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Brassinosteroids as a multidimensional regulator of plant physiological and molecular responses under various environmental stresses

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Abstract

Biotic and abiotic stresses, especially heavy metal toxicity, are becoming a big problem in agriculture, which pose serious threats to crop production. Plant hormones have recently been used to develop stress tolerance in a variety of plants. Brassinosteroids (BRs) are the sixth class of plant steroid hormones, with pleiotropic effects on plants. Exogenous application of BRs to boost plant tolerance mechanisms to various stresses has been a major research focus. Numerous studies have revealed the role of these steroidal hormones in the up-regulation of stress-related resistance genes, as well as their interactions with other metabolic pathways. BRs interact with other phytohormones such as auxin, cytokinin, ethylene, gibberellin, jasmonic acid, abscisic acid, salicylic acid, and polyamines to regulate a variety of physiological and developmental processes in plants. BRs regulate expressions of many BR-inducible genes by activating the brassinazole-resistant 1 (BZR1)/BRI1-EMS suppressor 1 (BES1) complex. Moreover, to improve plant development under a variety of stresses, BRs regulate antioxidant enzyme activity, chlorophyll concentration, photosynthetic capability, and glucose metabolism. This review will provide insights into the mechanistic role and actions of brassinosteroids in plants in response to various stresses.

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References

  • Acharya BR, Assmann SM (2009) Hormone interactions in stomatal function. Plant Mol Biol 69:451–462

    Article  CAS  Google Scholar 

  • Ahammed GJ, Li X, Liu A, Chen S (2020) Brassinosteroids in plant tolerance to abiotic stress. J Plant Growth Regul:1–14

  • Ahanger MA, Mir RA, Alyemeni MN, Ahmad P (2020) Combined effects of brassinosteroid and kinetin mitigates salinity stress in tomato through the modulation of antioxidant and osmolyte metabolism. Plant Physiol Biochem 147:31–42

    Article  CAS  Google Scholar 

  • Ahmad P, Ahanger MA, Egamberdieva D, Alam P, Alyemeni MN, Ashraf M (2018) Modification of osmolytes and antioxidant enzymes by 24-epibrassinolide in chickpea seedlings under mercury (Hg) toxicity. J Plant Growth Regul 37:309–322

    Article  CAS  Google Scholar 

  • Alam MM, Hayat S, Ali B, Ahmad A (2007) Effect of 28-homobrassinolide treatment on nickel toxicity in Brassica juncea. Photosynthetica 45:139–142

    Article  CAS  Google Scholar 

  • Ali B, Hasan S, Hayat S, Hayat Q, Yadav S, Fariduddin Q, Ahmad A (2008) A role for brassinosteroids in the amelioration of aluminium stress through antioxidant system in mung bean (Vigna radiata L. Wilczek). Environ Exp Bot 62:153–159

  • Alper SL, Sharma AK (2013) The SLC26 gene family of anion transporters and channels. Mol Asp Med 34:494–515

    Article  CAS  Google Scholar 

  • Amuthavalli P, Sivasankaramoorthy S (2012) Effect of salt stress on the growth and photosynthetic pigments of pigeon pea (Cajanus cajan). J Appl Pharm Sci 2:131

  • Anuradha S, Rao SSR (2001) Effect of brassinosteroids on salinity stress induced inhibition of seed germination and seedling growth of rice (Oryza sativa L.). Plant Growth Regul 33:151–153

  • Anuradha S, Rao SSR (2003) Application of brassinosteroids to rice seeds (Oryza sativa L.) reduced the impact of salt stress on growth, prevented photosynthetic pigment loss and increased nitrate reductase activity. Plant Growth Regul 40:29–32

  • Anuradha S, Rao S (2007) The effect of brassinosteroids on radish (Raphanus sativus L.) seedlings growing under cadmium stress. Plant Soil Environ 53:465

  • Arora N, Bhardwaj R, Sharma P, Arora HK (2008) Effects of 28-homobrassinolide on growth, lipid peroxidation and antioxidative enzyme activities in seedlings of Zea mays L. under salinity stress. Acta Physiol Plant 30:833–839

  • Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93

    Article  CAS  Google Scholar 

  • Ashraf M, Akram N, Arteca RN, Foolad MR (2010) The physiological, biochemical and molecular roles of brassinosteroids and salicylic acid in plant processes and salt tolerance. Crit Rev Plant Sci 29:162–190

    Article  CAS  Google Scholar 

  • Baghel M, Nagaraja A, Srivastav M, Meena NK, Kumar MS, Kumar A, Sharma R (2019) Pleiotropic influences of brassinosteroids on fruit crops: a review. Plant Growth Regul 87:375–388

    Article  CAS  Google Scholar 

  • Bajguz A (2000) Effect of brassinosteroids on nucleic acids and protein content in cultured cells of Chlorella vulgaris. Plant Physiol Biochem 38:209–215

