Exogenously applied brassinosteroids (BRs) improve plant response to drought. However, many important aspects of this process, such as the potential differences caused by different developmental stages of analyzed organs at the beginning of drought, or by BR application before or during drought, remain still unexplored. The same applies for the response of different endogenous BRs belonging to the C27, C28-and C29- structural groups to drought and/or exogenous BRs. This study examines the physiological response of two different leaves (younger and older) of maize plants exposed to drought and treated with 24-epibrassinolide (epiBL), together with the contents of several C27, C28-and C29-BRs. Two timepoints of epiBL application (prior to and during drought) were utilized to ascertain how this could affect plant drought response and the contents of endogenous BRs. Marked differences in the contents of individual BRs between younger and older maize leaves were found: the younger leaves diverted their BR biosynthesis from C28-BRs to C29-BRs, probably at the very early biosynthetic steps, as the levels of C28-BR precursors were very low in these leaves, whereas C29-BR levels vere extremely high. Drought also apparently negatively affected contents of C28-BRs (particularly in the older leaves) and C29-BRs (particularly in the younger leaves) but not C27-BRs. The response of these two types of leaves to the combination of drought exposure and the application of exogenous epiBL differed in some aspects. The older leaves showed accelerated senescence under such conditions reflected in their reduced chlorophyll content and diminished efficiency of the primary photosynthetic processes. In contrast, the younger leaves of well-watered plants showed at first a reduction of proline levels in response to epiBL treatment, whereas in drought-stressed, epiBL pre-treated plants they were subsequently characterized by elevated amounts of proline. The contents of C29- and C27-BRs in plants treated with exogenous epiBL depended on the length of time between this treatment and the BR analysis regardless of plant water supply; they were more pronounced in plants subjected to the later epiBL treatment. The application of epiBL before or during drought did not result in any differences of plant response to this stressor.

Department of Genetics and Microbiology Faculty of Science Charles University Prague Czechia

Laboratory of Growth Regulators Centre of the Region Haná for Biotechnological and Agricultural Research Institute of Experimental Botany Czech Academy of Sciences v v i and Palacký University Olomouc Czechia

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Ábrahám E., Rigó G., Székely G., Nagy R., Koncz C., Szabadosz L. (2003). Light-dependent induction of proline biosynthesis by abscisic acid and salt stress is inhibited by brassinosteroid in Arabidopsis . Plant Mol. Biol. 51, 363–372. doi: 10.1023/a:1022043000516 PubMed DOI

Ahammed G. J., Li X., Liu A., Chen S. (2020). Brassinosteroids in plant tolerance to abiotic stress. J. Plant Growth Regul. 39, 1451–1464. doi: 10.1007/s00344-020-10098-0 DOI

Ahammed G. J., Sharma A., Yu J. (2022). Brassinosteroids in plant developmental biology and stress tolerance (Cambridge: Academic Press; ). doi: 10.1016/C2016-0-04006-8 DOI

Ahmed A. H. H., Darwish E., Alobaidy M. G. (2017). Impact of putrescine and 24-epibrassinolide on growth, yield and chemical constituents of cotton (Gossypium barbadense l.) plant grown under drought stress conditions. Asian J. Plant Sci. 16, 9–23. doi: 10.3923/ajps.2017.9.23 DOI

Anjum S. A., Wang L. C., Farooq M., Hussain M., Xue L. L., Zou C. M. (2011). Brassinolide application improves the drought tolerance in maize through modulation of enzymatic antioxidants and leaf gas exchange. J. Agron. Crop Sci. 197, 177–185. doi: 10.1111/j.1439-037X.2010.00459.x DOI

Bajguz A., Chmur M., Gruszka D. (2020). Comprehensive overview of the brassinosteroid biosynthesis pathways: substrates, products, inhibitors, and connections. Front. Plant Sci. 11. doi: 10.3389/fpls.2020.01034 PubMed DOI PMC

