Harnessing Brassinosteroids for Heat Resilience in Wheat: A Comprehensive Review

Adil Rahim Margay *

ICAR-National Institute for Plant Biotechnology, New Delhi, 110012, India.

Suhail Ashraf *

CeBiTec- Center for Biotechnology, Bielefeld University, Bielefeld, 33501, Germany.

Nusrat Fatimah

Division of Agricultural Entomology, Faculty of Agriculture, Sher-e-Kashmir University of Agricultural Sciences and Technology, Srinagar, 190006, India.

Saliah Gul Jabeen

Division of Genetics and Plant Breeding, Sher-e-Kashmir University of Agricultural Sciences and Technology of Kashmir, 190006, India.

Mansoor Showkat

Department of Plant Biotechnology, University of Agricultural Sciences, GKVK, 560065, Bengaluru, India.

Krishna Nayana R U

Department of Plant Biotechnology, Centre for Plant Biotechnology and Molecular Biology, Kerala Agricultural University, Thrissur, 680654, Kerala, India.

Aadil Gani

ICAR – Indian Institute of Agricultural Biotechnology (IIAB), Garhkhatanga, Ranchi - 834003, Jharkhand, India.

Sampatirao Dilip

ICAR-National Institute for Plant Biotechnology, New Delhi, 110012, India.

Sudhakar Reddy Basu

Genetics and Plant Breeding ICAR- Indian Agricultural Research Institute, 110012, New Delhi, India.

Boddu Aruna

Professor Jayashankar Telangana state agriculture University, Rajendranagar, Hyderabad, India.

*Author to whom correspondence should be addressed.


Abstract

This comprehensive review focused on understanding the critical interplay between Brassinosteroids (BRs), a class of plant hormones, and the high-temperature stress response in wheat (Triticum aestivum) in the context of climate change. In 2022-23, heat stress caused by a spike in temperatures in mid-March 2022 reduced India's wheat crop yields by 10-15%. This lowered the country's forecasted wheat production from 110 million metric tons (MMT) to 99 MMT for the 2022/23 market year (April-March) (USDA, 2023). The adverse effects of climate change and abiotic stresses on agriculture and crop productivity are well-established, with rising temperatures identified as a significant factor in the decline of plant growth and yield. In light of this, this review aims to delve into the intricate relationship between BRs and wheat's response to high-temperature stress. Given that global mean surface temperatures have already increased and are projected to continue rising throughout the 21st century, it is imperative to explore innovative strategies to mitigate the detrimental impacts on crop productivity. To this end, the study seeks to enhance our understanding of how BRs influence the growth and yield of wheat when exposed to high-temperature stress conditions. The overarching goal is to develop effective strategies that can bolster the resilience and productivity of wheat, which is a cornerstone staple crop worldwide, facing the escalating challenge of climate change. This review builds on the existing body of knowledge, synthesizing current research findings and shedding light on the potential of BRs as a key player in ameliorating the consequences of climate change in agriculture.

Keywords: Plant hormone, abiotic stress, plant growth, Brassinosteroids, heat resilience, plant stress, plant resilience, crop rotation


How to Cite

Margay, Adil Rahim, Suhail Ashraf, Nusrat Fatimah, Saliah Gul Jabeen, Mansoor Showkat, Krishna Nayana R U, Aadil Gani, Sampatirao Dilip, Sudhakar Reddy Basu, and Boddu Aruna. 2024. “Harnessing Brassinosteroids for Heat Resilience in Wheat: A Comprehensive Review”. International Journal of Plant & Soil Science 36 (7):111-27. https://doi.org/10.9734/ijpss/2024/v36i74713.

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References

Sahni S, Prasad BD, Liu Q, Grbic V, Sharpe A. The role of brassinosteroids in mitigating the impact of environmental stresses on plants. In Plant Hormones. Humana Press. 2016;289-312.

Bajguz A, Tretyn A. The chemical characteristic and distribution of brassinosteroids in plants. Phytochemistry. 2003;62(7):1027-1046.

Wang Y, Cao JJ, Wang KX, Xia XJ, Shi K, Zhou YH, Yu JQ, Zhou J. BZR1 Mediates Brassinosteroid-Induced Autophagy and Nitrogen Starvation in Tomato. Plant Physiology. 2019;179(2):671–685.

Iqbal, Muhammad Javid, Naureen Shams, and Kalsoom Fatima. Nutritional quality of wheat. In Wheat-Recent Advances. IntechOpen; 2022.

Zhang, Zhilu, Zhongyu Chen, Haina Song, Shiping Cheng. From plant survival to thriving: Exploring the miracle of brassinosteroids for boosting abiotic stress resilience in horticultural crops. Frontiers in Plant Science. 2023;14:1218229.

