., 2008). It helps identify genes found in the mapping population and provides new crop platforms for regulatory processes like mineral accumulation, cross-talk, stress

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resilience, and transportation. It exhibits the mechanisms of ion uptake, transport, compartmentalization, and exclusion, and it has a wide range of applications in variant screening, reverse and forward genetics, and so on. It is useful in understanding the activities of abiotic stresses in plants because it exhibits the mechanisms of ion uptake, transport, compartmentalization, and exclusion, and it has a wide range of applications in variant screening, reverse and forward genetics, and so on (Salt et al., 2008). As a result, ionomics has emerged as the most functional and structural genomics technology. For comprehensive ionomics profiling, inductively coupled plasma-optical emission spectrometry (ICP-OES), X-ray crystallography, inductively coupled plasma-mass spectrometry (ICP-MS), neutron activation analysis (NAA), and other analytical methods are used (Ali et al., 2021). These technologies enable comprehensive analysis of the ions found in plants. The information generated by these technologies is saved in the Purdue Ionomics Information Management System database (PiiMS). The study of the organism’s structural and functional genomics is aided by this massive amount of data. The concept of the ionome was first proposed about ten years ago, and significant progress has been made in the field of ionomics since then, largely due to the use of genetics and other high-throughput technologies to identify the genes that control the ionome (Danku et al., 2013). Ionomics has been used to study Zea mays, Olea europaea, Vitis vinifera, Brassica napus, Glycine max, and Oryza sativa (Ali et al., 2021). Environmental monitoring, food safety, nutrient consumption, and biofortification are just a few of the applications (Pita-Barbosa et al., 2019). Shakoor et al. (2016) demonstrated that ionomics can improve food safety and combat hunger. They carried out ionomic research on staple foods like grains and beans. Arabidopsis thaliana, the model plant used to conduct the research early on ionomics. Arabidopsis thaliana has emerged as a critical component in the expansion of other agricultural crops (Lahner et al., 2003). Sorghum bicolor, A. thaliana, O. sativa, Triticum aestivum, Medicago truncatula, Z. mays, Populus trichocarpa, Setaria italica, G. max, and Setari viridis have a total of 1764 ionome-regulating genes (Whitt et al., 2020). Ionomics-based biomarkers in plant stress biology can assist to evaluate whether a specific biochemical and physiological state reached in a plant in response to diverse abiotic stimuli. It may also be used to screen plants which are more susceptible to biotic and abiotic stressors, which is impossible to do with conventional high-throughput methods. Ionomic analysis in spring wheat grain produced in Kazakhstan and Russia was evaluated by Abugalieva et al. (2021). They discovered that spring wheat grain produced in Kazakhstan and Omsk is extremely safe to eat. For ionomics analysis, Qin et al. (2021) provide new insights into the co-enrichment of cadmium and zinc in wheat grains. Their findings revealed that high-Cd accumulating varieties were also able to accumulate mineral elements such as calcium, magnesium, manganese, iron, and zinc, whereas low-Cd accumulating varieties were deficient in many essential nutrients, particularly zinc (Zn). Multiomics analysis reveals the molecular mechanisms for wheat adaptation to potassium deprivation (Zhao et al., 2020). There has been little work on ionomic responses to nutritional stress in wheat, although ionomics-based methodologies are rapidly becoming effective research methods for investigating plant physiology (Wu et al., 2013; Zeng et al., 2015). The literature on ionomics techniques is scarce; nonetheless, highly effective ion profiling will open new doors in understanding abiotic stress tolerance signaling mechanisms. As a result, ionomics is a low-cost but comprehensive physiological profile tool. Researchers will be able to harness the potential of ionomics for gene discovery, genetics, and modeling by using the right combination of instruments. For example, T. aestivum has 267 ionome-regulating genes. TaIPK1, TaABCC13, Ta-PHR1, HKT2, and HKT1 are some of the key genes with Fe, Zn, P, Na +, and Ca2 as target elements. It is found in the seed, shoot, and root tissue (Ali et al., 2021).

Conclusion and future projections Abiotic stresses such as salinity, drought, and high and low temperatures are extremely complicated, affecting plant dynamisms at the genomic, transcriptome, and metabolomics levels, ultimately lowering crop yields and posing a severe danger to food security. New techniques other than conventional breeding techniques are required to increase crop production and yield under abiotic stress. Among these new impetuses to crop improvement are molecular markers and gene editing. Functional genomics encompasses both the forward and reverse genetics approaches such as RNA interference (RNAi), genome editing, transcriptional activator-like effector nucleases (TALENS), targeting-induced local lesions IN genomes (TILLING), MicroRNAs (miRNAs), transcriptomics: suppression subtractive hybridization (SSH), serial analysis of gene expression (SAGE), microarray technology, expressed sequence tags (ESTs), and RNAseq (massively parallel sequencing of cDNA). Understanding molecular processes and stress-responsive genes (candidate genes) is essential for increasing stress-tolerance crops. To create genetic maps, molecular markers such as RAPD, AFLP, RFLP, SSR, and SNP can be utilized. NGS technologies have recently been developed, making genotyping based on sequencing more efficient and worthwhile. Other effective approaches such as genome-wide association study (GWAS), functional genomics using proteomics, metabolomics-driven plant functional genomics, and ionomics have all produced unique

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and intriguing possibilities for improving abiotic stress tolerance enhancement. Plant biotechnologists will soon have a better understanding of stress-tolerant mechanisms in plants, allowing farmers to grow high-yielding stress-tolerant crops in the fields.

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Chapter 14

Role of transcriptomics in countering the effect of abiotic stresses in wheat Fahad Alotaibi⁎, Saif Alharbi, and Abdullah Alrajhi National Center for Agriculture Technology, Life Science and Environment Research Institute, King Abdulaziz City for Science & Technology, Saudi Arabia *

Corresponding author. e-mail: [email protected]

Introduction Feeding a growing population is increased by the conflicting land allocation problems for housing vs. agricultural production. Uncertainty over food supplies is further aggravated by deterioration of soil fertility conditions, lower agricultural production due to climate change, and it is predicted to increase in the future. Under severe climatic conditions, increasing the agricultural yield is one of the most challenging tasks. Growing crops suited for a specific environment in a defined location is essential to agriculture. High temperatures in a region for an extended period of time cause drought stress. It is also possible that exposure to high temperatures will increase salt content due to water evaporation from the soil. There are two primary factors impacting crop output worldwide: drought and salt stress, although it is not uncommon for heat to be present at the same time. This fact might result in a significant drop in crop productivity. As the earliest cultivated crop, wheat has become a global staple meal (Tack et al., 2015). Compared to rice or maize, wheat has a higher protein content per gram (12%–15%), making it a superior grain of choice. There are large areas of wheat cultivation in the world, even though output levels are considerably lower than those of rice and maize (FAO, 2017). Challinor et al. (2014) evaluated a meta-analysis of 1700 published models of wheat production loss due to every 2°C rise in temperature in temperate and tropical regions. Another study anticipated a 6% decline in wheat output comparable to an estimated 42 Mt/ °C reduction (Asseng et al., 2019). As a result, decreasing wheat production levels in present agriculture is a significant problem, and mitigation methods must streamline toward improving the output under restricted resources. Crop improvement by the conventional breeding method is laborious and time-consuming that involves complex genes regulating many physiological and molecular processes. Moreover, the considerable amount of diversity in the tolerance levels among different cultivars under identical stress conditions has enhanced the mechanical complexity (Abhinandan et al., 2018). In general, plant stress comprises abiotic and biotic stressors. Excessive temperatures, drought, cold, elevated salinity levels, metals, and mechanical destruction are all examples of abiotic stress conditions. Plants alter throughout the growth at the cellular, organ, physiological, biochemical, and molecular levels to adapt to adversity, which is reflected in the form of morphological changes in plants. Adaptation in the molecular processes under stress conditions helps the plants reduce cellular damage due to stress. Abiotic stresses in crop plants, including wheat, have become a significant obstacle to contemporary agriculture due to climate change, and thus, research on plant stress-responsive mechanisms is of great interest (Wang et al., 2020). The plant’s response to stress is a complicated biological process whose molecular mechanism has not been understood yet. The transcriptome is a term used to refer to the range of RNAs synthesized by one cell or tissue in a particular functional state, encompassing both messenger and nonmessenger RNA. It entails investigating gene transcription and its regulatory roles in cells globally and studies on noncoding region functions, transcript structure, gene transcription level, and novel transcriptional region. Consequently, transcriptomics may be used to analyze changes in plant gene expression across time, quantitatively exposing the complicated regulatory network and expression at the entire genome level under stress and figuring out new transcripts related to plant resistance (Lian et al., 2015). Abiotic stresses can occur alone or in combination with biotic stresses, causing cellular damage at various plant growth and development phases and varying degrees of phenotypic lethality such as reduced growth, wilting, and leaf loss (Chinnusamy et al., 2004). Due to the abiotic stress, the plant’s signal transduction pathways genes are activated, resulting in stress-responsive genes activation that leads to transcriptional reprogramming in the cell and helps the plant to survive at different growth stages (Xiong and Zhu, 2001). Therefore, it is necessary to understand the precise biological mechanism by Abiotic Stresses in Wheat. https://doi.org/10.1016/B978-0-323-95368-9.00005-9 Copyright © 2023 Elsevier Inc. All rights reserved.

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which plants respond under various abiotic stresses. Several proteins coding and noncoding genes, including microRNAs, were found during the stress response processes (Liu et al., 2008) and have been linked with different transcription factors (TFs), biological pathways, and epigenetic processes (Kilian et al., 2012), that finally develops tolerance (Roy et al., 2011) and adaptation in plants (Mirouze and Paszkowski, 2011). TFs are significant regulatory elements that bind with the cisregulatory compounds and trigger the expression of many downregulated genes and, as a result, develop stress tolerance (Agarwal and Jha, 2010). Transcriptional profiling has been extensively used in Arabidopsis thaliana, Triticum aestivum, Zea mays, Glycine max, and Oryza sativa L. since the advent of sequencing technologies. Several essential genes linked to abiotic stress have been discovered in Arabidopsis. Recent research studies have shown that the DREB1/CBF, DREB2, AREB/ABF, and NAC regulons play vital roles in response to abiotic stresses in cereals, including wheat (Nakashima et al., 2009). Significant progress has been made in discovering regulatory genes involved in stress responses that confer abiotic stress tolerance in plants (Galiba et al., 2009). Advancements in the cumulative omics strategies help determining a group of genes and TFs important for physiological concerns linked with molecular genetics in wheat (Alotaibi et al., 2021). The advancements in the transcriptome studies, adaptation in the metabolic pathways, differentially expressed genes (DEGs) under abiotic stresses in wheat crops provide a roadmap against abiotic stresses. The current chapter evaluates the advancements in the transcriptome studies for the wheat crop. Furthermore, the involvement of these transcriptomes in different metabolic pathways and expression of DEGs under various environmental stress conditions has been discussed to look forward to future directions for improving the wheat transcriptome under different abiotic stress conditions.

Abiotic stress and transcriptome A comparative analysis of transcriptome data might help researchers to understand how the plants balance growth and survival under abiotic stress conditions. Several abiotic stressors might cause plants to regulate their physiological and cellular processes to adjust to adverse situations. Analysis and screening of plant tissues and organs for differentially expressed functional genes can provide a better understanding of transcriptional level to know how plants respond to injury and stress and identify the link between critical functional genes and transcripts to overcome abiotic stress in wheat (Fig. 1).

Salt stress and transcriptomics in wheat Salinity stress negatively impacts crops due to ion toxicity, nutritional restrictions, oxidative damage, and osmotic stressors (Shrivastava and Kumar, 2015). Physiological, cellular, molecular, and metabolic adaptive responses are necessary for salt tolerance in plants. With next-generation sequencing technology, the molecular foundation of the plant’s salt stress response may be uncovered by comparing the transcriptome profiles of various species under various environmental circumstances. Stress perception and stress signaling genes, transcriptional regulators, and salinity genes are all types of genes essential for salt stress response (Zhang et al., 2011). Signal transduction pathways are critical in the plant’s response to various stressors. It is one of the first reactions of the cytosol’s calcium concentration, and Ca2+ moving elements actively regulate the calcium-binding protein, activate calcium-dependent protein kinases, and help to activate the stress-responsive genes that maintain the plant phenotype under harsh conditions (Singh et al., 2014a). Salt tolerance is regulated by a group of genes, TF, ion transporter, kinases, proteins, and osmolytes at the molecular level (Tuteja, 2007b). Salt overly sensitive

FIG. 1 Climate resilience abiotic stress wheat improvement with integrated plants omics strategies.

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(SOS) and calcium signaling pathways and MAPK and proline metabolism play crucial functions in the resistance to salt stress (Danquah et al., 2014). Higher transcript abundance of SOS genes was recorded in the genotype of the intolerant wheat (Kharchia 65) in roots and leaves relative to the sensitive wheat genotype (HD 2687). As a result, it prevents the Na+ entry in the leaves and enhances the sodium/potassium ratio (Sathee et al., 2015). Salt tolerance is a quantitative characteristic controlled by several genetic factors (Chinnusamy et al., 2005). The salt tolerance network must be improved through genetic engineering by discovering essential components that underlie it. Bread wheat shoots in salinity conditions were examined using RNA-sequencing technologies in a few recent publications (Amirbakhtiar et al., 2021; Luo et al., 2019). A comparative study from shoot transcriptomes of wild-type and spaceflight induced wheat mutant (st1) was used to determine the genes involved in stress response pathways and transcriptome sequence variation caused by spaceflight induced mutants. The results suggested that salt tolerance genes such as polyamine oxidase and arginine decarboxylase and hormone-related genes were up-regulated in the wheat mutant relative to wild-type wheat. Furthermore, “Butanoate metabolism” was identified as a novel salt stress response mechanism and indicated that oxidation-reduction (redox) balance is essential for salt tolerance (Xiong et al., 2017). Meanwhile, Mahajan et al. (2017) conducted transcriptome profiling under salt stress conditions at the flag leaves stage from the salt-tolerant cultivar (Kharcha) using RNA-sequencing. The results suggested that up-regulated genes were identified for flavonoid biosynthesis, signal transduction, ion transport, phytohormone, osmoregulatory activities, and ROS homeostasis biological pathways. Luo et al. (2019) evaluated bread wheat cultivars, Xiaoyan 60 (XY60), and Zhongmai 175 (ZM175) under salinity stress. In leaves of XY60, the enriched GO and the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways were linked with polyunsaturated fatty acid (PUFA) metabolism, while in ZM175, these pathways were linked to energy and photosynthesis metabolism. In the roots of both genotypes, glucosinolate biosynthesis was the most significantly enriched KEGG pathway. Furthermore, the results suggested that the photosynthetic system and JA-related pathways were also identified as dominant characters and enhanced the salt tolerance. Betaine aldehyde dehydrogenase (BADH) gene is essential for osmotic and salinity salt tolerance. Overexpressed HvBADH1 genes were transformed in wheat crops to determine the osmotic/salinity tolerance mechanism, and physiological parameters (Na+, K+, K+/Na+ ratio, relative conductivity, glycine betaine (GB), and malondialdehyde) were measured to determine the response toward osmotic or salinity stress. Significant improvements in K+ recruitments were recorded in transgenic cultivars relative to the wild-type in the cytosol. Moreover, 11.59–21.82 folds greater GB accumulation was recorded in transgenic wheat cultivars under 150 mM salt stress condition, and overexpression of HvBADH1 enhanced the tolerance level in transgenic wheat (Li et al., 2019). Zhang et al. (2016) compared the root transcriptome response of a salt-tolerant cultivar with a salt-sensitive cultivar and discovered two NAC (TFs), a MYB TF (homologous to AtMYB33), and a gene (TaRSL4) responsible for producing root hairs and a gene (AtSDG16) encoding histone-lysine N-methyl transferase significant for improvement tolerance level against salinity. Amirbakhtiar et al. (2019) analyzed the transcriptome profile to understand better how a salt-tolerant bread wheat cultivar responds to salinity stress. Plant hormone signal transduction, phenylpropanoid biosynthesis, transporters TFs, glutathione metabolism, and glycosyltransferases were identified as the most significant pathways involved in salt stress response. Mahajan et al. (2020) sequenced a salt-tolerant wheat cultivar’s root transcriptome at the anthesis stage. The results suggested that salt stress up-regulated the genes related to ROS homeostasis, ion transport, signal transduction, ABA biosynthesis, and osmoregulation. Furthermore, it was also suggested that different transcripts and genes, i.e., expansion, dehydrins, xyloglucan endotransglucosylase, and peroxidases, were also up-regulated in root development under salinity stress conditions. The upregulation of the CaM-binding TFs CBP60 during salt stress was discovered by Amirbakhtiar et al. (2021). Overexpression of bZIP1 in wheat susceptible variety (Chinese Spring) and downregulation in a tolerant cultivar (Mahouti) under salt stress were registered under long-term salinity stress (Rahaie et al., 2013). The sequences of 15 wheat cDNAs encoding putative WRKY proteins were acquired by Wu et al. (2008) under salinity stress. Based on phylogenetic analysis, the 15 WRKY genes were categorized into three main WRKY groups, and expression analysis indicated that most genes were highly expressed in leaves. TaWRKY10 TFs were expressed more in the crown region; however, some genes are significantly up-regulated during the leaf senescence (Wu et al., 2008). Similarly, the results of another study suggested that wheat WRKYs (WRKY1 and WRKY2) were up-regulated in salt-tolerant wheat genotypes (Rahaie et al., 2011). The differential expression of MYB TF was investigated in two wheat recombinant inbred lines (RIL), and their expression was determined using qPCR against salt stress. The results suggested that TaMYBsdu1 was up-regulated and recorded higher transcript abundance in salttolerant wheat genotype (Rahaie et al., 2010). A comparative transcriptome study was done on salt-tolerant wheat genotype and TaMYB1 was identified to be one of the up-regulated genes in the wheat with 34 times greater expression levels under stress conditions relative to control (Mott and Wang, 2012).

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Recently, chromosome level genome sequence assembly was done at the osmotic and ionic stage to determine the candidate genes involved in salt stress response in bread wheat. The results suggested that calcium-binding and cell wall synthesis genes were activated initially during the osmotic stage intolerant genotypes, which may play a role in the mechanisms that improved photosynthetic stability and overall salt stress adaptation intolerant wheat genotype (Duarte-Delgado et al., 2020). Another study on salt-tolerant (Kharchia) bread wheat genotype was used to determine the molecular mechanism of salt tolerance and functional annotation using root differential transcriptome analysis. The results reported a total of 14,898 unigenes, and 77 TFs families, 826 unigenes, and 310 metabolic pathways were identified under salinity stress conditions (Goyal et al., 2016).

Drought stress and transcriptomics in wheat Wheat is commonly cultivated under irrigated and rain-fed conditions in various areas. Drought has been the most significant environmental limit on wheat output because of global warming and caused an annual average loss of around 5.5% every year (Zampieri et al., 2017). Therefore, to address the problem of global climate, food safety is urgently required to exploit and use drought-tolerant genes to develop wheat species with increased tolerance to drought (Reynolds et al., 2009). At the molecular level, drought response is complicated in hexaploid wheat (Ga´lvez et al., 2019) involving different genes, proteins, cofactors, hormones, TFs, metabolites, ions, and microRNA (Budak and Akpinar, 2015). Recently, there have been tremendous strides in discovering the drive response molecular mechanism and many drought-responsive genes in wheat (Morran et al., 2011). Furthermore, the previous research/comparative studies of wild and bread wheat were used to determine droughtresponsive genes from different plant organs. Moreover, micro-RNA studies from root organs could help to find the drought-responsive genes using transcriptome sequence analysis (Cagirici et al., 2017). Alptekin et al. (2017) studied the comparative analysis of miRNAs in bread wheat and their diploid descendants, Aegilops, under drought stress conditions. The results identified several uncovered miRNAs expressed in one genotype relative to others, representing greater diversity among Aegilops sharonensis populations. Earlier wheat drought stress transcriptome investigations were limited to the leaves (Lv et al., 2018), and then research extended to flowering tissues at different time intervals and stages. Comparative research was done to determine the transcriptional response to water scarcity in two soft white springs at the flag leaf stage in wheat cultivars. Alotaibi (2018) studied two wheat genotypes, i.e., Idaho and Alpowa, which are sensitive and drought-tolerant wheat cultivars, respectively, using RNA sequencing and transcriptome profiling. Differentially expressed genes (DEGs) and their related gene ontology-based biological activities were identified. The results identified different transcription factors (TFs) related to different drought-responsive (biosynthesis, pollen recognition, embryo development, and seed dormancy) pathways were seen and recorded a significant shift in their expression levels in drought-tolerant wheat genotypes relative to control under drought conditions. Roots have been suggested as the most effective research alternative for improving crop response to drought stress situations (Vadez, 2014) as the root is the first organ to feel the stress of drought (water shortage). Drought adaptation strongly depends upon root architecture. Although research has been done on drought-related transcriptomic changes in wheat, there is still a big gap (Wang et al., 2016). A root-based comparative transcriptome study was conducted based on drought stress in sensitive and tolerant wheat genotypes. The results suggested 8197 drought-responsive genes related to phytohormone signal transduction, carbon metabolism, and flavonoids. Furthermore, the DEGs about the antioxidative and anti-osmotic stress-related genes were up-regulated in drought-tolerant wheat genotypes relative to control (Hu et al., 2018). However, studies like these do not examine the most significant effects of drought stress on wheat production, based on root phenotyping at different development stages (Ihsan et al., 2015). The transcriptomic approach may be used to reveal associated signaling pathways that transfer signals to the roots and shoots in contrast to genotypes varying in drought adaptation mechanisms for molecular responses to fetch biochemical and morphological changes to protect water loss and survive stress (Janiak et al., 2016). To enhance water absorption, plants use an adaptive approach that includes developing new absorptive surfaces and changing their root thickness. Microarray is a highperformance method to analyze the transcriptome linked to different characteristics in wheat (Singh et al., 2014b). C2H2 zinc finger proteins (ZFPs) have a lot of DNA-binding motifs, eukaryotic TFs subfamily containing QALGGH amino acid performed best under drought stress conditions (Bateman et al., 2004). The ZFP family is a developmental characteristic for numerous vegetative and floral organs in wheat, and it performs a variety of roles in biological processes under drought stress (Takatsuji, 1999), shoot gravitropism (Morita et al., 2006), and leaf senescence (Krichevsky et al., 2007). After receiving precise signals from roots to shoots, the plant is stimulated to adapt to drought stress by up-regulating and accumulating dry mass in wheat (Tardieu, 1996). From the current database’s knowledge, 47 C2H2 zinc finger genes have been identified in bread wheat (Agarwal et al., 2007; Sekimata and Homma, 2004).

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Similarly, TaZFP42 can influence genes involved in seed storage protein synthesis for starch accumulation (Kam et al., 2008), and TaZFP15 contributes to drought by increasing starch buildup in the leaves and transmitting signals from the root to the shoot. Moreover, TaZFP15 also functioned in ABA-regulated pathways by adapting drought-responsive genes in wheat (Kam et al., 2008). ABA is a plant hormone that plays various roles in plant growth and abiotic stress tolerance and controls many drought-responsive genes under drought stress conditions. These genes have an ABA-responsive element (ABRE) on their promoter region, which controls expression in response to ABA by binding to bZIP TFs (Ying et al., 2011). Under drought, bZIP TFs regulate the expression of specific genes, which are responsible for alterations such as root growth maintenance, leaf development inhibition, higher levels of chaperone proteins, and stomatal closure (Hamanishi and Campbell, 2011). WRKY TFs are one of the top 10 plant TFs families, and more than a hundred of these TFs € have been identified in various species (Ulker and Somssich, 2004). Plant defense systems and other processes such as germination and senescence are all influenced by WRKYs TFs. WRKY TFs play a vital part with MAP kinases, calmodulin proteins, histone deacetylase, and resistance proteins to upregulate or downregulate specific genes under drought stress conditions in wheat (Ali et al., 2020). TaNAC 8 TF functions as a transcriptional activator and engages in biotic and abiotic defensive responses (Xia et al., 2010). Overexpression of TaNAC improved the tolerance level under drought conditions in wheat. TaNAC 69 genes are elevated during drought and are involved in normal root cellular functions. Overexpression of TaNAC 69 enhanced the drought resistance mechanism, and water use efficiency was improved in the root zone area (Rahaie et al., 2013). Suggestions reported similar findings that the thiol protease gene was overexpressed in wheat under drought conditions (Kumar et al., 2018). In addition, MT protein enhanced the overexpression tolerance against numerous abiotic stressors including drought in transgenic wheat (Zhang et al., 2014a,b). Similarly, phospholipase transcript played an essential role against abiotic stress in wheat. An elevated level of phospholipase improved the stress signaling under drought conditions in wheat (Singh et al., 2012). Another study suggested that elevated lipase class 3 genes expression levels enhanced the abiotic stress tolerance (Ma and Bohnert, 2007). The overexpression of TaNAC69 TF was shown to improve the drought tolerance of bread wheat (Xue et al., 2011), as well as TaSAP5 might change the reactions to drought stress through the promotion of DRIP (DREB interacting protein) degradation (Zhang et al., 2017). Furthermore, the TaMYBsdu1 gene was discovered to be up-regulated under severe stress in wheat across sensitive and resistant genotypes, suggesting that it is essential to control drought tolerance (Rahaie et al., 2010).

Heat stress and transcriptomics in wheat Heat stress is significant for wheat as wheat seeds germinate at a lower temperature (0–5°C). The stress negatively impacts wheat growth in different ways at different phenological stages. However, a strong negative impact has been recorded during the reproductive stage (terminal heat stress) compared to the vegetative stage. During the grain filling stage, temperature increase declined the grain number and yield (Wollenweber et al., 2003). Indeed, high temperatures influence yield (Wardlaw and Willenbrink, 1994) and grain quality during the postheading phases in wheat (Blumenthal et al., 1995). The capacity of plants to withstand extreme temperatures to grow is called basal temperature. Plants can withstand deadly hightemperature stress if they are pretreated with a modest nonlethal temperature (heat acclimation) or if the temperature is progressively increased to a lethal level (acquired thermotolerance) (Hong et al., 2003). High-temperature stress interrupts and hinders auxin production in reproductive organs, particularly in the anthers, and is linked to increased male sterility and pollen abortion (Sakata et al., 2010). However, little is known about the heat stress changes at the molecular level that influence regulatory and metabolic processes in plants (Junaid et al., 2004). As a result, discovering new genes and analyzing their expression patterns in response to heat stress will give a molecular foundation for increasing heat tolerance in wheat. However, uncontrolled changes to auxin production, signaling, or transport tend to have unfavorable pleiotropic consequences from a biotechnological viewpoint because they are so widespread and essential throughout development. Many processes such as heat shock protein (HSPs) and metabolic enzymes encoding genes triggered physiological processes under heat stress and enhanced tolerance. Molecular chaperones, i.e., Hsp60/Hsp10 and Dnaj/Dnak/NEF (Nucleotide Exchange Factor), convert proteins to active conformations, while Caseinolytic proteases (Clp) play a crucial role in protein aggregation under heat stress. HSG transcription is triggered by conserved heat shock elements (HSEs) in the promoter region. Plant heat shock factors (HSFs) are a large gene family that regulates transcription in response to heat stress (Nover et al., 2001). The HSF family members are poorly researched in wheat, and their involvement as individual members and their roles in heat stress adaptation are not adequately explained yet. Fifty-six multiple copies of HSFs were reported in the wheat (Xue et al., 2014). Hexaploid wheat (Triticum aestivum L.) HSF family structure differs from diploid species. Only two members of the wheat HSF family, HsfA4a and Hsf3 (HsfB2a), have been functionally studied. TaHsfA4a is a cadmium-up-regulated gene that has a role in wheat cadmium tolerance (Shim et al., 2009). Under nonstress conditions, the endosperm is abundant in

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TaHsfA proteins, implying that translational differences between TaHsfA subclasses are minimal. Wheat productivity relies heavily on the endosperm. Some enzymes involved in starch synthesis in various crop species, such as soluble starch synthase from the wheat endosperm by specific genes, are known to be thermolabile (Keeling et al., 1993). Biochemical results revealed that a 15-minute treatment at 30°C significantly reduces the crude extract of soluble starch synthase enzyme activity from the wheat endosperm, and a 2-hour treatment at 25°C results in significant drop-in enzyme activity (Keeling et al., 1993). Similarly, the wheat crop is facing problems in warm-climate regions. Elevated temperature up to 30°C at the grain filling stage causes a considerable drop in grain production and quality in wheat (Skylas et al., 2002). The results suggest that differences in the expression of some critical regulators—TaHsfs—play a role in the genetic variability in Hsp levels and thermotolerance in wheat (Skylas et al., 2002). Another study was done to determine the HSFS functions against heat stress in wheat. Bioinformatic and phylogenetic investigations revealed 56 Tahsf members directly involved in heat stress tolerance in wheat. The results suggested that many TaHsfs were expressed constitutively. Under nonstress conditions, subclass A6 members were primarily found in the endosperm. The transcript levels of A2 and A6 members became the dominant HSFS in response to heat stress, implying that they play an essential regulatory role during heat stress (Xue et al., 2014). Vishwakarma et al. (2018) studied two wheat cultivars (heat-resistant and heat-sensitive) to validate the differential expression of 10 chosen genes under heat stress. The results suggested that an increased GPX gene expression level was observed in heat-sensitive wheat cultivar, representing antioxidants’ role in overcoming heat stress response. Furthermore, it was also recommended that antioxidants enzymes decrease the ROS level (H2O2, O2) under heat stress. The upregulation of ESTs with homology to metallothionein was found elevated, indicating that they play a significant role in heat stress. Also, PPlase expression was recorded maximum at 42°C in wheat (sensitive) cultivar relative to its expression in wheat (tolerant). TaHsp90, a potential gene for producing heat tolerance in agricultural plants or stressinducible promoters, helps improve the breeding processes and transgenic engineering for resilient climate agriculture (Vishwakarma et al., 2018). Earlier research has also suggested that metallothionein has a role in ROS scavenging (Zhu et al., 2010). The enzyme PPIase is made up mainly of the amino acid proline, and it acts as a chaperone for correct protein folding under HS, which is consistent with the results of Goswami et al. (2016). Similarly, Seni et al. (2021) determined that Aegilops speltoides (SS), a diploid B genome progenitor of wheat, represents a possible heat stress tolerance donor. The study compares the entire transcriptome profile of heat-tolerant in Ae. speltoides accession (AS3809) along with tetraploid and hexaploid wheat cultivars (PDW274) and (PBW725), respectively. Across the three wheat transcriptomes study, there was a high degree of consistency in GO terms such as biological, molecular, and cellular processes, implying gene conservation function. In the AS3809 genotype transcriptome data, 12 (HSFs) with the highest FPKM value were discovered, and six of these HSFs, namely, HSFA9, HSFA5, HSFA3, HSFB2a, HSFB2b, and HSFC1b, were verified using qRT PCR. The expression results of these 6 HSFs genes are the evidence of thermotolerance in the wheat (AS3809) genotype. Previous research has demonstrated relevant functions of (HSFs) in wheat under heat stress (Xue et al., 2014; Agarwal and Khurana, 2019; Chauhan et al., 2013). Similarly, TaHSFA2d transcription factor, now known as TaHSFA6b, was cloned for the first time in wheat (Chauhan et al., 2013), and their overexpression results confirmed their thermotolerance function in Arabidopsis. Similarly, another heat stress-based induction of HSFA2 and HSFA6 was reported in wheat (Xue et al., 2014), and the overexpression of TaHSFC2a gene during grain filling in the leaves was provided thermotolerance at the grain-filling stage (Hu et al., 2017).