Bajguz A., Orczyk W., Gołębiewska A., Chmur M., Piotrowska-Niczyporuk A. (2019). Occurrence of brassinosteroids and influence of 24-epibrassinolide with brassinazole on their content in the leaves and roots of Hordeum vulgare l. cv. golden promise. Planta. 249, 123–137. doi: 10.1007/s00425-018-03081-3 PubMed DOI

Bancos S., Nomura T., Sato T., Molnar G., Bishop G. J., Koncz C., et al. . (2002). Regulation of transcript levels of the Arabidopsis cytochrome P450 genes involved in brassinosteroid biosynthesis. Plant Physiol. 130, 504–513. doi: 10.1104/pp.005439 PubMed DOI PMC

Bariş Ç.Ç., Sağlam-Çağ S. (2016). The effects of brassinosteroids on sequential leaf senescence occurring in Glycine max l. Int. J. Biotechnol. Res. 6, 7–16.

Basit F., Liu J., An J., Chen. M., He C., Zhu X., et al. . (2021). Brassinosteroids as a multidimensional regulator of plant physiological and molecular responses under various environmental stresses. Environ. Sci. pollut. Res. Int. 28, 44768–44779. doi: 10.1007/s11356-021-15087-8 PubMed DOI

Bates L. S., Waldren R. P., Teare I. D. (1973). Rapid determination of free proline for water-stress studies. Plant Soil. 39, 205–207. doi: 10.1007/BF00018060 DOI

Behnamnia M., Kalantari K., Ziaie J. (2009). The effects of brassinosteroid on the induction of biochemical changes in Lycopersicon esculentum under drought stress. Turk. J. Bot. 33, 417–428. doi: 10.3906/bot-0806-12 DOI

Benešová M., Holá D., Fischer L., Jedelský P. L., Hnilička F., Wilhelmová N., et al. . (2012). The physiology and proteomics of drought tolerance in maize: early stomatal closure as a cause of lower tolerance to short-term dehydration? PloS One 7, e38017. doi: 10.1371/journal.pone.0038017 PubMed DOI PMC

Budič M., Cigić B., Šoštarič M., Sabotič J., Meglič V., Kos J., et al. . (2016). The response of aminopeptidases of Phaseolus vulgaris to drought depends on the developmental stage of the leaves. Plant Physiol. Biochem. 109, 326–336. doi: 10.1016/j.plaphy.2016.10.007 PubMed DOI

Čatský J. (1960). Determination of water deficit in disks cut out from leaf blades. Biol. Plant 2, 76–78.

Cechin I., Rossi S. C., Oliveira V. C., Fumis T. F. (2006). Photosynthetic tresponses and proline content of mature and young sunflower leaves under water deficit. Photosynthetica. 44, 144–461. doi: 10.1007/s11099-005-0171-2 DOI

Chandrasekaran P., Sivakumar R., Nandhitha G., Vishnuveni M., Boominathan P., Senthilkumar M. (2017). Impact of PPFM and PGRs on seed germination, stress tolerant index and catalase activity in tomato (Solanum lycopersicum l) under drought. Int. J. Curr. Microbiol. App. Sci. 6, 540–549. doi: 10.20546/ijcmas.2017.606.064 DOI

Chen Y., Chen Y., Shi Z., Jin Y., Sun H., Xie F., et al. . (2019). Biosynthesis and signal transduction of ABA, JA, and BRs in response to drought stress of Kentucky bluegrass. Int. J. Mol. Sci. 20, 1289. doi: 10.3390/ijms20061289 PubMed DOI PMC

Chen Y., Chen H., Xiang J., Zhang Y., Wang Z., Zhu D., et al. . (2021). Rice spikelet formation inhibition caused by decreased sugar utilization under high temperature is associated with brassinolide decomposition. Environ. Exp. Bot. 190, 104585. doi: 10.1016/j.envexpbot.2021.104585 DOI

Chmur M., Bajguz A. (2021). Brassinolide enhances the level of brassinosteroids, protein, pigments, and monosaccharides in Wolffia arrhiza treated with brassinazole. Plants. 10, 1311. doi: 10.3390/plants10071311 PubMed DOI PMC