Raza, Ali, Sidra Charagh, Shiva Najafi-Kakavand, Saghir Abbas, Yasira Shoaib, Sultana Anwar, Sara Sharifi, Guangyuan Lu, Kadambot HM Siddique. Role of phytohormones in regulating cold stress tolerance: Physiological and molecular approaches for developing cold-smart crop plants. Plant Stress. 2023;100152.

Li J, Chory J. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell. 1997;90(5):929-938.

Li J, Nam KH. Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science. 2002;295(5558):1299-1301.

Clouse SD. Brassinosteroid signal transduction: From receptor kinases to transcription factors. Annual Review of Plant Biology. 2011;62:291-311.

Wang W, Vinocur B, Altman A. Plant responses to drought, salinity and extreme temperatures: Towards genetic engineering for stress tolerance. Planta. 2003;218(1):1-14.

Wang X, Xin C, Cai J, Zhou Q, Dai T, Cao W, Jiang D. Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using Wheat Genome Array. BMC Genomics. 2019;20(1):1-16.

Wang X, Xin C, Cai J, Zhou Q, Dai T, Cao W, Jiang D. Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using Wheat Genome Array. BMC Genomics. 2019;20(1):1-16.

Wardlaw IF, Blumenthal C, Larroque O, Wrigley CW. Contrasting effects of chronic heat stress and heat shock on kernel weight and flour quality in wheat. Functional Plant Biology. 2002;29(1):25-34.

Vriet C, Russinova E, Reuzeau C. Boosting crop yields with plant steroids. Plant Cell. 2012;24(3):842-857.

Wu X, Yao X, Chen J, et al. Brassinosteroids protect photosynthesis and antioxidant system of eggplant seedlings from high-temperature stress. Acta Physiol Plant. 2014;36:251–261.

Kim EJ, Russinova E. Brassinosteroid Signalling. Current Biology. 2020;30(14):R294-R298.

Choudhary, Sikander Pal, Jing-Quan Yu, Kazuko Yamaguchi-Shinozaki, Kazuo Shinozaki, Lam-Son Phan Tran. "Benefits of brassinosteroid crosstalk. Trends in Plant Science. 2012;17(10):594-605.

Sahni S, Prasad BD, Liu Q, Grbic V, Sharpe A. The role of brassinosteroids in mitigating the impact of environmental stresses on plants. In Plant Hormones. Humana Press. 2016;289-312.

Kothari A, Lachowiec J. Roles of Brassinosteroids in Mitigating Heat Stress Damage in Cereal Crops. International Journal of Molecular Sciences. 2021;22(5):2706. Available:https://doi.org/10.3390/ijms22052706.

Jennifer Lachowiec. Roles of brassinosteroids in mitigating heat stress damage in cereal crops International Journal of Molecular Sciences. 2021; 22(5):2706.

Huang J, Li Z, Biener G, Xiong E, Malik KA. Brassica juncea plant growth and resistance to pathogens under jasmonate mimic coronalon treatment. Acta Biologica Cracoviensia Series Botanica. 2010;52(2):13-19.

Ogweno JO, Song XS, Shi K, Hu WH, Mao WH, Zhou YH, et al. Brassinosteroids Alleviate Heat-Induced Inhibition of Photosynthesis by Increasing Carboxylation Efficiency and Enhancing Antioxidant Systems in Lycopersicon esculentum. Journal of Plant Growth Regulation. 2008;27:49-57.

Wang Q, Yu F, Xie Q. Balancing growth and adaptation to stress: Crosstalk between brassinosteroid and abscisic acid signaling. Plant, Cell and Environment. 2020;43(10):2325–2335.

Basit F, Bhat JA, Dong Z, Mou Q, Zhu X, Wang Y, Hu J, Jan BL, Shakoor A, Guan Y, Ahmad P. Chromium toxicity induced oxidative damage in two rice cultivars and its mitigation through external supplementation of brassinosteroids and spermine. Chemosphere. 2022; 302:134423.

Yokota T, Nomura T, Nakayama T. Localization of C-6 oxidation of castasterone in etiolated mung bean seedlings by tissue-print autoradiography. Phytochemistry. 1997;45(1):35-40.

Wang ZY, Seto H, Fujioka S, Yoshida S, Chory J. BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature. 2001;410(6826): 380-383.

Wang ZY, Bai MY, Oh E, Zhu JY. Brassinosteroid signal transduction: From receptor kinases to transcription factors. Annual Review of Plant Biology. 2012;63:225-253.

Serna M, Coll Y, Zapata PJ, Botella MÁ, Pretel MT, Amorós A. A brassinosteroid analogue prevented the effect of salt stress on ethylene synthesis and polyamines in lettuce plants. Scientia Horticulturae. 2015;185:105-112.