    Article  CAS  Google Scholar 

  • Bajguz A (2002) Brassinosteroids and lead as stimulators of phytochelatins synthesis in Chlorella vulgaris. J Plant Physiol 159:321–324

    Article  CAS  Google Scholar 

  • Bajguz A, Hayat S (2009) Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem 47:1–8

    Article  CAS  Google Scholar 

  • Bal W, Kasprzak KS (2002) Induction of oxidative DNA damage by carcinogenic metals. Toxicol Lett 127:55–62

    Article  CAS  Google Scholar 

  • Barcelo J, Poschenrieder C (2002) Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review. Environ Exp Bot 48:75–92

    Article  CAS  Google Scholar 

  • Belkhadir Y, Jaillais Y (2015) The molecular circuitry of brassinosteroid signaling. New Phytol 206:522–540

    Article  CAS  Google Scholar 

  • Bergonci T, Ribeiro B, Ceciliato PH, Guerrero-Abad JC, Silva-Filho MC, Moura DS (2014) Arabidopsis thaliana RALF1 opposes brassinosteroid effects on root cell elongation and lateral root formation. J Exp Bot 65:2219–2230

    Article  CAS  Google Scholar 

  • Bhakuni G, Dube B, Sinha P, Chatterjee C (2009) Copper stress affects metabolism and reproductive yield of chickpea. J Plant Nutr 32:703–711

    Article  CAS  Google Scholar 

  • Bhandari S, Nailwal TK (2020) Role of brassinosteroids in mitigating abiotic stresses in plants. Biologia:1–28

  • Bobrovskikh A, Zubairova U, Kolodkin A, Doroshkov A (2020) Subcellular compartmentalization of the plant antioxidant system: an integrated overview. PeerJ 8:e9451

    Article  CAS  Google Scholar 

  • Caño-Delgado A, Yin Y, Yu C, Vafeados D, Mora-García S, Cheng J-C, Nam KH, Li J, Chory J (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131:5341–5351

    Article  CAS  Google Scholar 

  • Castiglione S, Franchin C, Fossati T, Lingua G, Torrigiani P, Biondi S (2007) High zinc concentrations reduce rooting capacity and alter metallothionein gene expression in white poplar (Populus alba L. cv. Villafranca). Chemosphere 67:1117–1126

  • Choudhary SP, Bhardwaj R, Gupta BD, Dutt P, Gupta RK, Biondi S, Kanwar M (2010) Epibrassinolide induces changes in indole-3-acetic acid, abscisic acid and polyamine concentrations and enhances antioxidant potential of radish seedlings under copper stress. Physiol Plant 140:280–296

    CAS  Google Scholar 

  • Choudhary SP, Kanwar M, Bhardwaj R, Yu JQ, Tran LSP (2012a) Chromium stress mitigation by polyamine-brassinosteroid application involves phytohormonal and physiological strategies in Raphanus sativus L. PLoS One 7:e33210

  • Choudhary SP, Oral HV, Bhardwaj R, Yu J-Q, Tran L-SP (2012b) Interaction of brassinosteroids and polyamines enhances copper stress tolerance in Raphanus sativus. J Exp Bot 63:5659–5675

    Article  CAS  Google Scholar 

  • Choudhary SP, Yu J-Q, Yamaguchi-Shinozaki K, Shinozaki K, Tran L-SP (2012c) Benefits of brassinosteroid crosstalk. Trends Plant Sci 17:594–605

    Article  CAS  Google Scholar 

  • Chung Y, Kwon SI, Choe S (2014) Antagonistic regulation of Arabidopsis growth by brassinosteroids and abiotic stresses. Mol Cell 3:795

    Article  CAS  Google Scholar 

  • Clouse SD, Langford M, McMorris TC (1996) A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. J Plant Physiol 111:671–678

    Article  CAS  Google Scholar 

  • Çoban Ö, Baydar NG (2016) Brassinosteroid effects on some physical and biochemical properties and secondary metabolite accumulation in peppermint (Mentha piperita L.) under salt stress. Ind Crop Prod 86:251–258

  • Coll Y, Coll F, Amorós A, Pujol M (2015) Brassinosteroids roles and applications: an up-date. Biologia 70:726–732

    Article  Google Scholar 

  • De Vleesschauwer D, Van Buyten E, Satoh K, Balidion J, Mauleon R, Choi I-R, Vera-Cruz C, Kikuchi S, Höfte M (2012) Brassinosteroids antagonize gibberellin-and salicylate-mediated root immunity in rice. Plant Physiol 158:1833–1846

    Article  CAS  Google Scholar 

  • Depuydt S, Hardtke CS (2011) Hormone signalling crosstalk in plant growth regulation. Curr Biol 21:365–373

  • Eremina M, Unterholzner SJ, Rathnayake AI, Castellanos M, Khan M, Kugler KG, May ST, Mayer KF, Rozhon W, Poppenberger B (2016) Brassinosteroids participate in the control of basal and acquired freezing tolerance of plants. Proc Natl Acad Sci U S A 113:5982–5991