Cold stress and transcriptomics in wheat Frequent extreme low-temperature events are linked with unpredicted temperature variability. Temperature fluctuation due to climate change affects wheat’s vegetative and reproductive growth, resulting in a loss in yield. Wheat plants activate their cold-tolerant mechanism in response to these changes, including the accumulation of soluble carbohydrates, signaling molecules, and cold tolerance-based gene expression (Hassan et al., 2021). Cold acclimation and the development of a tolerant cultivar against freezing injury need the coordination of several physiological and biochemical changes. Differential expression of numerous genes has a role in these alterations, at least in different parts. Some of these genes produce stress-relieving effector chemicals, while others code for signal transduction proteins or TFs that regulate genes expression (Winfield et al., 2010). Many temperate cereals (spring or winter) types can withstand a certain amount of cold. These genes are activated by the cold or relative dehydration caused by low-temperature injury (Griffith and Yaish, 2004). Transcriptome analysis has revealed many of these cold-regulated genes. Hundreds of transcripts were discovered to be expressed in Arabidopsis under low-temperature stress (Vogel et al., 2005). Several genes were present in temperate (perennial) grasses (Zhang et al., 2009a,b) and ryegrass (Svensson et al., 2006). Monroy et al. (2007) discovered that approximately 450 genes regulate cold tolerance in wheat. Though these genes were activated under low-temperature stress, their role in cold acclimatization has not yet been determined (Tsuda et al., 2000). Several cold-regulated genes

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have been ascribed roles as TFs that operate upstream in cold acclimation or as effector molecules that protect the plant from the possible damaging effects of cold stress (Winfield et al., 2010). The identification of stimulus (sensing) of specific stress, followed by signal perception, transduction, and activation of cold-tolerant gene expression, purely depends upon the plant’s response and reaction under freezing temperature (Ganeshan et al., 2008). A recent study suggested that the inducer of CBF expression (ICE) TFs was discovered to completely control cold tolerance by activating C-repeat binding factors (CBFs). The CBF (TFs) activated cold-regulated (COR) genes by binding to the C-repeat (CRT)/dehydration-receptive area, resulting in increased cold (freezing) tolerance. The CBF transcription factors activated cold-regulated (COR) genes by binding to the C-repeat (CRT)/dehydration-responsive region, resulting in increased cold (freezing) tolerance (Ding et al., 2020). MeJA was involved in regulating vernalization and blooming time in einkorn wheat. Overexpression of another TFs TaAOC1 improves the allene oxide cyclase that enhances the salt tolerance in bread wheat (Movahedi et al., 2015). Due to polyploidy, the transcriptional control of metabolic pathway activity in wheat may be considered as more complex (Powell et al., 2017). In hexaploid wheat, jasmonate pathway-related genes represent a huge gene family and play a tremendous role in the abiotic stress tolerance mechanism (Pearce et al., 2015). Wlip19, an encoding bZIP-type transcription factors homolog, was identified to have its role in response to cold stress (Kobayashi et al., 2008). In wheat, low-temperature-induced Wlip19 expression in seedlings was reported, and freezing tolerance in wheat cultivars has been recorded. Drought and exogenous ABA treatment also stimulated Wlip19 expression. A substantial increase in abiotic stress tolerance, particularly freezing tolerance, was seen when Wlip19 was expressed in tobacco. In wheat callus and tobacco plants, the addition of expression of four wheat Cor/Lea genes, Wdhn13, Wrab17, Wrab18, and Wrab19 suggested that WLIP19 functions as a transcriptional regulator of Cor/Lea genes in helping abiotic stress tolerance in wheat. Furthermore, direct protein-protein interactions were observed among WLIP19 and other bZIP-type TFs in wheat, such as OBF1 ortholog TaOBF1, and suggested that this relationship is conserved across cereals. Zhang et al. (2012) discovered TaMYB56 (on chromosomes 3B and 3D) in wheat under cold stress. TaMYB56-B is likely implicated in plant responses to freezing and salt stressors, according to a detailed characterization of Arabidopsis transgenic plants that overexpressed TaMYB56-B. Another MYB gene, TaMYB3R1, is essential in wheat response to drought, salt, and cold stress. TaNAC2 was implicated in drought, salt, cold, and ABA treatment, and these results were confirmed during the gene expression profiling study by Xue et al. (2006). Dehydrin (DHN), late embryogenesis abundance (LEA), cold-responsive (COR), and response to abscisic acid (RBA) are just a few of the cold-responsive genes discovered in wheat (Guo et al., 2019). These genes are divided into two groups (Seki et al., 2003), one that responds directly to low-temperature stress, such as LEA (Liu et al., 2019), and another that directly controls cold tolerance expressions. These proteins have several roles in response to cold stress and are directly engaged in coping with other abiotic stresses like drought and salinity (Seki et al., 2003). Multiple genes are expressed during cold tolerance and start a cascade of transcriptional, metabolic, and physiological activities at the cellular level in wheat (Kosova´ et al., 2008). ABA-dependent signaling activates ABA TFs under cold stress conditions. Different TFs such as MYC/MYB, RD22BPI, AREB1, and DREB2A are directly involved in the activation and expression of these TFs linked with ABA under cold stress conditions in wheat crops (Tuteja, 2007a; Morran et al., 2011). Similarly, MYB/ MYC (myeloblasts) TFs are also required for the ABA-dependent pathway (Abe et al., 2003). Fifteen of wheat’s 60 MYB genes have been identified that worked as ABA-regulated genes (Zhang et al., 2012), including TaMYB33, and were involved in the antioxidant synthesis, ROS scavenging, proline accumulation, and osmotic balance (Qin et al., 2012). Another study suggested that CBF TFs (CBF1, CBF2, and CBF3) are the major regulators of COR gene expression (Thomashow, 2001). CBF has been linked to a variety of signaling pathways in wheat and increased cold tolerance mechanism (Morran et al., 2011). COR expression and wheat cold acclimation strongly connect to cold acclimatization (Va´gu´jfalvi et al., 2003). Fowler et al. (2001) suggested that WCS120 is a cold-responsive gene present in wheat. Some other genes (WCS180, WCS200, WCS66, and WCS40) were also involved in cold tolerance (Sarhan et al., 1997).

Nutrient’s stress and transcriptomics in wheat The nutrient deficiency or toxicity also leads to decreased crop biomass and yield worldwide. Many TFs have been identified recently that are known to modulate the expression of genes involved in root development and uptake of P and N (Zhang et al., 2014a,b). Various mechanisms mediate the complex gene networks, controlling N intake, assimilation, remobilization, and storage (McAllister et al., 2012). Increased fertilizer consumption has resulted in inefficient fertilizer use and environmental issues. Finding nutrient-efficient genes will make it easier and facilitate fertilizer use for wheat growth more efficiently. Furthermore, microRNAs play an essential role in N and P signaling (Fischer et al., 2013; Zeng et al., 2014), and some microRNAs are regulated by both N and P supply levels (Chiou et al., 2006; Pant et al., 2009). The miR169 has a

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positive role in inducing N and P signaling and targets the NFYAs TFs for modulating the N and P utilization in wheat crops (Qu et al., 2015). Genome-wide analysis of nuclear factor Y (NFY) genes was done in wheat to determine the phosphorus and nitrogen response availability in the seedling. The results reported 18 NFYAs, 34 NFYBs, and 28 NFYCs were discovered using sequence mining and gene cloning. The overexpression results of NFYAs were significantly recorded at low P and N availability. Overexpressing of TaNFYA-B1 accelerated root development and up-regulated the expression of both N and P transports in the roots, which may have resulted in higher N and P intake (Qu et al., 2015). A wheat PHR1 homolog (TaPHR1) was used to induce lateral branching, improve P absorption and grain production, and upregulate a subset of Pi starvation response genes (Wang et al., 2013). Wheat is a significant food and cereal crop that has been genetically modified to increase grain micronutrient content, particularly iron and zinc contents. Modulating the expression of plant transporters involved in Fe and Zn homeostasis has proven to be a promising approach in this direction. Many studies were reported for wheat transporters used for zincinduced facilitator (ZIFL) family genes regulating nutrient contents in the wheat. The transcriptional expression response of the wheat ZIFL genes was studied in relation to micronutrient fluctuations and heavy metal exposure (Sharma et al., 2019). The presence of excess Zn or a Fe deficiency increases the abundance of multiple membrane proteins (Briat et al., 2015). Generation of Zn responsive genes could also be a key step in limiting the nonspecific transport activity of transporters that are primarily induced for Fe deficiency under Fe limiting conditions. The response of ZIFL to the presence of excess Zn is well known (Haydon and Cobbett, 2007). Overexpression results of ZIFL, i.e., (1.1, 1.2, 4.2, and 6.2) TaZIFL, were concerned by Fe and Zn in the shoot and root region. A study was conducted to determine that the expression of ZIFL genes was checked in wheat cultivars using RNA-seq expression analysis of Fe insufficiency in roots for 20 days exposure. TaZIFL4.1 and TaZIFL4.2 are most expressed in the late stages of Fe deficiency (Kaur et al., 2019). These findings suggest that only a few ZIFL genes are involved in the overlapping Ferris and Zinc modulation pathways. Grain protein contents (GPC) (Zn, Fe) and Mn concentrations (GZnC, GFeC, and GMnC) in wheat are all influenced by the wild emmer gene Gpc-B1, which belongs to the NAC-domain TF (Distelfeld et al., 2007). The study also recorded that GPC gene has been linked to decrease the grain weight and yield in different wheat cultivars under different environments (Brevis and Dubcovsky, 2010; Tabbita et al., 2013). In cereals, tolerance to boron (B) toxicity has been linked to lower B concentration in tissue accumulation. Genes were cloned from the roots of B-tolerant wheat cultivar with high similarity previously reported B efflux transporters from Arabidopsis and rice. The results suggested that the ability of tolerant genotypes to lower the concentration of B in roots was strongly correlated with the expression of these genes (Reid, 2007). Another study was investigated the molecular basis of wheat, maize, and rice for low B tolerance. For that purpose, quantitative real-time (qPCR) polymerase chain reaction was used for expression of BOR1-like genes and efflux-type B transporters determined at transcript levels and compared in different organs between B-efficient and B-inefficient genotypes. Some of the important transcripts and genes functions under abiotic stress were revealed (Table 1). The findings revealed that the transcript levels of BOR1-like genes differ between the two genotypes (Leaungthitikanchana et al., 2014).

TABLE 1 Important transcription factors (TFs) used in wheat crop under different abiotic stress conditions. Stress Salinity

TFs

Function

Expression

References +

+

Betaine aldehyde dehydrogenase (BADH)

Osmotic and salinity tolerance

Regulate Na and K ratio

Li et al. (2019)

NAC (TFs)

Salinity tolerance

Root hairs management

Zhang et al. (2016)

MYB TF, AtMYB33

Salinity tolerance

Zhang et al. (2016)

TaRSL4

Salinity tolerance

Zhang et al. (2016)

TaWRKY10, WRKY1, and WRKY2

Salinity tolerance

Leaf senescence

Wu et al. (2008)

TaMYBsdu1

Salinity tolerance

Leaf senescence

Rahaie et al. (2010)

TaMYB1

Salinity tolerance

Mott and Wang (2012)

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TABLE 1 Important transcription factors (TFs) used in wheat crop under different abiotic stress conditions—cont’d Stress

Drought

TFs

Function

Expression

References

CaM-binding TFs

Salinity management

Root and leaves growth

Amirbakhtiar et al. (2021)

TaMYB32

Salinity tolerance

Root, stem, leaf, and pistil

Zhang et al. (2009a,b)

TaZFP42

Drought

Storage protein synthesis

Kam et al. (2008)

ABA-regulated pathways

Kam et al. (2008)

Germination and senescence

Ali et al. (2020)

Transcriptional activator and root cellular functions

Xia et al. (2010)

TaZFP15 WRKY

Drought

TaNAC 8

Heat stress

Cold stress

Nutrient stress

TaNAC 69

Drought resistance

Water use efficiency

Rahaie et al. (2013)

Thiol protease gene

Drought resistance

Water regulation from root area

Kumar et al. (2018)

DREB-interacting protein

Drought resistance

Water regulation from root area

Zhang et al. (2017)

HsfA4a and Hsf3 (HsfB2a)

Resistance against heat stress

Starch synthase from the wheat endosperm

Shim et al. (2009)

TaHsfs

Thermotolerance

Thermotolerance regulators

Skylas et al. (2002)

GPX gene

Thermotolerance

Antioxidant’s role in heat stress

Vishwakarma et al. (2018)

HSFA3, HSFA5, HSFA9, HSFB2a, HSFB2b, and HSFC1b

Thermotolerance

Seni et al. (2021)

TaHSFA6b

Thermotolerance

Xue et al. (2014)

TaHSFC2a

Thermotolerance

Grain filling

MeJA

Cold tolerance

Regulation of vernalization and blooming time

TaAOC1

Cold tolerance

Wlip19, Wdhn13, Wrab17, Wrab18, and Wrab19

Cold stress tolerance

Exogenous ABA

Kobayashi et al. (2008)

TaMYB56-B

Freezing tolerance

Regulate ABA

Zhang et al. (2012)

TaNAC2

Freezing tolerance

Xue et al. (2006)

WCS180, WCS200, WCS66, and WCS40

Cold acclimation

Va´gu´jfalvi et al. (2003)

Zinc-induced facilitator (ZIFL)

Nutrients management

Fe and Zn homeostasis

Sharma et al. (2019)

TaZIFL

Nutrients management

Fe and Zn in the shoot and root region

Haydon and Cobbett (2007)

TaZIFL4.1 and TaZIFL4.2

Fe root deficiency

Overexpression enhanced the Fe contents in the root

Kaur et al. (2019)

Gpc-B1, linked with NAC domain

Nutrient’s deficiency

Grain protein management

Tabbita et al. (2013)

BOR1-like genes

B deficiency

Hu et al. (2017)

Movahedi et al. (2015)

Leaungthitikanchana et al. (2014)

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Abiotic stresses in wheat

Future concerns Transcriptome technology can swiftly anticipate important stress defense components and reveal the link between stressresponsive genes, signal perception and transduction, metabolic pathways, and defense response that are significant for enhancing tolerance and understanding the plant stress resistance mechanism. Plants respond under specific conditions (abiotic stress) via cellular complex, physiological, metabolic networks, and molecular processes. Recent progress has been made in discovering putative abiotic stress tolerance-related genes. Cloning of several genes linked to the abiotic stress tolerance and the gradual unraveling of their molecular processes has enhanced our understanding of these genes that help to figure out their involvement in different pathways for enhancing the stress tolerance mechanisms. Furthermore, plants have evolved adaptable molecular and cellular response mechanisms to respond under various abiotic stresses, as evidenced by the discovery of several TFs and other regulatory genes involved in stress responses. Information about the regulatory networks, coding, and noncoding protein provides deep insight into stress-responsive genes and their role in adaptive stress-tolerant wheat genotypes under specific conditions. This data will also help understanding the metabolic, physiological, and cellular systems involved in such activities. To date, several abiotic stressresponsive transcription factor genes have been examined in wheat. Furthermore, the discovery of putative RNA-binding protein, transcriptional regulatory cascade genes would help to enhance the abiotic stress tolerance in wheat. Understanding the unique and comprehensive information of signal perception and transduction signals in the form of the transcriptome (transcription factors) associated with condition-specific metabolic pathways is of prime importance for wheat research and identifying potential new genes (over-or-under expression) would facilitate the wheat-breeding programs. In the future, we will increasingly use a systems biology approach that includes reverse genetics, functional genomics, proteomics, and metabolomics to elucidate the function of the various stress-responsive TFs and their association in transcriptional control in wheat during various developmental stages and stress conditions. Moreover, abiotic stress tolerance and agronomic characters of transgenic wheat using stress-responsive TFs genes should be tested under stressed field conditions in the coming years. To fully utilize the potential of transcriptome studies, it will be necessary to clarify the differential function of individual stress-responsive TF genes from different families of TFs for the control of abiotic stress and other biological processes such as biotic stress tolerance, growth regulation, senescence, and yield.

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Chapter 15

Patterns of protein expression in wheat under stress conditions and its identification by proteomics tools Yamini Agrawala, Disha Agarwala, Ashal Ilyasb, Shreya Sharmab, Aneta Myskovac, and Nitesh Kumar Poddara,⁎ a

Department of Biosciences, Manipal University Jaipur, Jaipur, Rajasthan, India, b Department of Biotechnology, Invertis University, Bareilly, Uttar

Pradesh, India, c Department of Analytical Chemistry, University of Chemistry & Technology Prague, Prague, Czech Republic *

Corresponding author. e-mail: [email protected]

Introduction Wheat is a grass that is commonly farmed for its seed, a cereal grain that is consumed all over the world (Dupont et al., 2011; Shewry, 2009). It is the primary component of the meal, accounting for nearly 20%–25% of the calories ingested by the people. The genus Triticum has several wheat species, the most frequently grown of which being common wheat (Triticum aestivum). Wheat was initially farmed in the Fertile Crescent during 9600 BCE, according to archeological evidence. Nowadays, the demand of wheat has increased due to gluten proteins, distinctiveness, and its viscoelastic and adhesion qualities that assisted the creation of different varieties of resultant products, whose consumption is expanding as a result of global industrialization and diet modernization (Uthayakumaran and Wrigley, 2017). To increase the amount of gluten proteins, various hybrids of wheat varieties have been produced. Due to the self-pollinating property of wheat, producing of hybrid seed is exceedingly labor-intensive, and after over 90 years of work, the increased cost of cross-breed wheat seed as compared to its intermediate advantages has prevented farmers from widely adopting it (Dupont et al., 2011; Calanca, 2017; Bindraban et al., 2009). Every organism must adjust according to the different stressful conditions that may be because of the environment or due to many different microorganisms, to sustain life. (Rabbani and Choi, 2018). A stress in a plant is an external circumstance that can impair its growth, maturation, or production. Physiological strain generally involves abrupt changes in environmental variables that alter gene expression, metabolism in cells, growth rates, agricultural yields, and other factors. Plants respond to stress in a variety of ways. Plant stress may be classified into two parts: biotic stress and abiotic stress. (Agarwal et al., 2006). Unfavorable stress conditions such as temperature, drought, salt, shortage of essential nutrition, heavy metals, radiations, chemical toxins, and oxidative stress are among environmental factors that threaten agriculture. Water is the most common and among the prime abiotic elements that affect wheat generation in the global environment (Calanca, 2017). Salt stress intensifies all morphological and physiological stages of wheat (Belderok et al., 2000), reducing the number of viable tillers (Munns and Tester, 2008), spikelet quantity (Abbas et al., 2013), and kernel weight (Munns and Tester, 2008), and negatively affecting grain output (Frank et al., 1987). In the salt-stress condition, the yield of wheat was found to be lowered by 45% (Sorour et al., 2019). These adverse conditions result in lowering down the plant’s metabolic activity, adversely affecting the growth of the plant. The biotic pressure differs largely from the environmental stresses, which are due to nonliving factors such as sunshine, salinity, cold, temperature, floods, and the dry season, all of which enforce a lethal effect on crop yield. The environment in which the yield occurs determines the type of biotic pressure that may be applied to crop plants as well as the harvest species’ ability to withstand that stress (Sharma et al., 2014). Photosynthesis is influenced by a variety of biotic loads, such as biting pests that reduce leaf area and virus contaminations that slow photosynthesis per leaf region. Abiotic stressors for example due to water stress such as drought and water logging or overwatering, temperature effect (cold, heat, and ice), saline stress, and toxicity due to mineral excess all influence the maturation, progress, production, and seed nature of harvest (Li et al., 2014) (Table 2). The stress conditions have a significant influence on agriculture crops, reducing average yields by more than half (Shewry, 2009). The change in the types of proteins expressed normally or under the stress condition can be identified Abiotic Stresses in Wheat. https://doi.org/10.1016/B978-0-323-95368-9.00026-6 Copyright © 2023 Elsevier Inc. All rights reserved.

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using proteomics. The goal is to develop plants that are water stress-tolerant and function simultaneously by discovering or changing the pathways which come into effect when the supply of water is in excess or reduced (Cattivelli et al., 2008). Proteomics is a useful method for gaining deep knowledge of the events at the molecular level that occurs during grain formation (Timperio et al., 2008). Proteomic techniques such as 2D gel electrophoresis and mass spectrometry have been widely applied in wheat and barley during the last decade to explore grain growth under different environmental stress conditions also known as the abiotic strain (Calanca, 2017) (Rollins et al., 2013). In the latter part of the chapter, a brief discussion about the abiotic stress conditions is done to give some recap about the various abiotic stresses which have a severe effect on the plant growth as well as various metabolic activities and proteomics of the plant. In this chapter, emphasis is laid on the abiotic stresses; however, biotic stresses are also discussed to some extent.

Biotic and abiotic stresses in plants Stress caused by cold Low temperature has become the primary abiotic stress that reduces the value of rural crops by affecting the character of harvests and their life after the harvest. Plants that are fixed in environment are always concerned with adjusting their systems to avoid such stresses. Plants are exposed to chilling and freezing temperatures under certain circumstances, which are extremely dangerous to them as pressure (Choudhary et al., 2016). Plants develop chilling and freezing tolerance against such fatal conditions through a process known as acclimation. Regardless, many substantial yields are still stumbling through the cold adaption process (Hassan et al., 2021). In each case, the cold which is an abiotic stress has an impact on the cell components of plants (Fig. 1). These stress response signals are transmitted by a number of signaling pathways such as reactive oxygen species pathway, protein kinase cascade, protein phosphate mediated pathway, ABA signaling cascade, and Ca2+ pathways.

Stress caused in drought conditions The continual expansion of temperature and barometric CO2 levels in today’s atmosphere has flipped the world upside down. The distribution of precipitation is skewed due to environmental changes, which act as a strong pressure on course Triggers signaling

Environmental Stress PLASMA MEMBRANE

Changes in membrane and membrane proteins composition

Activation of transport of protective and signaling compounds from cell

Stress perception

Protein Degradation

Cascade of signals

ROS formation

Changes in gene expression

Alteration in protein biosynthesis Changes in energy metabolism

Stress Response Biosynthesis of stress related proteins

Respiration-ATP, NADPH, ROS

Sugar catabolism

PhotosynthesisSugars, ROS

FIG. 1 A simplistic model of a plant cell’s reaction to stimuli, which includes signaling sequence activation, gene expression changes, protein biosynthetic pathway and degradation activation, and significant impact on energy metabolism, including increased biosynthesis of ATP and synthesis of ROS in mitochondria and chloroplasts, results in reactive oxygen species-induced signaling (RS). Alteration in synthesis of proteins results in increased synthesis of proteinaceous and nonproteinaceous stress-tolerant compounds, such as reactive oxygen species (ROS) scavenging enzymes and metabolites, which function in a plant’s effective stress acclimatization response, which includes a feedback-mediated stress-induced signaling, gene, and mechanism for expression of proteins.

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with dry season. Due to excessive dry season circumstances, soil water available to plants expands on a regular basis, causing plants to die prematurely. The predominant response effect on agricultural plants during the latter dry season is development arrest (Siddique et al., 2000). During a dry season, plants slow down the production of new branches and reduce their metabolic demands. Plants arrange defense combinations later during a dry spell by activating metabolites required for osmotic change (Fig. 1).

Stress caused by heat Temperature rises throughout the world have become a major worry, affecting plant growth and efficiency, notably in agricultural harvests. As a result of heat stress plants undergo decreased seed germination, photosynthetic productivity, and yield. The capability of tapetal cells is reduced under heat pressure during the regenerative development time frame, and the anther becomes dysplastic (Akter and Rafiqul Islam, 2017). Proceeding forward to the next section of the chapter, the main emphasis is on the impact of the various abiotic stresses caused on different varieties on wheat and studying the various protein expressions in the different wheat plant in response to stresses (Fig. 1).

Stress caused by presence of excessive salt Salt stress is a worldwide issue and threat to global horticulture by decreasing harvest yields and, eventually, yield usefulness in the salt-affected areas. In a variety of ways, salt pressure reduces the maturation of crops and yield. Salt pressure has two important effects on agricultural plants: osmotic pressure and particle. Because there is more salt in the soil arrangement, the osmotic tension in soil exceeds the osmotic tension in plant cells, limiting the capacity of plants absorbing water and minerals like potassium and calcium. These basic effects of salt stress result in auxiliary impact such as reducing expansion of cell and layer work and reduced cytosolic digestion (Vanisree et al., 2022).

