Abstract
Brassinosteroids have been identified as polyhydroxylated steroidal plant hormones which are known for their response against stress and development processes like flowering, germination and crop production. Because of their multiple properties, brassinosteroids occupy a significant place among hormones. These naturally occurring plant hormones induce tolerance against abiotic and biotic stresses such as temperature variation (extreme cold/hot), salinity, water scarcity or drought, injury, fungal infection and metal toxicity. As a result of these stresses free radicals, like superoxide ions and peroxide are produced which cause damage to the plant system. Exogenous application of brassinosteroids at appropriate time can save plants from oxidative stresses. Brassinosteroids enhance carbon dioxide assimilation capacity, chlorophyll contents, antioxidants including ascorbate, carotenoids and proline under adverse environmental conditions. Besides inducing resistance against stresses, brassinosteroids also regulate growth, increase seed germination and ripening of fruits. It has been also noticed that the brassinazole-resistant-dependent brassinosteroid signaling up-regulates the expression of autophagy-related genes and autophagosome formation under stress. We have summarized, in this review, the information available until 2021, the impact of BRs application on plant growth and development under abiotic stress.
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Abbreviations
- 24-EBL:
-
24-epibrassinolide
- 28-HBL:
-
28-homobrassinolide
- ABA:
-
Abscisic acid
- APX/APOX:
-
Ascorbate peroxidase
- ATGs:
-
Autophagy-related gene
- BL:
-
Brassinolide
- BR:
-
Brassinosteroid
- BZR1:
-
BRASSINAZOLE RESISTANT 1
- BAK1:
-
brassinosteroids associated kinase1
- BRI1:
-
brassinosteroid insensitive1
- CaCl2 :
-
Calcium chloride
- CaSO4 :
-
Calcium sulfate
- CAT:
-
Catalase
- DHAR:
-
Dehydroascorbate reductase
- GP:
-
Guaiacol peroxidase
- GSH:
-
Glutathione
- GSSG:
-
Glutathione disulphide
- GPX:
-
Glutathione peroxidase
- GR:
-
Glutathione reductase
- H2O2 :
-
Hydrogen peroxide
- HCl:
-
Hydrogen chloride
- HM:
-
Heavy Metal
- IAA:
-
Indole acetic acid
- NBR1:
-
next-to-BRCA1
- KCl:
-
Potassium chloride
- MDA:
-
Malondialdehyde
- MAPK:
-
Mitogen-activated protein kinases
- MDHAR:
-
Monodehydroascorbate reductase
- K:
-
Potassium
- P:
-
Phosphate
- NaCl:
-
Sodium chloride
- NaOH:
-
Sodium hydroxide
- PC:
-
Phytochelatin
- Prxs:
-
Peroxiredoxins
- ROS:
-
Reactive oxygen species
- RWC:
-
Relative water content
- SOD:
-
Superoxide dismutase
- V-ATPase:
-
vacuolar H+-ATPase
References
Abbas S, Latif HH, Elsherbiny EA (2013) Effect of 24-epibrassinolide on the physiological and genetic changes on two varieties of pepper under salt stress conditions. Pak J Bot 45:1273–1284
Aghdam MS, Asghari M, Farmani B, Mohayeji M, Moradbeygi H (2012) Impact of post harvest brassinosteroids treatment on PAL activity in tomato fruit in response to chilling stress. Sci Hort 144:116–120. https://doi.org/10.1016/j.scienta.2012.07.008
Aghdam MS, Mohammadkhani N (2014) Enhancement of chilling stress tolerance of tomato fruit by postharvest brassinolide treatment. Food Bioproc Technol 7:909–914. https://doi.org/10.1007/s11947-013-1165-x
Ahammed GJ, Choudhary SP, Chen S, Xia X, Shi K, Zhou Y, Yu J (2013) Role of brassinosteroids in alleviation of phenanthrene cadmium co-contamination-induced photosynthetic inhibition and oxidative stress in tomato. J Exp Bot 64:199–213. https://doi.org/10.1093/jxb/ers323
Ahmad F, Ahmad M, Khan S (2005) Indole acetic acid production by the indigenous isolates of Azotobacter and fluorescent Pseudomonas in the presence and absence of tryptophan. Turk J Biol 29:29–34
Ali Q, Athar HUR, Ashraf M (2006) Influence of exogenously applied brassinosteroids on the mineral nutrient status of two wheat cultivars grown under saline conditions. Pak J Bot 38:1621–1632
Ali B, Hayat S, Ahmad A (2007) 28-Homobrassinolide ameliorates the saline stress in chickpea (Cicer arietinum L.). Environ Exp Bot 59:217–223. https://doi.org/10.1016/j.envexpbot.2005.12.002
Ali B, Hayat S, Fariduddin Q, Ahmad A (2008a) 24-Epibrassinolide protects against the stress generated by salinity and nickel in Brassica juncea. Chemosphere 72:1387–1392. https://doi.org/10.1016/j.chemosphere.2008.04.012
Ali B, Hasan SA, Hayat S, Hayat Q, Yadav S, Fariduddin Q, Ahmad A (2008b) 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. https://doi.org/10.1016/j.envexpbot.2007.07.014
Alyemeni MN, Hayat S, Wijaya L, Anaji A (2013) Foliar application of 28-homobrassinolide mitigates salinity stress by increasing the efficiency of photosynthesis in Brassica juncea. Acta Bot Bras 27:502–505. https://doi.org/10.1590/S0102-33062013000300007
Amjad M, Akhtar J, Anwar-ul-Haq M, Yang A, Akhtar SS, Jacobsen SE (2014) Integrating role of ethylene and ABA in tomato plants adaptation to salt stress. Sci Hortic 172:109–116. https://doi.org/10.1016/j.scienta.2014.03.024
Anuradha S, Ram Rao SS (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. https://doi.org/10.1023/A:1023080720374
Anuradha S, Rao SSR (2007) The effect of brassinosteroids on radish (Raphanus sativus L.) seedlings growing under cadmium stress. Plant Soil Environ 53:465–472
Anuradha S, Rao SSR (2009) Effect of 24-epibrassinolide on the photosynthetic activity of radish plants under cadmium stress. Photosynthetica 47:317–320. https://doi.org/10.1007/s11099-009-0050-3
Anwar A, Liu Y, Dong R, Bai L, Yu X, Li Y (2018) The physiological and molecular mechanism of brassinosteroid in response to stress: a review. Biol Res 51:46. https://doi.org/10.1186/s40659-018-0195-2
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. https://doi.org/10.1007/s11738-008-0188-9
Arora P, Bhardwaj R, Kanwar MK (2010) 24-Epibrassinolide induced antioxidative defense system of Brassica juncea L. under Zn metal stress. Physiol Mol Biol Plant 16:285–293. https://doi.org/10.1007/s12298-010-0031-9
Avalbaev AM, Yuldashev RA, Fatkhutdinova RA, Urusov FA, Safutdinova YV, Shakirova FM (2010) The influence of 24-epibrassinolide on the hormonal status of wheat plants under sodium chloride. Appl Biochem Microbiol 46:99–102
Avalbaev A, Bezrukova M, Allagulova C, Lubyanova AR, Kudoyarova GR, Fedorova K, Maslennikova D, Yuldashev R, Shakirova F (2020) Wheat germ agglutinin is involved in the protective action of 24-epibrassinolide on the roots of wheat seedlings under drought conditions. Plant Physiol Biochem 146:420–427. https://doi.org/10.1016/j.plaphy.2019.11.038
Babaloa OO (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 32:1559–1570. https://doi.org/10.1007/s10529-010-0347-0
Bai MY, Shang JX, Oh E, Fan M, Bai Y, Zentella R, Sun TP, Wang ZY (2012) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14:810–817. https://doi.org/10.1038/ncb2546