Ding J., Wu J. H., Liu J. F., Yuan B. F., Feng Y. Q. (2014). Improved methodology for assaying brassinosteroids in plant tissues using magnetic hydrophilic material for both extraction and derivatization. Plant Methods 10, 39. doi: 10.1186/1746-4811-10-39 PubMed DOI PMC

Duan F., Ding J., Lee D., Lu X., Feng Y., Song W. (2017). Overexpression of SoCYP85A1, a spinach cytochrome p450 gene in transgenic tobacco enhances root development and drought stress tolerance. Front. Plant Sci. 8. doi: 10.3389/fpls.2017.01909 PubMed DOI PMC

Efimova M. V., Savchuk A. L., Hasan J. A. K., Litvinovskaya R. P., Khripach V. A., Kholodova V. P., et al. . (2014). Physiological mechanisms of enhancing salt tolerance of oilseed rape plants with brassinosteroids. Russ. J. Plant Physiol. 61, 733–743. doi: 10.1134/S1021443714060053 DOI

Farooq M., Wahid A., Basra S. M. A., Din I. U. (2009). Improving water relations and gas exchange with brassinosteroids in rice under drought stress. J. Agron. Crop Sci. 195, 262–269. doi: 10.1111/j.1439-037X.2009.00368.x DOI

Fedina E., Yarin A., Mukhitova F., Blufard A., Chechetkin I. (2017). Brassinosteroid-induced changes of lipid composition in leaves of Pisum sativum l. during senescence. Steroids. 117, 25–28. doi: 10.1016/j.steroids.2016.10.009 PubMed DOI

Filek M., Sieprawska A., Kościelniak J., Oklestkova J., Jurczyk B., Telk A., et al. . (2019). The role of chloroplasts in the oxidative stress that is induced by zearalenone in wheat plants–the functions of 24-epibrassinolide and selenium in the protective mechanisms. Plant Physiol. Biochem. 137, 84–92. doi: 10.1016/j.plaphy.2019.01.030 PubMed DOI

Fu J., Sun P., Luo Y., Zhou H., Gao J., Zhao D., et al. . (2019). Brassinosteroids enhance cold tolerance in Elymus nutans via mediating redox homeostasis and proline biosynthesis. Environ. Exp. Bot. 167, 103831. doi: 10.1016/j.envexpbot.2019.103831 DOI

Ghosh U. K., Islam M. N., Siddiqui M. N., Cao X., Khan M. A. R. (2022). Proline, a multifaceted signalling molecule in plant responses to abiotic stress: understanding the physiological mechanisms. Plant Biol. 24, 227–239. doi: 10.1111/plb.13363 PubMed DOI

Gilgen A. K., Feller U. (2014). Effects of drought and subsequent rewatering on Rumex obtusifolius leaves of different ages: reversible and irreversible damages. J. Plant Interact. 9, 75–81. doi: 10.1080/17429145.2013.765043 DOI

Gomes M. M. A., Pinheiro D. T., Bressan-Smith R., Campostrini E. (2018). Exogenous brassinosteroid application delays senescence and promotes hyponasty in Carica papaya l. leaves. Theor. Exp. Plant Physiol. 30, 193–201. doi: 10.1007/s40626-018-0114-5 DOI

Gomes M. M. A., Torres Netto A., Campostrini E., Bressan-Smith R., Zullo M. A. T., Ferraz T. M., et al. . (2013). Brassinosteroid analogue affects the senescence in two papaya genotypes submitted to drought stress. Theor. Exp. Plant Physiol. 25, 186–195.

Gruszka D., Janeczko A., Dziurka M., Pociecha E., Oklešťková J., Szarejko I. (2016). Barley brassinosteroid mutants provide an insight into phytohormonal homeostasis in plant reaction to drought stress. Front. Plant Sci. 7. doi: 10.3389/fpls.2016.01824 PubMed DOI PMC

Gursude A., Mandavia C. K., Mandavia M. K., Raval L., Bangar S. (2014). Influence of brassinosteroids and gibberellic acid on biochemical parameters of chickpea (Cicer arietinum l.) under water stress. Ind. J. Agric. Biochem. 27, 227–230.