Various conditions leading to stress in wheat There are varieties of condition which acts as stress affecting the wheat plant proteomics and they are discussed below:

Alterations in wheat proteome composition as a result of salt stress Salinity strain influences more than 25% of land which can be used in agricultural process, and it is gradually developing due to weather extrude and industrialization. Salt stress intensifies all morphological and physiological stages of wheat (Ali et al., 2009), reducing the number of viable tillers (Levitt, 1980), spikelet quantity (Munns and Tester, 2008), and kernel weight (Munns and Tester, 2008), and negatively affecting grain output (Frank et al., 1987). In salt-stressed wheat, for example, yield reductions of up to 45% have been reported (Sorour et al., 2019). It also affects activity, germination, and yield quality. However, protein amount increases in wheat and triticale in saline conditions but protein quality decreases. The beta-carotene content of grains decreased dramatically in wheat varieties in saline conditions. Despite the fact that there is a significant link between resistance to stress and integration of proline in plants of higher level, but this connecting link may not be global (Lassalle, 2021). Proline is extensively distributed in higher plants and is generally accumulated in considerable amounts in saline conditions to safeguard the plant cell by regulating the osmosis process of the cytosol with that of the vacuole and the physical factors (Parvaiz and Satyawati, 2008) (Tables 1 and 2). Soluble proteins have been shown to rise in certain plants and decrease in others when salt level increases (Frank et al., 1987; Sorour et al., 2019). Salinity also inhibits certain proteins which are involved in shoot synthesis. Peroxiredoxin (2Cys) is an antioxidant enzyme found in salt-stressed seedling roots and shoots (Uniprot). The expression level of WRS15 was raised in SR3 wheat roots subjected to high salt concentration because peptide transcribed by WRS15 (myb-transcription factor) has a Bowman Birk domain with a higher degree of sequence (Kamal et al., 2010). Further experiments performed on various parts of the wheat plant for proteomics analysis in T. aestivum revealed reduction in the activity of Ribulose bisphosphate carboxylase oxygenase (RUBISCO) enzyme in the choloroplast when subjected to high salt concentration. Catalase (CAT), a well-known enzyme known for its antioxidant properties, was reported to have elevated levels in the chloroplast of the wheat affected by the salt stress (Sorour et al., 2019). Along with CAT, in chloroplasts of wheat, a-b binding proteins present in chlorophyll (CAB) were also altered irregularly under saline stress. Another chloroplasts protein, ATP synthase—dimer of two proteins namely the F1 sector and Fo sector, was found to

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TABLE 1 Studies conducted on the five wheat species, namely, Kukri, Excalibur, RAC875, Janz, and Kaunz inferred the following results. Wheat species

Survival

Number of proteins affected

Proteins affected

Metabolic activities affected

Excalibur

Tolerant

206

A type II metacaspase which is arginine-, lysine-, and cysteine-dependent

Programmed cell death

Ford et al. (2011) and Szegletes et al. (2000))

RAC875

Tolerant

177

Leucine aminopeptidase

N-terminal amino acid hydrolysis of proteins

Szegletes et al. (2000)

Kukri

Intolerant

168

Cytoplasmic cysteine synthase decreases

–

Ford et al. (2011)

Janz

Intolerant

–

ADP dependent glucose pyrophosphorylase,in combination with ascorbate peroxidase (APX) and G beta-like protein, found to be decreased

Photosynthesis

Komatsu et al. (2014)

Kaunz

Tolerant

–

WD40 repeat protein, late embryogenesis subunit (LEA), and alpha-amylase inhibitors showed more abundances in Kauz

Carbohydrate metabolism

Howell (2016)

Reference

be structurally altered due to saline stress. On analysis, it was deduced that excessive salt concentration led to alterations in α and β components of F1 sector of enzyme rendering it functionally inactive (Ali et al., 2009; Levitt, 1980; Parvaiz and Satyawati, 2008). In bread wheat chloroplasts, proteins which resemble the germin were continuously modified, but it was found elevated later under high saline conditions in bread wheat (Ali et al., 2009). Under salt stress, malate dehydrogenase (MDH) levels in wheat decreased (Ali et al., 2009). Other proteins such as ATPases—essential transport proteins linking ATP hydrolysis with proton migration across a membrane potential—are also known to hinder the mechanism of the plant under the saline conditions by varying the potential gradient (Levitt, 1980). In reaction to salt application, carbonic anhydrase was similarly elevated in wheat (Kamal et al., 2010). In saltstressed wheat chloroplasts, ferredoxin-NADP reductase and NADPH-quinone oxidoreductase also increased, a reaction that was previously seen in tomato leaves (Li et al., 2013) (Tables 1 and 2).

Stress on wheat seedlings due to drought conditions Abiotic stress drought is among the most frequent challenges which plants face as they grow and develop. It brings change in protein, production of antioxidants, adjustment in osmosis, composition of hormones, extension and depth of roots, stomatal closing and opening, thickness of cuticle and inhibition of photosynthesis (Agastian et al., 2000; Nishikawa et al., 2009). Some genes, such as dehydrins (Kamal et al., 2012), vacuolar acid invertase (Palmgren and Harper, 1999), glutathione S-transferase (GST) (Hacisalihoglu et al., 2003), and late embryo abundant (LEA) protein (Ford et al., 2011), are identified to be drought-affected as it produces proteins and enzymes in relation to drought; ABA genes expression and synthesis of proteins like RAB G-protein (member of the Ras superfamily), rubisco, helicase, proline, and carbohydrates are drought-tolerant. Plants change their gene expression and protein synthesis in response to stressful situations. The amount of knowledge known on drought-responsive genes, on the other hand, is still restricted since their functions have yet to be fully defined. The HVA1 gene produces a protein that belongs to the LEA group and includes 11 amino acid motifs in nine repetitions. Proline is an important protein that has a role in water stress tolerance. It is made from pyrroline5-carboxylate synthetase, or P5CR, and the gene responsible for the enzyme is identified in several crops, including petunia, soybean, and tobacco (Szegletes et al., 2000; Yordanov et al., 2000; Close, 1996). This data is the case study conducted on T. aestivum (Tables 1 and 2).

TABLE 2 Types of abiotic stresses on different wheat species and their impact. Abiotic factors(stress)

Part of the plant used

Variety

Waterlogging and hypoxia

Root

Waterlogging and hypoxia

Protein which was affected due to stress conditions and spring

Metabolic pathways affected

Functions

Destination

References

Shiroganegomugi

Carbohydrate (glycolysis)

Endothelial cell metabolism (EnMet) and protein metabolism

Cell wall

Holappa and WalkerSimmons (1995)

Seminal root

Bobwhite line SH 9826

Antioxidant defense

Phosphoinositide signaltransducing system

–

Haque et al. (2011)

Drought

Leaf

Ofanto

Carbohydrate catabolism (glycolysis, gluconeogenesis)

Protein transcript ratio (PTR)

–

Huo et al. (2004)

Drought

Root

Opata, Nesser

Metabolism of energy

Oxidoreductase and transduction

Found in cytoplasm, cell wall, mitonucleoplast, and vacuoles

Lee et al. (2007)

Drought

Chloroplast

Keumkang

Photosynthesis

–

Found in chlorophyll

Ali et al. (2009)

Drought

Chloroplast

Katya, Sadovo, ZlatitizaMiziya

Photosynthesis

–

Found in chlorophyll

Ali et al. (2009)

Drought

Leaf

Kukri, Excalibur, RAC87

Photosynthesis

Photosyntheis and proteinE

–

Ford et al. (2011)

Drought

Seed

JanzKauz

Carbohydrate metabolism

Carbohydrate metabolism and signal transduction

–

Jiang et al. (2012)

Heat and drought

Kernel

Vincent

Glycolysis

Carbohydrate metabolism

–

Ford et al. (2011)

Heat stress

Seed

Butte 86

Carbohydrate metabolism

Carbohydrate metabolism, nitrogen protein metabolism, and signal transduction

–

Levitt (1980)

Saline

Leaf

Zhengmai 9023

Carbohydrate metabolism

Carbohydrate metabolism and ATP

–

Huo et al. (2004) and Caruso et al. (2008)

Saline

Shoot

WyalkatchemJanz

–

–

Found in mitochondria

Jacoby et al. (2013)

Saline

Cholorplast

Keumkang

Photosynthesis

Photosynthesis

Chlorophyll

Kamal et al. (2012)

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Some plant proteins, such as late embryogenesis abundant (LEA), can be highly expressed when seeds are desiccated under drought stress and stored in vegetative tissues. Wheat’s Em gene, which codes for the first group of LEA proteins, has been extensively studied (Trouverie et al., 2003; Anderson and Davis, 2004; Pnueli et al., 2002). They also discovered that DREB proteins are abundant and significantly increased in root tissue rather than leaf tissue in response to drought. The study was conducted on wheat species of ageilops. This species has the highest ratio of genes which confers resistance to the abiotic stress conditions of drought (Table 1). The study mainly focuses on the proteins, namely, gliadin (Gli), glutenin (Glu), and their concentration in the drought. Protein and total pentosans content rose in the addition lines as a result of the stress, but β-glucan content reduced in many of the addition lines (Howell, 2016) (Table 1). The proteome study of wheat grains using linear and nonlinear 2-DE and MALDI-TOF MS indicated that in the variety Janz which is a sensitive to drought, both the large and small subunits of ADP-glucose pyrophosphorylase, as well as ascorbate peroxidase (APX) and G beta-like protein, found to be decreased, whereas the enzyme level in the kauz which is a drought-resistance variety of wheat did not displayed any important variations in reflex to strain of drought (Komatsu et al., 2014). The study is still going on in different varieties of wheat by replicating the drought conditions in the laboratories.

Impact of heat stress on wheat protein expression and calcium metabolism Heat and cold stresses are the main stress that any plant faces. Every plant responds to it in a different manner and some responses of wheat varieties are discussed here (Table 2). A comparative study of protein expression patterns in wheat cultivars was done which are heat-sensitive and heattolerant. In this study, 48 proteins were found to be differentially expressed, with 17 of them being heat shock proteins (Majoul et al., 2003; Xu et al., 2013). These results are supporting the findings of Majoul et al. (2003, 2004); he discovered 25 proteins that were differently expressed in response to heat shock, 24 were shown upregulation, and only one was under downregulation. Some of these enzymes were functional in various plant metabolisms, such as granule-bound starch synthase and glucose-1-phosphate adenyltransferase (both involved in starch synthesis), amylase (involved in carbohydrate metabolism), and the ATP synthase chain. In both flora and fauna, calcium is a universal chemical, and the transitory rise in Ca2+ level under heat stress is widely established in plants. Heat shock causes cytosolic Ca2+ bursts that are transduced by Ca2+ binding proteins (CBP) such calmodin (CaM), calcineurin (CBL), and annexin, which then help regulate the assembly of HSPs (Majoul et al., 2003). Short-term heat shock increases thioredoxin and ascorbate peroxidase levels more than longterm heat treatments (Gubisˇ et al., 2007). Tubulin proteins are linked to GTP binding proteins, which help plants withstand heat (Gubisˇ et al., 2007). Proteins such as serine carboxypeptidase, glucose-1-phosphate, glucose-6-phosphate, and Sadenosylmethionone synthetase have also been discovered.

Wheat responses to cold stress at morphological and physiological levels From cold-acclimated wheat, many cold-responsive genes with unknown functions were discovered (Ouellet et al., 1993). WCSP1 (cold shock protein 1) expression was specific to cold, since it was not stimulated by drought, salt, or heat stress (Litts et al., 1987). Biosynthesis is required for the resistance to freezing, and various different proteins integrate because of expression changes in the genes during cold exposure (Marcotte et al., 1988) (Table 2). ABA (abscisic acid) seems to have a key function in boosting wheat’s freezing resistance, which is impacted by water scarcity ( Jiang et al., 2012). Cyclophilin, aquaporin, and chitinase all play a significant role in the elevation of cold stress in wheat (Hawkesford and Lorence, 2016). In wheat seedlings, the impact of dehydrated conditions, low-temperature treatment, stress condition like osmotic and salt on the expression of an abscisic acid-responsive protein kinase mRNA (PKABA1) was investigated (Qin et al., 2008). When plants were exposed to low temperatures, three protein kinases, MAPKKK, MAPK, and homologue of ribosomal kinase, rose dramatically and concurrently (Breton et al., 2003). The progression of AP1 transcription corresponded to the progression of vernalization’s influence on flowering time (Karlson et al., 2002). From wild variety of wheat (Triticum urartu L.), samples were collected and submitted to proteome pattern analysis after 4 weeks of cold acclimation (4–6°C) and possible treatments for 12 h at 2°C. 34 proteins altered considerably in abundance in response to cold stress among the approximately 450 replicable protein spots exhibited in each 2-DE gel. Under stress, 25 and 9 proteins were increased and diminished, correspondingly (Gharechahi et al., 2014).

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Changes of protein profiles in two cultivars during hypoxia and water logging stress condition One of the key variables affecting wheat growth, especially at the seedling stage, is a lack of oxygen owing to waterlogging or flooding (Guy, 1999). Wheat genotypes differ in their waterlogging tolerance. In an experiment employed to detect the protein expression in hypoxia sensitive and tolerant wheat plants, it showed that both the growth and molecular responses of the two cultivars employed in this investigation to hypoxic stress were considerably different, supporting CIGM90.863SH64’s better resistance to waterlogging (Li et al., 2014; Xu et al., 2007, 2013); when compared to the sensitive cultivar, the tolerant cultivar showed less alterations in protein expression patterns under hypoxic stress (Table 2). An experiment was performed on different wheat species, for example, Shiroganekomug and Bobwhiteline SH 9826, which showed similar effects. Proteins found in high abundance in cell walls after flooding are believed to be defense- and disease-responsive proteins and they are the most affected ones, namely, methionine synthase, β-1,3-glucanase, β-galactosidase, and βglucosidase. A critical role is played by methionine synthase in the synthesis of methionine which is crucial for the growth of plant (Houde et al., 2006). In addition to β-1,3-glucanases, β-galactosidase, and β-glucosidase, another glycosyl hydrolase is responsible for the alterations in polysaccharides present in the cell wall (Holappa and Walker-Simmons, 1995). The reduction in such proteins shows that wheat seedlings react to overwatering stress by limiting cell development so that it may conserve energy. Proteins of cell wall appear to initiate a vital role in flooding stress adaptation in wheat by coordinating methionine absorption and hydrolysis of cell wall (Holappa and Walker-Simmons, 1995). These studies were conducted on the number of wheat species such as T. aestivum L., bread wheat, and spring wheat (Houde et al., 2006) (Tables 1 and 2). Another result confirmed that the wheat root proteins such as ADP-ribosylation factor 1 were increased. It is known that ADP-ribosylation factor 1 contributes to vesicular trafficking and phospholipase D induction (Zhang et al., 2009). Also the ubiquitin-conjugating enzyme spm2, which targets proteins for destruction in proteasomes with the help of the pathway of ubiquitin action, was similarly elevated in wheat seminal roots (Yan et al., 2003). Protein involved in pathogenesis in wheat roots, TaBWPR-1.2, has also been linked to flooding stress-response proteins. Rice blast fungal infection and different abiotic stressors, such as drought and salt, raise the homologous gene function, which is expressed specifically in roots. The presence of this protein in wheat seminal roots implies that it plays a role in behavioral mechanisms to hypoxic circumstances (Zhu et al., 2018; Zeng et al., 2014).

Other effects of stress on wheat physiology and metabolism Biotic and abiotic stresses both cause primary changes in the proteome of a plant, which aid in the adaptation of catabolism and anabolism to the changing environment and the improvement in the resistance to the stress by plant. The ability of plants to respond to stress is a dynamic process which may be categorized, each having its own proteome composition (Ali et al., 2009; Memon, 2004) (Table 2). An alarm stage, an acclimatization stage, a resistive stage, an exhaustion stage when strain is too strong or remains for longer time, and a recovery stage once the stress element is removed, all these may be identified as the stages stress response (Munns and Tester, 2008; Abbas et al., 2013; Memon, 2004). The vast majority of proteomic research on plant response to stress is relative studies based on proteome makeup comparisons in stressed versus control plants, and also stress-tolerance genotypes. Copper- and water-stressed wheat showed an increase in proteins as well as translationally controlled tumor protein homologs (Nandi et al., 2006; Qu et al., 2006; Haque et al., 2011; Caruso et al., 2008), and also affects functioning of the G protein which is a heterotrimeric β subunit that gives genotype specific responses (Huo et al., 2004). Almost all stresses cause an increase in the relative richness of carbohydrate catabolism enzymes such as glycolysis (glyceraldehyde-3-phosphate dehydrogenase GAPDH, triosephosphate isomerase TPI, enolase ENO) and Krebs cycle (mitochondrial NAD +-dependent malate dehydrogenase (Alvarez et al., 2014) and components of mitochondrial ATP-synthase, namely, β subunit of CF1 complex) (Larcher, 2003; Lott et al., 2013; Kang et al., 2012; Ghabooli et al., 2013) (Table 2). Concentration of several proteins involved in the photosynthetic process has been reportedly changed depending on the intensity of stress (Souid et al., 2016; Peng et al., 2009). A decrease in D1 and D2 proteins in the photosystem II reaction center (RC PSII), low concentrations of proteins of the oxygen evolving complex (OEC), a decrease in chlorophyll a-b binding proteins in both photosystems (PS) I and II, a decrease in the Fe-S complex in PSI, a downregulation of RubisCO, and key Calvin cycle enzymes phosphoglycerate kinase and phosphoribulokinase was found in the wheat plant which was experiencing cold and water logging condition (Vı´ta´mva´s et al., 2012) and in salt-treated durum wheat (Qin et al., 2008) (Table 2).

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Furthermore, under diverse conditions, a rise in proteins with signaling and protective attributes including RubisCOactivase A (Bahrman et al., 2004a; Patterson et al., 2007; Budak et al., 2013), a thermostable RubisCOactivase B (Qin et al., 2008), carbonic anhydrase (Kosova´ et al., 2008; Rollins et al., 2013), and RubisCO large and small subunit binding proteins CPN60- and CPN60- was found (Qin et al., 2008; Ghabooli et al., 2013; Peng et al., 2009).

Techniques involved in proteomics of wheat The word proteomics means the analysis of the proteome, which looks at how various proteins interact with one another and what roles they perform in the body. As emphasized by the word “proteome,” which refers to the whole complement of proteins in a genome or tissue. A proteomics-based technique is a potent way for gene expression investigation. All the techniques revolve around the central dogma (Fatehi et al., 2012) which states the interconversion of the DNA to mRNA which ends with protein synthesis and vice versa. Although the expression of mRNA may be used for protein expression prediction, the levels of mRNA expression do not always match the levels of protein expression. Moreover, mRNA research ignores protein posttranslational modification, cleavage, complex formation, and distribution, as well as the numerous different mRNA transcripts that may be generated, all of which are important for protein activity. Here are some techniques used in protein sequencing.

Identification and quantitative study of proteins using two-dimensional gel electrophoresis (2-DGel) The identification and quantitative study of proteins using two-dimensional gel electrophoresis (2DGel) works an effective technology. To describe and identify proteins, a proteomic investigation entails the use of high-resolution 2-DE, microanalytical methods, and bioinformatics to extract, solubilize, and separate proteins. As a result, it is more likely that variations in composition of proteins in a variety of biological systems will be clarified effectively (Maccaferri et al., 2019; Bahrman et al., 2004b). It is utilized in the investigation of complicated protein mixtures and was created by combining the 2DGel, IEF, and SDS-PAGE procedures. Protein is separated into its charges in the first phase using IEF, and then separated according to its mass in the second step (Fig. 2). Treatment with SDS makes the separated protein on the IEF gel charged, and electrophoresis is accomplished by inserting the gel horizontally into the SDS-PAGE gel. As a result, the proteins targeted on the pI are divided by their molecular weights. Protein reduction and alkylation are done by removing the protein

FIG. 2 Schematic representation of 2D gel electrophoresis principle.

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spots off the gel and overnight dyeing with a solution of 25 mM ammonium bicarbonate and 50% ACN. To perform the MS analysis of the reduced and alkylated gel fragments, enzymatic digestion is performed using ammonium bicarbonate, pH 8.0, containing trypsin or chymotrypsin, the peptides are then extracted by sonication.

Mass spectrometry: A novel ionization technique for proteomic investigation Protein mass spectrometry necessitates ionization of proteins in solution or solid form in the gas phase prior to injection and acceleration in an electrical or magnetic flux for analysis. Electrospray ionization (ESI) and matrix-assisted laser desorption/ionization is the two most used techniques for ionizing proteins (MALDI). Electrospray allows delicate molecules to be ionized in whole, sometimes retaining noncovalent connections, since the ions are produced from proteins in solution. In MALDI, proteins are placed in a matrix that is generally solid, and ions are generated by laser light pulses. MALDI generates more multiple-charged ions than electrospray, allowing for larger mass protein measurement and better fragmentation for identification, but MALDI is faster and less prone to contaminants, buffers, and additives (Zimin et al., 2017). Time-of-flight mass spectrometry (TOF MS) or Fourier transform ion cyclotron resonance (FT-ICR) are the most used methods for determining whole-protein mass (FT-ICR) (Switzer III et al., 1979). These two types of instruments are used here due to their vast mass ranges and, in the case of the FT-ICR, good mass accuracy. When a protein is electrospray ionized, it produces multiple charged species with masses of 802 m/z 2000, which can be deconvoluted to determine the protein’s average mass to within 50 ppm or better using TOF or ion-trap devices (Chait, 2011). Mass analysis of proteolytic peptides is a popular method of protein characterization since it may be done with low-cost equipment designs. Additionally, sample preparation becomes easier after whole proteins have been digested into smaller peptide fragments (Patterson et al., 2007). The MALDI-TOF devices are the most extensively utilized for peptide mass analysis because they allow for the rapid acquisition of peptide mass fingerprinting (PMFs) (1 PMF could be evaluated in approx. 10.1 s). The quadrupole ion trap and multiple stage quadrupole-time-of-flights are also used in this application (Patterson et al., 2007). Specific MS-based quantitative techniques like multiplex selective reaction monitoring (SRM) have recently shown to be effective in identifying specific proteins with causal activities in agronomically significant characteristics ( Jacoby et al., 2013). Researchers regard the SRM approach as a substitute to antibody-based immunodetection techniques because of its high sensitivity in selective quantification in complex combinations of low abundance protein components (Picotti et al., 2013). This SRM technique relies on very exact identification and quantization of proteotypic pairings made up of target precursor and matching fragment ions, and it was previously only used on triple quadrupoles due to the two layers of mass filters required MS systems. The benefits and drawbacks of this approach have already been studied and shown practically. The newest generation of Orbitrap-technology instruments, such as the Q Exactive hybrid quadrupole-Orbitrap, provides a quick and simple way to apply the SRM technique to statistical assay development in large-scale focused proteomics studies (Wu et al., 2014). The goal of the SRM technique in plant proteomics is to verify biomarkers in crops, which follows the discovery phase with more exploratory qualitative and quantitative comparative proteomic investigations aimed at identifying potential candidates significant in stress responses. This high sensitivity and specificity quantitative way has the potential to be useful not just for biomarker verification, as well as for the discovery of new stress tolerance evaluation tools, allowing for the recognition of genetic variants with greater durability and, eventually, gene targets for markerassisted breeding.

Conclusion Abiotic stresses and biotic stresses stimuli both trigger a biologically active stress response, which includes a significant remodeling of the plant proteome. Due to the high cost and complexity of comparative proteomic investigations, they are generally confined to a small number of plant species. They can, however, considerably contribute to the discovery of new proteins that exhibit a variable response or PTMs across differently resistant genotypes and serve as prospective stresstolerance protein markers. Potential indicators should be examined on a wide variety of genotypes with easy methods of quantification of protein like ELISA or immunoblots that producers and scientists may use. Proteomic investigations on cold-treated winter wheats, for instance, can lead to the discovery and testing of dehydrin proteins as FT indicators. The recent analysis of draught barley (The International Barley Genome Sequencing Consortium, 2012) and wheat (The International Wheat Genome Sequencing Consortium, 2014) sequences of genomes will greatly assist identification of protein, characterization of sequences, and preparation of antibodies, stimulating further investigations and cloning for enhanced strain tolerance.

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Acknowledgments Support by Enhanced Seed grant EF/2019-20/QE04-02 (to NKP) from Manipal University Jaipur, Rajasthan, India, is gratefully acknowledged.

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Chapter 16

Crosstalk between small-RNAs and their linked with abiotic stresses tolerance in wheat Pawan Kumara, Sudarshana Ranjanb, Megha Panwarb, Anjalib, Hanuman Rama, Manoj Kumarc, Himanshu Pandeyd, Hirdayesh Anuragie, Udit Nandan Mishraf, and Rajesh Kumar Singhalg,⁎ a

Division of Crop Improvement, ICAR-Central Institute for Arid Horticulture, Bikaner, Rajasthan, India, b Department of Plant Physiology, G.B. Pant

University of Agriculture and Technology, Pantnagar, Uttarakhand, India, c Department of Plant Breeding and Genetics, Agricultural Research Station, Agriculture University Kota, Kota, Rajasthan, India, d Department of Biotechnology, Dr. YSP UHF Nauni, Solan, Himachal Pradesh, India, e Tree Improvement Research, ICAR-Central Agroforestry Research Institute, Jhansi, Uttar Pradesh, India, f Faculty of Agriculture, Sri University, Cuttack, Odisha, India, g Division of Crop Improvement, ICAR-Indian Grassland and Fodder Research Institute, Jhansi, Uttar Pradesh, India * Corresponding author. e-mail: [email protected]; [email protected]

Introduction Wheat (Triticum aestivium L.) is a major cereal crop cultivated worldwide in a number of agro-climatic zones (Abhinandan et al., 2018) and the vital staple food crop that contributes nearly 20% of the intake calories and >25% of the protein to humans (FAO, 2015). However, climate change and global warming have adversely affected the crops yield and quality by the frequency and extent of numerous abiotic stresses such as drought, high temperature, salinity, etc. Moreover, rising global food demand can only be addressed through robust crop genotypes development to withstand in-field adversaries (Mickelbart et al., 2015). Plants have advanced intricate molecular networks, including signal transduction cascades that can mitigate stress condition by maintaining cellular redox equilibrium (Lamaoui et al., 2018). The veracity of some biotechnological procedures is much more precise and effective than conventional breeding in developing stress-resistant high-yielding cultivars, contributing to quick agricultural improvement (Varshney et al., 2011). Noncoding RNAs (ncRNAs) are momentous bioactive molecules that contribute to genotypic and phenotypic diversity. Contingent on the origin, functional principal and biogenesis, two categories of ncRNAs are found, namely, regulatory ncRNA and housekeeping ncRNA (Waititu et al., 2020). lncRNAs can regulate an array of drought-stress-responsive genes at their respective transcription check points (Zhang et al., 2018; Yan et al., 2019). lncRNAs are associated to be a major player in phytohormone synthesis, Ca2+ signaling, and primary metabolite (starch-sucrose) synthesis under unfavorable conditions in some notable agricultural crops such as rice (Weidong et al., 2020), switchgrass (Panicum virgatum L.) (Zhang et al., 2018), P. betulifolia (Wang et al., 2018), and cassava (Zhang et al., 2018; Ding et al., 2019; Yan et al., 2019). RNA sequencing study revealed the importance of miRNAs in novel targets for agricultural development, enhancing plant yield, and producing abiotic stress resistant plants (Pandita, 2019). Numerous lncRNAs altogether modulate stress by acting as target mimics for various miRNAs, which either up- or downregulate the expression level of abiotic stressresponsive genes such as drought (Gasparis et al., 2017), salinity (Bai et al., 2018), heat stress (Wang et al., 2012), cold (Wang et al., 2019), and heavy metals (Wang et al., 2013). Phenotypic suppression tests are used cytogenetic approaches to identify target sequences of miRNA for the flexibility of regulating miRNA gene expression. The RNAi method allows for the creation of a mutant miRNA with functional deficiency of phenotype. Biochemical inspectional methods for discovering targeted miRNA sequences are more precise than genetic ones and are typically combined with bioinformatics analysis of miRNA biogenesis and regulation is now easily decipherable with computational and bioinformatic tools which draw basic information from classical “Watson-Crick base complementarity” (between 2nd and 7th nucleotides), 30 -UTR (secondary structure, AU content) of mRNAs for (Pasquinelli, 2012). Various algorithms involving miRanda, PicTar algorithm, Stark technique, TargetScan, and Diana-microT are used as input for scoring target sites. Recently, target prediction focused on CLIP-seq-based expression analysis, single nucleotide Abiotic Stresses in Wheat. https://doi.org/10.1016/B978-0-323-95368-9.00010-2 Copyright © 2023 Elsevier Inc. All rights reserved.

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polymorphisms (SNPs) at target areas, or recognizing miRNA clusters, however, relied on base-pairing. Bioinformatics tools and databases support researchers in investigating new target sequence of miRNA; meanwhile, it is critical to choose the most appropriate prediction cum assay tool to obtain data accuracy which relies on the data maintenance, its utilization, and version of the tools.

Origin and biogenesis of wheat small RNAs (sRNAs) Small RNAs occupy 20–30 nucleotides (nt) noncoding regulatory elements genome component. The term sRNA is rather an inaccurate term, because all discovered ncRNAs are recognized as small RNAs. sRNAs are widespread for their gene regulatory function at various check points such as transcription, posttranscription, and translation (Mallory and Vaucheret, 2006). The regulatory endogenous sRNAs constitute three main classes: “short-interfering RNAs” (siRNAs), dicerindependent “piwi-interacting RNAs” (piRNAs), and dicer-dependent “microRNAs” (miRNAs) (Axtell, 2013). All sRNAs in plants are modified at the 30 -end by 20 -O-methylation, including miRNAs, which is essential to confer stability and protection from 30 -uridylation and degradation (Borges and Martienssen, 2015). The wheat genome is hexaploid (2n ¼ 42, AABBDD) evolved from three diverse ancestor species, namely, T. urartu (“A” genome), T. speltoides (“B” genome), and Triticum tauschii (“D” genome) (Middleton et al., 2014). The genome size of wheat is approximately 17 Gb majority of which are repetitive sequences (Martı´nez-Moreno et al., 2020). The recent tools allowed us to overcome sequencing lag through the detection of sRNAs. Conserved sequence and fold-back transcript of miRNAs give miRNAs upper hand in predictability factor over siRNAs. Cloning methods and next-generation sequencing (NGS) are very helpful in identifying and characterizing wheat sRNAs under a variety of strains.

Biogenesis of sRNAs (miRNAs and siRNAs) The Dicer enzymes are crucially required in the biosynthesis of sRNAs and processing of dsRNA into sRNAs. The RNAdependent RNA polymerases involved in the synthesis of dsRNAs, considerably to the expansion and multiplicity of smallRNA functions (Ravichandran et al., 2019). Most commonly, there are three major pathways that are employed for the synthesis of major sRNA portions in plants: one for the biosynthesis of miRNAs is 21–22 nt, secondary siRNAs, and another for the biogenesis of 24 nt hetsiRNAs (Axtell, 2013; Borges and Martienssen, 2015).