Bajguz A (2002) Brassinosteroids and lead asstimulators of phytochelatins synthesis in Chlorella vulgaris. J Plant Physiol 159:321–324. https://doi.org/10.1078/0176-1617-00654
Bajguz A, Tretyn A (2003) The chemical characteristic and distribution of brassinosteroids in plants. Phytochemistry 62:1027–1046. doi: 1016/s0031-9422(02)00656-8
Bajguz A, Hayat S (2009) Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem 47:1–8. https://doi.org/10.1016/j.plaphy.2008.10.002
Barry CS, Blume B, Bouzayen M, Cooper W, Hamilton AJ, Grierson D (1996) Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato. Plant J9:525–535. https://doi.org/10.1046/j.1365-313X.1996.09040525.x
Bartwal A, Mall R, Lohani P, Guru SK, Arora S (2013) Role of secondary metabolites and brassinosteroids in plant defense against environmental stresses. J Plant Growth Regul 32:216–232. https://doi.org/10.1007/s00344-012-9272-x
Behnamnia M, Kalantari KM, Rezanejad F (2009) Exogenous application of brassinosteroid alleviates drought-induced oxidative stress in Lycopersicon esculentum L. Gen Appl Plant Physiol 35:22–34
Belkhadir Y, Jaillais Y (2015) The molecular circuitry of brassinosteroid signaling. New Phytol 206:522–540. https://doi.org/10.1111/nph.13269
Bhattacharjee S (2008) Calcium-dependent signaling pathway in the heat-induced oxidative injury in Amaranthus lividus. Biol Plant 52:137. https://doi.org/10.1007/s10535-008-0028-1
Bjornson M, Dandekar AM, Chory J, Dehesh K (2016) Brassinosteroid's multi-modular interaction with the general stress network customizes stimulus-specific responses in Arabidopsis. Plant Sci 250:165–177. https://doi.org/10.1016/j.plantsci.2016.06.007
Bohnert HJ, Nelson DE, Jonsen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111. https://doi.org/10.1105/tpc.7.7.1099
Bukhari SA, Wang R, Wang W, Ahmed IM, Zheng W, Cao F (2016) Genotype-dependent effect of exogenous 24-epibrassinolide on chromium-induced changes in ultrastructure and physicochemical traits in tobacco seedlings. Environ Sci Pollut Res Int 23:18229–18238. https://doi.org/10.1007/s11356-016-7017-2
Chakma SP, Chileshe SM, Thomas R, Krishna P (2021) Cotton seed priming with brassinosteroid promotes germination and seedling growth. Agronomy 11:566. https://doi.org/10.3390/agronomy11030566
Chen J, Fei K, Zhang W, Wang Z, Zhang J, Yang J (2021) Brassinosteroids mediate the effect of high temperature during anthesis on the pistil activity of photo-thermosensitive genetic male-sterile rice lines. Crop J 9:109–119. https://doi.org/10.1016/j.cj.2020.07.001
Chi YH, Koo SS, Oh HT, Lee ES, Park JH, Phan KAT, Wi SD, Bae SB, Paeng SK, Chae HB, Kang CH, Kim MG, Kim W-Y, Yun D-J, Lee SY (2019) The physiological functions of universal stress proteins and their molecular mechanism to protect plants from environmental stresses. Front Plant Sci 10:750. https://doi.org/10.3389/fpls.2019.00750
Chi C, Li X, Fang P, Xia X, Shi K, Zhou Y, Zhou J, Yu J (2020) Brassinosteroids act as a positive regulator of NBR1-dependent selective autophagy in response to chilling stress in tomato. J Exp Bot 71:1092–1106. https://doi.org/10.1093/jxb/erz466
Choe S, Dilkes BP, Gregory BD, Ross AS, Yuan H, Noguchi T, Fujioka S, Takatsuto S, Tanaka A, Yoshida S, Tax FE, Feldmann KA (1999a) The Arabidopsis dwarf1 mutant is defective in the conversion of 24-methylenecholesterol to campesterol in brassinosteroid biosynthesis. Plant Physiol 119:897–907 doi:https://doi.org/10.1104/pp.119.3.897
Choe S, Noguchi T, Fujioka S, Takatsuto S, Tissier CP, Gregory BD, Ross AS, Tanaka A, Yoshida S, Tax FE, Feldmann KA (1999b) The Arabidopsis dwf7/ste1 mutant is defective in the delta7 sterol C-5 desaturation step leading to brassinosteroid biosynthesis. Plant Cell 11:207–221. https://doi.org/10.1105/tpc.11.2.207
Choe S, Fujioka S, Noguchi T, Takatsuto S, Yoshida S, Feldmann KA (2001) Overexpression of DWARF4 in the brassinosteroid biosynthetic pathway results in increased vegetative growth and seed yield in Arabidopsis. Plant J 26:573–582. https://doi.org/10.1046/j.1365-313x.2001.01055.x
Chung Y, Choe S (2013) The regulation of brassinosteroid biosynthesis in Arabidopsis. CRC Crit Rev Plant Sci 32:396–410. https://doi.org/10.1080/07352689.2013.797856
Clouse SD, Langford M, McMorris TC (1996) A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol 111:671–678. https://doi.org/10.1104/pp.111.3.671
Clouse SD (2016) Brassinosteroid/abscisic acid antagonism in balancing growth and stress. Dev Cell 38:118–120. https://doi.org/10.1016/j.devcel.2016.07.005
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. https://doi.org/10.1016/j.indcrop.2016.03.049
Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163. https://doi.org/10.1186/1471-2229-11-163
Cruz de Carvalho MH (2008) Drought stress and reactive oxygen species. Plant Signal Behav 3:156–165. https://doi.org/10.4161/psb.3.3.5536
Dalio RJD, Pinheiro HP, Sodek L, Haddad CRB (2013) 24-Epibrassinolide restores nitrogen metabolism of pigeon pea under saline stress. Bot Stud 54:9. https://doi.org/10.1186/1999-3110-54-9
Das T, Shukla YM, Poonia TC, Meena M, Meena MD (2013) Effects of brassinolide on physiological characteristics of rice (Oryza sativa L.) with different salinity levels. Ann Biol 29:228–231
Daur I, Tatar O (2013) Effects of gypsum and brassinolide on soil properties, and berseem (Trifolium alexandrinum L.) growth, yield and chemical composition grown on saline soil. Legume Res 36:306–311
de Oliveira VP, Lima MDR, da Silva BRS, Batista BL, da Silva Lobato AK (2019) Brassinosteroids confer tolerance to salt stress in Eucalyptus urophylla plants enhancing homeostasis, antioxidant metabolism and leaf anatomy. J Plant Growth Regul 38:557–573. https://doi.org/10.1007/s00344-018-9870-3
Ding HD, Zhu XH, Zhu ZW, Yang SJ, Zha DS, Wu XX (2012) Amelioration of salt-induced oxidative stress in eggplant by application of 24-epibrassinolide. Biol Plant 56:767–770. https://doi.org/10.1007/s10535-012-0108-0
Divi UK, Krishna P (2009) Brassinosteroid: a biotechnological target for enhancing crop yield and stress tolerance. New Biotechnol 26:131–136. https://doi.org/10.1016/j.nbt.2009.07.006
dos Santos Ribeiro DG, da Silva BRS, da Silva Lobato AK (2019) Brassinosteroids induce tolerance to water deficit in soybean seedlings: contributions linked to root anatomy and antioxidant enzymes. Acta Physiol Plant 41:82. https://doi.org/10.1007/s11738-019-2873-2
Durigan DRJ, Pinheiro HP, Sodek L, Haddad CRB (2011) The effect of 24-epibrassinolide and clotrimazole on the adaptation of Cajanus cajan (L.) Millsp to salinity. Acta Physiol. Plant 33:1887–1896. https://doi.org/10.1007/s11738-011-0732-x
Ekinci M, Yildirim E, Dursun A, Turan M (2012) Mitigation of salt stress in lettuce (Lactuca sativa L. var. Crispa) by seed and foliar 24-epibrassinolide treatments. Hortic Sci 47:631–636. https://doi.org/10.21273/HORTSCI.47.5.631
