Advertisement

Journal of Plant Growth Regulation

, Volume 37, Issue 4, pp 1007–1024 | Cite as

Brassinosteroids Regulate Growth in Plants Under Stressful Environments and Crosstalk with Other Potential Phytohormones

  • Mohammad Abass Ahanger
  • Muhammad Ashraf
  • Andrzej Bajguz
  • Parvaiz Ahmad
Article

Abstract

Brassinosteroids (BRs) are an important group of plant steroidal hormones that are actively involved in a myriad of key growth and developmental processes from germination to senescence. Moreover, BRs are known for their effective role in alleviation of stress-induced changes in normal metabolism via the activation of different tolerance mechanisms. Efforts to improve plant growth through exogenous application of BRs (through different modes such as foliar spray, presowing seed treatment, or through root growing medium) have gained considerable ground world over. It has been widely demonstrated that the exogenous application of BRs to stressed plants imparts the stress tolerance mechanisms. In BR-induced regulation of physio-biochemical processes in plants, interaction (crosstalk) of BRs with other phytohormones has been reported. This crosstalk may fine-tune the effective roles of other hormones in regulating stress tolerance. The multifaceted role of BRs consolidated so far has reflected their immense potential to help plants in counteracting the stress-induced changes. The effects of introgression and up- and down-regulation of BR-related genes reported so far to improve crop productivity have been presented here. Strong evidence exists that BRs are involved in signal transduction particularly in the regulation of the mitogen-activated protein kinase (MAPK) cascade, which in turn is involved in controlled development, cell death, and the perception of pathogen-associated molecular pattern (PAMP) signaling. How far BRs are involved in signal transduction pathways operative under stressful environments has also been comprehensively discussed in this review.

Keywords

Brassinosteroids Abiotic stress tolerance Signaling Crosstalk 

Notes

Compliance with Ethical Standards

Conflict of interest

The authors declare that no conflict exists among the authors.