The origin and biogenesis of miRNAs The single-stranded hairpin-like structure ranging between 64 and 303 nt is the precursors from which miRNAs are processed in plants. Most of the miRNA genes are species- or family-specific, signifying fast evolution and speedy turn-over rate (Cuperus et al., 2011). Almost exact-sequence complementarily in proto-miRNA hairpins has decreased, during evolution, results in refinement into smaller transcripts and processed as a single miRNA duplex by DCL1 (Axtell et al., 2011). The DCL1 cleaved pri-miRNAs into short stem-loop structures known as precursor miRNAs (pre-miRNAs), which are later refined by DCL1 to generate mature duplexes (both active and complementary miRNA strand) of miRNA. Gene of miRNAs, encoded genes, is annotated as MIR genes, which generate primary mi RNAs (pri-miRNAs) by RNA polymerase II (RNA pol II) (Kuan et al., 2016). In the occurrence of protein Hyponastic Leaves 1 (HYL1), the RNA pol II and Dicer-like 1 (DCL-1) facilitate in the making of miRNA duplex, i.e., miRNA-miRNA* (Papp et al., 2003). The Hua Enhancer 1 (HEN1) causes methylation by which duplex is stabilized (Horwich et al., 2007). This miRNA duplex transferred from nucleus to cytoplasm through HST assistance (HASTY) (Yu et al., 2005; Li et al., 2005). Duplex is unwinded by unknown helicases which facilitate the task for RNA-induced silencing complex (RISC) formation. Binding of miRNA with RISC directs the hybrid to target mRNA resulting in either translation repression or degradation (Mao et al., 2009; Guleria et al., 2011). siRNAs are intimately linked to miRNAs; however, they vary in aspects of their source, structure, linked effector protein, and mode of action (Carthew and Sontheimer, 2009). The precursors of siRNAs are long dsRNAs that can be originated from several pathways such as the hybridization of antisense and sense transcripts, the folding back of an invertedrepeat sequence, the hybridization of dissimilar RNA molecules with sequence complementarily, or generally, synthesis by RNA-dependent RNA polymerases (RDRs) (Axtell et al., 2011). In plants, primary processing of endogenous siRNAs by DCL2, DCL3, and DCL4 has been subdivided into secondary siRNAs and hetsiRNAs. The hetsiRNAs (24-nucleotide) are the most abundant sRNAs and mediate transcriptional silencing of transposons and pericentromeric repeats through RdDM (Matzke and Mosher, 2014). Transcription through Pol IV is involved in the biogenesis of hetsiRNAs, followed by dsRNA synthesis by RDR2 and processing by DCL3 (Borges and Martienssen, 2015). The secondary siRNAs (21–22 nucleotide)

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(viz. tasiRNAs, phasiRNAs and easiRNAs) are processed by DCL4, DCL2, followed by RNA polymerase II-mediated transcription and RDR6-mediated dsRNA synthesis. Further processing of siRNA requires “SUPPRESSOR OF GENE SILENCING 3” (SGS3), which cooperate with RDR6 (Peragine et al., 2004; Yoshikawa et al., 2005) and dsRNA-BINDING 4 (DRB4), with a downstream interaction with DCL4 in the production of endogenous and exogenous 21-nt siRNAs (Hiraguri et al., 2005).

Impact of sRNAs on wheat crop gene regulation Small RNAs (microRNAs and short-interfering RNAs) are central regulators of gene transcription (Vazquez, 2006). MIR gene family encodes miRNAs in plants (Kuan et al., 2016). Generation of small noncoding RNAs (sRNAs) takes place when double-stranded RNA (dsRNA) is cleaved by proteins belonging to the Dicer family that ultimately leads to the sequence-specific silencing after transcription (Baulcombe, 2004). miRNA can modulate the expression pattern of genes in three different ways: (i) degradation of target mRNA, (ii) translational repression, and (iii) miRNA-guided mRNA decay (Zhang et al., 2007). sRNAs-mediated mechanisms instantaneously respond as mobile signaling molecules in case of any environmental stress and developmental obstruction as compared to other epigenetic regulatory mechanism to modify respective target genes expression (Ragupathy et al., 2016; Ravichandran et al., 2019). Upon perception of stress signal by plant, there is activation of miRNA-mediated “calcium-dependent protein kinases” (CDPKs) and “receptor-like protein kinases” (RLKs). Thereafter, transduction of stress signal is governed by signaling regulators, such as phytohormones including ABA and ethylene. Many miRNAs are known for regulating hormonal responses via TF-pairing where multilayered networks are involved in the miRNA-guided stress-response (Liu et al., 2020). miRNA quickly reprograms the downstream genes’ expression profile governing adaptive physiological features such as enhanced root water intake and altered flowering time regarding abiotic stress. Stress-responsive miRNA in wheat species encompasses numerous genes governing stress tolerance genotypes. Some well-known examples include ROS scavenging via miR398 and SOD enzyme, modulation of auxin phytohormone signaling via miR167 and “auxin response factors” (ARFs), flowering time modulation via miR156 and SPL (Squamosa promoter binding protein-like) transcription factors, and intracellular protein conformational regulation via miR164 and HSPs (Liu et al., 2012; Kumar et al., 2014). With the known sequence of wheat genome, various conserved miRNA groups have been discovered across plant species (Su et al., 2014; Achakzai et al., 2018). The most frequent cleaved transcripts are NFYA (nuclear factor YA) subunits, ARF, transport inhibitor-1 (TIR1), and Apetala-2 (AP2) and are the target sequences of miR169, miR160, miR393, and miR172, respectively (Li et al., 2013). Monocot-specific miRNA is miR444 and is detected in wheat small RNA library. Transcripts encoding MADS box transcription factors are targeted by miR444 that control various aspects of reproductive and developmental processes (Sunkar et al., 2008; Lu et al., 2008). Cantu et al. (2010) reported that sRNA-directed transcriptional and posttranscriptional silencing suppresses TE activity whereas permanent TE silencing can be obtained by DNA methylation through methylated site mutation in wheat genome. Gupta et al. (2014a,b) reported that in wheat miRNAs, namely, miR168 and miR397 downregulated while miR172 showed upregulation under all the stress conditions. Stress adaptation mechanisms are well modulated by miRNAs at cellular level (Wang et al., 2013; Qiu et al., 2016; Song et al., 2017; Bai et al., 2018; Zhou et al., 2019). The important role of different miRNA in growth and development in wheat crop is highlighted in Fig. 1.

miRNAs in abiotic stress tolerance Wheat small miRNAs for drought stress resistance Drought is a substantial abiotic barrier to crop productivity that has had a large impact on worldwide crop production in recent decades (Matiu et al., 2017). Due to the climate changes across the world and diminishing precipitation, droughtrelated yield losses are expected to increase in the future. It is critical to improve the performance of agricultural crops under drought in order to obtain the requisite production level by accessing several drought tolerance mechanisms (Raza et al., 2019). Additionally, transgenic plants which overexpress some drought-responsive genes did not show substantial or no improvement in drought tolerance (Bartels and Sunkar, 2005). sRNAs (miRNAs and siRNAs) are the processed products of single-stranded hairpin precursor RNA and double-stranded RNAs (involvement of DICER/DICER-like protein), respectively (Zhang et al., 2019). Researchers reported various bread wheat-based miRNAs and their targets such as tae-miR159c-5p (dihydro-flavonoid reductase-like protein), tae-miR319c (Acyl-CoA synthetase), tae-miR396a,c,g (GRF), tae-miR159a,b (MYB3), tae-miR171f (sensor histidine kinase), taemiR166l-5p (FAM10 family protein), tae-miR444c.1 (MADS-box TF), tae-miR168b (dehydrogenase/reductase),

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FIG. 1 Highlights the crucial role of miRNAs in plant growth and development in wheat crop. There are numerous miRNAs present in wheat crop which regulates the stress tolerance, metabolism (photosynthesis), signal transduction, mineral nutrient transport, and regulation of transcription factors. These regulations ultimately regulates the development of embryo, leaf, grain, shoot, flower, and grain development at various growth stages.

tae-miR160a (ARF), tae-miR164b (NAC), tae-miR395i (ATP sulfurylase), tae-miR827-5p (finger-like protein), tae-miR393b, i (TIR1), and tae-miR169d (CCAAT-box TF) regulating drought tolerance (Ma et al., 2015). MiR164 accumulates in C-306 cultivar of wheat seedlings under drought stress (Gupta et al., 2014a,b), suggesting the role of miR164 in targeting NAC TFs and subsequent alteration in root architecture resulting in magnified stress response (Fang et al., 2019). MiR169 is another important family of miRNA that targets CAAT box NFY transcription factors (TFs) (Li et al., 2008). Interestingly, various plant miRNAs target peroxidase (miR528) and Cu/Zn superoxide dismutase (miR398) to modify oxidative stress networks. Phytohormone ABA can induce drought tolerance through numerous TFs such as MYB and NAC, which are also targeted by miRNAs (Khan et al., 2018). Plants overexpressing TaNAC29 showed increased tolerance to salinity and water stress. The overexpression of wheat MYB gene, TaMYBsm1, showed greater drought tolerance in transgenic A. thaliana resulting in high rate of germination (Li et al., 2016). Overexpression of TaNAC29, for example, increased some key ABA signaling genes expression like ABI5, SAG13, and SAG113. Auxin signaling mediated by ARF-10 and ARF-16, the miR160 family, affects directly the development of root cap (Yang et al., 2019). It was suggested that miR164 could be a downregulator of leaf senescence in Arabidopsis, on the basis of the fact that EIN2 (ETHYLENE INSENSITIVE 2),

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FIG. 2 Highlight the central mechanism of drought tolerance in wheat crop through the miRNAs. It involved the upregulation of stress responsive transcription factors (MADS, NAC, MYB), ABA signaling genes (ABI15, SAG13), auxin signaling genes (ARF10, TIR1), and antioxidant defense genes (SOD), which ultimately provide drought tolerance.

which is a signaling protein of ethylene in Arabidopsis, downregulates miR164 in case of older leaves. The TIR1 (transport inhibitor response1) enzyme promotes the ubiquitination of Aux/IAA proteins, which positively regulates signaling of auxin (Dharmasiri and Estelle, 2022). It was found that 1-day drought treatment slows down the growth of miR393overexpressing rice seedlings relative to control plants (Xia et al., 2012). Rice overexpressing miR393 also showed hyposensitivity toward treatments of synthetic auxin analog (Xia et al., 2012). The mechanism of drought tolerance through miRNAs in wheat crop is highlighted in Fig. 2.

Wheat small miRNAs for salt stress resistance Plant prolificity and productivity are adversely threatened by salt stress. Studies have been conducted to understand the salt tolerance mechanism in rice (Shen et al., 2017), barley (Kuang et al., 2019), Arabidopsis thaliana (Schommer et al., 2014), pearl chestnut (Harshraj et al., 2020), and several other plants by regulating plant proliferation and stress response. The role of miRNAs in achieving tolerance against salt stress was recognized recently in the crops (Zhou et al., 2013); however, very little experimental evidences have been generated to prove the role of specific wheat miRNAs in determining the salinity tolerance. And thus, the underlining salt tolerance mechanism mediated by sRNAs in wheat is still ambiguous which moderates the genetic improvement of wheat cultivars (Han et al., 2018). Zeeshan et al. (2021) studied the miRNAs and target genes expression patterns using “high throughput sequencing” in Suntop (salt-tolerant) and Sunmate (salt-sensitive) cultivars of wheat under salt stress and identified 191 microRNAs consisting of 110 well-known miRNAs and 81 novel miRNAs. Wet lab analysis revealed about more than 850 recognized target mRNAs for the 75 well-known miRNAs and 15 candidate novel miRNAs that might be contributing to salt tolerance in Suntop. The miRNAs like tae-miR156and tae-miR160 negatively regulated with target squamosa promoter-binding like protein 3 (SPL3) and auxin-responsive factor 8-like protein (ARF8), respectively, which are directly involved in plant growth and developments under stress (Wang et al., 2012; Sharma et al., 2015). Overexpression of miR319 enhanced the K+/Na+ ratio and subsequent osmotic adjustment so as to help wheat salinity tolerance. The novel-mir59 targeted CBL proteins which address stress responsiveness of plant under adverse environmental cues (Huang et al., 2011). Similarly, miR319, miR159a-b, and miR9657 may regulate salt tolerance in Suntop by targeting transcription factors/proteins controlling stress responses and plant growth in many plant species. Another study identified the 11 upregulated mRNAs and 8 downregulated miRNAs (tae-miR319, tae-miR9666b-3p, tae-miR1131, tae-miR1131, Novel_72, tae-miR9774, taemiR9668-5p, and tae-miR1122a) and enhanced salinity tolerance in QM6 variety of wheat either through regulating MYB transcription factor, enhancing antioxidant stress capacity, promoting nutrient uptake, or by maintaining lipid balance during salt stress (He et al., 2021). The 98 known and 219 novel miRNA sequences and corresponding targets controlling salinity stress tolerance in SR3 cultivar of wheat were reported degradome sequencing (Han et al., 2018). The miRNAs novel112 and novel392 were upregulated whereas miRNA novel84 was downregulated by the salt stress.

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FIG. 3 Represents the mechanism of salt tolerance through the miRNA in wheat crop. The miRNA 319, 1131, 156, 160, 408 are important in regulating the osmotic adjustment, ABA biosynthesis, antioxidant defense, and elevate the stress responsive transcription factors, which ultimately provide stress tolerance.

Salt stress

miR319

mir319, miR1131, miR9774

Reduce Na+/K+ ratio

Enhance osmotic adjustment

Regulate MYB transcription factor

miR156, miR160

miR408

SPL3 and ARF8

Osmoprotectant biosynthesis, remodeling ABA biosynthesis pathway

Regulate plant growth and development

Enhance antioxidant defence, and promoting nutrient absorption

Salt stress tolerance

The overexpression of tae-miR1120c and tae-miR9664 was seen under salt stress. Amirbakhtiar et al. (2021) recognized 2346 upregulated genes and 1944 downregulated genes through Illumina HiSeq 2500 platform in an Iranian salt-tolerant cultivar in wheat. Clustering of the DEGs using Kyoto Encyclopedia of Genes and Genomes (KEGG) revealed that the sequence involved in transporters, transcription factors, phenyl-propanoid biosynthesis, phytohormone signal transduction, glycosyl transferases, exosome, and MAPK signaling might be contributing toward salinity tolerance in wheat. The small RNAs were earlier reported to express and regulate the transcriptional factors/target genes conferring salt tolerance by altering the biological mechanisms like transcriptional regulation, antioxidant stress tolerance, nutrient uptake, stress tolerance, lipid balance, and many other essential functions under an increased level of salinity stress. An enhanced understanding of small RNAs involved in salt tolerance may potentially help in breeding salt tolerant wheat varieties. The mechanism of salinity tolerance through miRNAs in wheat crop is highlighted in Fig. 3.

Wheat small miRNAs for temperature stress (high/low) resistance The yield attributes are negatively affected by abiotic stresses, such as temperature (hot and cold). Various genetic and molecular engineering studies have made significant contributions, showing that abiotic stress is the main cause of plant yield loss. The discovery of RNA-mediated gene silencing provides a feasible alternative technique for gene functional investigation through the simultaneous suppression of expression of several related gene copies. RNA-mediated gene silencing can cause blockage at one of the two or both (transcriptional and posttranscriptional) (Ding et al., 2010). By regulating copper metabolism, miR398 participates in systems that regulate plant responses to abiotic stressors such as low temperature, ozone, heavy metals, sucrose, salt, and biological stresses (Leng et al., 2017; Zeng et al., 2018; Ga´lvez et al., 2019). Park and Grabau (2017) reported that the target for Cu-Zn type superoxide dismutase (CSD) has been downregulated by miR398. Overexpression of transgenic miR398 can improve tolerance to salt, cold, and oxidative stress, but it also increases susceptibility to drought and osmotic stress (Ding et al., 2019; Li et al., 2017). According to recent finding, the vast portion of the genome is transcribed, but only a small portion of those transcripts encode proteins. The greater number of transcripts that do not code for proteins is called nonprotein coding RNAs (npcRNA). These npcRNAs are subclassified into two categories: house-keeping pcRNAs (like ribosomal and transfer RNAs) and ribo-regulators or regulatory npcRNAs, latter further subdivided into long regulatory npcRNAs (>300 bp in length) and short regulatory npcRNAs ( 0.41, P < .001) between salinity tolerance and NaCl-induced K+ efflux in the leaf mesophyll of bread wheat and NaCl in 48 wheat genotypes. Osmoregulation Maintaining the osmotic potential and cell turgidity is quite important to continue the proper metabolic function of the cell in abiotic stresses. As plants become stressed by salinity or drought, they accumulate various solutes through osmotic adjustments. Synthesis of metabolomic solutes, such as polyamine, polyhydric alcohol, proline, and betaine, is a major contributor to salt and alkali stress tolerance (Guo et al., 2015). Screening of tolerant genotypes, therefore, focused on searching of germplasms having higher activity of H+-ATPase, greater retention ability of K+ in leaf mesophyll, and higher osmolyte accumulation.

Transgenic approaches to combat salt stress in wheat Integration of antiporter gene High Na+ in the cytosol imparts detrimental effects to the plant growth inhibiting the activities of enzymes (Munns et al., 1983) and transcription factors (Xue, 2002). Leaf tissues are more vulnerable to Na toxicity than the roots. Na+/H+ antiporter proteins are reported to play a vital role in pumping excess Na+ either out of the cell by plasma membrane antiporter or to the vacuole by vacuolar antiporter. Transformation of wheat lines with Arabidopsis thaliana-derived AtNHX1 gene improved biomass, seed germination, and yield under salt stress. Transgenic wheat lines were reported to possess an elevated K+/Na+ ratio, even under severe salinity stress (Xue et al., 2004). Engineering for better osmoregulation Among polyols, mannitol is one of the most common photosynthetically derived osmolytes that many plants accumulate under lesser water potential (Ψ w) during salt stress (Patonnier et al., 1999; Conde et al., 2007; Seckin et al., 2009). However, the accumulation of mannitol does not take place in bread wheat, leading scientists to introduce the mannitol synthesis mechanism into wheat to enhance stress tolerance. Bacterial (Escherichia coli) gene mtlD encodes for mannitol-1phosphate dehydrogenase, which catalyzes the formation of mannitol-1-phosphate from fructose-6-phosphate (Davis et al., 1988). Wheat (T. aestivum) cultivar Bobwhite transformed with mtlD gene and evaluated for the salt stress at both the calli and whole-plant (T2) level. We saw no significant growth reduction in calli plants under salt stress, but T2 plants showed dramatic improvements in their fresh weight, height, flag leaf length, and dry weight when compared to control plants (Abebe et al., 2003). Integration of transcription factors Salt stress can be improved by regulating the expression of stress-responsive genes by manipulating transcription factors, like DREBP (dehydration-responsive element-binding protein) (Agarwal et al., 2006; Hussain et al., 2011). Although ciselements of DRE were identified initially from Arabidopsis, further investigation led us to identify approximately 40 homologs of DREB in 20 types of plants. Soybean (Glycine max)-specific DREB (GmDREB) gene introduced into the wheat genome was effective to ameliorate yield performance by enhancing stress tolerance and improving various agronomic traits. Enhanced tolerance of transgenic lines was dissected through proteomics analysis, which showed upregulation of oxidative and osmotic stress-related

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proteins. Additionally, increased levels of betaine and proline, and greater membrane stability, were also found to be associated with the salt-tolerant transgenic lines ( Jiang et al., 2014). Similarly, cotton (Gossypium hirsutum)-specific GhDREB, driven by ubiquitin and rd29A promoter, was integrated into the genome of another wheat cultivar Yangmai 10 by the particle bombardment method. Transgenic plants were found to possess two to four copies of gene insertion based on the promoter used. Lesser chlorophyll destruction in transgenic lines, and thereby maintaining normal photosynthesis under the salt stress, was explained by the GhDREB-mediated upregulation of downstream genes (Gao et al., 2009). Upregulation of glycine betaine Under different abiotic stresses, including salt stress, plants accumulate glycine betaine (GB), a quaternary ammonium compound (Ashraf and Foolad, 2007). Biosynthesis of GB is stress-inducible, and it follows two distinct pathways where either choline or glycine is used as the substrate (Rhodes and Hanson, 1993; Sakamoto and Murata, 2002). Winter wheat (T. aestivum) cultivar Jinan 17 was transformed with betA gene encoding for choline dehydrogenase via Agrobacteriummediated gene transfer (He et al., 2010). The conversion of choline to GB via betaine aldehyde as an intermediate is catalyzed by this specific enzyme. The alien gene was derived from E. coli and expressed under maize-specific ubiquitin promoter. Transgenic plants showed better performance over the wild type in terms of membrane stability, water retention, chlorophyll content, lower Na+/K+ ratio, and solute potential (Ψ s). The abundance of GB biosynthesis is found in the chromoplast where it plays a pivotal role in maintaining photosynthetic activity by protecting the thylakoid membrane (Genard et al., 1991; Robinson and Jones, 1986). NAC transgenic NAC is a large family of transcription factors that contains three major groups of proteins, viz., CUC2 (cup-shaped cotyledon), NAM (no apical meristem), and ATAF1-2. Highly conserved N-terminal DNA binding domains and diversified C-terminal domains of these transcription factors are key characteristics of this protein family (Souer et al., 1996; Aida et al., 1997). SNACs (stress-responsive NACs) play an important role in stress tolerance in plants and have been shown to be plant-specific ( Jeong et al., 2010; Xia et al., 2010; Xue et al., 2011). The introduction of rice-specific SNAC1 gene into the Chinese wheat cultivar Yangmai12 improved salinity tolerance by increased ABA sensitivity, chlorophyll retention, and relative water content (Saad et al., 2013).

Metabolic pathways protecting plants from heavy metal stress Plants have evolved to incorporate mechanisms to nullify the toxic effects of heavy metals. Some of these mechanisms are as follows. Restricting uptake and transport of heavy metals Plants limit heavy metal absorption in the rhizosphere by complexing or precipitating metals (Shahid et al., 2013). Heavy metals are precipitated by plants by raising the pH of the rhizosphere or discharging ions as phosphates (Shahid et al., 2014). Cell exclusion of heavy metals Metal ions are excluded from cells’ apoplastic or symplastic spaces by metal transporter proteins (Uzu et al., 2011). For example, a sensitive wheat cultivar accumulated more symplastic Al than the tolerant cultivar when external Al concentrations were similar, suggesting an exclusion mechanism (Masion and Bertsch, 1997). Cd may be detoxified in plants through a family of sulfur-rich peptides known as phytochelatins (Cobbett and Goldsbrough, 2002). Heavy metal complexation in plasma membrane The cell wall plasma membrane (CWPM) interface is involved in metal/metalloid stress detection, perception, and signaling (Wani et al., 2018). Phospholipases, transcription factors, salt overly sensitive kinases (SOS), dehydration-sensitive element-binding proteins, C-repeat binding factor, abscisic acid-responsive binding factors, and mitogen-activated protein kinases and phosphatases are the main (CWPM) signaling molecules under various stress conditions (Ihsan et al., 2017; Dar et al., 2017).

364 Abiotic stresses in wheat

Vacuole compartmentalization For severely accumulated metal contaminants, the central vacuole is an ideal storage location. Most solutes are accelerated through vacuoles through channels and transporters by proton pumps found in the tonoplast, especially proton ATPase (VATPase) and pyrophosphate (VPPase) (Yan et al., 2010; Socha and Guerinot, 2014).

Progress in transgenic wheat varietal development for heavy metal stress Wheat (Triticum aestivum L.) is the world’s first domesticated cereal, accounting for almost 20% of all cultivated land (Gill, 2004; Clemens et al., 2013). Heavy metal stress-tolerant varieties of wheat are a necessity for modern cultivators in contaminated soils. Upregulation of TaPUB1 The wheat (Triticum aestivum) U-box E3 ligase TaPUB1 had been overexpressed in transgenic lines to confer heavy metal stress tolerance against Cd. Overexpression vectors (TaPUB1-OE, OE) and RNAi vectors (TaPUB1-RNAi, R) were created and then individually transformed into hexaploid wheat to evaluate the function of the TaPUB1 gene (Bobwhite). Under Cd stress, overexpressing lines showed better results than control lines, while RNAi lines had a negative effect and performed worse than both the lines. In higher Cd stress, TaPUB1 interacts with TaIRT1, a key transporter for Cd uptake from roots, and degrades the protein. Under Cd stress, TaPUB1 also regulates the expression of associated genes, lowering ROS levels and increasing antioxidant enzyme activity (Zhang et al., 2021). Incorporation of AemNAC2 NAC (NAM/ATAF/CUC2) transcription factors (TFs) are members of one of the largest TF families known to exist in plants (Yokotani et al., 2009), and they contribute to many physiological processes in plants, such as heavy metal tolerance, protein accumulation, senescence, root growth, and stress (abiotic and biotic) responses ( Jung et al., 2008; Lu et al., 2007). AemNAC2, a specific NAC gene, was extracted from a wild wheat cousin, Aegilops markgrafii, and introduced into bread wheat. Among wheat’s wild relatives, this plant had the highest Cd tolerance capability. It was observed that the transgenic wheat lines showed significantly lower Cd concentration in plant biomass than the wild type. Expression of two important metal transport genes, viz., TaNRAMP5 and TaHMA2, which were sensitive to Cd stress, was also inhibited by NAC gene AemNAC2 (Du et al., 2020). Wheat to other plants Several wheat genes have been shown to increase heavy metal stress resistance in a variety of plants. Heavy metal ATPases (HMAs) are essential for metal transport and buildup. In Arabidopsis, one such HMA, TaHMA2 of wheat, has exhibited enhanced Zn2+ and Cd2+ accumulation (Qiao et al., 2018). TpNRAMP5, a natural resistance-associated macrophage protein (NRAMP) isolated from Triticum polonicum, increased Co, Cd, and Mn concentrations in Arabidopsis shoots, roots, and entire plants. This suggests that TpNRAMP5 is a metal transporter in wheat and that it can be exploited in transgenic breeding (Peng et al., 2018). Wheat expansin gene, TaEXPA2, showed higher root elongation, germination rate, and biomass accumulation in transgenic tobacco than the wild type under Cd stress (Ren et al., 2018). A wheat prolyl aminopeptidase named as TaPAP1, when incorporated in Arabidopsis, showed increased tolerance to Zn stress by improving proline levels and PAP enzyme activity (Wang et al., 2015). By energizing the pH gradient created by proton pumps, cations/H+ exchangers, such as CAXs, can directly transfer Cd into vacuoles. To see if ectopically expressing wheat vacuolar H+-pyrophosphatase (V-H-PPase) in transgenic tobacco will improve Cd tolerance, a cDNA (TaVP1) encoding wheat vacuolar H+-pyrophosphatase (V-H-PPase) was used. When exposed to varied doses of Cd, TaVP1-expressing plants demonstrated greater tolerance to Cd than wild-type plants (Khoudi et al., 2012).

Heat stress Climate change has shown its most conspicuous effect by raising the average temperature globally, especially in the tropics that account for maximum wheat supplies across the world (Braun et al., 2010). Wheat cultivation is best suited at a temperature of  15°C; however, being a cool-season crop, it adversely suffers from the heat stress; for every 1°C rise in temperature, it may cause about 6% yield reduction (Asseng et al., 2015). Environmental change such as the gradual shortening of spring that results in a sudden transformation of winter to summer influences the growth period of the plants and

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ultimately reduces the crop yield and productivity (Kaur et al., 2019). Besides quantity, heat stress also influences the bread-making quality and starch properties of wheat kernels by affecting biochemical properties such as the ratio of gliadin to gluten and amylopectin to amylose, respectively (Stone and Nicolas, 1995). Different physiological and metabolic processes can interfere with a yield reduction in response to heat stress. Suppression of CO2 fixation, dark respiration, starch and protein synthesis, ion uptake, on the other hand, aggregation and denaturation of many proteins, and injury to the cellular membrane are caused by heat stress (Fu and Ristic, 2010). The growing demand for wheat-based food products necessitates increased wheat production under available land and other resources. Transgenic approaches help to meet the ever-rising food requirements, offering a promising way to generate heat stress-resilient, high-yielding wheat varieties.

Adverse effect of heat stress on wheat Elevated air temperature beyond the threshold level may result in irrevocable damage to the plant, especially in wheat leading to heat stress. The extent of heat stress not only varies among the plant species but also significantly varies within the plant species. Plants respond to heat stress differentially based on their tolerance mechanism and adaptation. Several other factors, like the developmental stage of the plants as well as the duration of exposure to the elevated temperature, are also important determinants of the severity of the heat stress (Akter and Islam, 2017). Although wheat may face the adverse effect of heat stress throughout its life cycle, reproductive and grain-filling stages were reported to be the most sensitive (Parent et al., 2017). A prolonged elevation of temperature is commonly followed by the depletion in soil water content. Consequently, in a majority of the cases, plants display symptoms of drought stress due to the loss of cell turgidity and poor water-use efficiency. Severe cellular damage and impairment of protein structures lead to the damage of photosynthetic enzymes and the formation of ROS that causes a marked reduction in grain size and number. Oxidative stress due to the production of ROS eventually causes the death of plants if it remains undetected (Kaur et al., 2019). Some common effects of heat stress on wheat cultivation are presented in Table 1.