Hashemi N. B., Sadeghipour O., Asl A. R. (2015). The study effect of brassinosteroid application on yield and yield components of cowpea (Vigna unguiculata) under water stress conditions. Int. J. Biol. Pharm. Allied Sci. 4, 593–605.

Hemmati K., Ebadi A., Khomari S., Sedghi M. (2018). Influence of ascorbic acid and 24-epibrassinolide on physiological characteristics of pot marigold under water-stress condition. J. Plant Interact. 13, 364–372. doi: 10.1080/17429145.2018.1483033 DOI

Hodges D. M., DeLong J. M., Forney C. F., Prange R. K. (1999). Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta. 207, 604–611. doi: 10.1007/s004250050524 PubMed DOI

Holá D. (2019). “Role of brassinosteroids in the plant response to drought: do we know anything for certain?,” in Brassinosteroids: plant growth and development. Eds. Hayat S., Yusuf M., Bhardwaj R., Bajguz A. (Singapore: Springer; ), 101–168. doi: 10.1007/978-981-13-6058-9_5 DOI

Holá D. (2022). “Brassinosteroids and primary photosynthetic processes,” in Brassinosteroids in plant developmental biology and stress tolerance. Eds. Ahammed G. J., Sharma A., Yu J. (Cambridge: Academic Press; ), 59–104. doi: 10.1016/B978-0-12-813227-2.00015-1 DOI

Jager C. E., Symons G. M., Ross J. J., Reid J. B. (2008). Do brassinosteroids mediate the water stress response? Physiol. Plant 133, 417–425. doi: 10.1111/j.1399-3054.2008.01057.x PubMed DOI

Jan S., Abbas N., Ashraf M., Ahmad P. (2019). Roles of potential plant hormones and transcription factors in controlling leaf senescence and drought tolerance. Protoplasma. 256, 313–329. doi: 10.1007/s00709-018-1310-5 PubMed DOI

Janeczko A., Biesaga-Kościelniak J., Oklešt'ková J., Filek M., Dziurka M., Szarek-Łukaszewska G., et al. . (2010). Role of 24-epibrassinolide in wheat production: physiological effects and uptake. J. Agron. Crop Sci. 196 (4), 311–321. doi: 10.1111/j.1439-037X.2009.00413.x DOI

Janeczko A., Biesaga-Koscielniak J., Dziurka M., Oklešťková J., Kocurek M., Szarek-Lukaszewska G., et al. . (2011). Response of polish cultivars of soybean (Glycine max (L.) merr.) to brassinosteroid application;. Acta Sci. Pol. Agric. 10, 33–50.

Janeczko A., Swaczynová J. (2010). Endogenous brassinosteroids in wheat treated with 24-epibrassinolide. Biol. Plant 54, 477–482. doi: 10.1007/s10535-010-0084-1 DOI

Jiang Y., Bao L., Jeong S. Y., Kim S. K., Xu C., Li X., et al. . (2012). XIAO is involved in the control of organ size by contributing to the regulation of signaling and homeostasis of brassinosteroids and cell cycling in rice. Plant J. 70, 398–408. doi: 10.1111/j.1365-313X.2011.04877.x PubMed DOI

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. Biochem. 143, 119–128. doi: 10.1016/j.plaphy.2019.08.024 PubMed DOI

Khamsuk O., Sonjaroon W., Suwanwong S., Jutamanee K., Suksamrarn A. (2018). Effects of 24-epibrassinolide and the synthetic brassinosteroid mimic on chili pepper under drought. Acta Physiol. Plant 40, 106. doi: 10.1007/s11738-018-2682-z DOI