  • Fahad S, Hussain S, Bano A, Saud S, Hassan S, Shan D, Khan FA, Khan F, Chen Y, Wu C (2015a) Potential role of phytohormones and plant growth-promoting rhizobacteria in abiotic stresses: consequences for changing environment. Environ Sci Pollut Res 22:4907–4921

    Article  Google Scholar 

  • Fahad S, Hussain S, Matloob A, Khan FA, Khaliq A, Saud S, Hassan S, Shan D, Khan F, Ullah N (2015b) Phytohormones and plant responses to salinity stress: a review. Plant Growth Regul 75:391–404

    Article  CAS  Google Scholar 

  • Fahad S, Hussain S, Saud S, Hassan S, Chauhan BS, Khan F, Ihsan MZ, Ullah A, Wu C, Bajwa AA (2016a) Responses of rapid viscoanalyzer profile and other rice grain qualities to exogenously applied plant growth regulators under high day and high night temperatures. PLoS One 11:e0159590

    Article  CAS  Google Scholar 

  • Fahad S, Hussain S, Saud S, Hassan S, Ihsan Z, Shah AN, Wu C, Yousaf M, Nasim W, Alharby H (2016b) Exogenously applied plant growth regulators enhance the morpho-physiological growth and yield of rice under high temperature. Front Plant Sci 7:1250

    Article  Google Scholar 

  • Fahad S, Hussain S, Saud S, Khan F, Hassan S, Nasim W, Arif M, Wang F, Huang J (2016c) Exogenously applied plant growth regulators affect heat-stressed rice pollens. J Agron Crop Sci 202:139–150

    Article  CAS  Google Scholar 

  • Fariduddin Q, Yusuf M, Ahmad I, Ahmad A (2014) Brassinosteroids and their role in response of plants to abiotic stresses. Biol Plant 58:9–17

    Article  CAS  Google Scholar 

  • Fariduddin Q, Ahmed M, Mir BA, Yusuf M, Khan TA (2015) 24-Epibrassinolide mitigates the adverse effects of manganese induced toxicity through improved antioxidant system and photosynthetic attributes in Brassica juncea. Environ Sci Pollut Res 22:11349–11359

    Article  CAS  Google Scholar 

  • Farooq M, Wahid A, Basra S (2009) Improving water relations and gas exchange with brassinosteroids in rice under drought stress. J Agron Crop Sci 195:262–269

    Article  CAS  Google Scholar 

  • Filová A (2014) Production of secondary metabolities in plant tissue cultures. Res J Agric Sci 46

  • Gallego-Bartolomé J, Arana MV, Vandenbussche F, Žádníková P, Minguet EG, Guardiola V, Van Der Straeten D, Benkova E, Alabadí D, Blázquez MA (2011) Hierarchy of hormone action controlling apical hook development in Arabidopsis. Plant J 67:622–634

    Article  CAS  Google Scholar 

  • Gupta P, Srivastava S, Seth CS (2017) 24-Epibrassinolide and sodium nitroprusside alleviate the salinity stress in Brassica juncea L. cv. Varuna through cross talk among proline, nitrogen metabolism and abscisic acid. Plant Soil 411:483–498

  • Haubrick LL, Assmann S (2006) Brassinosteroids and plant function: some clues, more puzzles. Plant Cell Environ 29:446–457

    Article  CAS  Google Scholar 

  • Hayat S, Hasan SA, Hayat Q, Ahmad A (2010a) Brassinosteroids protect Lycopersicon esculentum from cadmium toxicity applied as shotgun approach. Protoplasma 239:3–14

    Article  CAS  Google Scholar 

  • Hayat S, Hasan SA, Yusuf M, Hayat Q, Ahmad A (2010b) Effect of 28-homobrassinolide on photosynthesis, fluorescence and antioxidant system in the presence or absence of salinity and temperature in Vigna radiata. Environ Exp Bot 69:105–112

    Article  CAS  Google Scholar 

  • Hegazi AM, El-Shraiy AM, Ghoname A (2017) Mitigation of salt stress negative effects on sweet pepper using arbuscular mycorrhizal fungi (AMF), Bacillus megaterium and brassinosteroids (BRs). Gesunde Pflanzen 69:91–102

    Article  CAS  Google Scholar 

  • Hou S, Niu H, Tao Q, Wang S, Gong Z, Li S, Weng Y, Li Z (2017) A mutant in the CsDET2 gene leads to a systemic brassinosteriod deficiency and super compact phenotype in cucumber (Cucumis sativus L.). Theor Appl Genet 130:1693–1703

  • Houimli SIM, Denden M, Mouhandes BD (2010) Effects of 24-epibrassinolide on growth, chlorophyll, electrolyte leakage and proline by pepper plants under NaCl-stress. EurAsian J Biosci 4:96–104