Ali Mumtaz M, Hao Y, Mehmood S, Shu H, Zhou Y, Jin W, Chen C, Li L, Altaf MA, Wang Z. Physiological and Transcriptomic Analysis Provide Molecular Insight into 24-Epibrassinolide Mediated Cr (VI)-Toxicity Tolerance in Pepper Plants. Environmental Pollution. 2022;306: 119375.

Gao S, Fang J, Xu F, Wang W, Chu C, Li X. Comparative analysis of response and mechanism to drought stress in two contrasting Brassica napus varieties. Industrial Crops and Products. 2020;154:112647.

Hayat S, Alyemeni MN, Hasan SA. Foliar spray of brassinosteroid enhances yield and quality of Solanum lycopersicum under cadmium stress. Saudi Journal of Biological Sciences. 2012;19(3): 325-335.

Jiroutova P, Oklestkova J, Strnad M. Crosstalk between Brassinosteroids and Ethylene during Plant Growth and under Abiotic Stress Conditions. International Journal of Molecular Sciences. 2018;19(10):3283.

Ye H, Li L, Guo H. Yin-yang in gibberellin action: Gibberellin metabolic inactivation. Plant Cell. 2011;23(10):3699-3710.

Divi UK, Krishna P. Brassinosteroid: A biotechnological target for enhancing crop yield and stress tolerance. New Biotechnology. 2009;26(3-4): 131-136.

Khripach VA, Zhabinskii VN, De Groot A. Twenty years of brassinosteroids: Steroidal plant hormones warrant better crops for the XXI century. Annals of Botany. 2010;105(5):709-735.

Wang ZY, Bai MY, Oh E, Zhu JY. Brassinosteroid signaling network and regulation of photomorphogenesis. Annual Review of Genetics. 2012;46: 701-724.

Divi UK, Krishna P. Brassinosteroid: A biotechnological target for enhancing crop yield and stress tolerance. New Biotechnology. 2009;26(3-4):131-136.

Sahni S, Prasad BD, Liu Q, Grbic V, Sharpe A. The role of brassinosteroids in mitigating the impact of environmental stresses on plants. In Plant Hormones. Humana Press. 2016;289-312.

Gao S, Fang J, Xu F, Wang W, Chu C, Li X. Comparative analysis of response and mechanism to drought stress in two contrasting Brassica napus varieties. Industrial Crops and Products. 2020;154:112647.

Wang YT, Chen ZY, Jiang Y, Duan BB, Xi ZM. Involvement of ABA and antioxidant system in brassinosteroid-induced water stress tolerance of grapevine (Vitis vinifera L.). Scientia Horticulturae. 2019;256:108596.

Li J, Wen JQ, Lease KA, Doke JT, Tax FE, Walker JC. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell. 2002;110(2):213-222.

Wahid A, Gelani S, Ashraf M, Foolad MR. Heat tolerance in plants: An overview. Environmental and Experimental Botany. 2007;61(3):199-223.

Ye H, Li L, Guo H. Yin-yang in gibberellin action: Gibberellin metabolic inactivation. Plant Cell. 2010;23(10):3699-3710.

He JX, Gendron JM, Yang Y, Li J, Wang ZY. The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proceedings of the National Academy of Sciences. 2002;99(15):10185-10190.

Gill SS, Anjum NA, Gill R, Jha M, Tuteja N. Superoxide dismutase—mentor of abiotic stress tolerance in crop plants. Environmental Science and Pollution Research. 2015;22(14): 10375-10394.

Bishop, Gerard J, Csaba Koncz. Brassinosteroids and plant steroid hormone signaling. The Plant Cell. 2002;14(1):S97-S110.

Bishop GJ, Nomura T, Yokota T, Harrison K, Noguchi T, Fujioka S, Kamiya Y. The tomato DWARF enzyme catalyses C-6 oxidation in brassinosteroid biosynthesis. Proceedings of the National Academy of Sciences. 1996;93(17): 14979-14983.

Xia XJ, Huang LF, Zhou YH, et al. Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. Planta. 2009;230:1185–1196.

Asami T, Min YK, Nagata N, Yamagishi K, Takatsuto S, Fujioka S, Murofushi N. Characterization of brassinazole, a triazole-type brassinosteroid biosynthesis inhibitor. Plant Physiology. 2003; 133(4):1641-1651.

Turk EM, Fujioka S, Seto H, Shimada Y, Takatsuto S, Yoshida S, Denzel MA. BAS1 and SOB7 act redundantly to modulate Arabidopsis photomorphogenesis via unique brassinosteroid inactivation pathways. Cell. 2003;113(3):409-422.

Kim TW, Wang ZY. Brassinosteroid signal transduction from receptor kinases to transcription factors. Annual Review of Plant Biology. 2010;61:681-704.