Kim H. B., Kwon M., Ryu H., Fujioka S., Takatsuto S., Yoshida S., et al. . (2006). The regulation of DWARF4 expression is likely a critical mechanism in maintaining the homeostasis of bioactive brassinosteroids in Arabidopsis . Plant Physiol. 140, 548–557. doi: 10.1104/pp.105.067918 PubMed DOI PMC

Kim Y., Park S. U., Pham G., Jeong Y. S., Kim S. H. (2019). ATBS1-INTERACTING FACTOR 2 negatively regulates dark-and brassinosteroid-induced leaf senescence through interactions with INDUCER OF CBF EXPRESSION 1. J. Exp. Bot. 71, 1475–1490. doi: 10.1093/jxb/erz533 PubMed DOI PMC

Kolbe A., Schneider B., Porzel A., Schmidt J., Adam G. (1995). Acyl-conjugated metabolites of brassinosteroids in cell suspension cultures of Ornithopus sativus . Phytochemistry. 38, 633–636. doi: 10.1016/0031-9422(94)00742-C DOI

Li K. R., Feng C. H. (2011). Effects of brassinolide on drought resistance of Xanthoceras sorbifolia seedlings under water stress. Acta Physiol. Plant 33, 1293–1300. doi: 10.1007/s11738-010-0661-0 DOI

Li Y. H., Liu Y. J., Xu X. L., Jin M., An L. Z., Zhang H. (2012). Effect of 24-epibrassinolide on drought stress-induced changes in Chorispora bungeana . Biol. Plant 56, 192–196. doi: 10.1007/s10535-012-0041-2 DOI

Li S., Zheng H., Lin L., Wang F., Sui N. (2021). Roles of brassinosteroids in plant growth and abiotic stress response. Plant Growth Regul. 93, 29–38. doi: 10.1007/s10725-020-00672-7 DOI

Liu C., Feng B., Zhou Y., Liu C., Gong X. (2022). Exogenous brassinosteroids increases tolerance to shading by altering stress responses in mung bean (Vigna radiata l.). Photosynth. Res. 151, 279–294. doi: 10.1007/s11120-021-00887-3 PubMed DOI

Lu H., Wang Z., Xu C., Li L., Yang C. (2021). Multiomics analysis provides insights into alkali stress tolerance of sunflower (Helianthus annuus l.). Plant Physiol. Biochem. 166, 66–77. doi: 10.1016/j.plaphy.2021.05.032 PubMed DOI

Luo X. T., Cai B. D., Yu L., Ding J., Feng Y. Q. (2018). Sensitive determination of brassinosteroids by solid phase boronate affinity labeling coupled with liquid chromatography-tandem mass spectrometry. J. Chromatogr. A. 1546, 10–17. doi: 10.1016/j.chroma.2018.02.058 PubMed DOI

Lv J., Zong X. F., Shakeel Ahmad A., Wu X., Wu C., Li Y. P., et al. . (2020). Alteration in morpho-physiological attributes of Leymus chinensis (Trin.) tzvelev by exogenous application of brassinolide under varying levels of drought stress. Chil. J. Agric. Res. 80, 61–71. doi: 10.4067/S0718-58392020000100061 DOI

Malaga S., Janeczko A., Janowiak F., Waligórski P., Oklestkova J., Dubas E., et al. . (2020). Involvement of homocastasterone, salicylic and abscisic acids in the regulation of drought and freezing tolerance in doubled haploid lines of winter barley. Plant Growth Regul. 90, 173–188. doi: 10.1007/s10725-019-00544-9 DOI

Mao J., Zhang D., Li K., Liu Z., Liu X., Song C., et al. . (2017). Effect of exogenous brassinolide (BR) application on the morphology, hormone status, and gene expression of developing lateral roots in Malus hupehensis . Plant Growth Regul. 82, 391–401. doi: 10.1007/s10725-017-0264-5 DOI

Mostajeran A., Rahimi-Eichi V. (2009). Effects of drought stress on growth and yield of rice (Oryza sativa l.) cultivars and accumulation of proline and soluble sugars in sheath and blades of their different ages leaves. Agric. Environ. Sci. 5, 264–272.