References

  1. Aghdam MS, Mohammadkhani N (2014) Enhancement of chilling stress tolerance of tomato fruit by postharvest brassinolide treatment. Food Bioproc Technol 7:909–914Google Scholar
  2. Aghdam MS, Asghari M, Farmani B, Mohayeji M, Moradbeygi H (2012) Impact of postharvest brassinosteroids treatment on PAL activity in tomato fruit in response to chilling stress. Sci Hort 144:116–120Google Scholar
  3. Ahanger MA, Agarwal RM (2017a) Potassium improves antioxidant metabolism and alleviates growth inhibition under water and osmotic stress in wheat (Triticum aestivum L.). Protoplasma 254:1471–1486PubMedGoogle Scholar
  4. Ahanger MA, Agarwal RM (2017b) Salinity stress induced alterations in antioxidant metabolism and nitrogen assimilation in wheat (Triticum aestivum L.) as influenced by potassium supplementation. Plant Physiol Biochem 115:449–460PubMedGoogle Scholar
  5. Ahanger MA, Tyagi SR, Wani MR, Ahmad P (2014) Drought tolerance: roles of organic osmolytes, growth regulators and mineral nutrients. In: Ahmad P, Wani MR (eds) Physiological mechanisms and adaptation strategies in plants under changing environment Volume Ist. Springer, New York, pp 25–56Google Scholar
  6. Ahanger MA, Agarwal RM, Tomar NS, Shrivastava M (2015) Potassium induces positive changes in nitrogen metabolism and antioxidant system of oat (Avena sativa L. cultivar Kent). J Plant Int 10:211–223Google Scholar
  7. Ahanger MA, Moad-Talab N, Abd-Allah EF, Ahmad P, Hajiboland R (2016) Plant growth under drought stress: Significance of mineral nutrients. In Ahmad P. (eds) Water stress and Crop Plants: A sustainable approach Wiley Blackwell, New York 649–668Google Scholar
  8. Ahanger MA, Akram NA, Ashraf M, Alyemni MN, Wijaya L, Ahmad P (2017a) Plant responses to environmental stresses – from gene to biotechnology. Annals Bot (AoB) Plants.  https://doi.org/10.1093/aobpla/plx025 CrossRefGoogle Scholar
  9. Ahanger MA, Tomar NS, Tittal M, Argal S, Agarwal RM (2017b) Plant growth under water/salt stress: ROS production; antioxidants and significance of added potassium under such conditions. Physiol Mol Biol Plants 23:731–744PubMedPubMedCentralGoogle Scholar
  10. Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of Enzymatic and non-enzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 30(3):161–175PubMedGoogle Scholar
  11. Ahmad P, Nabi G, Ashraf M (2011) Cadmium-induced oxidative damage in mustard [Brassica juncea (L.) Czern. & Coss.] plants can be alleviated by salicylic acid. S Afr J Bot 77:36–44Google Scholar
  12. Ahmad P, Sarwat M, Bhat NA, Wani MR, Kazi AG, Tran LSP (2015) Alleviation of cadmium toxicity in Brassica juncea L. (Czern. & Coss.) by calcium application involves various physiological and biochemical strategies. PLoS ONE 10(1):e0114571PubMedPubMedCentralGoogle Scholar
  13. Ahmad P, Latef AA, Abd_Allah EF, Hashem A, Sarwat M, Anjum NA, Gucel S (2016a) Calcium and potassium supplementation enhanced growth, osmolytes, secondary metabolite production, and enzymatic antioxidant machinery in cadmium-exposed chickpea (Cicer arietinum L.). Front Plant Sci 7:513PubMedPubMedCentralGoogle Scholar
  14. Ahmad P, Latef AA, Hashem A, Abd_Allah EF, Gucel S, Tran LSP (2016b) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7:347PubMedPubMedCentralGoogle Scholar
  15. Ahmad P, Ahanger MA, Alyemeni MN, Wijaya L, Egamberdieva D, Bhardwaj R, Ashraf M (2017a) Zinc application mitigates the adverse effects of NaCl stress on mustard [Brassica juncea (L.) Czern & Coss] through modulating compatible organic solutes, antioxidant enzymes, and flavonoid content. J Plant Inter 12:429–437Google Scholar
  16. Ahmad P, Ahanger MA, Egamberdieva D, Alam P, Alyemeni MN, Ashraf M (2017b) Modification of osmolytes and antioxidant enzymes by 24-epibrassinolide in chickpea seedlings under mercury (hg) toxicity. J Plant Growth Regul 37:309–322Google Scholar
  17. Ahmad P, Ahanger MA, Alam P, Alyemeni MN, Wijaya L, Ali S, Ashraf M (2018a) Silicon (Si) supplementation alleviates NaCl toxicity in mung bean [Vigna radiata (L.) Wilczek] through the modifications of physio-biochemical attributes and key antioxidant enzymes. J Plant Growth Regul.  https://doi.org/10.1007/s00344-018-9810-2 CrossRefGoogle Scholar
  18. Ahmad P, Ahanger MA, Alam P, Alyemeni MN (2018b) Modification of osmolytes and antioxidant enzymes by 24-epibrassinolide in chickpea seedlings under mercury (Hg) toxicity. J Plant Growth Regul 37:309–322Google Scholar
  19. Ali B, Hayat S, Ahmad A (2007) 28-Homobrassinolide ameliorates the saline stress in chickpea (Cicer arietinumL.). Environ Exp Bot 59:217–223Google Scholar
  20. Ali B, Hasan SA, Hayat S, Hayat Q, Yadav S, Fariduddin Q, Ahmad A (2008a) A role for brassinosteroids in the amelioration of aluminium stress through antioxidant system in mung bean (Vigna radiata L. Wilczek). Environ Exp Bot 62:153–159Google Scholar
  21. Ali B, Hayat S, Fariduddin Q, Ahmad A (2008b) 24-Epibrassinolide protects against the stress generated by salinity and nickel in. Brassica juncea Chemosphere 72:1387–1392PubMedGoogle Scholar