El-Khallal SM, Hathout TA, Ashour AERA, Kerrit AAA (2009) Brassinolide and salicylic acid induced antioxidant enzymes, hormonal balance and protein profile of maize plants grown under salt stress. Res J Agric Biol Sci 5:391–402
El-Mashad A, Mohamed H (2012) Brassinolide alleviates salt stress and increases antioxidant activity of cowpea plants (Vigna sinensis). Protoplasma 249:625–635. https://doi.org/10.1007/s00709-011-0300-7
Embiale A, Hussein A, Husen A, Sahile S, Mohammed K (2016) Differential sensitivity of Pisum sativum L. cultivars to water-deficit stress: changes in growth, water status, chlorophyll fluorescence and gas exchange attributes. J Agron 15:45–57. https://doi.org/10.3923/ja.2016.45.57
Evans RM (1988) The steroid and thyroid hormone receptor superfamily. Science 240:889–895. https://doi.org/10.1126/science.3283939
Fariduddin Q, Khanam S, Hasan SA, Ali B, Hayat S, Ahmad A (2009a) Effect of 28-homobrassinolide on the drought stress-induced changes in photosynthesis and antioxidant system of Brassica juncea L. Acta Physiol Plant 31:889–897. https://doi.org/10.1007/s11738-009-0302-7
Fariduddin Q, Yusuf M, Hayat S, Ahmad A (2009b) Effect of 28-homobrassinolide on antioxidant capacity and photosynthesis in Brassica juncea plants exposed to different levels of copper. Environ Exp Bot 66:418–424. https://doi.org/10.1016/j.envexpbot.2009.05.001
Fariduddin Q, Yusuf M, Chalkoo S, Hayat S, Ahmad A (2011) 28-homobrassinolide improves growth and photosynthesis in Cucumis sativus L. through an enhanced antioxidant system in the presence of chilling stress. Photosynthetica 49:55–64. https://doi.org/10.1007/s11099-011-0022-2
Fariduddin Q, Khalil RRAE, Mir BA, Yusuf M, Ahmad A (2013a) 24-Epibrassinolide regulates photosynthesis, antioxidant enzyme activities and proline content of Cucumis sativus under salt and/or copper stress. Environ Monit Assess 185:7845–7856. https://doi.org/10.1007/s10661-013-3139-x
Fariduddin Q, Mir BA, Yusuf M, Ahmad A (2013b) Comparative roles of brassinosteroids and polyamines in salt stress tolerance. Acta Physiol Plant 35:2037–2053. https://doi.org/10.1007/s11738-013-1263-4
Fedina EO (2013) Effect of 24-epibrassinolide on pea protein tyrosine phosphorylation after salinity action. Russ J Plant Physiol 60:351–358. https://doi.org/10.1134/S1021443713020088
Feng RJ, Ren MY, Lu LF, Peng M, Guan X, Zhou DB, Zhang MY, Qi DF, Li K, Tang W, Yun TY, Chen YF, Wang F, Zhang D, Shen Q, Liang P, Zhang YD, Xie JH (2019) Involvement of abscisic acid-responsive element-binding factors in cassava (Manihot esculenta) dehydration stress response. Sci Rep 9:12661. https://doi.org/10.1038/s41598-019-49083-3
Fujioka S, Li J, Choi YH, Seto H, Takatsuto S, Noguchi T, Watanabe T, Kuriyama H, Yokota T, Chory J, Sakurai A (1997) The Arabidopsis deetiolated 2 mutant is blocked early in brassinosteroid biosynthesis. Plant Cell 9:1951–1962. https://doi.org/10.1105/tpc.9.11.1951
Gao W, Long L, Zhu LF, Xu L, Gao WH, Sun LQ, Liu LL, Zhang XL (2013) Proteomic and virus-induced gene silencing (VIGS) analyses reveal that gossypol, brassinosteroids, and jasmonic acid contribute to the resistance of cotton to Verticillium dahliae. Mol Cell Proteomics 12:3690–3703. https://doi.org/10.1074/mcp.M113.031013
Getnet Z, Husen A, Fetene M, Yemata G (2015) Growth, water status, physiological, biochemical and yield response of stay green sorghum {Sorghum bicolor (L.) Moench} varieties - a field trial under drought-prone area in Amhara regional state, Ethiopia. J Agron 14:188–202. https://doi.org/10.3923/ja.2015.188.202
Gilroy S, Suzuki N, Miller G, Choi WG, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci 19:623–630. https://doi.org/10.1016/j.tplants.2014.06.013
Gomes MMA, Netto AT, Campostrini E, Bressan-Smith R, Zullo MAT, Ferraz TM, Siqueira LN, Leal NR, Núñez-Vázquez M (2013) Brassinosteroid analogue affects the senescence in two papaya genotypes submitted to drought stress. Theor Exp Plant Phys 25:186–195
González-Olmedo JL, Cordova A, Aragon CE, Pina D, Rivas M, Rodrıguez R (2005) Effect of an analogue of brassinosteroid on FHIA-18 plantlets exposed to thermal stress. Infomusa 14:18–20
Gudesblat GE, Schneider-Pizoń J, Betti C, Mayerhofer J, Vanhoutte I, van Dongen W, Boeren S, Zhiponova M, de Vries S, Jonak C, Russinova E (2012) SPEECHLESS integrates brassinosteroid and stomata signalling pathways. Nat Cell Biol 14:548–554. https://doi.org/10.1038/ncb2471
Guedes FRCM, Maia CF, Silva BRSD, Batista BL, Alyemeni MN, Ahmad P, Lobato AKDS (2021) Exogenous 24-Epibrassinolide stimulates root protection, and leaf antioxidant enzymes in lead stressed rice plants: central roles to minimize Pb content and oxidative stress. Environ Pollut 280:116992. https://doi.org/10.1016/j.envpol.2021.116992
Guiboileau A, Avila-Ospina L, Yoshimoto K, Soulay F, Azzopardi M, Marmagne A, Lothier J, Masclaux-Daubresse C (2013) Physiological and metabolic consequences of autophagy deficiency for the management of nitrogen and protein resources in Arabidopsis leaves depending on nitrate availability. New Phytol 199:683–694. https://doi.org/10.1111/nph.12307
Guo H, Li L, Aluru M, Aluru S, Yin Y (2013) Mechanisms and networks for brassinosteroid regulated gene expression. Curr Opin Plant Biol 16:545–553. https://doi.org/10.1016/j.pbi.2013.08.002
Hamilton AJ, Lycett GW, Grierson D (1990) Antisense gene that inhibits synthesis of the hormone ethylene in transgenic plants. Nature 346:284–287. https://doi.org/10.1038/346284a0
Hasan SA, Hayat S, Ahmad A (2011) Brassinosteroids protect photosynthetic machinery against the cadmium induced oxidative stress in two tomato cultivars. Chemosphere 84:1446–1451. https://doi.org/10.1016/j.chemosphere.2011.04.047
Hasan SA, Hayat S, Ali B, Ahmad A (2008) 28-Homobrassinolide protects chickpea (Cicer arietinum) from cadmium toxicity by stimulating antioxidants. Environ Pollut 151:60–66. https://doi.org/10.1016/j.envpol.2007.03.006
Hayat S, Ali B, Hasan SA, Ahmad A (2007) Brassinosteroid enhanced the level of antioxidants under cadmium stress in Brassica juncea. Environ Exp Bot 60:33–41. https://doi.org/10.1016/j.envexpbot.2006.06.002
Hayat S, Hasan SA, Hayat Q, Ahmad A (2010a) Brassinosteroids protect Lycopersicon esculentum from cadmium toxicity applied as shotgun approach. Protoplasma 239:3–14. https://doi.org/10.1007/s00709-009-0075-2
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 doi: 10.1016/j.envexpbot.2010.03.004
Hayat S, Yadav S, Ali B, Ahmad A (2010c) Interactive effect of nitric oxide and brassinosteroids on photosynthesis and the antioxidant system of Lycopersicon esculentum. Russ J Plant Physiol 57:212–221. https://doi.org/10.1134/S1021443710020081
Hayat S, Alyemeni M, Hasan S (2012) Foliar spray of brassinosteroid enhances yield and quality of Solanum lycopersicum under cadmium stress. Saudi J Biol Sci 19:325–335. https://doi.org/10.1016/j.sjbs.2012.03.005