Friedrichsen DM, Joazeiro CA, Li J, Hunter T, Chory J. Brassinosteroid-insensitive-1 is a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase. Plant Physiology. 2000;123(4): 1247-1256.

Gou X, Yin H, He K, Du J, Yi J, Xu S, Lin H. Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling. Plos Genetics. 2012;8(1):e1002452.

Kim TW, Guan SH, Burlingame AL, Wang ZY. The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2. Molecular Cell. 2011;43(4):561-571.

Kim TW, Michniewicz M, Bergmann DC, Wang ZY. Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature. 2011;482(7385):419-422.

Kim TW, Michniewicz M, Bergmann DC, Wang ZY. Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature. 2013;482(7385):419-422.

Gonzalez-Garcia MP, Vilarrasa-Blasi J, Zhiponova M, Divol F, Mora-Garcia S, Russinova E, Cano-Delgado AI. Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development. 2011; 138(5):849-859.

Vardhini BV. Brassinosteroids are Potential Ameliorators of Heavy Metal Stresses in Plants. In P. Ahmad (Ed.), Plant Metal Interaction. Elsevier. ISBN 9780128031582. 2016;209-237.

Devi LL, Pandey A, Gupta S, Singh AP. The interplay of auxin and brassinosteroid signaling tunes root growth under low and different nitrogen forms. Plant Physiology. 2022;189(3):1757–1773.Z

Fu FQ, Mao WH, Shi K, Zhou YH, Asami T, Yu JQ. A role of brassinosteroids in early fruit development in cucumber. Journal of Experimental Botany. 2008;59(9):2299–2308.

Xiong J, Yang F, Yao X, Zhao Y, Wen Y, Lin H, Guo H, Yin Y, Zhang D. The deubiquitinating enzymes UBP12 and UBP13 positively regulate recovery after carbon starvation by modulating BES1 stability in Arabidopsis thaliana. The Plant Cell. 2022;34(11):4516–4530. Available:https://doi.org/10.1093/plcell/koac245.

Nakashita H, Yasuda M, Nitta T, Asami T, Fujioka S, Arai Y. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant Journal. 2003;33(5):887-898.

Wahid A, Gelani S, Ashraf M, Foolad MR. Heat tolerance in plants: An overview. Environmental and Experimental Botany. 2007;61(3):199-223.

Farooq M, Bramley H, Palta JA, Siddique KHM. Heat stress in wheat during reproductive and grain-filling phases. Critical Reviews in Plant Sciences. 2011;30(6):491-507.

Prasad PVV, Boote KJ, Allen Jr, LH, Sheehy JE. Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crops Research. 2008;108(1):1-16.

Rizhsky L, Liang H, Mittler R. The water-water cycle is essential for chloroplast protection in the absence of stress. Journal of Biological Chemistry. 2002; 277(34):31835-31838.

Mittler R, Finka A, Goloubinoff P. How do plants feel the heat? Trends in Biochemical Sciences. 2012;37(3):118-125.

Rizhsky L, Liang H, Mittler R. The water-water cycle is essential for chloroplast protection in the absence of stress. Journal of Biological Chemistry. 2002; 277(34):31835-31838.

Prasad PVV, Boote KJ, Allen Jr LH, Sheehy JE. Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crops Research. 2008;108(1):1-16.

Sah SK, Reddy KR, Li J. Abscisic acid and abiotic stress tolerance in crop plants. Frontiers in Plant Science. 2016;7:571.

Sah SK, Reddy KR, Li J. Abscisic acid and abiotic stress tolerance in crop plants. Frontiers in Plant Science. 2016;7:571.

Giraldo JP, Benavides MP, Tseng TS, Villafranco NM. BR6ox2 and Peroxidases Cooperatively Regulate the Formation of Brassinolide, a Phytohormone. Plant Physiology. 2007; 144(1):161-172.

Gupta M, Sahi VP. Brassinosteroid confer stress tolerance in Arabidopsis by increasing antioxidant activity and reducing oxidative damage. Plant Growth Regulation. 2014;74(1):1-10.

Choudhury SR, Roy S, Sengupta DN. DNAJ and HSP70 homologs: A genome-wide comparative analysis of sequences and expression patterns of two new members of the HSP40 family of rice. DNA Research. 2012;19(3):255-26.

Dupont FM, Vensel WH, Tanaka CK, Hurkman WJ. Heat stress‐induced changes in the wheat flour proteome. Journal of Cereal Science. 2006; 43(2):172-183.

Ye K, Li H, Ding Y, Shi Y, Song C, Gong Z, Yang S. BRASSINOSTEROID-INSENSITIVE2 Negatively Regulates the Stability of Transcription Factor ICE1 in Response to Cold Stress in Arabidopsis. The Plant Cell. 2019;31(11):2682–2696.