  22. Anjum SA, Wang LC, Farooq M, Hussain M, Xue LL, Zou CM (2011) Brassinolide application improves the drought tolerance in maize through modulation of enzymatic antioxidants and leaf gas exchange. J Agron Crop Sci 197:177–185Google Scholar
  23. 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 40:29–32Google Scholar
  24. Anuradha S, Rao SSR (2007) The effect of brassinosteroids on radish (Raphanus sativus L.) seedlings growing under cadmium stress. Plant Soil Environ 53:465–472Google Scholar
  25. Arora P, Bhardwaj R, Kanwar MK (2010a) 24-epibrassinolide regulated diminution of Cr metal toxicity in Brassica juncea L. plants. Braz J Plant Physiol 22:159–165Google Scholar
  26. Arora P, Bhardwaj R, Kanwar MK (2010b) 24-epibrassinolide induced antioxidative defense system of Brassica juncea L. under Zn metal stress. Physiol Mol Biol Plants 16:285–293PubMedPubMedCentralGoogle Scholar
  27. Asgher M, Khan NA, Khan MIR, Fatma M, Masood A (2014) Ethylene production is associated with alleviation of cadmium-induced oxidative stress by sulfur in mustard types differing in ethylene sensitivity. Ecotoxicol Environ Saf 106:54–61PubMedGoogle Scholar
  28. Bajguz A (2002) Brassinosteroids and lead as stimulators of phytochelatins synthesis in Chlorella vulgaris. J Plant Physiol 159:321–324Google Scholar
  29. Bajguz A, Hayat S (2009) Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem 47:1–8PubMedGoogle Scholar
  30. Bajguz A, Piotrowska-Niczyporuk A (2013) Synergistic effect of auxins and brassinosteroids on the growth and regulation of metabolite content in the green alga Chlorella vulgaris (Trebouxiophyceae). Plant Physiol Biochem 71:290–297PubMedGoogle Scholar
  31. Bajguz A, Piotrowska-Niczyporuk A (2014) Interactive effect of brassinosteroids and cytokinins on growth, chlorophyll, monosaccharide and protein content in the green alga Chlorella vulgaris (Trebouxiophyceae). Plant Physiol Biochem 80:176–183PubMedGoogle Scholar
  32. Bao F, Shen J, Brady SR, Muday GK, Asami T, Zhenbiao Y (2004) Brassinosteroids interact with auxin to promote lateral root development in Arabidopsis. Plant Physiol 134:1624–1631PubMedPubMedCentralGoogle Scholar
  33. Bar M, Sharfman M, Ron M, Avni A (2010) BAK1 is required for the attenuation of ethylene-inducing xylanase (Eix)-induced defense responses by the decoy receptor LeEix1. Plant J 63:791–800PubMedGoogle Scholar
  34. Behnamnia M (2015) Protective roles of brassinolide on tomato seedlings under drought stress. Int J Agri Crop Sci 8:455–462Google Scholar
  35. Buer CS, Sukumar P, Muday GK (2006) Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis. Plant Physiol 140:1384–1396PubMedPubMedCentralGoogle Scholar
  36. Calzadilla PI, Maiale SJ, Ruiz OA, Escaray FJ (2016) Transcriptome response mediated by cold stress in Lotus japonicus. Front Plant Sci 7:374.  https://doi.org/10.3389/fpls.2016.00374 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Campos ML, deAlmeida M, Rossi ML, Martinelli AP, Junior CGL, Figueira A, Rampelotti-Ferreira FT, Vendramim JD, Benedito VA, Peres LEP (2009) Brassinosteroids interact negatively with jasmonates in the formation of anti-herbivory traits in tomato. J Exp Bot 60:4347–4361PubMedGoogle Scholar
  38. Cao YY, Zhao H (2008) Protective roles of brassinolide in rice seedlings under heat stress. Rice Sci 15:63–68Google Scholar
  39. Cerezoa M, Garcia-Agustina P, Sernab MD, Primo-Millob E (1997) Kinetics of nitrate uptake by Citrus seedlings and inhibitory effects of salinity. Plant Sci 126:105–112Google Scholar
  40. Chaiwanon J, Wang ZY (2015) Spatio-temporal brassinosteroid signaling and antagonism with auxin pattern stem cell dynamics in Arabidopsis roots. Curr Biol 25:1031–1042PubMedPubMedCentralGoogle Scholar
  41. Chen J, Nolan TM, Ye H, Zhang M, Tong H, Xin P, Chu J, Chu C, Li Z, Yin Y (2017) Arabidopsis WRKY46, WRKY54, and WRKY70 transcription factors are involved in brassinosteroid-regulated plant growth and drought responses. Plant Cell 29:1425–1439PubMedPubMedCentralGoogle Scholar
  42. Choudhary SP, Kanwar M, Bhardwaj R, Gupta BD, Gupta RK (2011) Epibrassinolide ameliorates Cr(VI) stress via influencing the levels of indole-3-acetic acid, abscisic acid, polyamines and antioxidant system of radish seedlings. Chemosphere 84:592–600PubMedGoogle Scholar
  43. Chung Y, Maharjan PM, Lee O, Fujioka S, Jang S, Kim B, Takatsuto S, Tsujimoto M, Kim H, Cho S, Park T, Cho H, Hwang I, Choe S (2011) Auxin stimulates DWARF4 expression and brassinosteroid biosynthesis in Arabidopsis. Plant J 66(4):564–578PubMedGoogle Scholar
  44. Clarke SM, Cristescu SM, Miersch O, Harren FJ, Wasternack C, Mur LA (2009) Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana. New Phytol 182:175–187PubMedGoogle Scholar
  45. Clouse SD (2015) A history of brassinosteroid research from 1970 through 2005: thirty-five years of phytochemistry, physiology, genes, and mutants. J Plant Growth Regul 34:828–844Google Scholar