Physiological responses under heat stress Water imbalance Plant water potential is one of the most important and unstable factors under heat stress. Higher temperature promotes dehydration of the plant tissues, and a consequent increase in temperature ultimately affects photosynthetic activity, reducing leaf water potential and relative water content. Concurrently, the transpiration rate and growth of the plants are severely affected (Akter and Islam, 2017). Significant reduction in water potential at anthesis and after anthesis, especially in susceptible genotypes, was reported in wheat upon imposing high temperature (35°C-day/25°C-night) after tillering (Almeselmani et al., 2009). Increased transpiration rate and decline in osmotic potential of stressed leaves stimulate the production of antioxidants associated with heat stress. Hydraulic conductivity of the cell membrane and cell membrane also gets induced as a result of increased aquaporin activity and decreased water viscosity (Akter and Islam, 2017).

TABLE 1 Effects of heat stress on wheat growth and development at different stages. Heat stress

Growth stage

Major effects

References

34/26°C (day/ night), 16 days

During the grainfilling process

Increase in leaf temperature; decrease in leaf chlorophyll and maximum quantum yield of photosystem II; reduction in individual grain weight and productivity

Pradhan and Prasad (2015)

45°C, 2 h

After 7 days of germination

Shortening of shoot length and reduction in dry mass; decreased chlorophyll and membrane stability index

Gupta et al. (2013)

42°C, 24 h

Seedling stage

Impaired development of roots and first leaf; increased ROS and LP (lipid peroxidation) products in the developing organ and coleoptile

Savicka and Sˇkute (2010)

37/28°C day/night

After anthesis for 10–20 days until the crop is mature

Reduction of grain-filling period and maturation; severely decreased FW (fresh weight), DW (dry weight), grain protein and starch content; reduction in grain size and productivity

Hurkman et al. (2009)

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Photosynthesis and respiration Heat stress causes crop failure primarily due to reduced photosynthesis, which leads to reduced leaf area expansion, premature leaf senescence, and disrupted photosynthetic machinery (Ashraf and Harris, 2013; Mathur et al., 2014). The main photosynthetic reaction centers, viz., thylakoid lamellae and stroma, the reaction center for photochemical reactions and carbon metabolism, respectively, are affected under heat stress. Inhibition of the membrane-associated enzyme activities and electron carriers due to the disruption of the thylakoid membrane was found to be associated with the photosynthetic reduction in wheat (Ristic et al., 2008). The complex photosynthetic phenomenon of photosystem (PS) II, which is more heat labile than the relatively stable PS I, is affected by heat stress. Depletion of RuBisco, soluble proteins, and RuBiscobinding proteins is the important factor for the suppression of carbon assimilation and net photosynthesis (Akter and Islam, 2017). The rate of respiration increases initially under heat stress; however, it starts to decline after a certain limit due to the stress-induced damage in the respiratory apparatus (Prasad et al., 2008). Heat stress hampers the solubility of O2, CO2, and the kinetics of Rubisco, which in turn reduces ATP production but promotes ROS generation due to an enhanced rate of respiratory C loss in the rhizosphere (Akter and Islam, 2017). Oxidative damage Plants suffer from oxidative damage under abiotic stresses, including heat stress due to the formation of toxic chemicals like ROS, including 1O2 (singlet oxygen), O2 (superoxide radical), OH (hydroxyl radical), and H2O2 (hydrogen peroxide). Oxidative stress is responsible for increased peroxidation and decreased thermostability of the cell membrane in wheat and other crops as well. Incremental heat stress in plants may lead to ROS accumulation in the cell plasma membrane with the activation of ROS-producing enzyme RBOHD, depolarization of cell membrane, and trigger of PCD (programmed cell death). However, plants are adapted with the antioxidant defense mechanism to escape from ROS damage. Antioxidants like POX (peroxidase), CAT (catalase), GR (glutathione reductase), APX (ascorbate peroxidase), and SOD (superoxide dismutase) have been reported to show heat stress amelioration in wheat (Akter and Islam, 2017).

Transgenic approaches to combat heat stress in wheat Engineering plastid-related genes Membrane instability, denaturation, and irreversible aggregation of proteins are the major causes of alteration in metabolic fluxes in the plants. Chloroplast elongation factor EF-Tu (45–46 kDa), which comes under a highly conserved nuclearencoded multigene family, plays an important role in protecting cellular proteins from thermal aggregation by promoting the guanosine triphosphate (GTP)-dependent binding of aminoacyl-tRNA to the “A-site” of the ribosome during translation (Ristic et al., 2008). It has been reported that transgenic bread wheat expressing a maize gene (Zmeftu1) which codes for plastidial protein synthesis elongation factor (EF-Tu) exhibits greater heat tolerance than nontransgenic wheat varieties (Fu et al., 2008). Transgenic plants displayed a monogenic segregation pattern, reduced heat injury to photosynthetic membranes (thylakoids), reduced thermal aggregation of leaf proteins, enhanced rate of CO2 fixation, and increased grain yield under heat stress (Fu and Ristic, 2010; Fu et al., 2008). Upregulation of ferritin gene Ferritin (FER) is a polypeptide containing 24 homologous and heterologous subunits that functions as an iron storage protein. Through the absorption and release of iron, FERs regulate plant intracellular iron levels. The Vigna cylindrica (L.) Skeels (Green-kernel black bean) ferritin gene (VeFER), driven with maize ubiquitin1 promoter, was integrated into the wheat cultivar via biolistic transformation. Heat-treated transgenic lines were found to possess a significantly higher expression of VeFER gene, lower malondialdehyde (MDA) content, and similar relative electrical conductivities to the heat-resistant variety TAM107 (Zhao et al., 2016). Proteins and nucleic acids can be affected by MDA in a negative manner, further disrupting the cellular membranes’ structural and functional integrity. A lower level of MDA is associated with better membrane thermal stability and transgenic line heat tolerance. Recently, wheat-specific novel ferritin gene TaFER-5B (mapped to chromosome 5B) has been identified and cloned in the wheat cultivar TAM107. Overexpression of the TaFER-5B gene by transforming both the wheat (cv. Jimai 5265) and Arabidopsis has been reported to enhance the heat and other abiotic stress-related oxidative stresses (Zang et al., 2017). Transgenic plants were found to accumulate lesser amounts of O2 and H2O2. Under the temperature-induced oxidative stress, ferritin is considered to transform toxic Fe2+ to the nontoxic chelate complex and thereby protects cells against oxidative stress.

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Integration of transcription factor Transcription factors have a pivotal role in recognizing promoters to regulate gene expression, metabolic functions, organismal function, and so on. Several reports on the transgenic approach via the overexpression of certain genes and transcription factors have shown to enhance the abiotic stress tolerance by the induction of downstream stress-related genes (Gao et al., 2009; El-Esawi and Alayafi, 2019). WRKY, which is an important stress-induced transcription factor family, controls downstream-related genes and has several other roles, including environmental stress tolerance, leaf senescence, and seed development. Wheat plants possessing Arabidopsis-specific WRKY30 gene (AtWRKY30) have been reported to perform better antioxidant enzyme activities (higher APX, CAT, POX, SOD) and lower malondialdehyde, electrolyte leakage, and H2O2 than nontransgenic counterparts under heat and drought stress (El-Esawi et al., 2019). In another study, Xue et al. (2015) overexpressed TaHsfA6f, a member of the A6 subclass of heat shock transcription factors in bread wheat, and found their constitutive expression in green organs but a marked upregulation under heat stress. In transgenic plants, a number of HSP promoter-driven reporter genes were activated, showing improved thermotolerance. Integration of PEP carboxylase gene Better agronomic characteristics, higher nutrient-use efficiency, and excellent photosynthetic capacity due to special morphophysiological attributes give C4 plants an adaptive advantage over C3 plants, especially under drought and heat stress (Zhang et al., 2014). C4 plants make more efficient use of the Calvin cycle to fix more CO2 during photosynthesis. Therefore, modern transgenic techniques are aiming to utilize the superior photosynthetic characteristics of C4 plants to improve the potential yield of C3 crops. The maize-specific ZmPEPC gene (encoding for phosphoenolpyruvate carboxylase enzyme) driven with Cauliflower mosaic virus-derived constitutive promoter (CaMV-35S) was introduced into the background of the common bread wheat using the particle bombardment method (Zhang et al., 2014). Interestingly, wheat plants containing the ZmPEPC gene had improved photochemical and antioxidant enzyme activity, upregulated expression of photosynthesis-related genes, slower chlorophyll degradation, and changed levels of proline and other metabolites, which ultimately contributed to improved heat tolerance (Qi et al., 2017). Upregulation of starch synthesis Starch is a major component of wheat grain (55%–75% of the total dry grain weight). Thus, the grain yield of wheat mainly depends on the endosperm-accumulated starch. There are two main types of glucose molecules in higher plants: linear or less-branched amylose (25%–30%) and large and highly branched amylopectin (70%–75%) molecules ( James et al., 2003; Myers et al., 2000). Both amylose and amylopectin are engendered from ADP-glucose and SSS (soluble starch synthase) enzymes help to extend the linear glucan chains through the addition of glucose units to the nonreducing ends of glucan through α-1,4 linkages, followed by cleaving and reattachment of the glucan segments by starch-branching enzymes to form branches on the polymers ( Jeon et al., 2010; Myers et al., 2000). Reduction in wheat grain yield above 25°C is resulted due to the inactivation of heat-labile SSS1, which limits the starch deposition. However, thermostable SSS1 in subtropical rice species Oryza sativa L. has been reported to produce endosperms with long chains of amylopectin ( Jiang et al., 2003). T. aestivum L. cv. “Bobwhite,” bread wheat lines were transformed with OsSS1, driven by constitutive (maize ubiquitin-1) and endosperm-specific HMW (high-molecular-weight) glutenin Dy10 promoter to improve the heat stress (Tian et al., 2018). Under heat stress conditions, transgenic plants were recorded with an increased (21%–34%) thousand-kernel weight and longer photosynthetic duration.

Cold stress Each year during March and April, about 85% of wheat crops around the world are affected by frost, especially during the early booting stage (Yue et al., 2016). Temperatures below 0°C are observed during the spring season, resulting in severe frost damage (Zheng et al., 2015; Frederiks et al., 2015). As a result of occasional low temperatures during spring, cell organelles are damaged, producing ROS and LP (Thakur et al., 2010). Vegetative and reproductive growth of the plants may be hindered even due to a short-term freezing air during frost stress (Frederiks et al., 2015). Cold stress disrupts root water uptake, which in advertently results in drought stress due to water inadequacy (Aroca et al., 2012). This root damage hinders smooth nutrient uptake, limits nutrient transport, and decreases root ion absorption rate, ultimately causing stunted plant growth (Nezhadahmadi et al., 2013). Cold stress also affects grain-filling rate and grain number per spike, which finally reduces wheat production (Thakur et al., 2010). Cold stress-mediated yield losses are reflected through several yield parameters such as shorter stems, decreased photosynthetic capacity, lower leaf area, spikes, lesser productive tillers and

368 Abiotic stresses in wheat

grains/spike (Li et al., 2015; Valluru et al., 2012). The endurance of cold unaffecting the plant growth and development is called “cold tolerance” (Liu et al., 2019). Plants respond to cold stress in four different phages according to Larcher (2003): (i) initial shock response, (ii) destruction due to prolonged stress or increased severity, (iii) restoration, and (iv) acclimatization (increasing freeze tolerance due to exposure to cold but nonfreezing temperatures). Furthermore, after cold stress (i.e., after temperatures have revived to optimum), an innate recovery response is activated, which is an active process of plant regeneration necessary for further regeneration of plants (Hasanfard et al., 2021). Mitigation of cold tolerance through the implementation of integrated multidisciplinary systems such as the development of improved cold-tolerant wheat cultivars by screening and utilization of cold-tolerant genes, seed treatment with compatible osmolytes, and growth hormones at critical stages are considered the promising strategies (Hassan et al., 2021).

Transgenic approaches to combat cold stress in wheat Integration of barley lipid transfer protein BLT101 (barley lipid transfer protein) from barley has been observed to be upregulated by cold stress (Brown, 1998; Goddard et al., 1993). A promoter analysis revealed the presence of known sequence elements in the upstream region of BLT101, including the dehydration-responsive element/C-repeat (DRE/CRT) and abscisic acid-responsive element, suggesting the involvement of the ABA signaling pathway in the expression of BLT101 (Koike et al., 2008). The BLT101 gene may play a crucial role in protecting cells of the crown region from environmental stress-induced water loss (Brown, 1998). Wheat transgenic plants incorporated with the BLT101 gene were observed to possess similar water content as nontransgenic lines under normal growth conditions. However, 7 days of cold acclimatization resulted in less overall decrease in water content of transgenic lines than that of the nontransgenic ones, indicating that overexpression of BLT101 could improve the water retention ability of wheat plants during cold stress. The plant heights of the transgenic lines were 15%–30% shorter than those of nontransgenic lines under cold stress. BLT101, found to be a negative regulator of growth and development under low-temperature conditions, slowed the growth and development of transgenic lines. In contrast to the nontransgenic lines, the transgenic lines did not show necrotic spots on the first leaf (Choi et al., 2000). Overproduction of Glycine betaine gene from Atriplex hortensis When wheat is exposed to low temperatures (0–2°C), overaccumulation of glycine betaine (GB) protects the plasma membrane (PM). Transgenic wheat lines using the BADH gene isolated from Atriplex hortensis L. GB-rich transgenic lines maintained membrane integrity better under cold stress and displayed higher plasma membrane H+-ATPase activity. The transgenic lines produced lower levels of ROS and membrane lipid peroxidation with an increase in antioxidative enzyme activity and compatible solute content. Overproduction of GB may have led to an increased cold tolerance (Zhang et al., 2010). Integration of GhDREB gene Several factors, including drought, cold stress, and high salt levels, induce the GhDREB gene in cotton (G. hirsutum L.) seedlings. Through improved accumulation of soluble sugars and chlorophyll in leaves, the transgenic plants were found to be more resistant to cold, drought, and high salt stress. There was no phenotypic variation among the transgenic and nontransgenic lines. In the results, GhDREB showed promise as a genetic technique for improving wheat cold tolerance (Gao et al., 2009).

Conclusions Transgenic approaches are one of the most efficient and promising tools for continuing the steady production of wheat coping with the adverse environmental effects. The incorporation of various genes from different organisms to facilitate the production of stress-responsive proteins as well as inducing downstream genes has been widely administered under this approach. Nevertheless, several genes have negative impacts on plants under stress. Although ROS have essential roles in plant’s signaling, overproduction of this molecule has several adverse effects on plants, which already have been discussed in this chapter. Advanced genome editing techniques such as CRISPR-CAS, RNAi may be used to target genes that produce excessive ROS, reduce antioxidant activity, and promote programmed cell death (PCD), as well as an imbalance in hormonal homeostasis, making plants susceptible to abiotic stresses.

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Zang, X., Geng, X., Wang, F., Liu, Z., Zhang, L., Zhao, Y., Tian, X., Ni, Z., Yao, Y., Xin, M., Hu, Z., 2017. Overexpression of wheat ferritin gene TaFER5B enhances tolerance to heat stress and other abiotic stresses associated with the ROS scavenging. BMC Plant Biol. 17 (1), 1–13. Zang, X., Geng, X., He, K., Wang, F., Tian, X., Xin, M., Yao, Y., Hu, Z., Ni, Z., Sun, Q., Peng, H., 2018. Overexpression of the wheat (Triticum aestivum L.) TaPEPKR2 gene enhances heat and dehydration tolerance in both wheat and Arabidopsis. Front. Plant Sci. 9, 1710. Zhang, X.Y., Liang, C., Wang, G.P., Luo, Y., Wang, W., 2010. The protection of wheat plasma membrane under cold stress by glycine betaine overproduction. Biol. Plant. 54 (1), 83–88. https://doi.org/10.1007/s10535-010-0012-4. Zhang, H., Xu, W., Wang, H., Hu, L., Li, Y., Qi, X., Zhang, L., Li, C., Hua, X., 2014. Pyramiding expression of maize genes encoding phosphoenolpyruvate carboxylase (PEPC) and pyruvate orthophosphate dikinase (PPDK) synergistically improve the photosynthetic characteristics of transgenic wheat. Protoplasma 251 (5), 1163–1173. Zhang, G., Yang, J., Zhang, M., Li, Q., Wu, Y., Zhao, X., Zhang, H., Wang, Y., Wu, J., Wang, W., 2021. Wheat TaPUB1 regulates Cd uptake and tolerance by promoting the degradation of TaIRT1 and TaIAA17. J. Agric. Food Chem. 69 (21), 5818–5829. Zhao, Y., Shui, X., Wang, X., Hou, Q., Li, B., Ni, Z., Sun, Q., Liang, R., 2016. Ectopic expression of the Vigna eylindrica ferritin gene enhanced heat tolerance in transgenic wheat (Triticum aestivum L.). Euphytica 209 (1), 23–30. Zheng, B., Chapman, S.C., Christopher, J.T., Frederiks, T.M., Chenu, K., 2015. Frost trends and their estimated impact on yield in the Australian wheatbelt. J. Exp. Bot. 66, 3611–3623. https://doi.org/10.1093/jxb/e rv163. Zobel, R.W., Kinraide, T.B., Baligar, V.C., 2007. Fine root diameters can change in response to changes in nutrient concentrations. Plant Soil 297, 243–254.

Further reading Ashrafzadeh, S., Lehto, N.J., Oddy, G., McLaren, R.G., Kang, L., Dickinson, N.M., Welsch, J., Robinson, B.H., 2018. Heavy metals in suburban gardens and the implications of land-use change following a major earthquake. J. Appl. Geochem. 88, 10–16. Choi, C., Hwang, C.H., 2015. The barley lipid transfer protein, BLT101, enhances cold tolerance in wheat under cold stress. Plant Biotechnol. Rep. 9 (4), 197–207. https://doi.org/10.1007/s11816-015-0357-4. Ji, X., Shiran, B., Wan, J., Lewis, D.C., Jenkins, C.L., Condon, A.G., Richards, R.A., Dolferus, R., 2010. Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat. Plant Cell Environ. 33 (6), 926–942. Karthikeyan, B., Jaleel, C.A., Gopi, R., Deiveekasundaram, M., 2007. Alterations in seedling vigour and antioxidant enzyme activities in Catharanthus roseus under seed priming with native diazotrophs. J. Zhejiang Univ. Sci. B 8 (7), 453–457. Khan, S., Anwar, S., Yu, S., Sun, M., Yang, Z., Gao, Z.Q., 2019. Development of drought-tolerant transgenic wheat: achievements and limitations. Int. J. Mol. Sci. 20 (13), 3350. Lajayer, B.A., Ghorbanpour, M., Nikabadi, S., 2017. Heavy metals in contaminated environment: destiny of secondary metabolite biosynthesis, oxidative status and phytoextraction in medicinal plants. Ecotoxicol. Environ. Saf. 145, 377–390. Lawlor, D.W., Cornic, G., 2002. Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ. 25 (2), 275–294. Powell, W., Morgante, M., Andre, C., Hanafey, M., Vogel, J., Tingey, S., Rafalski, A., 1996. The comparison of RFLP, RAPD, AFLP and SSR (microsatellite) markers for germplasm analysis. Mol. Breed. 2 (3), 225–238. Russell, J.R., Fuller, J.D., Macaulay, M., Hatz, B.G., Jahoor, A., Powell, W., Waugh, R., 1997. Direct comparison of levels of genetic variation among barley accessions detected by RFLPs, AFLPs, SSRs and RAPDs. Theor. Appl. Genet. 95 (4), 714–722. Shahid, M., Khalid, S., Abbas, G., Shahid, N., Nadeem, M., Sabir, M., Aslam, M., Dumat, C., 2015. Heavy metal stress and crop productivity. In: Crop Production and Global Environmental Issues. Springer, Cham, pp. 1–25. Suzuki, H., Oshita, E., Fujimori, N., Nakajima, Y., Kawagoe, Y., Suzuki, S., 2015. Grape expansins, VvEXPA14 and VvEXPA18 promote cell expansion in transgenic Arabidopsis plant. Plant Cell Tiss. Org. Cult. 120, 1077–1085. Tang, L., Ying, R.R., Jiang, D., Zeng, X.W., Morel, J.L., 2013. Impaired leaf CO2 diffusion mediates Cd-induced inhibition of photosynthesis in the Zn/Cd hyperaccumulator Picris divaricata. Plant Physiol. Biochem. 73, 70–76. Tripathi, D.K., Mishra, R.K., Singh, S., Singh, S., Vishwakarma, K., Sharma, S., Singh, V.P., Singh, P.K., Prasad, S.M., Dubey, N.K., Pandey, A.C., Sahi, S., Chauhan, D.K., 2017. Nitric oxide ameliorates zinc oxide nanoparticles phytotoxicity in wheat seedlings: implication of the ascorbate–glutathione cycle. Front. Plant Sci. 8, 1–10. Wu, G., Kang, H., Zhang, X., Shao, H., Chu, L., Ruan, C., 2010. A critical review on the bio-removal of hazardous heavy metals from contaminated soils: issues, progress, eco-environmental concerns and opportunities. J. Hazard. Mater. 174, 1–8. Yang, X., Lu, C., 2005. Photosynthesis is improved by exogenous glycinebetaine in salt-stressed maize plants. Physiol. Plant. 124 (3), 343–352.

Chapter 24

Plant-microbe interactions in wheat to deal with abiotic stress Xiaolan Lia,⁎,#, Qunli Rena, Chengcheng Liaoa, Qian Wanga, Mingjian Renb, Mingsheng Zhangb, Xiaokang Qianc, Shengwei Yangd, Huan Hua, Miao Wanga, and Jianguo Liua a

Microbial Resources and Drug Development Key Laboratory of Guizhou Tertiary Institution, Life Sciences Institute, School of Preclinical Medicine,

Zunyi Medical University, Zunyi, Guizhou Province, China, b College of Agriculture, College of Life Sciences, Guizhou University, Guiyang, Guizhou Province, China, c Zunyi City Rural Development Service Center, Zunyi, Guizhou Province, China, d Zunyi Agricultural Science and Technology Research Institute, Zunyi, Guizhou Province, China ⁎

Corresponding author. e-mail: [email protected]

Introduction Plant-microbe interactions In nature, plants live in an environment full of various microbes. In order to survive, plants and microbes will form an interactive relationship. This is a complex, dynamic, and continuous process. When microbes invade plants, they may have beneficial effects on plants such as promoting growth, enhancing stress resistance, providing nutrients, bioremediation and may also have harmful effects such as causing disease and death (Alexander et al., 2021; Cheng et al., 2019; Dolatabadian, 2020; Sharma et al., 2020). At the same time, plants can also regulate the microbial community and diversity by producing secondary metabolites and providing nutrients (Uroz et al., 2019). The interaction between plants and microbes is widespread in nature. For example, when rhizobia formed a symbiotic relationship with legumes, differentiated bacteria were enclosed in intracellular compartments and became symbionts within root nodules, and nodules and associated symbiont structures may effectively fix nitrogen for plant growth (Oldroyd et al., 2011). Wheat endophytic fungi may also be passed on to their progeny and facilitated their recovery from stress (Vujanovic et al., 2019). Plants interact with environmental microbes throughout their lives. These interactions determine plant development, nutrition, and health in dynamic and stressful environments. Plants and their interacting microbes are not separate entities, but a unified evolutionary unit (Uroz et al., 2019).

How do plants interact with microbes? The interaction between plants and microbes is a common phenomenon in nature, but the principles are complex and diverse, including: (1) Homologous plant immune receptors sense microbial signals and initiate defense or symbiotic responses; (2) Microbial DNA and/or protein secretion systems will transport of effector molecules to plant cells to modulate host cell functions; (3) Microbes and plants coordinate to form specialized nutrient exchanges or to generate new organs (such as nodules and galls) during symbiotic and pathogenic interactions; (4) Binary and community-level adversarial responses in plant-microbe interactions (Cheng et al., 2019). Plants have evolved a multilayered immune system in the process of adapting to the environment, with precise defense strategies against pathogen attack. Multiple subcellular compartments and their interactions coordinate multiple immune signaling pathways, which play an important role in the immune response. Pathogens use a variety of strategies, either directly attacking the plant’s immune system or indirectly manipulating the plant’s physiological state to suppress the immune response. Membrane transport events, cytoskeletal reorganization, subcellular dynamics, and intercellular communication are involved in the immune response (Park et al., 2018). Rhizobium entered legume root cells, which required proper recognition of the rhizobia Nod factor signaling molecule, # Foundation: Zunyi Medical University 2018 special project for the cultivation of new academic seedlings and innovative exploration (Qian ke he platform talent [2018]5772-062; [2018]5772-075); Science and technology project of Zunyi city (Zun shi ke he HZ (2020) No.55); Guizhou Province Traditional Chinese Medicine Administration Project (QZYY-2019-064). Abiotic Stresses in Wheat. https://doi.org/10.1016/B978-0-323-95368-9.00022-9 Copyright © 2023 Elsevier Inc. All rights reserved.

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which activated a series of events including polarized root hair tip growth, invagination associated with bacterial infection, and promotion of cortical cells division leading to nodular meristems, terminal differentiation of bacteria within nodules which may lead to loss of bacterial viability, and complex exchange of metabolites and regulatory peptides forcing bacteria into a nitrogen-fixing organelle-like state for efficient nitrogen fixation (Oldroyd et al., 2011). Uncovering plant-microbe interrelationships is a key to identifying positive and negative effects of microbes on plants (Sharma et al., 2020), providing direction for the development of technologies for the application of beneficial microbes in sustainable agriculture and nature restoration (Haldar and Sengupta, 2015). Studies have shown that the nature of plant-endophyte interactions ranging from mutualistic to pathogenic, depending on abiotic and biotic factors, including plant and microbial genotypes, environmental conditions, and dynamic networks of interactions within plant biomes (Hardoim et al., 2015).

Where do the microbes that interact with plants come from? The sources of microbes that interact with plants can be soil rhizosphere microbes, plant endophytes, etc. Rhizosphere microbes from soil interact extensively with plants. There are about tens of thousands of microbes associated with plant roots, forming a complex microbial community. It is the second genome of plants and is essential for plant health and stress resistance, which is one of the important sources of microbes that interact with plants. Studies of plant-microbe interactions have found that plants can form rhizosphere microbial communities and that different plant species have specific microbial communities when growing on the same soil. When attacked by pathogens or insects, plants are able to recruit protective microbes and enhance microbial activity to suppress rhizosphere pathogens, which provides an opportunity to control plant root microbial community selection and activity mechanisms, thereby increasing crop yields (Berendsen et al., 2012). Endophytes isolated from plants are also an important source of interacting microbes. All plants are inhabited by diverse microbial communities, including bacterial, archaeal, fungal, and protist groups, which colonized various plant tissues and organs. These microbes play a role in plant development, growth, health, and diversification and can also form new plantmicrobe interactions with other plants and become endophytes to other plants after isolation, culture, and reinoculation (Hardoim et al., 2015; Santoyo et al., 2016). For example, Pseudomonas strain LTGT-11-2Z isolated from the roots of the desert plant Alhagi sparsifolia can interact with wheat to enhance its drought resistance (Zhang et al., 2020). Plant growth-promoting microbes (PGPM) isolated from plants are also widely inoculated in crops to enhance their stress resistance and yield (Dubey et al., 2020; Santoyo et al., 2016).

Plant selectivity for interacting microbes Although there are many types of microbes that interact with plants, not all plants interact with the same microbes. In other words, different plants have their own preferences for interacting microbes, which means that each plant has its own dominant microbes, and even the same plant will have special dominant microbe communities in different living environments. Microbes isolated from soil, root, and shoot samples of four different Salsola plants and wheat plants showed that Proteobacteria and Actinobacteria were the most abundant phyla in Salsola and wheat. However, Firmicutes, Acidobacteria, Bacteroidetes, Planctomycetes, Thermotogae, Verrucomicrobia, Chloroflexi, and Euryarchaeota were predominant groups from halophyte, whereas Actinobacteria, Proteobacteria, Firmicutes, Cyanobacteria, Acidobacteria, Bacteroidetes, Planctomycetes, and Verrucomicrobia were predominant phyla of wheat samples (Mukhtar et al., 2017). When we studied the endophyte of Dendrobium officinale root, we found that the predominant microbe groups of Dendrobium officinale varied in different regions. All of these indicate that plants have selectivity for interacting microbes, and this selectivity may exist in order to adapt to different living environments.