    Article  CAS  Google Scholar 

  • Hu Y, Xia S, Su Y, Wang H, Luo W, Su S, Xiao L (2016) Brassinolide increases potato root growth in vitro in a dose-dependent way and alleviates salinity stress. Biomed Res Int:2016

  • Hussain MA, Fahad S, Sharif R, Jan MF, Mujtaba M, Ali Q, Ahmad A, Ahmad H, Amin N, Ajayo BS (2020) Multifunctional role of brassinosteroid and its analogues in plants. Plant Growth Regul 1–16

  • Issa A, Abdel-Basset R, Adam M (1995) Abolition of heavy metal toxicity on Kirchneriella lunaris (Chlorophyta) by calcium. Ann Bot 75:189–192

    Article  CAS  Google Scholar 

  • Iwata H, Gaston A, Remay A, Thouroude T, Jeauffre J, Kawamura K, Oyant LHS, Araki T, Denoyes B, Foucher F (2012) The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry. Plant J 69:116–125

    Article  CAS  Google Scholar 

  • Jan S, Noman A, Kaya C, Ashraf M, Alyemeni MN, Ahmad P (2020) 24-Epibrassinolide alleviates the injurious effects of Cr (VI) toxicity in tomato plants: insights into growth, physio-biochemical attributes, antioxidant activity and regulation of Ascorbate–glutathione and Glyoxalase cycles. J Plant Growth Regul 39:1587–1604

    Article  CAS  Google Scholar 

  • Järup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182

    Article  Google Scholar 

  • Kagale S, Divi UK, Krochko JE, Keller WA, Krishna P (2007) Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225:353–364

    Article  CAS  Google Scholar 

  • Kanwar MK, Bhardwaj R, Chowdhary SP, Arora P, Sharma P, Kumar S (2013) Isolation and characterization of 24-Epibrassinolide from Brassica juncea L. and its effects on growth, Ni ion uptake, antioxidant defense of Brassica plants and in vitro cytotoxicity. Acta Physiol Plant 35:1351–1362

  • Kartal-Alacam G, Yilmaz S, Marakli S, Gozukirmizi N (2014) Sukkula retrotransposon insertion polymorphisms in barley. Russ J Plant Physiol 61:828–833

    Article  CAS  Google Scholar 

  • Kaya C, Ashraf M, Alyemeni MN, Ahmad P (2020) The role of nitrate reductase in brassinosteroid-induced endogenous nitric oxide generation to improve cadmium stress tolerance of pepper plants by upregulating the ascorbate-glutathione cycle. Ecotoxicol Environ Saf 196:110483

    Article  CAS  Google Scholar 

  • Khripach VA, Zhabinskii V, de Groot AE (1998) Brassinosteroids: a new class of plant hormones. Academic Press

  • Kim E-J, Russinova E (2020) Brassinosteroid signalling. Curr Biol 30:R294–R298

    Article  CAS  Google Scholar 

  • Kohli SK, Handa N, Sharma A, Gautam V, Arora S, Bhardwaj R, Alyemeni MN, Wijaya L, Ahmad P (2018) Combined effect of 24-epibrassinolide and salicylic acid mitigates lead (Pb) toxicity by modulating various metabolites in Brassica juncea L. seedlings. Protoplasma 255:11–24

  • Kumar Tewari R, Kumar P, Nand Sharma P (2008) Morphology and physiology of zinc-stressed mulberry plants. J Plant Nutr Soil Sci 171:286–294

    Article  CAS  Google Scholar 

  • Kumar SS, Kadier A, Malyan SK, Ahmad A, Bishnoi NR (2017) Phytoremediation and rhizoremediation: uptake, mobilization and sequestration of heavy metals by plants. Plant-microbe interactions in agro-ecological perspectives:367–394

  • Küpper H, Küpper F, Spiller M (1998) In situ detection of heavy metal substituted chlorophylls in water plants. Photosynth Res 58:123–133

    Article  Google Scholar 

  • Latha P, Vardhini BV (2017) Effect of homobrassinolide on bio-chemical activities and chlorophyll pigments of mustard plants grown in semi-arid tropics of Nizamabad. Eur J Biomed Pharm Sci 4:613–618

    CAS  Google Scholar 

  • Latha P, Vidya Vardhini B (2018) Effect of homobrassinolide on the growth of mustard crops grown in semi-arid tropics of nizamabad. Int J Curr Res Life Sci 7:2320–2326

    Google Scholar 

  • Li F, Fan G, Lu C, Xiao G, Zou C, Kohel RJ, Ma Z, Shang H, Ma X, Wu J (2015) Genome sequence of cultivated Upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Nat Biotechnol 33:524–530

    Article  CAS  Google Scholar 

  • Lin Y-F, Aarts MG (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206

    Article  CAS  Google Scholar 

  • Madhan M, Mahesh K, Rao S (2014) Effect of 24-epibrassinolide on aluminium stress induced inhibition of seed germination and seedling growth of Cajanus cajan (L.) Millsp. Int J Multidiscipl Current Res 2:286–290