Nakamura A., Fujioka S., Sunohara H., Kamiya N., Hong Z., Inukai Y., et al. . (2006). The role of OsBRI1 and its homologous genes, OsBRL1 and OsBRL3, in rice. Plant Physiol. 140, 580–590. doi: 10.1104/pp.105.072330 PubMed DOI PMC

Nie S., Huang S., Wang S., Mao Y., Liu J., Ma R., et al. . (2019). Enhanced brassinosteroid signaling intensity via SlBRI1 overexpression negatively regulates drought resistance in a manner opposite of that via exogenous BR application in tomato. Plant Physiol. Biochem. 138, 36–47. doi: 10.1016/j.plaphy.2019.02.014 PubMed DOI

Nishikawa N., Shida A., Toyama S. (1995). Metabolism of 14C-labeled epibrassinolide in intact seedlings of cucumber and wheat. J. Plant Res. 108, 65–69. doi: 10.1007/BF02344307 DOI

Parada F., Oklestkova J., Arce-Johnson P. (2022). Characterization of endogenous levels of brassinosteroids and related genes in grapevines. Int. J. Mol. Sci. 23, 1827. doi: 10.3390/ijms23031827 PubMed DOI PMC

Pavlović I., Mlinarić S., Tarkowská D., Oklestkova J., Novák O., Lepeduš H., et al. . (2019). Early brassica crops responses to salinity stress: a comparative analysis between Chinese cabbage, white cabbage, and kale. Front. Plant Sci. 10. doi: 10.3389/fpls.2019.00450 PubMed DOI PMC

Pavlović I., Petřík I., Tarkowská D., Lepeduš H., Vujčić Bok V., Radić Brkanac S., et al. . (2018). Correlations between phytohormones and drought tolerance in selected brassica crops: Chinese cabbage, white cabbage and kale. Int. J. Mol. Sci. 19, 2866. doi: 10.3390/ijms19102866 PubMed DOI PMC

Ramirez V. E., Poppenberger B. (2020). Modes of brassinosteroid activity in cold stress tolerance. Front. Plant Sci. 11. doi: 10.3389/fpls.2020.583666 PubMed DOI PMC

Rehman A., Shahzad B., Haider F. U., Ullah A., Khan I. (2022). “Brassinosteroids in plant response to high temperature stress,” in Brassinosteroids in plant developmental biology and stress tolerance. Eds. Ahammed G. J., Sharma A., Yu J. (Cambridge: Academic Press; ), 173–187. doi: 10.1016/B978-0-12-813227-2.00014-X DOI

Rittenberg D., Foster G. L. (1940). A new procedure for quantitative analysis by isotope dilution, with application to the determination of amino acids and fatty acids. J. Biol. Chem. 133, 737–744.

Sağlam-Çağ S. (2007). The effect of epibrassinolide on senescence in wheat leaves. Biotechnol. Biotechnol. Equip. 21, 63–65. doi: 10.1080/13102818.2007.10817415 DOI

Schneider B., Kolbe A., Porzel A., Adam G. (1994). A metabolite of 24-epi-brassinolide in cell suspension cultures of Lycopersicon esculentum . Phytochemistry. 36, 319–321. doi: 10.1016/S0031-9422(00)97068-7 DOI

Setsungnern A., Treesubsuntorn C., Thiravetyan P. (2019). Exogenous 24-epibrassinolide enhanced benzene detoxification in Chlorophytum comosum via overexpression and conjugation by glutathione. Sci. Total. Environ. 662, 805–815. doi: 10.1016/j.scitotenv.2019.01.258 PubMed DOI

Shahana T., Rao P. A., Ram S. S., Sujatha E. (2015). Mitigation of drought stress by 24-epibrassinolide and 28-homobrassinolide in pigeon pea seedlings. Int. J. Mult. Curr. Res. 3, 905–911.