He RY, Wang GJ, Wang XS (1991) Effect of brassinolide on growth and chilling resistance of maize seedlings, In: Cutler HG, Yokota T, Adam G(Eds), Brassinosteroids: Chemistry, Bioactivity and Applications, American Chemical Society, Washington, DC, pp. 220–230
Heidari P, Mazloomi F, Nussbaumer T, Barcaccia G (2020) Insights into the SAM synthetase gene family and its roles in tomato seedlings under abiotic stresses and hormone treatments. Plants (Basel) 9:586. https://doi.org/10.3390/plants9050586
Hosseinpour M, Ebadi A, Habibi H, Nabizadeh E, Jahanbakhsh S (2020) Enhancing enzymatic and nonenzymatic response of Echinacea purpurea by exogenous 24-epibrassinolide under drought stress. Ind Crop Prod 146:112045. https://doi.org/10.1016/j.indcrop.2019.112045
Hu X, Jiang M, Zhang J, Zhang A, Lin F, Tan M (2007) Calcium–calmodulin is required for abscisic acid-induced antioxidant defense and functions both upstream and downstream of H2O2 production in leaves of maize (Zea mays) plants. New Phytol 173:27–38. https://doi.org/10.1111/j.1469-8137.2006.01888.x
Hu WH, Yan XH, Xiao YA, Zeng JJ, Qi HJ, Ogweno JO (2013) 24-Epibrassinosteroid alleviate drought-induced inhibition of photosynthesis in Capsicum annuum. Sci Hortic 150:232–237. https://doi.org/10.1016/j.scienta.2012.11.012
Huang B, Chu CH, Chen SL, Juan HF, Chen YM (2006) A proteomics study of the mung bean epicotyl regulated by brassinosteroids under conditions of chilling stress. Cell Mol Biol Lett 11:264–278. https://doi.org/10.2478/s11658-006-0021-7
Husen A, Iqbal M, Aref IM (2016) IAA-induced alteration in growth and photosynthesis of pea (Pisum sativum L.) plants grown under salt stress. J Environ Biol 37:421–429
Husen A, Iqbal M, Aref IM (2017) Plant growth and foliar characteristics of faba bean (Vicia faba L.) as affected by indole-acetic acid under water-sufficient and water-deficient conditions. J Environ Biol 38:179–186
Husen A, Iqbal M, Aref IM (2014) Growth, water status and leaf characteristics of Brassica carinata under drought and rehydration conditions. Braz J Bot 37:217–227 doi:https://doi.org/10.1007/s40415-014-0066-1
Hussain MA, Fahad S, Sharif R, Jan MF, Mujtaba M, Ali Q, Ahmad A, Ahmad H, Amin N, Ajayo BS, Sun C, Gu L, Ahmad I, Jiang Z, Hou J (2020) Multifunctional role of brassinosteroid and its analogues in plants. Plant Growth Regul 92:141–156. https://doi.org/10.1007/s10725-020-00647-8
Hussain S, Khaliq A, Matloob A, Wahid MA, Afzal I (2013) Germination and growth response of three wheat cultivars to NaCl salinity. Soil Environ 32:36–43
Hwang H, Ryu H, Cho H (2021) Brassinosteroid signaling pathways interplaying with diverse signaling cues for crop enhancement. Agronomy 11:556. https://doi.org/10.3390/agronomy11030556
Iqbal N, Nazar R, Iqbal MRK, Masood A, Nafees AK (2011) Role of gibberellins in regulation of source sink relations under optimal and limiting environmental conditions. Curr Sci 100:998–1007
Iqbal N, Umar S, Khan NA, Khan MIR (2014) A new perspective of phytohormones in salinity tolerance: regulation of proline metabolism. Environ Exp Bot 100:34–42. https://doi.org/10.1016/j.envexpbot.2013.12.006
Janeczko A, Koscielniak J, Pilipowicz M, Szarek-Lukaszewska G, Skoczowski A (2005) Protection of winter rape photosystem 2 by 24-epibrassinolide under cadmium stress. Photosynthetica 43:293–298. https://doi.org/10.1007/s11099-005-0048-4
Janeczko A, Gullner G, Skoczowski A, Dubert F, Barna B (2007) Effects of brassinosteroid infiltration prior to cold treatment on ion leakage and pigment contents in rape leaves. Biol Plant 51:355–358. https://doi.org/10.1007/s10535-007-0072-2
Jeandroz S, Lamotte O (2017) Editorial: plant responses to biotic and abiotic stresses: lessons from cell signaling. Front Plant Sci 8:1772. https://doi.org/10.3389/fpls.2017.01772
Jiang YP, Cheng F, Zhou YH, Xia XJ, Mao WH, Shi K, Chen Z, Yu JQ (2012) Cellular glutathione redox homeostasis plays an important role in the brassinosteroids induced increase in CO2 assimilation in Cucumis sativus. New Phytol 194:932–943. https://doi.org/10.1111/j.1469-8137.2012.04111.x
Jiang YP, Huang LF, Cheng F, Zhou YH, Xia XJ, Mao WH, Shi K, Yu JQ (2013) Brassinosteroids accelerate recovery of photosynthetic apparatus from cold stress by balancing the electron partitioning, carboxylation and redox homeostasis in cucumber. Physiol Plant 148:133–145. https://doi.org/10.1111/j.1399-3054.2012.01696.x
Kagale S, Divi UK, Krochko JE, Keller WA, Krishna P (2007) Brassinosteroids confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225:353–364. https://doi.org/10.1007/s00425-006-0361-6
Kang HM, Saltveit ME (2002) Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol Plant 115:571–576. https://doi.org/10.1034/j.1399-3054.2002.1150411.x
Kang YY, Guo SR, Li J, Duan JJ (2009) Effect of root applied 24-epibrassinolide on carbohydrate status and fermentative enzyme activities in cucumber (Cucumis sativus L.) seedlings under hypoxia. Plant Growth Regul 57:259–269. https://doi.org/10.1007/s10725-008-9344-x
Kanwar MK, Bhardwaj R, Arora P, Chowdhary SP, Sharma P, Kumar S (2012) Plant steroid hormones produced under Ni stress are involved in the regulation of metal uptake and oxidative stress in Brassica juncea L. Chemosphere 86:41–49. https://doi.org/10.1016/j.chemosphere.2011.08.048
Karlidag H, Yildirim E, Turan M (2011) Role of 24-epibrassinolide in mitigating the adverse effects of salt stress on stomatal conductance, membrane permeability, and leaf water content, ionic composition in salt stressed strawberry (Fragaria x ananassa). Sci Hort 130:133–140. https://doi.org/10.1016/j.scienta.2011.06.025
Kaya C, Ashraf M, Wijaya L, Ahmad P (2019) The putative role of endogenous nitric oxide in brassinosteroid-induced antioxidant defence system in pepper (Capsicum annuum L.) plants under water stress. Plant Physiol Biochem143:119–128 doi: https://doi.org/10.1016/j.plaphy.2019.08.024
Khorasaninejad S, Mousavi A, Soltanloo H, Hemmati K, Khalighi A (2010) The effect of salinity stress on growth parameters, essential oil yield andconstituent of peppermint (Mentha piperita L.). World ApplSci J 11:1403–1407
Kim TW, Michniewicz M, Bergmann DC, Wang ZY (2012) Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature 482:419–422. https://doi.org/10.1038/nature10794
Kim J, Liu Y, Zhang X, Zhao B, Childs KL (2016) Analysis of salt-induced physiological and proline changes in 46 switchgrass (Panicum virgatum) lines indicates multiple response modes. Plant Physiol Biochem 105:203–212. https://doi.org/10.1016/j.plaphy.2016.04.020
Klahre U, Noguchi T, Fujioka S, Takatsuto S, Yokota T, Nomura T, Yoshida S, Chua NH (1998) The Arabidopsis DIMINUTO/DWARF1 gene encodes a protein involved in steroid synthesis. Plant Cell 10:1677–1690. https://doi.org/10.1105/tpc.10.10.1677
Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45:41–59. https://doi.org/10.1146/annurev-genet-110410-132507
Koca N, Karaman S (2015) The effects of plant growth regulators and L-phenylalanine on phenolic compounds of sweet basil. Food Chem 166:515–521. https://doi.org/10.1016/j.foodchem.2014.06.065
Kong Q, Mostafa HHA, Yang W, Wang J, Nuerawuti M, Wang Y, Song J, Zhang X, Ma L, Wang H, Li X (2021) Comparative transcriptome profiling reveals that brassinosteroid-mediated lignification plays an important role in garlic adaption to salt stress. Plant Physiol Biochem 158:34–42. https://doi.org/10.1016/j.plaphy.2020.11.033
Kothari A, Lachowiec J (2021) Roles of Brassinosteroids in mitigating heat stress damage in cereal crops. Int J Mol Sci 22:2706. https://doi.org/10.3390/ijms22052706
Kroutil M, Hejtmankova A, Lachman J (2010) Effect of spring wheat (Triticum aestivum L.) treatment with brassinosteroids on the content of cadmium and lead in plant aerial biomass and grain. Plant Soil Environ 56:43–50. https://doi.org/10.17221/148/2009-PSE
Kulaeva ON, Burkhanova EA, Fedina AB, Khokhlova VA, Bokebayeva GA, Vorbrodt HM, Adam G (1991) Effect of brassinosteroids on protein synthesis and plant-cell ultrastructure under stress conditions, in: Cutler HG, Yokota T, Adam G(Eds.), Brassinosteroids: chemistry, bioactivity and applications, American Chemical Society, Washington, DC, ACS symposium series pp. 141–155. https://doi.org/10.1021/bk-1991-0474.ch012
Kumar A, Kumar V, Dubey AK, Ansari MA, Narayan S, Meenakshi KS, Pandey V, Pande V, Sanyal I (2021) Chickpea glutaredoxin (CaGrx) gene mitigates drought and salinity stress by modulating the physiological performance and antioxidant defense mechanisms. Physiol Mol Biol Plants 27:923–944. https://doi.org/10.1007/s12298-021-00999-z
Kurepin LV, Qaderi MM, Back TG, Reid DM, Pharis RP (2008) A rapid effect of applied brassinolide on abscisic acid concentrations in Brassica napus leaf tissue subjected to short-term heat stress. Plant Growth Regul 55:165–167. https://doi.org/10.1007/s10725-008-9276-5
Kwak JM, Nguyen V, Schroeder JI (2006) The role of reactive oxygen species in hormonal responses. Plant Physiol 141:323–329 doi:https://doi.org/10.1104/pp.106.079004
Laxmi A, Paul LK, Peters JL, Khurana JP (2004) Arabidopsis constitutive photomorphogenic mutant bls1, displays altered brassinosteroid response and sugar sensitivity. Plant Mol Biol 56:185–201. https://doi.org/10.1007/s11103-004-2799-x
Le J, Liu XG, Yang KZ, Chen XL, Zou JJ, Wang HZ, Wang M, Vanneste S, Morita M, Tasaka M, Ding ZJ, Friml J, Beeckman T, Sack F (2014) Auxin transport and activity regulate stomatal patterning and development. Nat Commun 5:3090. https://doi.org/10.1038/ncomms4090
Li L, van Staden J, Jager AK (1998) Effects of plant growth regulators on the antioxidant system in seedlings of two maize cultivars subjected to water stress. Plant Growth Regul 25:81–87. https://doi.org/10.1023/A:1010774725695
Li KR, Wang HH, Han G, Wang QJ, Fan J (2008) Effects of brassinolide on the survival, growth and drought resistance of Robinia pseudoacacia seedlings under water-stress. New Forest 35:255–266. https://doi.org/10.1007/s11056-007-9075-2
Li KR, Feng CH (2011) Effects of brassinolide on drought resistance of Xanthoceras sorbifolia seedlings under water stress. Acta Physiol Plant 33:1293–1300. https://doi.org/10.1007/s11738-010-0661-0
Li YH, Liu YJ, Xu XL, Jin M, An LZ, Zhang H (2012) Effect of 24-epibrassinolide on drought stress-induced changes in Chorispora bungeana. Biol Plant 56:192–196. https://doi.org/10.1007/s10535-012-0041-2
Li M, Ahammed GJ, Li C, Bao X, Yu J, Huang C, Yin H, Zhou J (2016) Brassinosteroid ameliorates zinc oxide nanoparticles-induced oxidative stress by improving antioxidant potential and redox homeostasis in tomato seedling. Front Plant Sci 7:615. https://doi.org/10.3389/fpls.2016.00615
Li X, Wei JP, Ahammed GJ, Zhang L, Li Y, Yan P, Zhang LP, Han WY (2018) Brassinosteroids attenuate moderate high temperature-caused decline in tea quality by enhancing theanine biosynthesis in Camellia sinensis L. Front Plant Sci 9:1016. https://doi.org/10.3389/fpls.2018.01016
Liu H, Guo T, Zhu Y, Wang C, Kang G (2006) Effects of epi-brassinolide (epi-BR) application at anthesis on starch accumulation and activities of key enzymes in wheat grains. Acta Agron Sinica 32:924–930
Liu Y, Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Biol 63:215–237. https://doi.org/10.1146/annurev-arplant-042811-105441
Liu L, Jia C, Zhang M, Chen D, Chen S, Guo R, Wang Q (2014) Ectopic expression of a BZR1-1D transcription factor in brassinosteroid signalling enhances carotenoid accumulation and fruit quality attributes in tomato. Plant Biotechnol J12:105–115. https://doi.org/10.1111/pbi.12121
Liu J, Yang R, Jian N, Wei L, Ye L, Wang R, Gao H, Zheng Q (2020a) Putrescine metabolism modulates the biphasic effects of brassinosteroids on canola and Arabidopsis salt tolerance. Plant Cell Environ 43:1348–1359. https://doi.org/10.1111/pce.13757
Liu J, Yang R, Jian N, Wei L, Ye L, Wang R, Gao H, Zheng Q (2020b) Putrescine metabolism modulates the biphasic effects of brassinosteroids on canola and Arabidopsis salt tolerance. Plant Cell Environ 43:1348–1359. https://doi.org/10.1111/pce.13757
Mahesh B, Parshavaneni B, Ramakrishna B, Rao SSR (2013) Effect of brassinosteroids on germination and seedling growth of radish (Raphanus sativus L.) under PEG-6000 induced water stress. Am J Plant Sci 4:2305–2313. https://doi.org/10.4236/ajps.2013.412285
Marshall RS, Vierstra RD (2018) Autophagy: the master of bulk and selective recycling. Annu Rev Plant Biol 69:173–208. https://doi.org/10.1146/annurev-arplant-042817-040606
Masood A, Shah NA, Zeeshan M, Abraham G (2006) Differential response of antioxidant enzymes to salinity stress in two varieties of Azolla (Azolla pinnata and Azolla filiculoides). Environ Exp Bot 58:216–222. https://doi.org/10.1016/j.envexpbot.2005.08.002
Matsoukas IG (2014) Interplay between sugar and hormone signaling pathways modulate floral signal transduction. Front Genet 5:218. https://doi.org/10.3389/fgene.2014.00218
Mazorra LM, Nunez M, Hechavarria M, Coll F, Sanchez-Blanco MJ (2002) Influence of brassinosteroids on antioxidant enzymes activity in tomato under different temperatures. Biol Plant 45:593–596. https://doi.org/10.1023/A:1022390917656
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. https://doi.org/10.1016/s1360-1385(02)02312-9
Mousavi EA, Kalantari KM, Jafari SR (2009) Change of some osmolytes accumulation in water-stressed colza (Brassica napus L.) as affected by 24-epibrassinolide. Iranian J Sci Technol Transac A Sci 33:1–11