  46. Coban O, Baydar NG (2016) Brassinosteroid effects on some physical and biochemical properties and secondary metabolite accumulation in peppermint (Mentha piperita L.) under salt stress. Ind Crops Prod 86:251–258Google Scholar
  47. De Vleesschauwer D, Van Buyten E, Satoh K, Balidion J, Mauleon R, Choi IR, Ver-Cruz C, Kikuchi S, Hofte M (2012) Brassinosteroids antagonize gibberellin– and salicylate-mediated root immunity in rice. Plant Physiol 158:1833–1846PubMedPubMedCentralGoogle Scholar
  48. Deng XG, Zhu T, Peng XJ, Xi DH, Guo H, Yin Y, Zhang DW, Lin HH (2016) Role of brassinosteroid signaling in modulating Tobacco mosaic virus resistance in Nicotiana benthamiana. Sci Rep 6:20576.  https://doi.org/10.1038/srep20579 CrossRefGoogle Scholar
  49. Dhaubhadel S, Chaudhary KS, Dobinson KF, Krishna P (1999) Treatment of 24-epibrassinolide, a brassinosteroid, increases the basic thermotolerance of Brassica napus and tomato seedlings. Plant Mol Biol 40:333–342PubMedGoogle Scholar
  50. Dhaubhadel S, Browning KS, Gallie DR, Krishna P (2002) Brassinosteroid functions to protect the translational machinery and heat-shock protein synthesis following thermal stress. Plant J 29:681–691PubMedGoogle Scholar
  51. Divi UK, Rahman T, Krishna P (2010) Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol 10:151PubMedPubMedCentralGoogle Scholar
  52. Divi UK, Rahman T, Krishna P (2016) Gene expression and functional analyses in brassinosteroid-mediated stress tolerance. Plant Biotech J 14:419–432Google Scholar
  53. El-Mashad AAA, Mohamed HI (2012) Brassinolide alleviates salt stress and increases antioxidant activity of cowpea plants (Vigna sinensis). Protoplasma 249:625–635PubMedGoogle Scholar
  54. Ernst WHO (1980) Biochemical aspects of cadmium in plants. In: Nriagu JO (ed) Cadmium in the environment, Wiley, New York, pp 639–653Google Scholar
  55. Fariduddin Q, Khanam S, Hasan SA, Ali B, Hayat S, Ahmad A (2009) Effect of 28-homobrassinolide on the drought stress-induced changes in photosynthesis and antioxidant system of Brassica juncea L. Acta Physiol Plant 31:889–897Google Scholar
  56. 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 49:55–64Google Scholar
  57. Fariduddin Q, Khalil RRAE, Mir BA, Yusuf M, Ahmad A (2013) 24-Epibrassinolide regulates photosynthesis, antioxidant enzyme activities and proline content of Cucumis sativus under salt and/or copper stress. Environ Monit Assess 185:7845–7856PubMedGoogle Scholar
  58. Fariduddin Q, Mir BA, Yusuf M, Ahmad A (2014) 24-epibrassinolide and/or putrescine trigger physiological and biochemical responses for the salt stress mitigation in Cucumis sativus L. Photosynthetica 52:464–474Google Scholar
  59. Gampala SS, Kim TW, He JX, Tang W, Deng Z, Bai MY, Guan S, Lalonde S, Sun Y, Gendron JM, Chen H, Shibagaki N, Ferl RJ, Ehrhardt D, Chong K, Burlingame AL, Wang ZY (2007) An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev Cell 13:177–189PubMedPubMedCentralGoogle Scholar
  60. Gonzalez-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 14:18–20Google Scholar
  61. Greeff C, Roux M, Mundy J, Petersen M (2012) Receptor-like kinase complexes in plant innate immunity. Front Plant Sci 3:209PubMedPubMedCentralGoogle Scholar
  62. Gruszka D, Janeczko A, Dziurka M, Pociecha E, Oklestkova J, Szarejko I (2016) Barley brassinosteroid mutants provide an insight into phytohormonal homeostasis in plant reaction to drought stress. Front Plant Sci 7:1824.  https://doi.org/10.3389/fpls.2016.01824 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Hasan SA, Hayat S, Ali B, Ahmad A (2008) 28-Homobrassinolide protects chickpea (Cicer arietinum) from cadmium toxicity by stimulating antioxidants. Environ Poll 151:60–66Google Scholar
  64. Hasan SA, Hayat S, Ahmad A (2011) Brassinosteroids protect photosynthetic machinery against the cadmium induced oxidative stress in two tomato cultivars. Chemosphere 84:1446–1451PubMedGoogle Scholar
  65. Hatfield JL, Prueger JH (2015) Temperature extremes: Effect on plant growth and development. Weather Clim Ext 10:4–10Google Scholar
  66. Hayat S, Ali B, Hasan SA, Ahmad A (2007) Brassinosteroid enhanced the level of antioxidants under cadmium stress in Brassica juncea. Environ Exp Bot 60:33–41Google Scholar
  67. Hayat S, Hasan SA, Yusuf M, Hayat Q, Ahmad A (2010) 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 69:105–112Google Scholar
  68. 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 19:325–335PubMedPubMedCentralGoogle Scholar
  69. Hu Y, Yu D (2014) BRASSINOSTEROID INSENSITIVE2 Interacts with ABSCISIC ACID INSENSITIVE5 to mediate the antagonism of brassinosteroids to abscisic acid during seed germination in Arabidopsis. Plant Cell 26:4394–4408PubMedPubMedCentralGoogle Scholar
  70. Hu WH, Wu Y, Zeng JZ, He L, Zeng QM (2010) Chill-induced inhibition of photosynthesis was alleviated by 24-epibrassinolide pretreatment in cucumber during chilling and subsequent recovery. Photosynthetica 48:537–544Google Scholar