Shimada Y., Goda H., Nakamura A., Takatsuto S., Fujioka S., Yoshida S. (2003). Organ-specific expression of brassinosteroid biosynthetic genes and distribution of endogenous brassinosteroids in Arabidopsis . Plant Physiol. 131, 287–297. doi: 10.1104/pp.013029 PubMed DOI PMC

Sidhu G. P. S., Bali A. S. (2022). “Plant responses to drought stress: role of brassinosteroids,” in Brassinosteroids in plant developmental biology and stress tolerance. Eds. Ahammed G. J., Sharma A., Yu J. (Cambridge: Academic Press; ), 201–216. doi: 10.1016/B978-0-12-813227-2.00012-6 DOI

Sivakumar R., Nandhitha G. K., Chandrasekaran P., Boominathan P., Senthilkumar M. (2017). Impact of pink pigmented facultative methylotroph and PGRs on water status, photosynthesis, proline and NR activity in tomato under drought. Int. J. Curr. Microbiol. App. Sci. 6, 1640–1651. doi: 10.20546/ijcmas.2017.606.192 DOI

Sperdouli I., Moustakas M. (2015). Differential blockage of photosynthetic electron flow in young and mature leaves of Arabidopsis thaliana by exogenous proline. Photosynthetica. 53, 471–477. doi: 10.1007/s11099-015-0116-3 DOI

Stirbet A., Govindjee (2011). On the relation between the kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient. J. Photochem. Photobiol. B. Biol. 104, 236–257. doi: 10.1016/j.jphotobiol.2010.12.010 PubMed DOI

Strasser R. J., Srivastava A., Tsimilli-Michael M. (2000). “The fluorescence transient as a tool to characterize and screen photosynthetic samples,” in Probing photosynthesis: mechanism, regulation and adaptation. Eds. Yunus M., Pathre U., Mohanty P. (London: Taylor and Francis; ), 445–483.

Sullivan C. Y. (1972). “Mechanisms of heat and drought resistance in grain sorghum and methods of measurement,” in Sorghum in seventies. Eds. Ganga N., Rao P., House L. R. (New Delhi: Oxford & IBH Pub. Co; ), 247–264.

Symons G. M., Reid J. B. (2004). Brassinosteroids do not undergo long-distance transport in pea. implications for the regulation of endogenous brassinosteroid levels. Plant Physiol. 135, 2196–2206. doi: 10.1104/pp.104.043034 PubMed DOI PMC

Symons G. M., Ross J. J., Jager C. E., Reid J. B. (2008). Brassinosteroid transport. J. Exp. Bot. 59, 17–24. doi: 10.1093/jxb/erm098 PubMed DOI

Talaat N. B., Shawky B. T., Ibrahim A. S. (2015). Alleviation of drought-induced oxidative stress in maize (Zea mays l.) plants by dual application of 24-epibrassinolide and spermine. Environ. Exp. Bot. 113, 47–58. doi: 10.1016/j.envexpbot.2015.01.006 DOI

Tang S., Li L., Wang Y., Chen Q., Zhang W., Jia G., et al. . (2017). Genotype-specific physiological and transcriptomic responses to drought stress in Setaria italica (an emerging model for Panicoideae grasses). Sci. Rep. 7, 10009. doi: 10.1038/s41598-017-08854-6 PubMed DOI PMC

Tarkowská D., Krampolová E., Strnad M. (2020). Plant triterpenoid crosstalk: the interaction of brassinosteroids and phytoecdysteroids in Lepidium sativum . Plants. 9, 1325. doi: 10.3390/plants9101325 PubMed DOI PMC

Tarkowská D., Novák O., Oklestkova J., Strnad M. (2016). The determination of 22 natural brassinosteroids in a minute sample of plant tissue by UHPLC–ESI–MS/MS. Anal. Bioanal. Chem. 408, 6799–6812. doi: 10.1007/s00216-016-9807-2 PubMed DOI

Tůmová L., Tarkowská D., Řehořová K., Marková H., Kočová M., Rothová O., et al. . (2018). Drought-tolerant and drought-sensitive genotypes of maize (Zea mays l.) differ in contents of endogenous brassinosteroids and their drought-induced changes. PloS One 13, e0197870. doi: 10.1371/journal.pone.0197870 PubMed DOI PMC