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Physiol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Müssig C, Biesgen C, Lisso J, Uwer U, Weiler EW, Altmann TA (2000) Novel stress inducible 12-oxophytodienoate reductase from Arabidopsis thaliana provides a potential link between brassinosteroid-action and jasmonic-acid synthesis. J Plant Physiol 157:143–152. https://doi.org/10.1016/S0176-1617(00)80184-4
Nikoleta-Kleio D, Theodoros D, Roussos PA (2020) Antioxidant defense system in young olive plants against drought stress and mitigation of adverse effects through external application of alleviating products. Sci Hort 259:108812. https://doi.org/10.1016/j.scienta.2019.108812
Noguchi T, Fujioka S, Choe S, Takatsuto S, Tax FE, Yoshida S, Feldmann KA (2000) Biosynthetic pathways of brassinolide in Arabidopsis. Plant Physiol 124:201–209 doi:https://doi.org/10.1104/pp.124.1.201
Nolan T, Chen J, Yin Y (2017) Cross-talk of brassinosteroid signaling in controlling growth and stress responses. Biochem J 474:2641–2661. https://doi.org/10.1042/BCJ20160633
Nolan TM, Vukasinovi N, Liu D, Russinova E, Yin Y (2020) Brassinosteroids: multidimensional regulators of plant growth, development, and stress responses. Plant Cell 32:295–318. https://doi.org/10.1105/tpc.19.00335
Nunez M, Mazzafera P, Mazorra LM, Siqueira WJ, Zullo MAT (2003) Influence of a brassinsteroid analogue on antioxidant enzymes in rice grown in culture medium with NaCl. Biol Plant 47:67–70. https://doi.org/10.1023/A:1027380831429
Oeller PW, Lu MW, Taylor LP, Pike DA, Theologis A (1991) Reversible inhibition of tomato fruit senescence by antisense RNA. Science 254:437–439. https://doi.org/10.1126/science.1925603
Ogweno JO, Song XS, Shi K, Hu WH, Mao WH, Zhou YH, Yu JQ, Nogués N (2008) Brassinosteroids alleviate heat-induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum. J Plant Growth Regul 27:49–57. https://doi.org/10.1007/s00344-007-9030-7
Ohnishi T, Szatmari AM, Watanabe B, Fujita S, Bancos S, Koncz C, Lafos M, Shibata K, Yokota T, Sakata K, Szekeres M, Mizutani M (2006) C-23 hydroxylation by Arabidopsis CYP90C1 and CYP90D1 reveals a novel shortcut in brassinosteroid biosynthesis. Plant Cell 18:3275–3288. https://doi.org/10.1105/tpc.106.045443
Özdemir F, Bor M, Demiral T, Turkan I (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. https://doi.org/10.1023/B:GROW.0000026509.25995.13
Pereira YC, Rodrigues WS, Lima EJA, Santos LR, Silva MHL, Lobato AKS (2019) Brassinosteroids increase electron transport and photosynthesis in soybean plants under water deficit. Photosynthetica 57:181–191. https://doi.org/10.32615/ps.2019.029
Podlešáková K, Ugena L, Spíchal L, Doležal K, De Diego N (2019) Phytohormones and polyamines regulate plant stress responses by altering GABA pathway. New Biotechnol 48:53–65. https://doi.org/10.1016/j.nbt.2018.07.003
Qin G, Ma Z, Zhang L, Xing S, Hou X, Deng J, Liu J, Chen Z, Qu LJ, Gu H (2007) Arabidopsis AtBECLIN 1/AtAtg6/AtVps30 is essential for pollen germination and plant development. Cell Res 17:249–263. https://doi.org/10.1038/cr.2007.7
Rady MM (2011) Effect of 24-epibrassinolide on growth, yield, antioxidant system and cadmium content of bean (Phaseolus vulgaris L.) plants under salinity and cadmium stress. Sci Hortic 129:232–237. https://doi.org/10.1016/j.scienta.2011.03.035
Rajewska I, Talarek M, Bajguz A (2016) Brassinosteroids and response of plants to heavy metals action. Front Plant Sci 7:629. https://doi.org/10.3389/fpls.2016.00629
Ramakrishna B, Rao SSR (2013) Preliminary studies on the involvement of glutathione metabolism and redox status against zinc toxicity in radish seedlings by 28-homobrassinolide. Environ Expt Bot 96:52–58. https://doi.org/10.1016/j.envexpbot.2013.08.003
Rattan A, Kapoor D, Kapoor N, Bhardwaj R, Sharma A (2020) Brassinosteroids regulate functional components of antioxidative defense system in salt stressed maize seedlings. J Plant Growth Regul. https://doi.org/10.1007/s00344-020-10097-1
Rontein D, Basset G, Hanson AD (2002) Metabolic engineering of osmoprotectant accumulation in plants. Metab Eng 4:49–56. https://doi.org/10.1006/mben.2001.0208
Ruley AT, Sharma NC, Sahi SV (2004) Antioxidant defense in a lead accumulating plant, Sesbania drummondii. Plant Physiol Biochem 42:899–906. https://doi.org/10.1016/j.plaphy.2004.12.001
Sahni S, Prasad BD, Liu Q, Grbic V, Sharpe A, Singh SP, Krishna P (2016) Overexpression of the brassinosteroid biosynthetic gene DWF4 in Brassica napus simultaneously increases seed yield and stress tolerance. Sci Rep 6:28298. https://doi.org/10.1038/srep28298
Sakurai A, Fujioka S (1997) Studies on biosynthesis of brassinosteroids. Biosci Biotechnol Biochem 61:757–762. https://doi.org/10.1271/bbb.61.757
Sarker U, Oba S (2018) Catalase, superoxide dismutase and ascorbate-glutathione cycle enzymes confer drought tolerance of Amaranthus tricolor. Sci Rep 8:16496. https://doi.org/10.1038/s41598-018-34944-0
Sarker U, Oba S (2020) The response of salinity stress-induced a. tricolor to growth, anatomy, physiology, non-enzymatic and enzymatic antioxidants. Front plant Sci 11:559876 doi:https://doi.org/10.3389/fpls.2020.559876
Sasse JM (1991) The case for brassinosteroids as endogenous plant hormones, In: Cutler HG, Yokota T, Adam G (eds) Brassinosteroids: chemistry, bioactivity and applications. ACS symposium series 474. American Chemical Society, Washington, DC pp. 158–166
Sasse J (2002) Physiological actions of brassinosteroids: an update. J Plant Growth Regul 22:276–288. https://doi.org/10.1007/s00344-003-0062-3
Savaliya DD, Mandavia CK, Mandavia MK (2013) Role of brassinolide on enzyme activities in groundnut under water deficit stress. Indian J Agric Biochem 26:92–96
Schröder F, Lisso J, Obata T, Erban A, Maximova E, Giavalisco P, Kopka J, Fernie AR, Willmitzer L, Müssig C (2014) Consequences of induced brassinosteroid deficiency in Arabidopsis leaves. BMC Plant Biol 14:309. https://doi.org/10.1186/s12870-014-0309-0
Serna M, Coll Y, Zapata PJ, Botella MA, Pretel MT, Amorós A (2015) A brassinosteroid analogue prevented the effect of salt stress on ethylene synthesis and polyamines in lettuce plants. Sci Hort 185:105–112. https://doi.org/10.1016/j.scienta.2015.01.005
Shahbaz M, Ashraf M (2007) Influence of exogenous application of brassinosteroids on growth and mineral nutrients of wheat (Triticum aestivum L.) under saline conditions. Pak J Bot 39:513–522
Shahbaz M, Ashraf M, Athar HUR (2008) Does exogenous application of 24-epibrassinolide ameliorate salt induced growth inhibition in wheat (Triticum aestivum L.)? Plant Growth Regul 55:51–64. https://doi.org/10.1007/s10725-008-9262-y
Shahid MA, Pervez MA, Balal RM, Mattson NS, Rashid A, Ahmad R, Ayyub CM, Abba 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
Shahid MA, Balal RM, Pervez MA, Garcia-Sanchez F, Gimeno V, Abbas T, Mattson NS, Riaz A (2014) Treatment with 24-epibrassinolide mitigates NaCl-induced toxicity by enhancing carbohydrate metabolism, osmolyte accumulation, and antioxidant activity in Pisum sativum. Turk J Bot 38:511–525. https://doi.org/10.3906/bot-1304-45