Interactions between plants and microbes under abiotic stress Both plants and microbes live in natural environments and are constantly affected by abiotic and biotic stresses. These stresses may positively or negatively affect plant-microbe interactions. Among them, abiotic stresses such as cold, heat, drought, salt, heavy metal pollution, waterlogging can play a role directly or indirectly (Kumar and Verma, 2018; Sharma et al., 2020). Rainfall, which typically created a period of high atmospheric humidity, may promote disease outbreaks in plants, as water-soaked spots were often seen on infected plant leaves during pathogen infestation, which were early symptoms of disease. Specialized virulence proteins were used exclusively in the exosome to create an aqueous environment, suggesting that moisture was critical for pathogenesis, and the interaction between host, pathogen, and environment is known as the “disease triangle” (Aung et al., 2018). Drought stress affects various physiological and biochemical processes such as the number and activity of rhizosphere microbes, photosynthesis, respiration, transport, ion absorption, carbohydrate, and nutrient metabolism of plants. Plant growth-promoting rhizobacteria (PGPR) were able

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to protect plants from pathogen attack by enhancing the production of phytohormones, siderophores, biofilms, and exopolysaccharides (EPS) and by increasing the availability of nutrients in the rhizosphere, and produced EPS, which formed root sheaths around the roots, thereby protecting plant roots from drought stress for longer periods of time (Naseem et al., 2018). Climate and/or heavy metal stress effects affected the growth, physiology, biochemistry, and yield of crops. Elevated carbon dioxide in the atmosphere increased material production and metal accumulation in plants and helped plants support larger microbial populations and/or protect microbes from heavy metals stress, and climate change indirectly affected changes in plant root function and structure and the rhizosphere changes in the diversity and activity of microbes lead to changes in the bioavailability of metals in soils, which in turn affected plant growth (Rajkumar et al., 2013). It can be seen that the influence of abiotic stress on the interaction between plants and microbes is inevitable.

Plant-microbe interactions in wheat to deal with abiotic stress Wheat (Triticum aestivum L.) is a crop with important economic value, and there are great differences in soil type, temperature, pH, organic matter, and moisture status in the environment where it is grown. Global warming causes wheat crops to enter a heat stress environment. On the basis of the optimum temperature of 20–25°C, every 1°C increase will reduce the grain filling period and grain weight of wheat by 2.8 days and 1.5 mg, respectively. It has a serious impact on the growth period, grain setting rate, maturity period, grain growth rate, and final total grain yield, etc., resulting in a decline in wheat yield, which undoubtedly threatens human food supply and security. There are genetic resources for high temperature and stress tolerance in the wheat gene pool, but the proportion of these resources integrated into cultivated wheat is only about 15% (Ahlawat et al., 2022). Therefore, it is necessary to explore more efficient ways of stress resistance to ensure the sustainable production of wheat. Among the resources of plant-microbe interaction, it is a good, effective, and feasible way to mine and develop microbial inoculants that are beneficial to wheat stress resistance (Afridi et al., 2019). Almost all the organs of plants, such as roots, stems, leaves, flowers and fruits, are colonized with microbes. These microbes are called endophytes of plants. Endophytes form a mutually beneficial relationship with plants and can endow plants with the ability to survive in stress (Ahlawat et al., 2022). Many microbes such as Penicillium and Pseudomonas can interact with wheat and can enhance the stress resistance (Vujanovic et al., 2019; Zhang et al., 2020), which lays the foundation for studying the ability of microbes to confer abiotic stress tolerance in wheat.

Microbes providing wheat with a variety of abiotic stress resistance Although microbes have positive and negative effects on wheat, many high-quality stress-resistant microbial resources are left after double screening of stresses and plants, which can have a positive impact on wheat growth under abiotic stresses, including improving stress resistance, promoting growth, and maintaining survival. For example, endophytes contribute to plant performance especially under harsh conditions (Llorens et al., 2019).

Salt resistance and its mechanism Salt is one of the major obstacles to crop production in the world’s arid regions, and a variety of salt-tolerant microbes can confer salt resistance to wheat. At present, it has been found that microbes such as Bacillus, Trichoderma harzianum, and Trichoderma can interact with wheat and enhance its salt tolerance. Most of these microbes are plant growth-promoting microbes. Bacillus such as EGI 63071, EGI 63106, FAB10, PM13, PM15, PM19, B-16 (Amna et al., 2019; Ansari et al., 2019; Liu et al., 2019; Singh et al., 2021), Kocuria rhizophila KF875448 and Cronobacter sakazakii KM042090 (Afridi et al., 2019), Chaetomium coarctatum, Alternaria chlamydospora (Bouzouina et al., 2021), Enterobacter cloacae HG-1 ( Ji et al., 2020), Trichoderma Th4, Th6 (Oljira et al., 2020), and Trichoderma harzianum UBSTH-501 (Singh et al., 2021) have played an active role in the salt resistance of wheat (Table 1). TABLE 1 Microbes providing wheat with salt tolerance. Microbe

Strain

Mechanism

Reference

Bacillus sp.

EGI 63071

Promoting the growth of wheat seedling, the length of leaf, dry weight of leaf, and germination rate

Liu et al. (2019)

Bacillus sp.

EGI 63106

Promoting the length of root and dry weight of root

Liu et al. (2019) Continued

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TABLE 1 Microbes providing wheat with salt tolerance—cont’d Microbe

Strain

Mechanism

Reference

Kocuria rhizophila

KF875448 (14ASP)

Promoting fresh dry weight, root shoot length, proline, and chlorophyll contents, K+/Na+ ratio in the tissues; decreasing the Na+ contents

Afridi et al. (2019)

Cronobacter sakazakii

KM042090 (OF115)

Promoting fresh dry weight, root shoot length, proline, and chlorophyll contents, K+/Na+ ratio in the tissues; decreasing the Na+ contents

Afridi et al. (2019)

Chaetomium coarctatum

Improving wheat seedling emergence, root growth, proline content, leaf sugar level

Bouzouina et al. (2021)

Alternaria chlamydospora

Improving wheat seedling emergence, root growth, proline content

Bouzouina et al. (2021)

Fusarium equiseti

Improving root growth, proline content

Bouzouina et al. (2021)

Bacillus siamensis

PM13

A very positive influence on germination rate of wheat seedlings, root and shoot length, and photosynthetic pigments

Amna et al. (2019)

Bacillus sp.

PM15

Improving germination rate of wheat seedlings, root and shoot length, and photosynthetic pigments

Amna et al. (2019)

Bacillus methylotrophicus

PM19

Improving roots length, vegetative shoot growth, seedling’s fresh, and dry weights

Amna et al. (2019)

Arthrobacter crystallopoietes

GHD-E-6

Improving survival percentages

Albdaiwi et al. (2019)

Oceanobacillus picturae

GSF-E-11

Improving root length, survival percentages, degrading ACC

Albdaiwi et al. (2019)

Bacillus subtilis subsp.

GSW-E-5

Improving levels of IAA, root length

Albdaiwi et al. (2019)

Bacillus subtilis subsp.

GSW-E-6

Improving levels of IAA, germination percentages, root length, survival; degrading ACC

Albdaiwi et al. (2019)

Bacillus licheniformis

GSW-E-7

Improving germination percentages, root length, shoot projected area and shoot length, seedling growth

Albdaiwi et al. (2019)

Bacillus pumilus

FAB10

Improving photosynthesis, transpiration, content of proline, biofilm development, reducing in antioxidant enzyme activities (catalase, superoxide dismutase, and glutathione reductase), and malonaldehyde content

Ansari et al. (2019)

Enterobacter cloacae

HG-1

Improving root length, plant height, fresh weight, dry weight, the proline concentration in the leaves, K+, Ca2+; decreasing the malondialdehyde level, Na+

Ji et al. (2020)

Trichoderma yunnanense

Th4

Producing IAA; improving all photosynthetic parameters, net photosynthesis, biomass production

Oljira et al. (2020)

Trichoderma afroharzianum

Th6

Producing IAA; improving all photosynthetic parameters, net photosynthesis, biomass production

Oljira et al. (2020)

Bacillus licheniformis

C7

Producing IAA; improving all photosynthetic parameters

Oljira et al. (2020)

Trichoderma harzianum

UBSTH501

Improving accumulation of proline, total soluble sugar, organic solutes, antioxidant enzyme, the uptake and translocation of K+ and Ca2+; reducing Na+ content; higher expression of TaHKT-1 and TaNHX1 in the roots; increasing the expression of ZIP transporters; maintaining the Na+/K+ balance in the plant tissue; increasing biofortification of Zn in wheat grown

Singh et al. (2021)

Bacillus amyloliquefaciens

B-16

Improving accumulation of proline, total soluble sugar, organic solutes, antioxidant enzyme, the uptake and translocation of K+ and Ca2+; reducing Na+ content; higher expression of TaHKT-1 and TaNHX1 in the roots; increasing the expression of ZIP transporters; maintaining the Na+/K+ balance in the plant tissue; increasing biofortification of Zn in wheat grown

Singh et al. (2021)

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After the interaction between microbes and wheat, the salt tolerance of wheat is enhanced through a variety of mechanisms, which can be summed up in the following mechanisms: (1) Regulating the growth-promoting effect Microbes can promote wheat germination rate, seedling emergence rate, seedling root growth, survival rate, and plant growth, increase biomass production, and reduce seedling mortality to enhance wheat salt tolerance. Bacillus EGI 63071 and EGI 63106 can effectively promote the growth of common wheat (Wheat: Xindong 18) seedlings under salt stress (Liu et al., 2019). Inoculation of wheat with Kocuria rhizophila 14ASP and Cronobacter sakazakii OF-115 increased plant fresh and dry weight and rhizome length (Afridi et al., 2019). Chaetomium coarctatum (66.7%) and Alternaria chlamydospora (56.7%) improved wheat at moderate salinity (2.5 dS/m) compared with uninoculated controls (50%). Seedling emergence rate at severe salinity (14 dS/m), enhanced only by Alternaria chlamydospora. Furthermore, Alternaria chlamydospora and Fusarium equiseti promoted root growth under salinity stress (Bouzouina et al., 2021). PM13, PM15, and PM19 had very positive effects on germination rate, root, and shoot length of wheat seedlings (Amna et al., 2019). Arthrobacter crystallopoietes (GHD-E-6) improved water survival percentages; Oceanobacillus picturae (GSF-E-11) promoted root length and survival percentages; Bacillus subtilis subsp. (GSW-E-6) promoted root length, germination percentages and survival rate; Bacillus licheniformis (GSW-E-7) improved root length, germination percentages, antifungal activity against Fusarium culmorum, shoot projected area and shoot length, and seedling growth (Albdaiwi et al., 2019). Bacillus pumilus (FAB10) developed biofilm (Ansari et al., 2019). Enterobacter cloacae HG-1 increased in root length, plant height, fresh weight, and dry weight ( Ji et al., 2020). In addition, microbes can also promote wheat growth by regulating 1-aminocyclopropane-1-carboxylate (ACC). GSF-E-11 and GSW-E-6 degraded ACC content (Albdaiwi et al., 2019). ACC is a precursor of ethylene, reducing ACC thereby reduces ethylene levels during plant growth, which is helpful for plant growth. It can be seen that microbes can play the role of promoting growth by regulating multiple indicators related to wheat growth to resist salt stress. (2) Regulating auxin IAA A variety of strains can produce indole-3-acetic acid (IAA) after inoculation of wheat, such as GSW-E-5, GSW-E-6, Th4, and Th6 (Albdaiwi et al., 2019; Oljira et al., 2020), and IAA further promotes plant growth (Zhu et al., 2021). (3) Regulating antioxidant effects Antioxidant enzymes include superoxide dismutase, thioredoxin peroxidase, glutathione peroxidase, and catalase, which can convert peroxides formed in the plants into less toxic or harmless substances, thereby reducing the damage of peroxides to plants (Li et al., 2019). Multistrain inoculation of wheat can increase its antioxidant activity, such as 14ASP and OF115 increased the antioxidant activity of wheat (Afridi et al., 2019). Trichoderma harzianum (UBSTH501) and Bacillus amyloliquefaciens (B-16) increased antioxidant enzyme (Singh et al., 2021). However, FAB10 reduced in antioxidant enzyme activities (including catalase, superoxide dismutase, and glutathione reductase) (Ansari et al., 2019). It shows that the regulation of antioxidant effect of microbes may be varied due to different bacterial species, and the effect of enhancing salt resistance may not be the result of a single mechanism. (4) Regulation of ionic balance Salt stress disturbs the cellular osmotic and ionic balance, which then creates a negative impact on plant growth and development. The Na+ and Cl ions can enter into plant cells through various membrane transporters, including specific and nonspecific Na+, K+, and Ca2+ transporters (Saddhe et al., 2021). High accumulation of Na+ ions in plants causes toxicity that can result in yield reduction. Na+/K+ homeostasis is known to be important for salt tolerance in plants (Farooq et al., 2021). Microbes can regulate and balance the levels of these ions by interacting with wheat, thereby improving salt tolerance. Inoculation of wheat with 14ASP and OF115 reduced Na+ content, and the K+/Na+ ratio in plant tissues was higher than that of control (Afridi et al., 2019). HG-1 increased K+ and Ca2+ content and decreased Na+ content ( Ji et al., 2020). UBSTH-501 and B-16 increased the uptake and translocation of K+ and Ca2+ and reduced Na+ content, maintaining the Na+/K+ balance in the plant tissue (Singh et al., 2021). It indicated that microbes play an important role in regulating the ion concentration and balance in wheat. (5) Regulation of proline level Proline improves plant growth with increasing in seed germination, biomass, photosynthesis, gas exchange, and grain yield (El Moukhtari et al., 2020). Various microbes can increase proline content of wheat such as 14ASP, OF115, FAB10, UBSTH-501, B-16, HG-1, Chaetomium coarctatum, Alternaria chlamydospore, siderophore, and salt-tolerant bacteria, solubilizing phosphate, and salt-tolerant bacteria (Afridi et al., 2019; Ansari et al., 2019; Bouzouina et al., 2021; Emami et al., 2019; Ji et al., 2020; Singh et al., 2021). It was suggested that these microbes promoted wheat growth by increasing proline levels, thereby improving salt tolerance.

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(6) Regulation of photosynthesis Microbes can enhance salt resistance by regulating wheat chlorophyll content and net photosynthesis. 14ASP and OF115 inoculated wheat and increased chlorophyll content (Afridi et al., 2019). PM13, PM15, and PM19 have very positive effects on wheat photosynthetic pigments (Amna et al., 2019). Th4, Th6, and C7 were correlated with all photosynthetic parameters, and Th4 and Th6 enhanced net photosynthesis (Oljira et al., 2020). Photosynthesis is regulated by microbes and often affects the sugar content of wheat. Chaetomium coarctatum increased leaf sugar levels (Bouzouina et al., 2021). UBSTH-501 and B-16 increased the accumulation of total soluble sugar and organic solutes (Singh et al., 2021). The high sugar content is useful to protecting the structures of photosystems, enhancing photosynthetic performance and sucrose synthetase activity, as well as inhibiting sucrose degradation (Yang et al., 2019). (7) Regulating water use Microbes can improve wheat salt tolerance by regulating water use, such as GSF-E-11 improved water deficit tolerance (Albdaiwi et al., 2019) and FAB10 improved transpiration (Ansari et al., 2019). This indicates that microbes can regulate water utilization in different ways. (8) Regulate wheat gene expression Microbes can enhance salt tolerance by regulating wheat gene expression. UBSTH-501 and B-16 increased the expression of ZIP transporters, biofortification of Zn in wheat grown, the expression of TaHKT-1 and TaNHX1 in the roots (Singh et al., 2021). This indicated that the ZIP transporter may play an important role in microbial conferring salt tolerance in wheat. In addition to the above mechanisms, different varieties of wheat interact with the same salt-tolerant endophyte and have different salt-tolerance capabilities; various bacterial species have different influences on the same variety of wheat. Wheat variety Pasban 90 was more tolerant than Khirman to salt stress in all the measured morphological and biochemical parameters, while the bacterial strain OF115 performed significantly better in all morphological and biochemical parameters, such as fresh dry weight, root shoot length, proline and chlorophyll contents, compared with strain 14ASP (Afridi et al., 2019). In summary, the interaction between microbes and wheat can improve its salt stress tolerance through two or more mechanisms, and these mechanisms are mainly by directly or indirectly promoting the growth-related indicators or related pathways and maintenance of ion balance in wheat under salt stress. This is very important for the use of microbial resources to develop biological inoculants through interaction to improve the salt resistance of wheat.

Drought resistance and its mechanism Drought is one of the most destructive abiotic stresses limiting crop growth and yield worldwide. Understanding microbialmediated plant drought resistance is important for sustainable agriculture. This could open up new avenues for improving crop drought resistance under field conditions. Endophytes from drought-tolerant plants and rhizosphere microbes in arid soil have superior performance in improving the drought tolerance of wheat. A variety of microbes can play an active role in improving drought tolerance in wheat, such as Pseudomonas (Zhang et al., 2020), Klebsiella sp. (Zhang et al., 2017), and Pantoea alhagi sp. (Chen et al., 2017) (Table 2). The interaction of these microbes with wheat can improve drought resistance through a variety of mechanisms.

TABLE 2 Microbes providing wheat with drought tolerance. Microbe

Strain

Mechanism

Reference

Pseudomonas

LTGT-11-2Z

Improving shoot length, root length, total plant fresh weight, and dry weight; production of siderophore, ACC deaminase activity

Zhang et al. (2020)

Klebsiella sp.

LTGPAF-6F

Nitrogen fixation; production of IAA, acetoin, 2,3-butanediol, spermidine and trehalose

Zhang et al. (2017)

Pantoea alhagi sp. nov.

LTYR-11Z(T)

Promoting the growth, accumulation of soluble sugars; decreasing accumulation of proline, malondialdehyde (MDA, degradation of chlorophyll in leaves

Chen et al. (2017)

Ascomycete Trichoderma harzianum

TSTh20-1 (hereafter, TSTh)

Increasing germination speed, percent germination, biomass accumulation, the level of peroxidase, petrochemical mobilization; metabolizing 13C-phenanthrene to 13CO2 in 0.5% oxygen

Repas et al. (2017)

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TABLE 2 Microbes providing wheat with drought tolerance—cont’d Microbe

Strain

Mechanism

Reference

Aspergillus niger

581PDA1

Antibiotic sensitivity of Nystatin; production of ACCD; phosphate solubilization

Ripa et al. (2019)

Fusarium oxysporum

581PDA2

Production of IAA

Ripa et al. (2019)

Penicillium aurantiogriseum

581PDA3

Antibiotic sensitivity of Nystatin, Ketoconazole and Itraconazole; production of ACCD; phosphate solubilization

Ripa et al. (2019)

Fusarium incarnatum

581PDA4

Antibiotic sensitivity of Nystatin, Ketoconazole and Itraconazole; phosphate solubilization

Ripa et al. (2019)

Alternaria alternata

581PDA5

Production of ACCD; phosphate solubilization

Ripa et al. (2019)

Alternaria tenuissima

581PDA7

Production of ACCD and IAA; phosphate solubilization

Ripa et al. (2019)

Cladosporium cladosporioides

582PDA1

Antibiotic sensitivity of Ketoconazole and Itraconazole; production of ACCD

Ripa et al. (2019)

Talaromyces funiculosus

582PDA4

Antibiotic sensitivity of Nystatin; production of IAA; phosphate solubilization

Ripa et al. (2019)

Aspergillus flavus

582PDA5

Antibiotic sensitivity of Nystatin; production of ACCD and IAA

Ripa et al. (2019)

Trichoderma aureoviride

582PDA6

Antibiotic sensitivity of Nystatin, Ketoconazole and Itraconazole; production of ACCD and IAA; phosphate solubilization

Ripa et al. (2019)

Trichoderma harzianum

582PDA7

Antibiotic sensitivity of Nystatin, Ketoconazole and Itraconazole; production of ACCD and IAA; phosphate solubilization

Ripa et al. (2019)

Penicillium janthinellum

582PDA8

Antibiotic sensitivity of Ketoconazole and Itraconazole; production of IAA; phosphate solubilization

Ripa et al. (2019)

Fusarium proliferatum

582PDA9

Antibiotic sensitivity of Nystatin; production of IAA; phosphate solubilization

Ripa et al. (2019)

Fusarium equiseti

582PDA11

Antibiotic sensitivity of Ketoconazole and Itraconazole; production of IAA; phosphate solubilization

Ripa et al. (2019)

Aspergillus stellatus

582PDA13

Antibiotic sensitivity of Ketoconazole, Itraconazole; production of ACCD; phosphate solubilization

Ripa et al. (2019)

Kosakonia pseudosacchari

TL13

Production of IAA, siderophores, ammonia, ACC deaminase; solubilize phosphate

Romano et al. (2020)

Penicillium sp.

Improving yield, root systems, survival

Ridout and Newcombe (2016)

Candidatus Saccharibacteria and Planctomycetes

Increasing abundance of the 16S rRNA and acdS genes in plant roots, grain yield, photosynthetic capacity of plants

Yaghoubi Khanghahi et al. (2021)

Incertae sedis

SMCD 2206

Increasing seeds germination, average seed weight, total seed weight

Hubbard et al. (2014)

Incertae sedis

SMCD 2210

Increasing seeds germination, Fv/Fm values, average seed weight, total seed weight

Hubbard et al. (2014)

Incertae sedis

SMCD 2215

Increasing seeds germination, Fv/Fm values, average seed weight, total seed weight

Hubbard et al. (2014)

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Abiotic stresses in wheat

(1) Growth-promoting mechanism A variety of microbes can promote wheat growth under drought conditions. Penicillium sp. doubled yield, developed larger root systems, and improved survival (Ridout and Newcombe, 2016). Pantoea alhagi sp. Nov LTYR-11Z(T) promoted the growth (Chen et al., 2017). Ascomycete Trichoderma harzianum TSTh20-1 increased germination speed, germination percentage, and biomass accumulation (Repas et al., 2017). Pseudomonas strain LTGT-11-2Z promoted shoot length, root length, total plant fresh weight, and dry weight (Zhang et al., 2020). Candidatus Saccharibacteria and Planctomycetes improved grain yield (Yaghoubi Khanghahi et al., 2021). Incertae sedis SMCD 2206, SMCD 2215, and SMCD 2210 increased seeds germination, average seed weight, total seed weight (TSW) (Hubbard et al., 2014). Illustrating each growth-promoting microbes may promote wheat growth through different growth indicators. In addition, microbes can also exert growth-promoting effects by regulating ACC enzymes. LTGT-11-2Z and Kosakonia pseudosacchari TL13 produced ACC deaminase, respectively (Romano et al., 2020; Zhang et al., 2020); moreover, TL13 also produced ammonia (Romano et al., 2020). (2) Regulating plant hormones After a variety of microbes are inoculated with wheat, they can synthesize IAA, an important plant hormone that promotes growth. IAA accelerates plant growth and development by improving root/shoot growth and seedling vigor, and it involves in cell division, differentiation, and vascular bundle formation and is an essential hormone for nodule formation (Gopalakrishnan et al., 2015). Klebsiella sp. LTGPAF-6F, Fusarium oxysporum 581PDA2, and Kosakonia pseudosacchari TL13 can produce IAA, respectively (Ripa et al., 2019; Romano et al., 2020; Zhang et al., 2017). It indicates that IAA plays an important role in wheat drought resistance. (3) Regulation of photosynthesis After the interaction between microbes and wheat, photosynthesis can also be regulated by adjusting photosynthetic pigments and metabolizing carbon in organic matters. LTYR-11Z(T) decreased degradation of chlorophyll in leaves (Chen et al., 2017). TSTh20-1 metabolized 13C-phenanthrene to 13CO2 in 0.5% oxygen (Repas et al., 2017). Candidatus Saccharibacteria and Planctomycetes improved photosynthetic capacity of plants (Yaghoubi Khanghahi et al., 2021). It shows that various microbes use different ways to regulate wheat photosynthesis to improve its drought resistance. (4) Regulating antioxidant effects Drought stress can produce peroxides in wheat, and microbes can also play an active role in this field. TSTh20-1 improved the level of peroxidase (Repas et al., 2017). However, at present, there are not many microbial resources that play an antioxidant role to improve the drought resistance of wheat and need to be further explored. (5) Regulation of metabolites Microbes can resist drought stress by altering the accumulation of wheat metabolites. LTGT-11-2Z produced exopolysaccharide (Zhang et al., 2020), and exopolysaccharide may contribute to the structure and stability of complex aggregates of microorganisms in biofilms and flocs (Sutherland, 2001). LTYR-11Z(T) increased accumulation of soluble sugars and decreased accumulation of proline and malondialdehyde (MDA) (Chen et al., 2017). Klebsiella sp. LTGPAF-6F produced acetoin, 2,3-butanediol, spermidine and trehalose (Zhang et al., 2017). TL13 solubilized phosphate (Romano et al., 2020). Acetoin and butanediol against pests and pathogens; Trehalose is an osmoprotectant (Gopalakrishnan et al., 2015); Spermidine protects against the damage induced by different types of abiotic stresses (Alca´zar et al., 2020). It shows that different microbes have differences in the accumulation and regulation of wheat metabolites, and the metabolites are beneficial for wheat to resist various stresses. (6) Regulating water use efficiency Water use efficiency (WUE) is defined as the amount of carbon assimilated as biomass or grain produced per unit of water used by the crop. Climate change will affect plant growth, but enhancing WUE may offset the impact of a changing climate (Ellsworth and Cousins, 2016; Hatfield and Dold, 2019). TSTh20-1 improved plant water use efficiency and drought recovery (Repas et al., 2017). It shows that microbes have great potential in improving wheat water use efficiency and reducing the impact of drought. (7) Regulating siderophore Iron is a typical essential plant micronutrient. Siderophores are capable of sequestering Fe3+, they have high affinity for Fe3+ and thus make the iron available for plants. Otherwise, siderophores can also form stable complex with heavy metals such as Al, Cd, Cu and with radionuclides including U and NP. Thus, the siderophore producing microbes can relieve plants from heavy metal stress and assist in iron uptake (Gopalakrishnan et al., 2015). LTGT-11-2Z and TL13 can produce siderophore, respectively (Romano et al., 2020; Zhang et al., 2020). It is suggested that these microbes can improve drought resistance by providing available iron ions to wheat through siderophores and also enhance the ability to resist heavy metal stress.

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In addition, after the interaction between microbes and wheat, the microbes can also be passed from seeds to progeny, providing the progeny with drought resistance and helping progeny to actively recruit endosymbiotic communities to resist pathogens and abiotic stress, and the distribution of endophytes will be more regular. Droughtstressed plants experienced a positive shift in the seed mycobiome composition, moderated by the external acquisition of endophytic Penicillium (E +) at the seed level. E + plants hosted a relatively higher abundance of Ascomycota in the 2nd and 3rd seed generations of wheat, whereas higher abundance of Basidiomycota was detected in 1st generation seeds (Vujanovic et al., 2019). Moreover, the changes in the bacterial endophytes’ variabilities were associated preferentially with the drought stress varietal characteristics of the analyzed wheat instead of the applied stress conditions (Zˇiarovska´ et al., 2020).