Wang Z., Zheng P., Meng J., Xi Z. (2015). Effect of exogenous 24-epibrassinolide on chlorophyll fluorescence, leaf surface morphology and cellular ultrastructure of grape seedlings (Vitis vinifera l.) under water stress. Acta Physiol. Plant 37, 1729. doi: 10.1007/s11738-014-1729-z DOI

Wei Z., Li J. (2020). Regulation of brassinosteroid homeostasis in higher plants. Front. Plant Sci. 11. doi: 10.3389/fpls.2020.583622 PubMed DOI PMC

Wellburn A. R. (1994). The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol. 144, 307–313. doi: 10.1016/S0176-1617(11)81192-2 DOI

Xue X., Liu A., Hua X. (2008). Proline accumulation and transcriptional regulation of proline biothesynthesis and degradation in Brassica napus . BMB Rep. 42, 28–34. doi: 10.5483/bmbrep.2009.42.1.028 PubMed DOI

Yokota T., Sato T., Takeuchi Y., Nomura T., Uno K., Watanabe T., et al. . (2001). Roots and shoots of tomato produce 6-deoxo-28-norcathasterone, 6-deoxo-28-nortyphasterol and 6-deoxo-28-norcastasterone, possible precursors of 28-norcastasterone. Phytochemistry. 58, 233–238. doi: 10.1016/S0031-9422(01)00237-0 PubMed DOI

Younesian A., Norouzi H. A., Gholipoor M., Soltani A. (2017). Consequences of ultrasonic waves radiation and 24-epi-brassinolid foliar application for reduction of water deficit stress on qualitative properties of red beans (Akhtar). J. Res. Ecol. 5, 686–699.

Yuan G. F., Jia C. G., Li Z., Sun B., Zhang L. P., Liu N., et al. . (2010). Effect of brassinosteroids on drought resistance and abscisic acid concentration in tomato under water stress. Sci. Hortic. 126, 103–108. doi: 10.1016/j.scienta.2010.06.014 DOI

Yusuf M. A., Kumar D., Rajwanshi R. J., Strasser R., Tsimilli-Michael M., Govindjee K. (2010). Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a fluorescence measurements. Biochem. Biophys. Acta 177, 1428–1438. doi: 10.1016/j.bbabio.2010.02.002 PubMed DOI

Zhang W., Huang H., Zhou Y., Zhu K., Wu Y., Xu Y., et al. . (2022. b). Brassinosteroids mediate moderate soil-drying to alleviate spikelet degeneration under high temperature during meiosis of rice. Plant Cell Environ. 4, 1340–1362. doi: 10.1111/pce.14436 PubMed DOI

Zhang W., Sheng J., Fu L., Xu Y., Xiong F., Wu Y., et al. . (2020). Brassinosteroids mediate the effect of soil-drying during meiosis on spikelet degeneration in rice. Environ. Exp. Bot. 169, 103887. doi: 10.1016/j.envexpbot.2019.103887 DOI

Zhang H., Yang D., Wang P., Zhang X., Ding Z., Zhao L. (2022. a). Feedback inhibition might dominate the accumulation pattern of BR in the new shoots of tea plants (Camellia sinensis). Front. Genet. 12. doi: 10.3389/fgene.2021.809608 PubMed DOI PMC

Zhang M., Zhai Z., Tian X., Duan L., Li Z. (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. doi: 10.1007/s10725-008-9305-4 DOI

Zhang J., Zhang Y., Khan R., Wu X., Zhou L., Xu N., et al. . (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, 847–760. doi: 10.1007/s12298-021-00971-x PubMed DOI PMC

Zhu J., Lu P., Jiang Y., Wang M., Zhang L. (2014). Effects of brassinosteroid on antioxidant system in Salvia miltiorrhiza under drought stress. J. Res. Agric. Anim. Sci. 2, 1–6.

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