  • Mireles A, Solıs C, Andrade E, Lagunas-Solar M, Pina C, Flocchini R (2004) Heavy metal accumulation in plants and soil irrigated with wastewater from Mexico City. Nucl Instrum Methods Phys Res, Sect B 219:187–190

    Article  CAS  Google Scholar 

  • Mishra S, Bharagava RN, More N, Yadav A, Zainith S, Mani S, Chowdhary P (2019) Heavy metal contamination: an alarming threat to environment and human health, Environmental biotechnology: For sustainable future. Springer, pp. 103-125

  • Moullan N, Mouchiroud L, Wang X, Ryu D, Williams EG, Mottis A, Jovaisaite V, Frochaux MV, Quiros PM, Deplancke B (2015) Tetracyclines disturb mitochondrial function across eukaryotic models: a call for caution in biomedical research. Cell Rep 10:1681–1691

    Article  CAS  Google Scholar 

  • Nahar K, Kyndt T, Hause B, Höfte M, Gheysen G (2013) Brassinosteroids suppress rice defense against root-knot nematodes through antagonism with the jasmonate pathway. Mol Plant-Microbe Interact 26:106–115

    Article  CAS  Google Scholar 

  • Nassar A (2004) Effect of homobrassinolide on in vitro growth of apical meristems and heat tolerance of banana shoots. Int J Agric Biol 6:771–776

    CAS  Google Scholar 

  • Nawaz F, Naeem M, Zulfiqar B, Akram A, Ashraf MY, Raheel M, Shabbir RN, Hussain RA, Anwar I, Aurangzaib M (2017) Understanding brassinosteroid-regulated mechanisms to improve stress tolerance in plants: a critical review. Environ Sci Pollut Res 24:15959–15975

    Article  Google Scholar 

  • Niu J-h, Ahmad Anjum S, Wang R, J-h L, M-r L, J-x S, Zohaib A, Lv J, Wang S-g, X-f Z (2016) Exogenous application of brassinolide can alter morphological and physiological traits of Leymus chinensis (Trin.) Tzvelev under room and high temperatures. Chil J Agric Res 76:27–33

  • Nunez M, Mazzafera P, Mazorra L, Siqueira W, Zullo M (2003) Influence of a brassinosteroid analogue on antioxidant enzymes in rice grown in culture medium with NaCl. Biol Plant 47:67–70

  • Oh E, Zhu J-Y, Bai M-Y, Arenhart RA, Sun Y, Wang Z-Y (2014) Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. elife 3:e03031

    Article  CAS  Google Scholar 

  • Özdemir F, Bor M, Demiral T, Türkan İ (2004) Effects of 24-epibrassinolide on seed germination, seedling growth, lipid peroxidation, proline content and antioxidative system of rice (Oryza sativa L.) under salinity stress. Plant Growth Regul 42:203–211

  • Petridis A, Döll S, Nichelmann L, Bilger W, Mock HP (2016) Arabidopsis thaliana G2-LIKE FLAVONOID REGULATOR and BRASSINOSTEROID ENHANCED EXPRESSION1 are low-temperature regulators of flavonoid accumulation. New Phytol 211:912–925

    Article  CAS  Google Scholar 

  • Piotrowska-Niczyporuk A, Bajguz A (2014) The effect of natural and synthetic auxins on the growth, metabolite content and antioxidant response of green alga Chlorella vulgaris (Trebouxiophyceae). Plant Growth Regul 73:57–66

  • Polko JK, van Zanten M, van Rooij JA, Marée AF, Voesenek LA, Peeters AJ, Pierik R (2012) Ethylene-induced differential petiole growth in Arabidopsis thaliana involves local microtubule reorientation and cell expansion. New Phytol 193:339–348

    Article  CAS  Google Scholar 

  • Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, and detoxification in plants. Rev Environ Contam T volume 213:113–136

    CAS  Google Scholar 

  • Pretali L, Bernardo L, Butterfield TS, Trevisan M, Lucini L (2016) Botanical and biological pesticides elicit a similar induced systemic response in tomato (Solanum lycopersicum) secondary metabolism. Phytochemistry 130:56–63

    Article  CAS  Google Scholar 

  • Rajan I, Narayanan N, Rabindran R, Jayasree P, Kumar PM (2013) Zingerone protects against stannous chloride-induced and hydrogen peroxide-induced oxidative DNA damage in vitro. Biol Trace Elem Res 155:455–459

    Article  CAS  Google Scholar 

  • Rajewska I, Talarek M, Bajguz A (2016) Brassinosteroids and response of plants to heavy metals action. Front Plant Sci 7:629

    Article  Google Scholar 

  • Ramakrishna B, Rao SSR (2015) Foliar application of brassinosteroids alleviates adverse effects of zinc toxicity in radish (Raphanus sativus L.) plants. Protoplasma 252:665–677