Shang Q, Song S, Zhang Z, Guo S (2006) Exogenous brassinosteroid induced salt resistance of cucumber (Cucumis sativus L.) seedlings. Sci Agric Sinica 39:1872–1877
Sharma P, BhardwajR AN, Arora HK (2007) Effect of 28-homobrassinolide on growth, zinc metal uptake and antioxidative enzyme activities in Brassica juncea L. seedlings. Braz J Plant Physiol 19:203–210. https://doi.org/10.1590/S1677-04202007000300004
Sharma I, Pati PK, Bhardwaj R (2010) Regulation of growth and antioxidant enzyme activities by 28-homobrassinolide in seedlings of Raphanus sativus L. under cadmium stress. Indian J Biochem Biophys 47:172–177
Sharma I, Pati PK, Bhardwaj R (2011a) Effect of 28-homobrassinolide on antioxidant defence system in Raphanus sativus L. under chromium toxicity. Ecotoxicology 20:862–874. https://doi.org/10.1007/s10646-011-0650-0
Sharma I, Pati PK, Bhardwaj R (2011b) Effect of 24-epibrassinolide on oxidative stress markers induced by nickel-ion in Raphanus sativus L. Acta Physiol Plant 33:1723–1735. https://doi.org/10.1007/s11738-010-0709-1
Sharma I, Bhardwaj R, Pati PK (2013) Stress modulation response of 24-epibrassinolide against imidacloprid in an elite indica rice variety Pusa Basmati-1. Pesticide Biochem Physiol 105:144–153. https://doi.org/10.1016/j.pestbp.2013.01.004
Sharma P, Kumar A, Bhardwaj R (2016) Plant steroidal hormone epibrassinolide regulate–heavy metal stress tolerance in Oryza sativa L. by modulating antioxidant defense expression. Environ Exp Bot 122:1–9 doi: https://doi.org/10.1016/j.envexpbot.2015.08.005
Sheehy JE, Elmido A, Centeno G, Pablico P (2005) Searching for new plant for climate change. J Agric Meteorol 60:463–468. https://doi.org/10.2480/agrmet.463
Siddikee MA, Chauhan PS, Sa T (2012) Regulation of ethylene biosynthesis under salt stress in red pepper (Capsicum annuum L.) by 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase-producing halotolerant bacteria. J Plant Growth Regul 31:265–272. https://doi.org/10.1007/s00344-011-9236-6
Siddiqi KS, Husen A (2017) Plant response to strigolactones: current developments and emerging trends. Appl Soil Ecol 120:247–253. https://doi.org/10.1016/j.apsoil.2017.08.020
Siddiqi KS, Husen A (2019) Plant response to jasmonates: current developments and their role in changing environment. Bull Nat Res Cent 43:153. https://doi.org/10.1186/s42269-019-0195-6
Simonovicova M, Tamas L, Huttova J, Mistrik I (2004) Effect of aluminum on oxidative stress related enzymes activities in barley roots. Biol plant 48:261–266 ttps://doi.org/10.1023/B:BIOP.0000033454.95515.8a
Singh I, Shono M (2005) Physiological and molecular effects of 24-epibrassinolide, a brassinosteroid on thermotolerance of tomato. Plant Growth Regul 47:111–119. https://doi.org/10.1007/s10725-005-3252-0
Singh S, Prasad SM (2017) Effects of 28-homobrassinoloid on key physiological attributes of Solanum lycopersicum seedlings under cadmium stress: photosynthesis and nitrogen metabolism. Plant Growth Regul 82:161–173. https://doi.org/10.1007/s10725-017-0248-5
Sirhindi G, Kumar S, Bhardwaj R, Kumar M (2009) Effects of 24-epibrassinolide and 28-homobrassinolide on the growth and antioxidant enzyme activities in the seedlings of Brassica juncea L. Physiol Mol Biol Plants 15:335–341. https://doi.org/10.1007/s12298-009-0038-2
Soares C, de Sousa A, Pinto A, Azenha M, Teixeira J, Azevedo RA, Fidalgo F (2016) 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. https://doi.org/10.1016/j.envexpbot.2015.09.010
Soares TFSN, Dias DCFDS, Oliveira AMS, Ribeiro DM, Dias LADS (2020) Exogenous brassinosteroids increase lead stress tolerance in seed germination and seedling growth of Brassica juncea L. Ecotoxicol Environ Saf 193:110296. https://doi.org/10.1016/j.ecoenv.2020.110296
Soliman M, Elkelish A, Souad T, Alhaithloul H, Farooq M (2020) Brassinosteroid seed priming with nitrogen supplementation improves salt tolerance in soybean. Physiol Mol Biol Plants 26:501–511. https://doi.org/10.1007/s12298-020-00765-7
Song S, Liu W, Guo S, Shang Q, Zhang Z (2006) Salt resistance and its mechanism of cucumber under effects of exogenous chemical activator. Yingyong Shengtai Xuebao 17:1871–1876
Song YL, Dong YJ, Tian XY, Kong J, Bai XY, Xu LL, He ZL (2016) Role of foliar application of 24-epibrassinolide in response of peanut seedlings to iron deficiency. Biol Plant 60:1–14. https://doi.org/10.1007/s10535-016-0596-4
Sudo E, Itouga M, Yoshida-Hatanaka K, Ono Y, Sakakibara H (2008) Gene expression and sensitivity in response to copper stress in rice leaves. J Exp Bot 59:3465–3474. https://doi.org/10.1093/jxb/ern196
Sun Y, Fan XY, Cao DM, Tang W, He K, Zhu JY, He JX, Bai MY, Zhu S, Oh E, Patil S, Kim TW, Ji H, Wong WH, Rhee SY, Wang ZY (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 19:765–777. https://doi.org/10.1016/j.devcel.2010.10.010
Swamy KN, Rao SSR (2009) Effect of 24-epibrassinolide on growth, photosynthesis, and essential oil content of Pelargonium graveolens (L.) Herit. Russ J Plant Physiol 56:616–620
Tabur S, Demir K (2009) Cytogenetic response of 24-epibrassinolide on the root meristem cells of barley seeds under salinity. Plant Growth Regul 58:119–123
Tadaiesky LBA, da Silva BRS, Batista BL, Lobato AKDS (2021) Brassinosteroids trigger tolerance to iron toxicity in rice. Physiol Plant 171:371–387. https://doi.org/10.1111/ppl.13230
Takeuchi Y, Omigawa Y, Ogasawara M, Yoneyyama K, Konnai M, Worsham AD (1995) Effects of brassinosteroids on conditioning and germination of clover broom rape (Orobanche minor) seeds. Plant Growth Regul 16:153–160. https://doi.org/10.1007/BF00029536
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. https://doi.org/10.1007/s11738-012-1113-9
Tanaka K, Nakamura Y, Asami T, Yoshida S, Matsuo T, Okamoto S (2003) Physiological roles of brassinosteroids in early growth of Arabidopsis: brassinosteroids have a synergistic relationship with gibberellin as well as auxin in light-grown hypocotyl elongation. J Plant Growth Regul 22:259–271. https://doi.org/10.1007/s00344-003-0119-3
Tanaka Y, Nose T, Jikumaru Y, Kamiya Y (2013) ABA inhibits entry into stomatal lineage development in Arabidopsis leaves. Plant J74:448–457. https://doi.org/10.1111/tpj.12136
Upreti KK, Murti GSR (2004) Effects of brassinosteroids on growth, nodulation, phytohormone content and nitrogenase activity in French bean under water stress. Biol Plant 48:407–411. https://doi.org/10.1023/B:BIOP.0000041094.13342.1b
Vardhini BV, Rao SSR (2003) Amelioration of osmotic stress by brassinosteroids on seed germination and seedling growth of three varieties of sorghum. Plant Growth Regul 41:25–31. https://doi.org/10.1023/A:1027303518467
Vardhini BV, Rao SSR (2005) Influence of brassinosteroids on seed germination and seedling growth of sorghum under water stress. Indian J Plant Physiol 10:381–385