  71. 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 150:232–237Google Scholar
  72. Huang G, Han M, Yao W, Wang Y (2017) Transcriptome analysis reveals the regulation of brassinosteroids on petal growth in Gerbera hybrida. Peer J 5:e3382.  https://doi.org/10.7717/peerj.3382 CrossRefPubMedGoogle Scholar
  73. Iqbal N, Umar S, Khan NA (2015) Nitrogen availability regulates proline and ethylene production and alleviates salinity stress in mustard (Brassica juncea). J Plant Physiol 178:84–91PubMedGoogle Scholar
  74. Janeczko A, Gullner G, Skoczowski A, Dubert F, Barna B (2007) Effects of brassinosteroid in filtration prior to cold treatment on ion leakage and pigment contents in rape leaves. Biol Plant 51:355–358Google Scholar
  75. Janeczko A, Biesaga-Koscielniak J, Oklestkova J, Filek M, Dziurka M, Szarek-Łukaszewska M, Koscielniak J (2010) Role of 24-epibrassinolide in wheat production: physiological effects and uptake. J Agron Crop Sci 196:311–321Google Scholar
  76. Jatav KS, Agarwal RM, Tomar NS, Tyagi SR (2014) Nitrogen metabolism, growth and yield responses of wheat (Triticum aestivum L.) to restricted water supply and varying potassium treatments. J Indian Bot Soc 93:177–189Google Scholar
  77. 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 148:133–145PubMedGoogle Scholar
  78. Jin SH, Li XQ, Wang G, Zhu XT (2015) Brassinosteroids alleviate high-temperature injury in Ficus concinna seedlings via maintaining higher antioxidant defence and glyoxalase systems. AoB Plants 7:plv009.  https://doi.org/10.1093/aobpla/plv009 CrossRefPubMedPubMedCentralGoogle Scholar
  79. 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 225:353–364PubMedGoogle Scholar
  80. Kanwar MK, Poonam Bhardwaj R (2015) Arsenic inducted modulation of antioxidative defense system and brassinosteroids in Brassica juncea. L Ecotox Environ Safe 115:119–125Google Scholar
  81. Kapoor D, Rattan A, Gautam V, Kapoor N, Bhardwaj R (2014) 24-epibrassinolide mediated changes in photosynthetic pigments and antioxidative defence system of radish seedlings under cadmium and mercury stress. J Stress Physiol Biochem 10:110–121Google Scholar
  82. Kaur H, Sirhindi G, Bhardwaj R, Alyemeni MN, Siddique KHM, Ahmad P (2018) 28-homobrassinolide regulates antioxidant enzyme activities and gene expression in response to salt- and temperature-induced oxidative stress in Brassica juncea. Sci Rep 8:8735PubMedPubMedCentralGoogle Scholar
  83. Kazemi-Shahandashti SS, Maali-Amiri R, Zeinali H, Khazaei M, Talei A, Ramezanpour SS (2014) Effect of short-term cold stress on oxidative damage and transcript accumulation of defense-related genes in chickpea seedlings. J Plant Physiol 171:1106–1116PubMedGoogle Scholar
  84. Kemmerling B, Nurnberger T (2008) Brassinosteroid-independent functions of the BRI1-associated kinase BAK1/SERK3. Plant Sig Beh 3:116–118Google Scholar
  85. Khan M, Rozhon W, Bigeard J, Pflieger D, Husar S, Pitzschke A, Teige M, Jonak C, Hirt H, Poppenberger B (2013) Brassinosteroid-regulated GSK3/Shaggy-like kinases phosphorylate mitogen-activated protein (MAP) kinase kinases, which control stomata development in Arabidopsis thaliana. J Biol Chem 288:7519–7527PubMedPubMedCentralGoogle Scholar
  86. Khan MIR, Nazir F, Asgher M, Per TS, Khan NA (2015) Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol 173:9–18PubMedGoogle Scholar
  87. Kim TW, Michniewicz M, Bergmann DC, Wang ZY (2011) Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature 482:419–422Google Scholar
  88. Kitanaga Y, Jian C, Hasegawa M, Yazaki J, Kishimoto N, Kikuchi S, Nakamura H, Ichikawa H, Asami H, Yoshida S, Yamaguchi I, Suzuki Y (2006) Sequential regulation of gibberellin, brassinosteroid, and jasmonic acid biosynthesis occurs in rice coleoptiles to control the transcript levels of anti-microbial thionin genes. Biosci Biotech Biochem 70:2410–2419Google Scholar
  89. Kocova M, Rothova O, Hola D, Kvasnica M, Kohout L (2010) The effects of brassinosteroids on photosynthetic parameters in leaves of two field-grown maize inbred lines and their F1 hybrid. Biol Plant 54:785–788Google Scholar
  90. Kozuka T, Kobayashi J, Horiguchi G, Demura T, Sakakibara H, Tsukaya H, Nagatani A (2010) Involvement of auxin and brassinosteroid in the regulation of petiole elongation under the shade. Plant Physiol 153:1608–1618PubMedPubMedCentralGoogle Scholar
  91. Krumova S, Zhiponova M, Dankov K, Velikova V, Balashev K, Andreeva T, Russinova E, Taneva S (2013) Brassinosteroids regulate the thylakoid membrane architecture and the photosystem II function. J Photochem Photobio B 126:97–104Google Scholar
  92. Li J (2003) Brassinosteroids signal through two receptor-like kinases. Curr Opin Plant Biol 6:494–499PubMedGoogle Scholar
  93. Li J (2005) Brassinosteroid signaling: from receptor kinases to transcription factors. Curr Opin Plant Biol 8:526–531PubMedGoogle Scholar