  • Rao SSR, Vardhini BV, Sujatha E, Anuradha S (2002) Brassinosteroids–a new class of phytohormones. Curr Sci:1239–1245

  • Ravazzolo L, Trevisan S, Forestan C, Varotto S, Sut S, Dall’Acqua S, Malagoli M, Quaggiotti S (2020) Nitrate and ammonium affect the overall maize response to nitrogen availability by triggering specific and common transcriptional signatures in roots. Int J Mol Sci 21:686

    Article  CAS  Google Scholar 

  • Raza A, Razzaq A, Mehmood SS, 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

    Article  CAS  Google Scholar 

  • Roy AK, Sharma A, Talukder G (1988) Some aspects of aluminum toxicity in plants. Bot Rev 54:145–178

    Article  Google Scholar 

  • Saini S, Sharma I, Pati PK (2015) Versatile roles of brassinosteroid in plants in the context of its homoeostasis, signaling and crosstalks. Front Plant Sci 6:950

    Article  Google Scholar 

  • Saleem MH, Ali S, Rehman M, Rana MS, Rizwan M, Kamran M, Imran M, Riaz M, Soliman MH, Elkelish A (2020) Influence of phosphorus on copper phytoextraction via modulating cellular organelles in two jute (Corchorus capsularis L.) varieties grown in a copper mining soil of Hubei Province, China. Chemosphere 248:126032

  • Salt DE, Blaylock M, Kumar NP, Dushenkov V, Ensley BD, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Bio/technology 13:468–474

    CAS  Google Scholar 

  • Schädel C, Blöchl A, Richter A, Hoch G (2010) Quantification and monosaccharide composition of hemicelluloses from different plant functional types. Plant Physiol Biochem 48:1–8

    Article  CAS  Google Scholar 

  • Schippers JH, Jing H-C, Hille J, Dijkwel PP (2007) Developmental and hormonal control of leaf senescence. Senescence processes in plants 26:145–170

    Article  CAS  Google Scholar 

  • Setsungnern A, Muñoz P, Pérez-Llorca M, Müller M, Thiravetyan P, Munné-Bosch S (2020) A defect in BRI1-EMS-SUPPRESSOR 1 (bes1)-mediated brassinosteroid signaling increases photoinhibition and photo-oxidative stress during heat stress in Arabidopsis. Plant Sci 296:110470

    Article  CAS  Google Scholar 

  • Shahbaz M, Ashraf M (2007) Influence of exogenous application of brassinosteroid on growth and mineral nutrients of wheat (Triticum aestivum L.) under saline conditions. Pak J Bot 39:513

  • Shahid M, Pervez M, Balal R, Mattson N, Rashid A, Ahmad R, Ayyub C, Abbas T (2011) Brassinosteroid (24-epibrassinolide) enhances growth and alleviates the deleterious effects induced by salt stress in pea (Pisum sativum L.). Aust J Crop Sci 5:500–510

  • Shahnejat-Bushehri S, Tarkowska D, Sakuraba Y, Balazadeh S (2016) Arabidopsis NAC transcription factor JUB1 regulates GA/BR metabolism and signalling. Nat plants 2:1–9

    Article  CAS  Google Scholar 

  • Shahzad B, Tanveer M, Che Z, Rehman A, Cheema SA, Sharma A, Song H, Rehman S, Zhaorong D (2018) Role of 24-epibrassinolide (EBL) in mediating heavy metal and pesticide induced oxidative stress in plants: a review. Ecotoxicol Environ Saf 147:935–944

    Article  CAS  Google Scholar 

  • Shakirova F, Allagulova C, Maslennikova D, Fedorova K, Yuldashev R, Lubyanova A, Bezrukova M, Avalbaev A (2016) Involvement of dehydrins in 24-epibrassinolide-induced protection of wheat plants against drought stress. Plant Physiol Biochem 108:539–548

    Article  CAS  Google Scholar 

  • Shalygo N, Kolesnikova N, Voronetskaya V, Averina N (1999) Effects of Mn 2+, Fe 2+, Co 2+, and Ni 2+ on chlorophyll accumulation and early stages of chlorophyll formation in greening barley seedlings. Russ J Plant Physiol 46:496–501

    CAS  Google Scholar 

  • Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31:739–753

    Article  CAS  Google Scholar 

  • Sharma A, Kumar V, Kanwar M, Thukral A, Bhardwaj R (2017) Ameliorating imidacloprid induced oxidative stress by 24-epibrassinolide in Brassica juncea L. Russ J Plant Physiol 64:509–517

  • Soares C, Branco-Neves S, de Sousa A, Pereira R, Fidalgo F (2016a) Ecotoxicological relevance of nano-NiO and acetaminophen to Hordeum vulgare L.: combining standardized procedures and physiological endpoints. Chemosphere 165:442–452