Resistance to heavy metal stress Wheat is one of the main food crops, and heavy metals pose a major threat to crop growth and food security. Heavy metals such as Lead, Nickel, Copper, Cadmium, and Cobalt are environmental pollution often brought about in industrial production, and their persistence poses a serious threat to the ecosystem. Microbial-assisted phytoremediation is an effective tool for metal restoration, because microbes can improve availability and uptake of metals by host plants, or reduction in metal availability by binding to them intracellularly or extracellularly. There are various microbes that can help wheat resist heavy metal stress, such as Trichoderma aureoviride 582PDA6, Trichoderma harzianum 582PDA7 help to resist Nickel, Copper, Cadmium, Cobalt, and Lead (Ripa et al., 2019), Trametes hirsuta helps to resist Lead stress (Malik et al., 2020), Bacillus subtilis helps to resist Cr stress (Seleiman et al., 2020). Under Pb stress, microbes improved the survival rate and tolerance of wheat by promoting the growth of wheat and regulating the accumulation of photosynthetic pigments and Pb. Under 1500 mg/kg Pb stress, the growth accumulation and total chlorophyll content of wheat seedlings inoculated with endophytic fungus Trametes hirsuta increased by 24% and 18%, respectively. More Pb accumulation was measured in shoots of Pb-tolerant fungal-inoculated plants. Symbiosis with endophytic fungi can improve the survival of host plants in metal-contaminated soils, extracting heavy metals from contaminated sites by increasing their uptake of heavy metals (Malik et al., 2020). The increase in the availability of salt stress to Cd stress was regulated by microbes. Responses of soil bacterial communities under salt stress correlate with Cd availability in long-term wastewater-irrigated field soils. Long-term sewage irrigation promotes the bioaccumulation of heavy metals in plants, which may alter soil function, reduce soil health and farmland productivity, and even lead to land degradation. Salt in wheat soils increased Cd availability and altered the dominant microbes in Cd-contaminated soils. Increased salt stress improved taxa in Bacillus, Staphylococcus, and Pseudomonas bacterial families, while one family of Proteobacteria (Sphingomonas) was the most sensitive biomarker, compared to chromium stress without salt stress. It indicated that soil salinity stress leaded to an increase in soil Cd availability, and this increase was regulated by bacterial communities (Wang et al., 2019). Copper stress reduces microbial diversity, while the microbes provide stress resistance in wheat. Rhizosphere microbes play an important role in regulating crop development and stress resistance. Copper pollution reduced the microbial diversity of wheat rhizosphere, and the dominant microbes were Proteobacteria and Actinobacteria. Microbes such as Bacillus, Pseudomonas and Sphingomonas showed strong resistance to stress and could provide nutrients for wheat (Ge et al., 2021). Microbes contribute to the degradation of polycyclic aromatic hydrocarbons (PAHs) and tolerance to heavy metal stress in wheat. Plants can respond to stress conditions by indirectly regulating root-associated microbial structures. Heavy metals did not affect the dissipation of phenanthrene (PHE) in the rhizosphere, but significantly enhanced the accumulation of PHE in the rhizosphere, and the addition of PHE did not affect the uptake of Cu by wheat roots. Cu was the main factor affecting microbial community changes in each rhizosphere co-pollution treatment, and microbes such as Novosphingobium, Sphingomonas, Sphingobium, and Pseudomonas were enriched in the pollution treatments, and degraded PAHs and tolerated heavy metal stress (Xu et al., 2021b). Interacting microbes and melatonin enhance chromium stress resistance in wheat. Chromium-resistant microbes and melatonin reduced chromium absorption and toxicity, improving physiological and biochemical traits and yield of wheat in contaminated soil. Melatonin- and metal-resistant microbes can enhance plant defense responses to various abiotic stresses. Chromium stress caused oxidative damage in the form of electrolyte leakage, overproduction of hydrogen peroxide and malondialdehyde, which reduced wheat growth, biomass, chlorophyll, and relative moisture content. Foliar sprays of melatonin-enhanced plant growth, biomass, and photosynthesis by alleviating oxidative damage and Cr accumulation in plants. Melatonin significantly increased enzymatic and nonenzymatic antioxidant activity. Inoculation with microbes further enhanced the positive effects of melatonin on wheat growth and reduced plant uptake of chromium.

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Abiotic stresses in wheat

Bacillus subtilis inoculation increased chlorophyll a by 27%, chlorophyll b by 49%, ascorbic acid in leaves by 50%, and soluble protein by 72% in wheat grown in 50 mg Cr/kg DM soil. Application of Bacillus subtilis reduces oxidative stress and Cr toxicity by converting Cr6+ to Cr3+ in wheat sprouts and roots. In addition, Bacillus subtilis reduced the response of wheat plants to Cr6+ absorption. Combined application of melatonin and Bacillus subtilis reduced the toxicity and accumulation of Cr in wheat (Seleiman et al., 2020).

Heat stress resistance The increase in atmospheric temperature caused by global warming has become a major challenge to food security, seriously affecting food production and leading to a severe reduction in the production of major crops worldwide (Ahlawat et al., 2022; Shekhawat et al., 2021). Above the optimum temperature range for wheat growth of 20–25°C, for every 1°C increase in temperature, grain filling period, and grain weight decreased by 2.8 days and 1.5 mg, respectively, resulting in a decrease in wheat yield of 4–6 quintals per hectare. Rising food demand and multifaceted issues of global warming could further push wheat crops into a heat-stressed environment, which can severely impact heading, grain setting, maturity, grain growth rates, and ultimately total grain yield. Considerable genetic variation exists in the wheat gene pool for various attributes related to high temperature and stress tolerance. Endophytes exist inside plants and colonize almost all organs, such as roots, stems, leaves, flowers, and fruits. The relationship between plants and endophytes is critical for plant health, productivity, and overall survival under abiotic stress conditions (Ahlawat et al., 2022), and conventional and transgenic breeding strategies to improve plant heat tolerance are laborious and expensive. Therefore, the use of beneficial microbes may be an alternative approach (Shekhawat et al., 2021). The microbes may be endophytes (bacteria and fungi) isolated from different varieties of wheat. Their ingression and establishment mechanisms in plant organs, genes related to ingression, and survival advantages under abiotic stress conditions, etc., are important for sustainable wheat cultivation, which have potential benefits (Ahlawat et al., 2022). Endophytes in wheat confer its seeds with heat-tolerant transmission—intergenerational effects. Endophytes improved heat tolerance in wheat in terms of yield and second-generation seed vigor. Endophytic fungal symbiosis successfully affects the growth, ecophysiology, and reproduction of wheat exposed to heat stress. Endophytes SMCD 2206, SMCD 2210, and SMCD 2215 were beneficial to wheat in quantifying photosystem II (Fv/Fm), plant height, average seed weight (ASW), total seed weight (TSW), water use efficiency, etc. Moreover, seeds with endophytes and seeds produced from the stressed parent germinated faster (Llorens et al., 2019). Chromatin modification by endophytes induces plant heat tolerance. Root endophytes induce plant heat tolerance through constitutive chromatin modification at a heat stress memory gene locus. The root endophyte Enterobacter spp. SA187 induced heat tolerance in wheat. SA187 reprogramed the Arabidopsis transcriptome through HSFA2-dependent enhancement of H3K4me3 levels at heat stress memory gene loci. SA187-induced thermotolerance was mediated by ethylene signaling through the transcription factor EIN3, and SA187 induced constitutive H3K4me3 modification of heat stress memory genes, resulting in robust thermotolerance in plants. Furthermore, the microbial community composition of wheat in open-field farming was not affected by SA187, suggesting that beneficial microbes can be powerful tools for enhancing crop heat tolerance in a sustainable manner (Shekhawat et al., 2021). However, the current research on the interaction between microbes and wheat to resist heat stress still needs to be further deepened, and the microbial resource mining in response to heat stress and its mechanism need to be revealed.

Other abiotic stresses resistance In addition to the abovementioned abiotic stresses such as drought, salt, heavy metals, and heat, we also found that wheatinteracting microbes also play a positive role in resisting other abiotic stresses. (1) Fomesafen stress Biochar application to soil increases microbial diversity and wheat performance under herbicide fomesafen stress. The herbicide fomesafen is toxic to rotational wheat and may reduce its yield. Biochar can improve the remediation and biophysical conditions of contaminated soil environments and facilitate plant growth. Biochar added to soil significantly reduced the uptake of fomesafen by wheat, thereby eliminating its toxicity to wheat seedlings. Furthermore, biochar increased the abundance and diversity of plant beneficial bacterial and fungal taxa in the rhizosphere of wheat seedlings. Among them, 2% biochar modifier had the best effect on reducing the toxicity of fomesafen to wheat seedlings and maintaining the balance of soil microbial community structure in fomesafen-contaminated soil. The level of

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biochar application affected the structure and diversity of the soil microbiome (and fungal group) and plant performance under abiotic stress conditions (Meng et al., 2019). (2) Water-deficiency stress Among the 74 strains of salt-tolerant bacteria isolated from the rhizosphere and root of durum wheat (Triticum turgidum subsp. durum) cultivated in the saline-alkali environment of the Ghor region, east of the Dead Sea, three salt-tolerant PGPR strains such as GSW-E-6 can improve the tolerance of durum wheat to water-deficiency stress (Albdaiwi et al., 2019). Two endophytes (Acremonium sclerotigenum and Sarocladium implicatum) which were found in the ancestor of wheat, Sharon goat grass, infected wheat and improved sustainability and performance under waterdeficient conditions. The levels of stress injury markers in wheat plants treated with endophytes decreased, the accumulation of stress-adapted metabolites decreased, and the responses to water-deficiency stress were significantly different. The beneficial effects of the two endophytes from wild plants were shown to be related to altered physiological responses to water-deficient conditions (Llorens et al., 2019). Microbes regulate water-deficiency stress tolerance in wheat by regulating microRNAs. Arbuscular mycorrhizal fungi (AMF) are soil microbes that can establish symbiotic relationships with plants and positively influence plant resistance to abiotic stresses. AMF can make wheat respond to water deficit by regulating different microRNAs in wheat roots and leaves. After water-deficiency stress, seven miRNAs were regulated in the presence of AMF treatment, among which the most representative miRNA family was miR167, which was regulated by water deficit in leaf and root tissues. In roots, water deficit inhibited miR827-5p, miR394, miR6187, miR167e-3p, and miR9666b3p, thereby affecting transcription, RNA synthesis, protein synthesis, and protein modification. In leaves, mycorrhizae regulated miR5384-3p and miR156e-3p, affecting transport and cellular redox homeostasis. Mycorrhizae inhibited miR1432-5p and miR166h-3p which targeted and regulated DNA replication and transcription. This provided interesting insights into the posttranscriptional regulatory mechanisms of wheat in response to water deficit associated with mycorrhizal symbiosis (Fileccia et al., 2019). (3) Nitrogen deficiency Plant growth-promoting bacteria TL8 and TL13 isolated from the wheat rhizosphere cultivated under droughtstressed and nitrogen-deficient conditions exhibited various plant growth-promoting activities, such as the production of IAA, siderophores, ammonia and ACC deaminase, dissolving phosphate, and antibacterial activity against plant pathogens such as Botrytis spp. and Phytophthora spp. These two Kosakonia pseudosacchari strains can confer nitrogen-deficiency stress tolerance in wheat (Romano et al., 2020). Modern agriculture is facing many challenges, such as loss of soil fertility, climatic factor fluctuations, and increasing pathogens and pest attacks. The sustainability of agricultural production and environmental safety depend on the eco-friendly measures, such as biological fertilizer, biological pesticides, and crop residues recycling. Multiple beneficial effects of microbial inoculum, such as plant growth promoters which inhabit the rhizosphere for nutrients from plant root exudates. Moreover, they help in (1) promoted plant growth by nitrogen fixation, phosphate solubilization, siderophore production, and phytohormone production, (2) increased plant protection by regulating cellulase, protease, lipase, and β-1,3 glucanase productions and enhanced plant defense by triggering induced systemic resistance through lipopolysaccharides, flagella, homoserine lactones, acetoin, and butanediol against pests and pathogens. In addition, the microbial inoculum contains useful variation for tolerating abiotic stresses like extremes of temperature, pH, salinity, drought, heavy metal, and pesticide pollution. Seeking such tolerant microbial inoculum is expected to offer enhanced plant growth and yield even under a combination of stresses (Gopalakrishnan et al., 2015).

Sources of interacting microbes for wheat resistance to abiotic stress In the process of adapting to the environment, wheat interacts with a variety of microbes. These microbes can be fungi or bacteria. They are mainly derived from endophytes of plants, rhizosphere microbes in soil and artificially cultivated biological inoculants. These sources are described below.

Plant sources Microbes that interact with wheat can be endophytes of plant origin. Many plants have abundant resources of stressresistant microbes, such as wheat itself, wheat varieties, ancestors of wheat, and some wild plants. Plants surviving in stress have valuable resources of antistress endophytes. These plants include ancestors of wheat such as Sharon goat grass

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(Llorens et al., 2019), desert plants Alhagi sparsifolia (Zhang et al., 2017, 2020), Alhagi sparsifolia Shap. (Leguminosae) (Chen et al., 2017), halophyte Lycium ruthenicum Murr (Repas et al., 2017), Chenopodium album L. plant (Malik et al., 2020), dandelion (Repas et al., 2017). These Endophytes can inoculate with wheat and colonize its roots and plants to form an interactive relationship, such as Avena fatua L., Fusarium equiseti (Bouzouina et al., 2021). Wheat itself also provides abundant endophyte resources that are resistant to stress (Ahlawat et al., 2022), such as endophytic fungi Trichoderma strains isolated from healthy wheat plants from the North China, which showed salt, heavy metals, and drought tolerance at high levels and also exhibited resistance to all the tested antibiotics. Strain 582PDA4 was found to be the most temperature (55°C) tolerant isolate (Ripa et al., 2019).

Soil source Microbes in soil are one of the main sources of microbes that interact with wheat, including microbes in natural soil, soil microbes under abiotic stress conditions, and plant rhizosphere microbes. They can establish a symbiotic relationship with wheat and help wheat inhibit diseases, mitigate abiotic stress, and increase nutrient bioavailability (Prudence et al., 2021). Natural soil is rich in antistress microbial resources. Soil microbe arbuscular mycorrhizal fungi (AMF) can establish a symbiotic relationship with wheat and positively affect its resistance to abiotic stresses (Fileccia et al., 2019). Different strains of plant growth-promoting rhizosphere bacteria (PGPR) were isolated from natural soil collected from a field in Ilam province, Iran and screened for salt-tolerant bacteria that can produce siderophores and ACC deaminase and dissolve phosphate, and both wheat and barley were affected by physiological responses under normal and salt stress conditions (Emami et al., 2019). The saline-alkali soil and the rhizosphere of plants growing in it also have abundant resources of antistress microbes. Rhizosphere bacteria such as Pseudomonas (including Pseudomonas aeruginosa Ur83 and Pseudomonas fluorescens Ur67) and Stenotrophomonas (including Stenotrophomonas maltophilia Ur52) were isolated from the saline soil (Rouydel et al., 2021); Salt stress tolerant plant growth-promoting rhizobacteria (PGPR) such as Bacillus siamensis (PM13), Bacillus sp. (PM15), and Bacillus methylotrophicus (PM19) (Amna et al., 2019); 74 strains of salt-tolerant bacteria isolated from the rhizosphere and endorhizosphere of Triticum turgidum subsp. durum in the saline-alkali environment of the Ghor region. Of which 62 isolates were divided into Firmicutes (61.3%), Proteobacteria (29.0%), and Actinomycetes (9.7%). At the genus level, most of them were classified as Bacillus, Oceanobacter, and Halomonas (Albdaiwi et al., 2019). Enterobacter cloacae HG-1 was also isolated from saline-alkali soil ( Ji et al., 2020). In addition, 45 strains of salt-tolerant bacteria were obtained from the rhizosphere of wheat and Imperata in high-salt medium. W10 in the rhizosphere of wheat and IP8 in the rhizosphere of blady grass could enhance water deficit stress tolerance and promote plant growth in wheat (Chakraborty et al., 2013). Plant rhizosphere in nutrient-deficient and drought-stressed environments possesses resources of stress-resistant microbes. Thirteen potential plant growth-promoting bacteria were isolated from the rhizosphere of cultivated wheat under drought stress and nitrogen deficiency. Among them, TL8 and TL13 exhibited various plant growth-promoting activities and were able to tolerate abiotic stress and colonize plant roots efficiently (Romano et al., 2020). Piriformospora indica (syn. Serendipita indica) isolated from arid subtropical soils formed a mutualistic symbiosis with a wide range of host plants, increasing biomass production, resistance and tolerance to fungal pathogens and abiotic stresses (Rabiey et al., 2017). There are also antistress microbial resources in soils polluted by heavy metals. Microbes such as Bacillus, Pseudoxanthomonas, and Sphingomonas were isolated from the wheat rhizosphere under copper pollution, showing strong resistance to stress and providing nutrients for plants (Ge et al., 2021). It can be seen that the natural soil and the plant rhizosphere under stress conditions are rich in stress-resistant microbial resources, which can interact with wheat to produce stress-resistant characteristics.

Microbe inoculants Based on the microbes from the above two sources, humans can also artificially cultivate the selected high-quality microbes to make microbe inoculants and add them to the cultivation environment of wheat, then microbes and wheat form an interaction relationship to resist abiotic stress. A variety of root-associated symbiotic microbes used to promote crop growth, as biofertilizers, biofortifiers, and improving biotic and abiotic stresses of wheat. These microbes include nitrogen fixers, nutrient mobilizers, bioremediation agents, and biocontrol agents. The salt-tolerant microbial inoculants Trichoderma harzianum UBSTH-501 and Bacillus amyloliquefaciens B-16 significantly improved the salt tolerance of wheat grown in

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saline-alkali soils (Singh et al., 2021). A microbial inoculant consisting of four plant growth-promoting bacteria (PGPB) affected the wheat root endophyte community, and the changes in root endophyte were consistent with the increase in yield and photosynthetic capacity (Yaghoubi Khanghahi et al., 2021). It can be seen that after revealing the source and interaction mechanism of wheat-interacting microbes, these beneficial microbes can be artificially combined to microbe inoculants for conferring wheat the ability to resist stress, which has great potential for agricultural production and application.

The interaction between wheat-microbe-abiotic stress Among wheat, microbes and abiotic stress, in addition to the relationship between wheat and microbes to resist abiotic stress, there are more complex relationships. For example, abiotic stress can naturally screen microbial resources, and plants can further optimization.

The impact of abiotic stress on microbial resources Abiotic stress affects soil microbial communities. Long-term sewage irrigation promoted the accumulation of heavy metals in plants, salinity stress significantly altered soil microbes in cadmium-contaminated soil, and additional salinity stress increased bacterial families of Bacillus, Staphylococcus, and Pseudomonas in wheat soil. Moreover, a family of Proteobacteria (Sphingomonas family) was the most sensitive biomarker, showing that salt stress led to an increase in soil Cd availability, and this increase was regulated by bacterial communities (Wang et al., 2019). This also showed that abiotic stress was equivalent to a natural screening condition for microbial resources, and the screened microbes were likely to become biological weapons against corresponding abiotic stresses.

The influence of plants on microbes Different plants have specialized microbiomes. Among the microbiomes associated with subterranean (rhizosphere), inner (inner circle), and aboveground (phyllosphere) tissues of halophytes (Salsola stocksii) and in wheat planting soil, root, and shoot samples, Proteobacteria and Actinobacteria were the most abundant phyla among Salsola and wheat. Firmicutes, Acidobacteria, Bacteroidetes, Plankton, Cyanobacteria, Thermobacteria, Verrucobacterium, Chloroflexi, and Euryarchaeota were the main microbes in halophytes, while Actinobacteria, Proteobacteria, Firmicutes, Cyanobacteria, Acidobacteria, and Bacteroidetes were the main microbes of wheat (Mukhtar et al., 2017). The difference and connection of the microbial communities between halophytes and wheat indicated that different plants had certain selectivity for their own microbes. In addition, the growth cycle of plants also had an impact on microbes. Both Streptomyces and Burkholderia species decreased in abundance in wheat as plants age (Prudence et al., 2021).

Effects of stress-resistant microbes on wheat rhizosphere microbes There is a mutual selection relationship among microbes. Enterobacter cloacae HG-1 isolated from saline-alkali soil had effects on the community structure of nitrogen-fixing bacteria in rhizosphere soil and wheat salt-tolerant bacteria. After inoculation of wheat with HG-1 strain, compared with uninoculated wheat, HG-1 strain did not affect the species composition of nitrogen-fixing bacteria in the wheat rhizosphere soil at the phylum level, but the mean relative abundance of Proteobacteria increased significantly, while the abundance of Verructomyces significantly decreased, the abundance of Azospirillum, Rhodophyta, and Anchovy were also lower ( Ji et al., 2020), indicating that stress-resistant microbes affected the diversity and relative abundance of wheat rhizosphere microbes.

Effects of wheat metabolites and exogenous additives on microbes Wheat metabolites have effects on microbes. Benzoxazines (BX) are secondary metabolites present in Poaceae such as wheat and have effects on pests, microbes, and neighboring plants. BX released into soil affects plants and microbial communities (Niculaes et al., 2018). Diterpenoids are present in most plants, often function in species-specific chemical defense against herbivores and microbial diseases, below-ground allelopathic interactions, and abiotic stress responses. Speciesspecific diterpenoid-diversifying enzymes have also been found in wheat, and terpenoids mediate crop defenses against pests, pathogens, and climatic stress, improving crop resistance traits (Murphy and Zerbe, 2020). In addition, wheat root exudates can recruit Pseudomonas and Burkholderia family taxa into the wheat root microbiome (Prudence et al., 2021). This indicated that wheat metabolites affected the interacting microbial community and microbial recruitment.

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Various exogenous additives affect wheat rhizosphere microbes. ZnO and CuO nanoparticles (NPs) have different effects on microfilm formation in wheat roots, with Pseudomonas biofilms being less affected by ZnO NPs, whereas CuO NPs greatly reduce biofilms formation when introduced before biofilm maturation (Bonebrake et al., 2018). Mannose nanofibril hydrogels are able to provide specific interactions with soil microbial communities, enhancing the kinetics and selectivity of plant beneficial bacteria entry and colonization at the microscopic scale of soil. When contacted with the developing wheat root system, a small amount of permeable hydrogel containing mannose nanofibers is particularly close to the developing root zone, providing enhanced pathways for microbial entry, colonization, and continuous wetting and maintains important beneficial rhizobacterial communities under moisture stress, which increased microbial abundance and taxa selectivity in the rhizosphere-hydrogel regions compared with controls (Mathes et al., 2020). Melatonin enhanced plant resistance to a range of biotic and abiotic stressors, and reduced negative physiological effects from environmental stresses that affect yield and crop quality. In wheat grown under cadmium and salt stress conditions, melatonin application significantly altered soil bacterial and fungal abundance (alpha diversity) and community structure (beta diversity) (Madigan et al., 2019). At the same time, melatonin significantly increased the enzymatic and nonenzymatic antioxidant activities of wheat, and inoculation with microbes further enhanced the positive effect of melatonin on wheat growth and reduced the uptake of chromium in wheat (Seleiman et al., 2020). Soil application of biochar increased the abundance and diversity of plant beneficial bacterial and fungal taxa in the rhizosphere of wheat seedlings (Meng et al., 2019). It can be seen that these exogenous additives may regulate the interaction between wheat and microbes by affecting the rhizosphere microbes.

Application of omics in the study of interaction between microbes and wheat Close interactions between plant hosts and associated microbes are critical for determining plant health and promoting tolerance to abiotic stresses and diseases. Metabolomics can comprehensively detect the functional network of metabolites and has profound biological applications in agriculture, medicine, and pharmaceutical disciplines. This technique has been applied to a variety of crops, including maize, sunflower, soybean, and wheat, to study plant-microbe interactions, biological control measures, and abiotic stress tolerance. Its application areas include: (1) Plant and microbial metabolomics; (2) Metabolomics and its application in crop production; (3) Metabolomics workflows and techniques, explaining the advantages and disadvantages of analytical techniques and instruments; (4) Metabolism Metabolomics analysis of metabolic networks (Alawiye and Babalola, 2021). The plant microbiome is a low-cost, high-throughput assay, such as bacterial community data extraction from soil, rhizosphere and root interior. Amplicon-based bacterial 16S rRNA sequencing and fungal ITS sequencing when exploring the plant root microbiome are often the method of choice for characterizing microbial composition and diversity. Standardization of methods for collecting and extracting DNA from soil, rhizosphere, and root samples can reduce bias in analysis and comparison between samples and studies and has been used in a variety of plants such as sorghum, corn, wheat, strawberry, and agave (Simmons et al., 2018). However, a single omics cannot fully resolve the complex interactions between plants and microbes. Therefore, to achieve a more integrated perspective on plant-microbiome interaction, “holo-omics” incorporate data across multiple omics levels from both host and microbiota domains, which pair host-centered omics strategies, such as transcriptomics, metabolomics, epigenomics, and proteomics, with the more commonly used microbial-focused techniques, such as amplicon sequencing, shotgun metagenomic, metatranscriptomics, and exometabolomics. Holo-omics studies have the power to resolve the functionality of a plant microbiome ecosystem by generating an image of what is being expressed, translated, and produced during plant-microbiome interactions (Xu et al., 2021a).

Conclusions The interaction between microbes and wheat confers wheat with tolerance to various abiotic stresses, including drought, salt, heat, and heavy metal resistances. Most of its stress resistance mechanisms are related to promoting germination, growth, survival, yield, ion balance, photosynthesis, etc., through direct or indirect ways to promote the growth of plants in stress (Fig. 1). Therefore, by mining microbial resources that promote plant growth, and further through multiple natural screening of stress, plants, microbes, superior antistress microbial inoculants can be obtained. The application of these microbial inoculants in the agricultural production of wheat can greatly improve the resistance of wheat to cope with the threat of food production security brought by the deteriorating ecological environment.

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FIG. 1 Wheat-microbe interactions to deal with abiotic stress.

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Exploring the root microbiome: extracting bacterial community data from the soil, rhizosphere, and root endosphere. J. Vis. Exp., 57561. https://doi.org/10.3791/57561. Singh, U.B., Malviya, D., Singh, S., Singh, P., Ghatak, A., Imran, M., Rai, J.P., Singh, R.K., Manna, M.C., Sharma, A.K., et al., 2021. Salt-tolerant compatible microbial inoculants modulate physio-biochemical responses enhance plant growth, Zn biofortification and yield of wheat grown in salinesodic soil. Int. J. Environ. Res. Public Health 18, 9936. Sutherland, I.W., 2001. Exopolysaccharides in biofilms, flocs and related structures. Water Sci. Technol. J. Int. Assoc. Water Pollut. Res. 43, 77–86. Uroz, S., Courty, P.E., Oger, P., 2019. Plant symbionts are engineers of the plant-associated microbiome. Trends Plant Sci. 24, 905–916. Vujanovic, V., Islam, M.N., Daida, P., 2019. Transgenerational role of seed mycobiome—an endosymbiotic fungal composition as a prerequisite to stress resilience and adaptive phenotypes in Triticum. Sci. Rep. 9, 18483. Wang, M., Chen, S., Chen, L., Wang, D., Zhao, C., 2019. The responses of a soil bacterial community under saline stress are associated with Cd availability in long-term wastewater-irrigated field soil. Chemosphere 236, 124372. Xu, L., Pierroz, G., Wipf, H.M., Gao, C., Taylor, J.W., Lemaux, P.G., Coleman-Derr, D., 2021a. Holo-omics for deciphering plant-microbiome interactions. Microbiome 9, 69. Xu, Y., Ge, Y., Lou, Y., Meng, J., Shi, L., Xia, F., 2021b. Assembly strategies of the wheat root-associated microbiome in soils contaminated with phenanthrene and copper. J. Hazard. Mater. 412, 125340. Yaghoubi Khanghahi, M., Crecchio, C., Verbruggen, E., 2021. Shifts in the rhizosphere and endosphere colonizing bacterial communities under drought and salinity stress as affected by a biofertilizer consortium. Microb. 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Endophytic bacterial microbiome diversity in early developmental stage plant tissues of wheat varieties. Plants (Basel) 9, 266.

Chapter 25

Role of nanotechnology in combating abiotic stresses in wheat for improved yield and quality Tabinda Athara, Mohd. Kamran Khanb,∗, Sajad Majeed Zargarc, Anamika Pandeyb, Zeeshan Ahmadd, Muhammad Ameena, Hina Ahmed Malika, Mehmet Hamurcub, Sait Gezginb, Sadia Majeede, and Aneesa Batoolc a

Faculty of Agriculture, Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan, b Department of

Soil Science and Plant Nutrition, Faculty of Agriculture, Selcuk University, Konya, Turkey, c Proteomics Laboratory, Division of Plant Biotechnology, Sher-e-Kashmir University of Agricultural Sciences and Technology of Kashmir, Shalimar, Srinagar, Jammu and Kashmir, India, d MOE Key Laboratory of Plant-Soil Interactions, Department of Plant Nutrition, China Agricultural University, Beijing, China, e Department of Agronomy, Faculty of Agriculture, The Islamia University of Bahawalpur, Bahawalpur, Pakistan ∗ Corresponding author. e-mail: [email protected]; [email protected]

Introduction The world population is estimated to reach nine billion for the duration of the first half of the 21st century, and yet, global food production is unable to meet the growing dietary requirements of this ever-increasing population (Khan et al., 2021a). Plants are exposed to the detrimental effects of numerous stresses owing to their sessile nature (Faizan and Mehreen, 2021). Abiotic stresses change the soil–plant-atmosphere continuum, which resultantly, impacts crop productivity as well as plant growth by causing several physiological, morphological, biochemical, and molecular alterations (Mahto et al., 2021). Wheat is used as a staple food crop across the globe, and enhancing its production and quality can help to reduce malnutrition and undernourishment on a sustainable basis (Khan et al., 2021a). Wheat is being used by a significant portion of the population to fulfill their daily needs of protein and calorie intake (Kizilgeci et al., 2021). However, its growth development and yield are greatly affected due to abiotic stresses. Abiotic stresses are causing major yield and quality losses in the wheat crops, and this is adversely affecting food security all over the world. Results of studies have shown that 50% of the wheat yield losses are due to abiotic stresses and have a drastic contribution to food insecurity. Among various abiotic stresses are salinity, nutrient deficiency, drought, temperature (low or high), and different pollutants, which limit plant growth and production (Pereira, 2016; Husen et al., 2016). Current challenges of diverse environmental constraints, food security, and climate change have compelled researchers to explore novel and competent techniques to conquer these challenges in a skillful manner (Tripathi et al., 2017). Advancements in the field of plant sciences and genetics have led to the development of new technologies and investigations of better ways to facilitate plant growth in changing environments (Ahmad et al., 2022). Nanotechnology has been recognized as one of the most imperative emerging fields, contributing toward efficient competitiveness in several fields including agriculture with copious potentialities (Bandyopadhyay et al., 2013; Emamverdian et al., 2015; Tripathi et al., 2016). Nanotechnology has been proven to be a boom in agricultural systems with sufficient advantages through the application of nanofertilizers and nanopesticides and other nano-based materials (Li et al., 2017; Cao et al., 2020; Wang et al., 2021b). Numerous data exist in the literature regarding the beneficial role of nanotechnology in uplifting plant growth under normal as well as stressed conditions (Abdel Latef et al., 2017; Yassen et al., 2017; Abdel-Haliem et al., 2017; Hussein and Abou-Baker, 2018). Nanoparticles (NPs) have exhibited the tremendous potential to be used in agriculture (Azimi et al., 2014; Athar et al., 2022). Application of natural or synthetic (prepared from naturally occurring material) NPs can lessen the higher production costs and can be adopted as a suitable solution by the farmers for improving their crop productivity and stress tolerance (Gui et al., 2015a; P
erez-de-Luque, 2017; Guo et al., 2019). Nanomaterials employed in agriculture show the properties of fertilizers, pesticides, and bioregulators and are also used as major components of different sensors that monitor environmental quality. Nanoparticles (NPs) of carbon (C), copper (Cu), manganese (Mn), zinc (Zn), cesium (Cs), and precious metals Abiotic Stresses in Wheat. https://doi.org/10.1016/B978-0-323-95368-9.00020-5 Copyright © 2023 Elsevier Inc. All rights reserved.