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. https://doi.org/10.3389/fenvs.2014.00067
Vert G, Nemhauser JL, Geldner N, Hong F, Chory J (2005) Molecular mechanisms of steroid hormone signaling in plants. Annu Rev Cell Dev Biol 21:177–201. https://doi.org/10.1146/annurev.cellbio.21.090704.151241
Wang ZY, Wang Q, Chong K, Wang F, Wang L, Bai M, Jia C (2006) The brassinosteroid signal transduction pathway. Cell Res 16:427–434. https://doi.org/10.1038/sj.cr.7310054
Wang B, Zhang J, Xia X, Zhang WH (2011) Ameliorative effect of brassinosteroid and ethylene on germination of cucumber seeds in the presence of sodium chloride. Plant Growth Regul 65:407–413. https://doi.org/10.1007/s10725-011-9595-9
Wang ZY, Bai MY, Oh E, Zhu JY (2012) Brassinosteroid signaling network and regulation of photomorphogenesis. Annu Rev Genet 46:701–724. https://doi.org/10.1146/annurev-genet-102209-163450
Wang W, Bai MY, Wang ZY (2014) The brassinosteroid signaling network - a paradigm of signal integration. Curr Opin Plant Biol 21:147–153. https://doi.org/10.1016/j.pbi.2014.07.012
Wang P, Sun X, Wang N, Tan DX, Ma F (2015a) Melatonin enhances the occurrence of autophagy induced by oxidative stress in Arabidopsis seedlings. J Pineal Res 58:479–489. https://doi.org/10.1111/jpi.12233
Wang Y, Cai S, Yin L, Shi K, Xia X, Zhou Y, Yu J, Zhou J (2015b) Tomato HsfA1a plays a critical role in plant drought tolerance by activating ATG genes and inducing autophagy. Autophagy 11:2033–2047. https://doi.org/10.1080/15548627.2015.1098798
Wang YT, Chen ZY, Jiang Y, Duan BB, Xi ZM (2019) Involvement of ABA and antioxidant system in brassinosteroid-induced water stress tolerance of grapevine (Vitis vinifera L.). Sci Hortic 256:108596 doi:https://doi.org/10.1016/j.scienta.2019.108596
Wang RR (2020) Chromosomal distribution of genes conferring tolerance to abiotic stresses versus that of genes controlling resistance to biotic stresses in plants. Int J Mol Sci 21:1820. https://doi.org/10.3390/ijms21051820
Wang SG, Zhao HH, Zhao LM, Gu CM, Na YG, Xie B, Cheng SH, Pan GJ (2020) Application of brassinolide alleviates cold stress at the booting stage of rice. J Integr Agri 19:975–987. https://doi.org/10.1016/S2095-3119(19)62639-0
Xing J, Wang Y, Yao Q, Zhang Y, Zhang M, Li Z (2021) Brassinosteroids modulate nitrogen physiological response and promote nitrogen uptake in maize (Zea mays L.). https://doi.org/10.1016/j.cj.2021.04.004
Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ 25:131–139. https://doi.org/10.1046/j.1365-3040.2002.00782.x
Yang P, Wang Y, Li J, Bian Z (2019) Effects of brassinosteroids on photosynthetic performance and nitrogen metabolism in pepper seedlings under chilling stress. Agronomy 9:839. https://doi.org/10.3390/agronomy9120839
Yokota T, Arima M, Takahashi N (1982) Castasterone, a new phytosterol with plant-hormone potency, from chestnut insect gall. Tetrahedron Lett 23:1275–1278. https://doi.org/10.1016/S0040-4039(00)87081-1
Yoshimoto K (2012) Beginning to understand autophagy, an intracellular self-degradation system in plants. Plant Cell Physiol 53:1355–1365. https://doi.org/10.1093/pcp/pcs099
Yu JQ, Huang LF, Hu WH, Zhou YH, Mao WH, Ye SF, Nogués S (2004) A role for brassinosteroids in the regulation of photosynthesis in Cucumis sativus. J Exp Bot 55:1135–1143. https://doi.org/10.1093/jxb/erh124
Yuan GF, Jia C-G, Li Z, Sun B, Zhang L-P, Liu N, Wang QM (2010) Effect of brassinosteroids on drought resistance and abscisic acid concentration in tomato under water stress. Sci Hortic 126:103–108. https://doi.org/10.1016/j.scienta.2010.06.014
Yurchenko O, Kimberlin A, Mehling M, Koo AJ, Chapman KD, Mullen RT, Dyer JM (2018) Response of high leaf-oil Arabidopsis thaliana plant lines to biotic or abiotic stress. Plant Signal Behav 13:e1464361. https://doi.org/10.1080/15592324.2018.1464361
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. https://doi.org/10.1007/s00244-010-9535-0
Zafari M, Ebadi A, Sedghi M, Jahanbakhsh S, Miransari M (2020) Alleviating effect of 24- epibrassinolide on seed oil content and fatty acid composition under drought stress in safflower. J Food Comp Anal 92:103544. https://doi.org/10.1016/j.jfca.2020.103544
Zapata PJ, Botella MA, Petrel MT, Serrano M (2007) Responses of ethylenebiosynthesis to saline stress in seedlings of eight plant species. Plant Growth Regul 53:97–106. https://doi.org/10.1007/s10725-007-9207-x
Zeng H, Tang Q, Hua X (2010) Arabidopsis brassinosteroid mutants det2-1 andbin2-1 display altered salt tolerance. J Plant Growth Regul 29:44–52. https://doi.org/10.1007/s00344-009-9111-x
Zhai Y, Guo M, Wang H, Lu J, Liu J, Zhang C, Gong Z, Lu M (2016) Autophagy, a conserved mechanism for protein degradation, responds to heat, and other abiotic stresses in Capsicum annuum L. Front Plant Sci 7:131. https://doi.org/10.3389/fpls.2016.00131
Zhang S, Hu J, Zhang Y, Xie XJ, Knapp A (2007) Seed priming with brassinolide improves lucerne (Medicago sativa L.) seed germination and seedling growth in relation to physiological changes under salinity stress. Aust J Agric Res 58:811–815. https://doi.org/10.1071/AR06253
Zhang MC, Zhai ZX, Tian XL, Duan LS, Li ZH (2008) Brassinolide alleviated the adverse effect of water deficits on photosynthesis and the antioxidant of soybean (Glycine max L.). Plant Growth Regul 56:257–264. https://doi.org/10.1007/s10725-008-9305-4
Zhang Y, He J (2010) Sugar-induced plant growth is dependent on brassinosteroids. Plant signal Behav10:e1082700 doi:https://doi.org/10.1080/15592324.2015.1082700
Zhang J, Zhang Y, Khan R, Wu X, Zhou L, Xu N, Du S, Ma X (2021) Exogenous application of brassinosteroids regulates tobacco leaf size and expansion via modulation of endogenous hormones content and gene expression. Physiol Mol Biol Plants 27:847–860. https://doi.org/10.1007/s12298-021-00971-x
Zhao Y, Liang ZY, Yang YJ (2013) Effects of exogenous brassinosteroid on cd tolerance in Solatium nigrum seedlings. Zhongguo Shengtai Nongye Xuebao 21:872–876
Zhou Y, Xia X, Yu G, Wang J, Wu J, Wang M, Yang Y, Shi K, Yu Y, Chen Z, Gan J, Yu J (2015) Brassinosteroids play a critical role in the regulation of pesticide metabolism in crop plants. Sci Rep 5:9018. https://doi.org/10.1038/srep09018
Zhu T, Tan WR, Deng XG, Zheng T, Zhang DW, Lin HH (2015) Effects of brassinosteroids on quality attributes and ethylene synthesis in postharvest tomato fruit. Post Biol Technol 100:196–204. https://doi.org/10.1016/j.postharvbio.2014.09.016
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Siddiqi, K.S., Husen, A. Significance of brassinosteroids and their derivatives in the development and protection of plants under abiotic stress. Biologia 76, 2837–2857 (2021). https://doi.org/10.1007/s11756-021-00853-3
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DOI: https://doi.org/10.1007/s11756-021-00853-3