  • Soares C, de Sousa A, Pinto A, Azenha M, Teixeira J, Azevedo RA, Fidalgo F (2016b) Effect of 24-epibrassinolide on ROS content, antioxidant system, lipid peroxidation and Ni uptake in Solanum nigrum L. under Ni stress. Environ Exp Bot 122:115–125

  • Sri ND, Mohan MM, Mahesh K, Raghu K, Rao SSR (2016) Amelioration of aluminium toxicity in pigeon pea [Cajanus cajan (L.) Millsp.] plant by 24-epibrassinolide. Am J Plant Sci 7:1618–1628

  • Stobart AK, Griffiths WT, Ameen-Bukhari I, Sherwood RP (1985) The effect of Cd2+ on the biosynthesis of chlorophyll in leaves of barley. Physiol Plant 63:293–298

    Article  CAS  Google Scholar 

  • Sun Y, He Y, Irfan AR, Liu X, Yu Q, Zhang Q, Yang D (2020) Exogenous brassinolide enhances the growth and cold resistance of maize (Zea mays L.) seedlings under chilling stress. Agronomy 10:488

  • Surgun Y, Altunlu H, Türkekul S, Bürün B (2015) Effects of 24-epibrassinolide on growth and some antioxidant enzymes of cotton (Gossypium hirsutum L.) cultivars under NaCl stress. J Appl Biol Sci (JABS) 2146-0108(9):09–17

  • Swamy GJ, Muthukumarappan K (2017) Optimization of continuous and intermittent microwave extraction of pectin from banana peels. Food Chem 220:108–114

    Article  CAS  Google Scholar 

  • Swamy K, Vardhini B, Ramakrishna B, Anuradha S, Siddulu N, Rao S (2014) Role of 28-homobrassinolide on growth biochemical parameters of Trigonella foenu-graecum L. plants subjected to lead toxicity. Int Multidiscip Curr Res 2:317–321

  • Takatsuto S (1994) Brassinosteroids: distribution in plants, bioassays and microanalysts by gas chromatography—mass spectrometry. J Chromatogr A A 658:3–15

    Article  CAS  Google Scholar 

  • Talaat NB, Shawky BT (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 35:729–740

  • Talaat NB, Shawky BT (2014) Protective effects of arbuscular mycorrhizal fungi on wheat (Triticum aestivum L.) plants exposed to salinity. Environ Exp Bot 98:20–31

  • Talaat NB, Shawky BT (2016) Dual application of 24-epibrassinolide and spermine confers drought stress tolerance in maize (Zea mays L.) by modulating polyamine and protein metabolism. J Plant Growth Reg 35:518–533

  • Tangahu BV, Sheikh Abdullah SR, Basri H, Idris M, Anuar N, Mukhlisin M (2011) A review on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation. Int J Chem Eng 2011

  • Tanveer M, Shahzad B, Sharma A, Khan EA (2019) 24-Epibrassinolide application in plants: An implication for improving drought stress tolerance in plants. Plant Physiol Biochem 135:295–303

    Article  CAS  Google Scholar 

  • Thussagunpanit J, Jutamanee K, Sonjaroon W, Kaveeta L, Chai-Arree W, Pankean P, Suksamrarn A (2015) Effects of brassinosteroid and brassinosteroid mimic on photosynthetic efficiency and rice yield under heat stress. Photosynthetica 53:312–320

    Article  CAS  Google Scholar 

  • Upadhyaya CP, Bagri DS, Upadhyay DC (2015) Ascorbic acid and/or 24-epibrassinolide trigger physiological and biochemical responses for the salt stress mitigation in potato (Solanum tuberosum L.). Int J Appl Sci Biotechnol 3:655–667

  • Vardhini BV (2012) Mitigation of water stress and saline stress by brassinosteroids. Practical Applications in Agriculture, Forestry and Human Health Bentham Science Publishers, United States of America, ed. AB Pereira-Netto, Brassinosteroids, pp 16–25

  • Vardhini BV (2017) Modifications of morphological and anatomical characteristics of plants by application of brassinosteroids under various abiotic stress conditions-a review. Plant Gene 11:70–89

    Article  CAS  Google Scholar 

  • Vardhini B (2019) Does Application of Brassinosteroids mitigate the Temperature Stress in Plants. Int J Earth Sci Geol 1:59–65

    Article  Google Scholar 

  • Vardhini BV, Anjum NA (2015) Brassinosteroids make plant life easier under abiotic stresses mainly by modulating major components of antioxidant defense system. Front Environ Sci 2:67

    Article  Google Scholar 

  • Vardhini BV, Rao SSR (1998) Effect of brassinosteroids on growth, metabolite content and yield of Arachis hypogaea. Phytochemistry 48:927–930

    Article  CAS  Google Scholar 

  • Vardhini BV, Anuradha S, Rao S (2006) Brassinosteroids-New class of plant hormone with potential to improve crop productivity. Indian J Plant Physiol 11:1