  94. Li QF, He JX (2013) Mechanisms of signaling crosstalk between brassinosteroids and gibberellins. Plant Sig Behav 8:e24686.  https://doi.org/10.4161/psb.24686 CrossRefGoogle Scholar
  95. Li QF, Wang C, Jiang L, Sun SS, He JX (2012a) An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in Arabidopsis. Sci Signal 5(244):ra72.  https://doi.org/10.1126/scisignal.2002908 CrossRefPubMedGoogle Scholar
  96. Li YH, Liu YJ, Xu XL, Jin M, An LZ, Zhang H (2012b) Effect of 24-epibrassinolide on drought stress-induced changes in Chorispora bungeana. Bio Plant 56:192–196Google Scholar
  97. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  98. Liu YJ, Zhao ZG, Si J, Di CX, Han J, An LZ (2009) Brassinosteroids alleviate chilling-induced oxidative damage by enhancing antioxidant defense system in suspension cultured cells of Chorispora bungeana. Plant Growth Regul 59:207–214Google Scholar
  99. Liu J, Rowe J, Lindsey K (2014) Hormonal crosstalk for root development: a combined experimental and modeling perspective. Front Plant Sci 5:116.  https://doi.org/10.3389/fpls.2014.00116 CrossRefPubMedPubMedCentralGoogle Scholar
  100. Liu J, Zhang D, Sun X, Ding T, Lei B, Zhang C (2017) Structure-activity relationship of brassinosteroids and their agricultural practical usages. Steroids 124:1–17PubMedGoogle Scholar
  101. Lu XM, Yang W (2013) Alleviation effects of brassinolide on cucumber seedlings under NaCl stress. Ying Yong Sheng Tai Xue Bao 24:1409–1414PubMedGoogle Scholar
  102. Ma Y, Xue H, Zhang L, Zhang F, Ou C, Wang F, Zhang Z (2016) Involvement of auxin and brassinosteroid in dwarfism of autotetraploid apple (Malus × domestica). Sci Rep 6:26719.  https://doi.org/10.1038/srep26719 CrossRefPubMedPubMedCentralGoogle Scholar
  103. Machado RMA, Serralheiro RP (2017) Soil salinity: effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Hort 3:30.  https://doi.org/10.3390/horticulturae3020030 CrossRefGoogle Scholar
  104. Maharjan PM, Choe S (2011) High temperature stimulates DWARF4 (DWF4) expression to increase hypocotyle elongation in Arabidopsis. J Plant Biol 54:425–429Google Scholar
  105. Maharjan PM, Schulz B, Choe S (2011) BIN2/DWF12 antagonistically transduces brassinosteroid and auxin signals in the roots of Arabidopsis. J Plant Biol 54:126–134Google Scholar
  106. Mahesh K, Balaraj P, 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 4:2305–2313Google Scholar
  107. Maier F, Zwicker S, Huckelhoven A, Meissner M, Funk J, Pfitzner AJ, Pfitzner UM (2011) NONEXPRESSOR OF PATHOGENESIS-RELATED PROTEINS1 (NPR1) and some NPR1-related proteins are sensitive to salicylic acid. Mol Plant Pathol 12:73–91PubMedGoogle Scholar
  108. Mazorra LM, Holton N, Bishop GJ, Nunez M (2011) Heat shock response in tomato brassinosteroid mutants indicates that thermotolerance is independent of brassinosteroid homeostasis. Plant Physiol Biochem 49:1420–1428PubMedGoogle Scholar
  109. Mishra MK, Chaturvedi P, Singh R, Singh G, Sharma LK, Pandey V, Kumari N, Misra P (2013) Overexpression of wssgtl1 gene of Withania somnifera enhances salt tolerance, heat tolerance and cold acclimation ability in transgenic Arabidopsis Plants. PLoS ONE 8:e63064.  https://doi.org/10.1371/journal.pone.0063064 CrossRefPubMedPubMedCentralGoogle Scholar
  110. Mouchel CF, Osmont KS, Hardtke CS (2006) BRX mediates feedback between brassinosteroid and auxin signaling in root growth. Nature 443:458–461PubMedGoogle Scholar
  111. Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17:181–195PubMedGoogle Scholar
  112. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59(1):651–681PubMedGoogle Scholar
  113. Ogweno JO, Song XS, Shi K, Hu WH, Mao WH, Zhou YH, Yu JQ, Nogue S (2008) Brassinosteroids alleviate heat-induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum. J Plant Growth Regul 27:49–57Google Scholar
  114. Ogweno JO, Hu WH, Song XS, Shi K, Mao WH, Zhou YH, Yu JQ (2010) Photoinhibition-induced reduction in photosynthesis is alleviated by abscisic acid, cytokinin and brassinosteroid in detached tomato leaves. Plant Growth Regul 60:175–182Google Scholar
  115. Peleg Z, Reguera M, Tumimbang E, Walia H, Blumwald E (2011) Cytokinin-mediated source/sink modifications improve drought tolerance and increase grain yield in rice under water-stress. Plant Biotech J 9:747–758Google Scholar
  116. Peng Z, Han C, Yuan L, Zhang K, Huang H, Ren C (2011) Brassinosteroid enhances jasmonate-induced anthocyanin accumulation in Arabidopsis seedlings. J Integr Plant Biol 53:632–640PubMedGoogle Scholar
  117. Qu T, Liu R, Wang W, An L, Chen T, Liu G, Zhao Z (2011) Brassinosteroids regulate pectin methylesterase activity and AtPME41 expression in Arabidopsis under chilling stress. Cryobiology 63:111–117PubMedGoogle Scholar
  118. 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 129:232–237Google Scholar
  119. Ramakrishna B, Rao SSR (2015) Foliar application of brassinosteroids alleviates adverse effects of zinc toxicity in radish (Raphanus sativus L.) plants. Protoplasma 252:665–677PubMedGoogle Scholar