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such as gold (Au) and silver (Ag) are currently used for this purpose. NPs can simultaneously reduce the effects of abiotic stresses and become the source of biofortification in wheat (Khan et al., 2021b). Their beneficial roles under different abiotic stresses have been detailed below.

Nutrient stress Shortage of essential nutrients in the diet is a common problem in developing countries and has turned into a worldwide issue with severe side effects. Nearly, 50% of the children are unable to get vital vitamins in their food, which impairs their intelligence as well as mental capabilities. Clemens (2014) claimed that iron (Fe) and zinc (Zn) deficiencies in the diet result in the prevalence of high death risks in children. The application of chemical fertilizers to soils is a general practice in agricultural systems to improve plant growth. However, sometimes, they also result in the occurrence of soil nutrient imbalance, destruction of soil structure, and soil fertility, which may serve as crucial impediments on a long-term basis. Lack of nutrient uptake is manifested by abnormal plant growth and decreased yield. To deal with the condition, it is important to formulate smart materials, which can ensure nutrient release toward the targeted sites and contribution to a clean environment. Nanotechnology possesses the potential to revolutionize agriculture by improving the plant’s ability to absorb essential nutrients as well as withstand stressed circumstances (Khan et al., 2021b). It can improve crop yields and their nutritional aspects and uplift resistance/tolerance in plants against abiotic stresses (Tarafdar et al., 2013; Khan et al., 2021b) and thus can serve as a promising alternative to solve the problem of nutrient deficiency. Numerous efforts have been made in this regard to identify nanomaterials (NMs) that not only favor plant growth but also improve fertilizer use efficiency and thereby overcome nutrient deficiencies (Liu and Lal, 2015). Development of various types of nanofertilizers (NFs) or nanocoated nutrients that ensure sustained availability, as well as nutrient release, can serve as an effective tool to ensure sustainable agriculture. The NFs can be divided into four distinct classes, i.e., micronutrient NFs, macronutrient NFs, nutrient-loaded NFs, and plant growth-promoting NFs (Liu and Lal, 2015). The application of these NFs could be an ideal strategy to combat the nutrient deficiency problem of the soil and improve their plant acquisition. Xiumei et al. (2005) revealed that application of nanoCaCO3 combined with organic manure significantly increased the growth as well as the development of peanut plants. They also observed a tremendous increment in the protein and soluble sugar in the leaves and stem with a concomitant increase in the uptake of essential nutrients. Similarly, Tarafdar et al. (2014) testified that the application of Zn-NPs resulted in a notable improvement in the growth, physiology, total protein contents, plant biomass (dry), and enzyme activities (dehydrogenase, alkaline, and acid phosphatases and phytase) in 6-week-old pearl millet plants. Silicon nanoparticles (Si-NPs) exhibit distinctive physicochemical traits and can plant growth and metabolism under adverse environmental conditions by entering into them. Janmohammadi et al. (2016) examined the effect of the foliar application of SiO2-NPs on safflower along with organic and inorganic fertilization. They suggested that SiO2-NPs application in combination with organic fertilizers improved safflower production. Similarly, Lemraski et al. (2017) examined the response of two different Iranian rice cultivars to nano-potassium fertilization and N application and stated that consumption of NPs by rice cultivars improved their yield. In short, using NFs for tackling nutrient shortages in the soil may be a promising approach to improve plant development and produce under stressed conditions. Nanotechnology provides the platform to use elegant delivery structures for various agrochemicals, which are not only safe but also target bound and easy delivery mode (Rai et al., 2013; Dimkpa and Bindraban, 2016; Manjunatha et al., 2016). Nanofertilizers owing to their larger surface area (small size) are more efficient than traditional fertilizers. Their nature can also permit their slow and sustainable release and thereby can promote effective nutrient uptake by the plants. With the application of encapsulated NPs, zeolites, and nanoclays, fertilizer use efficiencies are increased, soil fertility status and plant growth are restored, agroecological degradation and environmental pollution are reduced (Manjunatha et al., 2016). Among the different components of NFs are iron, silica (SiO2), zinc oxide, TiO2, Al2O3, FeO, and CeO2 (Prasad et al., 2017). The success and realization of nanotechnology in agriculture depends upon several factors such as plant species, concentration, size, chemical properties, and composition of nanomaterials (Thakur et al., 2018). There are certain shortcomings with the use of chemical fertilizers such as nutrient leaching, pollution of underground water aquifers, hypoxia, and greenhouse gas emissions. These problems need abrupt consideration, and hence, nano fertilizers come as a solution for them (Suppan, 2013) as they ensure slow and timely release of nutrients on a prolonged basis and thereby minimize their leaching. Moreover, nanofertilizers (NFs) are more applicable than typical fertilizers as they can boost the efficacy of nutrients, lessen the necessity of chemical fertilizers, and are less harmful to environment (Table 1). They are easily absorbed by the plants due to their larger surface area, and the plants accumulate such nutrients and thereby overcome the gap of nutrient deficiencies. In addition, NMs can be engineered in such a way as to address only targeted deficient nutrients in plants (Table 1). Conventional fertilizers are not equipped to supply all the required plant nutrients,

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TABLE 1 Effects of different nanoparticles to reduce the adverse effects of abiotic stresses on growing plants. Type of abiotic stress

Nature of nanoparticles used

Results reported

References

Nutrient stress

Nano CaCO3 in combination with organic matter

Improved growth and development of peanut plants. Enhanced soluble sugar and proteins in the stems and leaves

Xiumei et al. (2005)

Zn Nanoparticles

Significant improvement in the growth, physiology, total protein contents, plant dry biomass, and enzyme activities.

Tarafdar et al. (2014)

SiO2 nanoparticles along with organic fertilizers

Greater increase in safflower production.

Janmohammadi et al. (2016)

Nanopotassium along with N fertilization

Significant increase in the growth and yield of rice plants.

Lemraski et al. (2017)

γ-Fe2O3-NPs

Increased root elongation in rice.

Alidoust and Isoda (2014)

γ-Fe2O3-NPs

Increased chlorophyll, protein, and soluble sugar contents in watermelon.

Wang et al. (2016)

Increased plant height, root and shoot length, and performance index of pigeon pea seedlings.

Shende et al. (2017)

Cu nanoparticles

Elevated mitotic index and growth

Nagaonkar et al. (2015)

TiO2 nanoparticles

Facilitation of N fixation and improved photosynthetic activities in spinach

Zheng et al. (2005)

TiO2 nanoparticles

Increased uptake of essential plant nutrients in the hydroponically grown maize

Daghan (2018)

TiO2 nanoparticles

Increased chlorophyll content, fresh and dry weight, and length of roots and shoots. Enhanced uptake of essential nutrients

Arshad et al. (2021)

CeO2 nanoparticles

Improved growth and development of lettuce

Gui et al. (2015b)

CeO2 nanoparticles

Increased chlorophyll contents and growth of soybean

Cao et al. (2017)

TiO2 nanoparticles

Modulation of membrane damage, and alleviation of oxidative damage in the chickpea

Mohammadi et al. (2014)

TiO2 nanoparticles

Higher rate of photosynthesis, reduced H2O2 contents, increased activities of Rubisco enzyme, and improved growth and development.

Hasanpour et al. (2015)

TiO2 nanoparticles

Establishment of cellular homeostasis and reduced oxidative stress in chickpea varieties

Amini et al. (2017)

Nanoparticles of graphene, silicon, selenium, and zinc

The reduced negative impact of cold stress in sugarcane enhanced photosynthetic pigments,

Elsheery et al. (2020)

Ag nanoparticles

Improved field emergence, seed germination, and physiological attributes of bean seedlings.

Prazak et al. (2020)

ZnO nanoparticles

Alleviation of adverse effects of cold stress on rice. Improved dry biomass production, root length, and plant height.

Song et al. (2021)

Se nanoparticles

Improved chlorophyll content and root volume of tomatoes.

Haghighi et al. (2014)

Cellulose nanoparticles along with chitosan

Improved antioxidant defense and reduced weight loss in strawberries

Resende et al. (2018)

chitosan-coated phenylalanine nanoparticles

Improved antioxidative capacity, suppression of adverse effects of cold stress, total soluble salts, and firmness of persimmon fruits.

Nasr et al. (2021)

Cold stress



Continued

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TABLE 1 Effects of different nanoparticles to reduce the adverse effects of abiotic stresses on growing plants—cont’d Type of abiotic stress Flooding stress

Drought

Nature of nanoparticles used

Results reported

References

Ag nanoparticles

Alleviation of adverse effects of flooding stress

Porwal et al. (2021)

Al nanoparticles

Regulation of metabolic pathways, improvement in the soybean plant growth.

Mustafa et al. (2015b)

Si nanoparticles

Improved growth and physiological processes of blueberry fruits.

Iqbal et al. (2021)

Ag nanoparticles in combination with potassium nitrate and nicotinic acid

Improved hypocotyl length, fresh weight, root length, and soybean weight.

Hashimoto et al. (2020)

Ag nanoparticles

Amelioration of negative effects of flooding improved amino acid synthesis, and wax formation.

Mustafa et al. (2016)

Al nanoparticles

Improved root length, enhanced production of ribosomal proteins, regulation of the membrane permeability, and tricarboxylic acid activity cycle

Mustafa and Komatsu (2016)

Nanosilver ions

Improved root length, fresh and dry weight of leaves and roots, in saffron plant

Rezvani et al. (2012)

CeO2 nanoparticles

Reduced oxidative damage and enhanced photosynthetic activities in rice.

Zhang et al. (2021)

Nanosilica and nanochelating fertilizers (Silicon, Boron, Zinc)

Improved water use efficiency, plant height, biological yield, spike length, number of grains.

Ahmadian et al. (2021)

Green synthesized Cu nanoparticles

Significant improvement in the stomatal conductance, morphological parameters, chlorophyll stability index, and leaf succulence.

Ahmed et al. (2021)

Cu nanoparticles

Enhanced maize growth and yield due to scavenging mechanisms of reactive oxygen species (ROS), and regulation of pigment systems

Van Nguyen et al. (2022)

Copper zinc nanoparticles based colloidal solution

Reduced adverse effects of drought on wheat plants, enhanced antioxidative enzymatic activities, reduced accumulation of thiobarbituric acid reactive substances, stabilization of photosynthetic pigments, and enhanced the relative water contents in the seedling leaves.

Taran et al. (2017)

Si nanoparticles

Improved seedling growth and physiological parameters.

Ashkavand et al. (2015)

TiO2 nanoparticles

Improved starch contents, seed gluten, and agronomic traits in wheat.

Jaberzadeh et al. (2013)

TiO2 nanoparticles

Improved water contents and antioxidative enzymatic activities in plants.

Faraji and Sepehri (2020)

Calcium nanoparticles

Improved drought tolerance by controlling proline levels

Das et al. (2016)

ZnO nanoparticles

Improved growth, dry weight, efficient utilization of seed reserves, and enhanced gibberellins activities.

Sedghi et al. (2013)

Fe nanoparticles

Improve drought tolerance in plants by the modification of stomatal movements and carbohydrate metabolism. Increase in starch and sucrose synthesis by modification of enzymatic activities

Sun et al. (2020)

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TABLE 1 Effects of different nanoparticles to reduce the adverse effects of abiotic stresses on growing plants—cont’d Type of abiotic stress

Heat stress

Salinity stress

Nature of nanoparticles used

Results reported

References

Urea having a facile coating of Zn nanoparticles

Reduced panicle initiation time, grain yield, and grain uptake of N, P, and Zn.

Dimkpa et al. (2020)

Bio-fabricated Se nanoparticles

Significant increase in the leaf length, leaf number, leaf area, root dry weight, root fresh weight, root length, shoot dry weight, shoot fresh weight, shoot length, and plant height.

Ikram et al. (2020)

CeO2 nanoparticles

ROS Scavenging and reduction in heat stress

Djanaguiraman et al. (2018)

ZnO nanoparticles

Significant growth improvement by protecting mungbean plants from heat stress

Kareem et al. (2022)

ZnO and magnetite nanoparticles

Reduced adverse effects of heat by activation of oxidative enzymatic activities, reduced MDA levels, and lipid peroxidation

Hassan et al. (2018)

Ag nanoparticles

Remarkable protective effects were observed. Significant improvement in morphological growth of wheat.

Iqbal et al. (2019)

ZnO nanoparticles along with plant growth-promoting rhizobacteria

Significant improvement in the growth, development, biomass production, photosynthetic pigments, indole acetic acid contents, proteins, and soluble sugars was observed.

Azmat et al. (2022)

ZnO nanoparticles

Significant regulation of antioxidants, lipid peroxidation, osmoprotection, chlorophyll contents, gaseous exchange, and yield attributes was observed.

Kareem et al. (2022)

Zn nanoparticles

Improved plant growth and development were observed.

Spano` et al. (2020)

Zn nanoparticles

Increased activities of alpha-amylase, reduced concentration of dehydrogenase, improved photosynthetic pigments, plant biomass, plant length, and increased activities of antioxidative enzymes.

Srivastav et al. (2021)

Fe nanoparticles

Restricted Cd uptake, increased photosynthetic pigments, reduced Na and Cl-, and enhanced concentration of N, P, and K.

Manzoor et al. (2021)

Nanosilica

Significantly improved wheat yield and quality under salt stress.

Ayman et al. (2020)

and hence, NPs owing to their active nature can address nutrient problems linked with the use of chemical fertilizers (Dimkpa and Bindraban, 2017). Recently, researchers have created a nanofertilizer named “Nano-Leucite,” which is not only ecofriendly but also can lessen the nutrient losses in food with a simultaneous increment in food production (Kamran et al., 2016). Moreover, different mineral materials such as zeolite have been incorporated into NFs in recent times due to their inexpensive and available nature and have been applied to improve maize growth and yields (Eroglu et al., 2017). Zeolite nanocomposites of phosphorous (P), potassium (K), and nitrogen (N) along with other macro- and micronutrients have been reported that get absorbed in the plants and improve their growth and productivity (Harper, 2015). Furthermore, Food and Drug Administration (FDA) and International Agency for Research on Cancer (IARC) have declared zeolite as nontoxic and have allowed their extensive application in agriculture recently (Eroglu et al., 2017). Manikandan and Subramanian (2016) observed a high N uptake by the plants when urea was applied along with zeolite (nanozeourea) as they facilitated the slow release of the nutrients. Such practice not only prevented the N toxicity in the soil leading to eutrophication and greenhouse gaseous release but also improved its plants’ uptake efficiency.

398 Abiotic stresses in wheat

Similarly, Zn deficiency in plants has been successfully overcome by application of zinc oxide nanoparticles (ZnO-NPs). The ZnO-NPs, with an approximate worldwide production ranging between 550 and 33,400 tons, serve as the 3rd highly employed metal-based nanomaterials (Bondarenko et al., 2013; Connolly et al., 2016; Peng et al., 2017). The levels of ZnO-NPs were found to be between 76 and 760 μg L 1 (in the water), and 3.1 and 31 μg kg 1 (in soil) (Ghosh et al., 2016). In this form, ZnO can be easily transferred, metabolized, and accumulated in plants. However, being a micronutrient, a higher concentration of ZnO-NPs can harm plant growth too by suppressing seed germination and root growth (Singh et al., 2013). One-third of the global human population has been exposed to Zn deficiency as per WHO recommendations due to poor Zn contents of diet especially cereals (Biesalski, 2013; Sadeghzadeh, 2013). The ZnO-NPs owing to their unique properties compared with the conventional Zn fertilizers can be regarded as a new Zn fertilizer. Earlier researchers have reported the increased Zn contents of wheat grains with the foliar application of ZnO-NPs and no ZnO-NPs were found in the wheat grains (Zhang et al., 2018). Nano-zinc oxide has widespread applicability in agriculture as it is not only applied as a fertilizer but also effectively acts as a blockage for UV radiations during plant growth and facilitates the soil recovery of essential plant nutrients (Kamran et al., 2016). Du et al. (2019) compared the efficiency of ZnO-NPs with zinc sulfate (ZnSO4) in alleviating the Zn deficiency in wheat under pot experimentation. They reported that ZnO-NPs were more efficient in uplifting the available grain Zn contents than ZnSO4. Both the sources improved grain yield and plant biomass at moderate doses; however, ZnSO4 showed more toxic behavior than ZnO-NPs at higher doses as pragmatic by its suppressive effects on seed germination, shoot, and root lengths and seedling dry biomass. Moreover, they also observed more structural damages in roots and alterations in the enzyme activities with the application of ZnSO4 in comparison with the ZnO-NPs. They concluded that the ZnO-NPs application did not cause any nanospecific risk. Among other major nutrients, iron (Fe) acts as a cofactor for several enzymes, forms some of the portion of cytochromes, and also correlates with certain biochemical reactions, i.e., respiration, nitrate synthesis, DNA synthesis, and hormone production (He et al., 2011). The Fe deficiency has become a widespread global issue and is particularly observed under calcareous soils (Klatte et al., 2009). To tackle this problem, the development of iron nanoparticles is a crucial strategy to ameliorate Fe deficiency and uplift Fe fertilization effectiveness during agricultural applications (Liu et al., 2016). Various studies have demonstrated an elevation in the chlorophyll contents of different plants after the application of Fe-based nanoparticles (Ren et al., 2011; Ghafariyan et al., 2013; Wang et al., 2015). Similarly, Rui et al. (2016) reported that Fe2O3-NPs can be used as a replacement for conventional Fe-fertilizers during the cultivation of the peanut (Arachis hypogaea) plant. Iron oxide nanoparticles (γ-Fe2O3-NPs) are the most extensively employed Fe-NPs, which have extensive applicability such as in controlled drug release, separation technologies, and medical diagnostics owing to their increased surface area, indigenous biocompatibility, and superparamagnetic behavior (He et al., 2011; Hu et al., 2017). Alidoust and Isoda (2013) stated that γ-Fe2O3-NPs exert no adverse impact on the soybean at any growth stage and generated a promising effect on root growth. In addition, rice exposure to γ-Fe2O3-NPs at various concentrations resulted in a remarkably increased root elongation than control, which indicated that the effect of γ- Fe2O3-NPs application can be nano specific (Alidoust and Isoda, 2014). Wang et al. (2016) performed an experiment where the watermelon seeds were grown in soil added with γ-Fe2O3-NPs at varying concentrations. They revealed that γ-Fe2O3-NPs @ 50 mg L 1 elevated soluble sugar, protein contents, and chlorophyll contents in the plant. However, γ-Fe2O3-NPs @ 50 mg L 1 and @ 100 mg L 1 concentrations induced osmotic stress, which was, however, mitigated with the watermelon growth. They concluded that γ-Fe2O3-NPs at proper concentrations can eliminate Fe deficiency as well as chlorosis and thereby can facilitate watermelon growth. Moreover, copper (Cu) is the 3rd most important metal because of its daily use and it is very important for most living beings (Liu et al., 2018). It is an important micronutrient needed by the plants and therefore should be administered at low doses. The development of nanotechnology offers new perspectives as CuO-NPs have found extensive utilization in fertilizers, pesticides, herbicides, plant growth regulators, and as soil additives for remediation (Xiong et al., 2017). Pestovsky and Martinez-Antonio (2017) reported that application of CuO-NPs @ 1000 mg L 1 released 0.3 mg Cu3+, which improved the plant growth and was not toxic to the plants. The toxicity of the Cu-NMs arises from their solubility in the medium of their application. The CuO-NPs have also demonstrated antimicrobial properties, which affect microbial activities of susceptible species (Xiong et al., 2017). Shende et al. (2017) checked the effect of Cu-NPs application on pigeon pea growth. They showed that Cu-NPs treatment resulted in a considerable increment in the plant height, root, and shoot lengths as well as the performance index of pigeon pea seedlings. They concluded that the administration of Cu-NPs contributed to the growth and development of pigeon pea owing to their growth-promoting activities. Similarly, Nagaonkar et al. (2015) examined the effect of Cu-NPs in the Allium cepa. They reported that application of Cu-NPs up to 20 μg L 1 elevated the mitotic index however, beyond that concentration, it was negatively correlated which indicated that 20 μg L 1 might be non-toxic for plant growth as well as development.

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Titanium dioxide nanoparticles (TiO2-NPs) have been extensively reported to facilitate N fixation as well as enhance photosynthesis in spinach and hence improve the overall plant growth (Zheng et al., 2005). Daghan (2018) applied TiO2-NPs to maize at varying concentrations in a hydroponic experiment to check their potential for improving plant growth, nutrient, and chlorophyll contents. They stated that TiO2-NPs application caused a significant increment in the uptake of essential plant nutrients except for Fe at increasing concentrations; however, increasing concentrations exhibited a negative trend with the growth attributes of maize. Similarly, Arshad et al. (2021) checked the effect of TiO2-NPs on the growth of rice and its nutrient profile under various textured soils in a greenhouse study. Their results indicated that application of TiO2-NPs @ 500 mg kg 1 increased the chlorophyll contents, lengths, and fresh/dry weights of roots and shoots and also favored the uptake of essential nutrients such as Ca, Fe, Cu, P, and Zn, and the beneficial effects of TiO2-NPs were more pragmatic in the sandy clay textured soils. Since Ca, P, and Fe are the primary nutrients that are responsible for the growth and yield increments in the plants, application of TiO2-NPs was proved to be a reliable option for improving the plant nutrient profile. Cerium oxide nanoparticles (CeO2-NPs) have also gained much importance in recent times due to their beneficial impacts on improving plant growth (Cao et al., 2018). Their impacts on the crops are highly concentration-dependent, soil composition as well as the plant species. When applied in minute concentrations, NPs bring about a remarkable increment in plant growth and vice versa under high-dose applications. Certain reports exist in the literature regarding the beneficial effect of CeO2-NPs on plant growth. Gui et al. (2015b) reported the enhanced growth of lettuce after treatment with 100 mg kg 1 concentration of CeO2-NPs but they also observed hindrance in the plant growth beyond 1000 mg kg 1 concentration of CeO2-NPs. Cao et al. (2017) also provided similar evidence and stated that application of CeO2-NPs uplifted the chlorophyll contents of soybean crops under increased soil moisture contents; however, effects were negligible under limited moisture conditions of the soil. The results were ascribed to the low moisture-mediated stomatal conductance, which decreased the photosynthetic process as well as gaseous exchange (Cao et al., 2018).

Cold stress Unusual and repeated prevalence of lower temperature is a major concern to the farmer community. Cold stress (0–15°C) is the result of temperature cool enough to induce injury in plant without the development of ice crystals, whereas freezing stress (temperature < 0°C) forms ice crystals in plant tissues and leads to frost killings in plants. Winter stress is threatening plant productivity globally owing to the climate change phenomenon, especially in recent decades (Budhathoki and Zander, 2019). Major effects of cold stress are the loss of membrane fluidity and electrolyte leakage and plants under cold stress exhibit stunted growth, poor germination, and decreased yield (Suzuki et al., 2008; Singh and Husen, 2019). Cold stress stimulates the same physiological effects as drought stress and results in the suppression of root germination and development, i.e., exposure of Brassica seeds to chilling stress (2°C) results in an almost 50% reduction in their germination potential after 15 days (Sonkar et al., 2021). In a similar study, Cong Dien and Yamakawa (2019) monitored the responses of rice cultivars (germination index, radicle length, and coleoptile length) toward chilling stress (13°C) for two weeks. They reported that out of 181 tested rice cultivars, 55 exhibited no or zero germination index and only 13 cultivars demonstrated a germination potential of 50%. Similarly, a significant decrement in the coleoptile and radicle lengths was also observed. The reduction in these measured attributes was ascribed to the decrease in the water conductivity under chilling stress. Seed imbibition is the most susceptible stage of seed sprouting to abiotic stresses, and cold stress particularly has the maximum effect on sprouting during this stage. Similarly, Bae et al. (2016) observed the symptoms of electrolyte leakage (EL) in tomato seeds under exposure to chilling stress (4°C). Plant species vary in their response to cold stress, and more membrane injury is observed in sensitive plant species in parallel with tolerant species (Heidarvand et al., 2011). Even short-term exposure to cold stress results in the depression of pollen growth in chickpea (Srinivasan et al., 1999), which was correlated with the low energy associated with the abscisic acid (ABA)-induced suppression of sugar and amino acids synthesis and supply via a reduction in the turgor pressure that ultimately led to the inhibition of pollen tube growth, fertilization, and seed formation (Thakur et al., 2010). In addition, cold stress disturbs metabolic balance by modulating the membrane properties and causes secondary injuries in the plants by producing toxic metabolites (Cai et al., 2019). Furthermore, the efficiency of the energy transferring rate toward photosystem II (PSII) is also decreased (Su et al., 2015). All these phenomena lead to the formation of reactive oxygen species (ROS). As low temperature slows down photosynthetic processes, the existence of light and the unevenness between light absorption and utilization affect the overall photosynthetic efficiency (van Buer et al., 2019). Also, with a decline in the temperature, several phenotypic symptoms, i.e., leaf area reduction, wilting, necrosis, and chlorosis are observed (Lei et al., 2019). Similarly, total chlorophyll contents have also been observed to decline under cold stress as attributed to the cold stress mediated generation of free radicals (Lei et al., 2019). Under cold stress, various symptoms related to water stress such as loss of leaf turgor are observed, which are also taken as cold stress-stimulated signs (Miura and Tada, 2014).

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Numerous researchers have tried to minimize the adverse impacts of cold stress on plant growth via the application of nanoparticles. Mohammadi et al. (2014) examined the effect of titanium oxide nanoparticles (TiO2-NPs) on the cold stress (4°C)-induced membrane damage indices such as malondialdehyde contents and electrolyte leakage in tolerant (Sel11,439) and sensitive (ILC533) chickpea genotypes. They observed increased bioaccumulation of NPs within chloroplast as well as vacuole of the sensitive genotype than the tolerant one, and more TiO2 contents were observed during cold stress exposure than the optimum temperature. Moreover, TiO2-NPs not only modulated membrane damage but also alleviated oxidative damage in chickpea under cold stressed conditions. They concluded that TiO2-NPs enhanced the redox status of chickpea genotypes due to thermal treatments. Following these results, Hasanpour et al. (2015) investigated the effect of TiO2-NPs application on the molecular as well as metabolic attributes of chickpea (cold tolerant; Sel96Th11439) and (coldsensitive ILC533) genotypes, which are directly involved in plant photosynthesis under cold stress (4°C). They suggested a considerable increment in the hydrogen peroxide (H2O2) contents of the sensitive genotype in comparison with the tolerant one under cold stress, whereas TiO2-NPs decreased the H2O2 contents where the tolerant plant genotype exhibited lower H2O2 contents than the susceptible chickpea genotype. The observed decline was accompanied by the higher photosynthetic potential in the tolerant plants. They observed that TiO2-NPs application resulted in a substantial increment in the activity of ribulose bisphosphate carboxylase (Rubisco), although its activities were considerably suppressed under cold stress in comparison with the optimum temperature. They concluded that TiO2-NPs application may confer cold stress tolerance in chickpea via ameliorating the cold stress-mediated damages to plant metabolic activities. Amini et al. (2017) checked effects of TiO2-NPs in imparting chilly tolerance to two different chickpea varieties (sensitive and tolerant) during the 1st and 6th days of cold stress (4°C). They also observed the protective role of TiO2-NPs against cold stressmediated oxidative stress. They attributed this induced tolerance to increased upregulation of various cold-responsive genes after treatment with TiO2-NPs under cold stress, which is responsible for establishing cellular homeostasis (Chinnusamy et al., 2007). Similarly, Elsheery et al. (2020) examined the ameliorative impacts of various nanoparticles such as silicon dioxide (nSiO2; 5–15 nm), selenium (nSe; 100 mesh), zinc oxide (nZnO;