    CAS  Google Scholar 

  • Wang Y, Sun S, Zhu W, Jia K, Yang H, Wang X (2013) Strigolactone/MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. Dev Cell 27:681–688

    Article  CAS  Google Scholar 

  • Werner T, Motyka V, Strnad M, Schmülling T (2001) Regulation of plant growth by cytokinin. Proc Natl Acad Sci U S A 98:10487–10492

    Article  CAS  Google Scholar 

  • Wright AV, Nuñez JK, Doudna JA (2016) Biology and applications of CRISPR systems: harnessing nature’s toolbox for genome engineering. Cell 164:29–44

    Article  CAS  Google Scholar 

  • Wu G, Broniscer A, McEachron TA, Lu C, Paugh BS, Becksfort J, Qu C, Ding L, Huether R, Parker M (2012) Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat Genet 44:251

    Article  CAS  Google Scholar 

  • Wu SM, Lin WY, Shen CC, Pan HC, Keh-Bin W, Chen YC, Jan YJ, Lai DW, Tang SC, Tien HR (2016) Melatonin set out to ER stress signaling thwarts epithelial mesenchymal transition and peritoneal dissemination via calpain-mediated C/EBP β and NF κB cleavage. J Pineal Res 60:142–154

    Article  CAS  Google Scholar 

  • Ye H, Liu S, Tang B, Chen J, Xie Z, Nolan TM, Jiang H, Guo H, Lin H-Y, Li L (2017) RD26 mediates crosstalk between drought and brassinosteroid signalling pathways. Nat Commun 8:1–13

    Article  CAS  Google Scholar 

  • Yildirim E, Karlidag H, Turan M, Dursun A, Goktepe F (2011) Growth, nutrient uptake, and yield promotion of broccoli by plant growth promoting rhizobacteria with manure. HortScience 46:932–936

    Article  CAS  Google Scholar 

  • Yuldashev R, Avalbaev A, Bezrukova M, Vysotskaya L, Khripach V, Shakirova F (2012) Cytokinin oxidase is involved in the regulation of cytokinin content by 24-epibrassinolide in wheat seedlings. Plant Physiol Biochem 55:1–6

    Article  CAS  Google Scholar 

  • Yusuf M, Fariduddin Q, Hayat S, Hasan SA, Ahmad A (2011) Protective response of 28-homobrassinolide in cultivars of Triticum aestivum with different levels of nickel. Arch Environ Contam Toxicol 60:68–76

    Article  CAS  Google Scholar 

  • Yusuf M, Fariduddin Q, Ahmad I, Ahmad A (2014) Brassinosteroid-mediated evaluation of antioxidant system and nitrogen metabolism in two contrasting cultivars of Vigna radiata under different levels of nickel. Physiol Mol Biol Plants 20:449–460

    Article  CAS  Google Scholar 

  • Zhao G, Xu H, Zhang P, Su X, Zhao H (2017) Effects of 2, 4-epibrassinolide on photosynthesis and Rubisco activase gene expression in Triticum aestivum L. seedlings under a combination of drought and heat stress. Plant Growth Regul 81:377–384

  • Zhu J-Y, Sae-Seaw J, Wang Z-Y (2013) Brassinosteroid signalling. Development 140:1615–1620

    Article  CAS  Google Scholar 

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Acknowledgements

This research was supported by the Key Research and Development Program of Zhejiang Province (No.2019C02004, 2019C02011), Hainan Provincial Science and Technology Plan-Sanya Yazhou Bay Science and Technology City Joint Project (No. 320LH032). National Natural Science Foundation of China (No. 32072127), Zhejiang Provincial Natural Science Foundation (No. LY21C130006), Dabeinong Funds for Discipline Development and Talent Training in Zhejiang University, and Jiangsu Collaborative Innovation Center for Modern Crop Production, P. R. China.

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  1. Farwa Basit and Jiaxin Liu contributed equally to this work.

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  1. Institute of Crop Sciences, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China

    Farwa Basit, Jiaxin Liu, Jianyu An, Min Chen, Can He, Xiaobo Zhu, Zhan Li, Jin Hu & Yajing Guan

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  1. Farwa Basit
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Contributions

Farwa Basit: Conceptualization, investigation, writing—original draft. Can He and Jin Hu: Investigation. Jianyu An and Zhan Li: Investigation, Min Chen: Funding acquisition. Xiaobo Zhu: Investigation. Jiaxin Liu: Writing—reviewing and editing. Yajing Guan: Conceptualization, supervision, validation, writing (reviewing, editing), and funding acquisition.

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Basit, F., Liu, J., An, J. et al. Brassinosteroids as a multidimensional regulator of plant physiological and molecular responses under various environmental stresses. Environ Sci Pollut Res 28, 44768–44779 (2021). https://doi.org/10.1007/s11356-021-15087-8

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