  120. Ren C, Han C, Peng W, Huang Y, Peng Z, Xiong X, Zhu Q, Gao B, Xie D (2009) A leaky mutation in DWARF4 reveals an antagonistic role of brassinosteroid in the inhibition of root growth by jasmonate in Arabidopsis. Plant Physiol 151:1412–1420PubMedPubMedCentralGoogle Scholar
  121. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  122. Saini S, Sharma I, Kaur N, Pati PK (2013) Auxin: a master regulator in plant root development. Plant Cell Rep 32:741–757PubMedGoogle Scholar
  123. 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.  https://doi.org/10.3389/fpls.2015.00950 CrossRefPubMedPubMedCentralGoogle Scholar
  124. Shahana T, Rao PA, Ram SS, Sujatha E (2015) Mitigation of drought stress by 24-epibarassinolide and 28-homobrassinolide in pigeon pea seedlings. Int J Multi Curr Res 3:905–911Google Scholar
  125. 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 39:513–522Google Scholar
  126. Shakirova FM, Bezrukova M (1998) Effect of 24-epibrassinolide and salinity on the levels of ABA and lectin. Russ J Plant Physiol 45:388–391Google Scholar
  127. Shakirova FM, Bezrukova MV, Avalbaev AM, Gimalov FR (2002) Stimulation of wheat germ agglutinin gene expression in root seedlings by 24-epibrassinolide. Russ J Plant Physiol 49:225–228Google Scholar
  128. Sharma P, Bhardwaj R, Arora N, 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 19:203–210Google Scholar
  129. 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 47:172–177PubMedGoogle Scholar
  130. Sharma I, Ching E, Saini S, Bhardwaj R, Pati PK (2013) Exogenous application of brassinosteroid offers tolerance to salinity by altering stress responses in rice variety Pusa Basmati-1. Plant Physiol Biochem 69:17–26PubMedGoogle Scholar
  131. 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 122:1–9Google Scholar
  132. Shin R, Jez JM, Basra A, Zhang B, Schachtman DP (2011) 14-3-3 Proteins fine-tune plant nutrient metabolism. FEBS Lett 585:143–147PubMedGoogle Scholar
  133. Siboza XI, Bertling I, Odindo AO (2014) Salicylic acid and methyl jasmonate improve chilling tolerance in cold-stored lemon fruit (Citrus limon). J Plant Physiol 171:1722–1731PubMedGoogle Scholar
  134. Singh I, Shono M (2005) Physiological and molecular effects of 24-epibrassinolide, a brassinosteroid on thermotolerance of tomato. Plant Growth Regul 47:111–119Google Scholar
  135. Singh I, Kumar U, Singh SK, Gupta C, Singh M, Kushwaha SR (2012) Physiological and biochemical effect of 24-epibrassinoslide on cold tolerance in maize seedlings. Physiol Mol Biol Plants 18:229–236PubMedPubMedCentralGoogle Scholar
  136. 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 122:115–125Google Scholar
  137. 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 Sheng Xuebao 17:1871–1876Google Scholar
  138. 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 60:329–342Google Scholar
  139. 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 Regul 35:518–533Google Scholar
  140. Talaat NB, Shawky BT, Ibrahim AS (2015) Alleviation of drought-induced oxidative stress in maize (Zea mays L.) plants by dual application of 24-epibrassinolide and spermine. Environ Exp Bot 113:47–58Google Scholar
  141. Tanaka K, Asami T, Yoshida S, Nakamura Y, Matsuo T, Okamoto S (2005) Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. Plant Physiol 138:1117–1125PubMedPubMedCentralGoogle Scholar
  142. Thussagunpanit J, Jutamanee K, Sonjaroon W, Kaveeta L, Chaiarree W, Pankean P, Suksamrarn A (2015) Effects of brassinosteroid and brassinosteroid mimic on photosynthetic efficiency and rice yield under heat stress. Photosynthetica 53:312–320Google Scholar
  143. Tong H, Xiao Y, Liu D, Gao S, Liu L, Yin Y, Jin Y, Qian Q, Chu C (2014) Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice. Plant Cell 26:4376–4393PubMedPubMedCentralGoogle Scholar
  144. Turkan I, Demiral T (2009) Recent developments in understanding salinity tolerance. Environ Exp Bot 67:2–9Google Scholar
  145. Unterholzner SJ, Rozhon W, Papacek M, Ciomas J, Lange T, Kugler KG, Mayer KF, Sieberer T, Poppenberger B (2015) Brassinosteroids are master regulators of gibberellin biosynthesis in Arabidopsis. Plant Cell 27:2261–2272PubMedPubMedCentralGoogle Scholar
  146. Upreti KK, Murti GSR (2004) Effects of brassinosteroids on growth, nodulation, phytohormone content and nitrogenase activity in French bean under water stress. Biol Plant 48:407–411Google Scholar
  147. Vandenbussche F, Callebert P, Zadnikova P, Benkova E, VanDer Straeten D (2013) Brassinosteroid control of shoot gravitropism interacts with ethylene and depends on auxin signaling components. Am J Bot 100:215–225PubMedGoogle Scholar
  148. Vercruyssen L, Gonzalez N, Werner T, Schmülling T, Inze D (2011) Combining enhanced root and shoot growth reveals crosstalk between pathways that control plant organ size in Arabidopsis. Plant Physiol 155:1339–1352PubMedPubMedCentralGoogle Scholar
  149. Wang Q, Ding T, Gao L, Pang J, Yang N (2012) Effect of brassinolide on chilling injury of green bell pepper in storage. Sci Hortic 144:195–200Google Scholar
  150. Xi Z, Wang Z, Fang Y, Hu Z, Hu Y, Deng M, Zhang Z (2013) Effects of 24-epibrassinolide on antioxidantion defense and osmoregulation systems of young grapevines (V. vinifera L.) under chilling stress. Plant Growth Regul 71:57–65Google Scholar
  151. Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen Z, Yu JQ (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814PubMedPubMedCentralGoogle Scholar
  152. Yadava P, Kaushal J, Gautam A, Parmar H, Singh I (2016) Physiological and biochemical effects of 24-epibrassinolide on heat-stress adaptation in maize (Zea mays L.). Nat Sci 8:171–179Google Scholar
  153. Yang GX, Jan A, Shen SH, Ishikawa JYM, Shimatani Z, Kishimoto N, Matsumoto SKH, Komatsu S (2004) Microarray analysis of brassinosteroids- and gibberellin-regulated gene expression in rice seedlings. Mol Genet Genom 271:468–478Google Scholar
  154. Yang CJ, Zhang C, Lu YN, Jin JQ, Wang XL (2011) The mechanisms of brassinosteroids’ action: from signal transduction to plant development. Mol Plant 4:588–600PubMedGoogle Scholar
  155. Yang X, Bai Y, Shang J, Xin R, Tang W (2016) The antagonistic regulation of abscisic acid-inhibited root growth by brassinosteroids is partially mediated via direct suppression of ABSCISIC ACID INSENSITIVE 5 expression by BRASSINAZOLE RESISTANT 1. Plant Cell Environ 39:1994–2003PubMedGoogle Scholar
  156. Ye H, Liu S, Tang B, Chen J, Xie Z, Nolan TM, Jiang H, Guo H, Lin HY, Li L, Wang Y, Tong H, Zhang M, Chu C, Li Z, Aluru M, Aluru S, Schnable PS, Yin Y (2017) RD26 mediates crosstalk between drought and brassinosteroid signalling pathways. Nat Comm 8:14573.  https://doi.org/10.1038/ncomms14573 CrossRefGoogle Scholar
  157. Yuan L, Zhua S, Shu S, Sun J, Guo S (2015a) Regulation of 2, 4-epibrassinolide on mineral nutrient uptake and ion distribution in Ca(NO3)2 stressed cucumber plants. J Plant Physiol 188:29–36PubMedGoogle Scholar
  158. Yuan LB, Peng ZH, Zhi TT, Zho Z, Liu Y, Zhu Q, Xiong XY, Ren CM (2015b) Brassinosteroid enhances cytokinin-induced anthocyanin biosynthesis in Arabidopsis seedlings. Biol Plant 59:99–105Google Scholar
  159. 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 55:1–6PubMedGoogle Scholar
  160. Yusuf M, Fariduddin Q, Ahmad A (2012) 24-Epibrassinolide modulates growth, nodulation, antioxidant system, and osmolyte in tolerant and sensitive varieties of Vigna radiata under different levels of nickel: a shot-gun approach. Plant Physiol Biochem 57:143–153PubMedGoogle Scholar
  161. 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 Plant 20:449–460Google Scholar
  162. 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 58:811–815Google Scholar
  163. Zhang S, Cai Z, Wang X (2009) The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling. Proc Natl Acad Sci USA 106:4543–4548PubMedGoogle Scholar
  164. Zhang S, Wang S, Xu Y, Yu C, Shen C, Qian Q, Geisler M, Jiang de A, Qi Y (2014) The auxin response factor, OsARF19, controls rice leaf angles through positively regulating OsGH3-5 and OsBRI1. Plant Cell Environ 38:638–654PubMedGoogle Scholar
  165. Zhao BT, Zhu XF, Jung JH, Xuan YH (2016) Effect of brassinosteroids on ammonium uptake via regulation of ammonium transporter and N-metabolism genes in Arabidopsis. Biol Plant 60:563–571Google Scholar
  166. Zhou A, Wang H, Walker JC, Li J (2004) BRL1, a leucine-rich repeat receptor-like protein kinase, is functionally redundant with BRI1 in regulating Arabidopsis brassinosteroid signaling. Plant J 40:399–409PubMedGoogle Scholar
  167. Zhou J, Wang J, Li X, Xia XJ, Zhou YH, Shi K, Chen Y, Yu JQ (2014) H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses. J Exp Bot 65:4371–4383PubMedPubMedCentralGoogle Scholar
  168. Zhu W, Wang H, Fujioka S, Zhou T, Tian H, Tian W, Wang X (2013) Homeostasis of brassinosteroids regulated by DRL1, a putative acyltransferase in Arabidopsis. Mol Plant 6:546–558PubMedGoogle Scholar
  169. Zhu T, Deng X, Zhou X, Zhu L, Zou L, Li P, Zhang D, Lin H (2016) Ethylene and hydrogen peroxide are involved in brassinosteroid induced salt tolerance in tomato. Sci Rep 6:35392.  https://doi.org/10.1038/srep35392 CrossRefPubMedPubMedCentralGoogle Scholar
  170. Zhu J, Li Y, Cao DM, Yang H, Oh E, Bi Y, Zhu S, Wang ZY (2017) The F-box protein KIB1 mediates brassinosteroid-induced inactivation and degradation of GSK3-like kinases in Arabidopsis. Mol Cell 66:648–657PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BotanyGovt Degree College, ShopianSrinagarIndia
  2. 2.College of Agronomy, Faculty of AgricultureUniversity of SargodhaSargodhaPakistan
  3. 3.Department of Plant Biochemistry and Toxicology, Institute of Biology, Faculty of Biology and ChemistryUniversity of BialystokBialystokPoland
  4. 4.Department of Botany & MicrobiologyKing Saud UniversityRiyadhSaudi Arabia
  5. 5.Department of BotanyS.P. CollegeSrinagarIndia

Personalised recommendations