biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 62:601-616, 2018 | DOI: 10.1007/s10535-018-0805-4

Physiological and molecular mechanisms of brassinosteroid-induced tolerance to high and low temperature in plants

I. Sadura1, A. Janeczko1,*
1 The Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Krakow, Poland

Brassinosteroids (BRs) are plant hormones that were isolated for the first time in the 1970s. This group currently includes more than 70 compounds that differ in their structure and physiological activity. BRs are present in plants in a free form or in the form of conjugates. BRs are known as plant growth regulators, but they also play a role in the plant response to environmental stresses. In the case of plants that are exposed to low/high temperature, exogenous BRs can counteract growth inhibition and reduce biomass losses as well as increase plant survival. BRs show a multidirectional activity in regulating the metabolism of plants exposed to extreme temperatures. The following BRs actions can be distinguished: changes in membrane physicochemical properties, regulation of the expression of selected genes (including stress-responsive genes), as well as indirect effects on metabolism through other hormones or signalling molecules (such as hydrogen peroxide). This review summarizes the current knowledge about the effects of BRs on the physiological and biochemical processes that occur in plants during exposure to low or high temperatures.

Keywords: plant acclimation; cell membranes; cold; freezing; gene expression; heat; oxidative damage; photosynthesis; proline
Subjects: brassinosteroids; heat; cold; acclimation; cell membranes; gene expression; oxidative stress; antioxidants; chlorophyll; net photosynthetic rate; proline; glycine betaine

Received: October 27, 2017; Revised: February 12, 2018; Accepted: March 7, 2018; Published: August 1, 2018  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Sadura, I., & Janeczko, A. (2018). Physiological and molecular mechanisms of brassinosteroid-induced tolerance to high and low temperature in plants. Biologia plantarum62(4), 601-616. doi: 10.1007/s10535-018-0805-4
Download citation

Supplementary files

Download filebpl-201804-0001_S1.pdf

File size: 92.25 kB

References

  1. Aghdam, M.S., Asghari, M., Farmani, B., Mohayeji, M., Moradbeygi, H.: Impact of postharvest brassinosteroids treatment on PAL activity in tomato fruit in response to chilling stress. - Sci. Hort. 144: 116-120, 2012. Go to original source...
  2. Ashraf, M., Foolad, M.R.: Roles of glycine betaine and proline in improving plant abiotic stress resistance. - Environ. exp. Bot. 59: 206-216, 2007. Go to original source...
  3. Bajguz, A.: Brassinosteroid enhanced the level of abscisic acid in Chlorella vulgaris subjected to short-term heat stress. - J. Plant Physiol. 166: 882-886, 2009. Go to original source...
  4. Bajguz, A., Tretyn, A.: The chemical characteristic and distribution of brassinosteroids in plants. - Phytochemistry 62: 1027-1046, 2003. Go to original source...
  5. Clouse, S.D.: A history of brassinosteroid research from 1970 through 2005: thirty-five years of phytochemistry, physiology, genes and mutants. - J. Plant Growth Regul. 34: 828-844, 2015. Go to original source...
  6. Cui, L., Zou, Z., Zhang, J., Zhao, Y., Yan, F.: 24-Epibrassinoslide enhances plant tolerance to stress from low temperatures and poor light intensities in tomato (Lycopersicon esculentum Mill.). - Funct. integr. Genomics 16: 29-35, 2016. Go to original source...
  7. Deng, Z., Zhang, X., Tang, W., Oses-Prieto, J.A., Suzuki, N., Gendron, J. M., Chen, H., Guan, S., Chalkley, R.J., Peterman, T.K., Burlingame, A.L., Wang, Z.-Y.: A proteomic study of brassinosteroid response in Arabidopsis. - Mol. Cell Proteomics 6: 2058-2071, 2007. Go to original source...
  8. Dhaubhadel, S., Browning, K.S., Gallie, D.R., Krishna, P.: Brassinosteroid functions to protect the translational machinery and heat-shock protein synthesis following thermal stress. - Plant J. 29: 681-691, 2002. Go to original source...
  9. Dhaubhadel, S., Chaudhary, S., Dobinson, K. F., Krishna, P.: Treatment with 24-epibrassinolide, a brassinosteroid, increases the basic thermotolerance of Brassica napus and tomato seedlings. - Plant mol. Biol. 40: 333-342, 1999. Go to original source...
  10. Divi, U.K., Rahman, T., Krishna, P.: Gene expression and functional analyses in brassinosteroid-mediated stress tolerance. - Plant Biotechnol. J. 14: 419-432, 2016. Go to original source...
  11. Dockter, C., Gruszka, D., Braumann, I., Druka, A., Druka, I., Franckowiak, J., Gough, S.P., Janeczko, A., Kurowska, M., Lundqvist, J., Lundqvist, U., Marzec, M., Matyszczak, I., Müller, A. H., Okle¹»ková, J., Schulz, B., Zakhrabekova, S., Hansson, M.: Induced variations in brassinosteroid genes define barley height and sturdiness, and expand the "Green Revolution" genetic toolkit. - Plant Physiol. 166: 1912-1927, 2014. Go to original source...
  12. Eremina, M., Unterholzner, S.J., Rathnayake, A.I., Castellanos, M., Khan, M., Kugler, K.G., May, S.T., Mayer, K.F.X., Rozhon, W., Poppenberger, B.: Brassinosteroids participate in the control of basal and acquired freezing tolerance of plants. - Proc. nat. Acad. Sci. USA 113: 5982-5991, 2016. Go to original source...
  13. Fahad, S., Hussain, S., Saud, S., Khan, F., Hassan, S., Amanullah, N.W., Arif, M., Wang, F., Huang, J.: Exogenously applied plant growth regulators affect heatstressed rice pollens. - J. Agron Crop Sci. 202: 139-150, 2016. Go to original source...
  14. Fariduddin, Q., Yusuf, M., Chalkoo, S., Hayat, S., Ahmad, A.: 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, 2011. Go to original source...
  15. Filek, M., Rudolphi-Skórska, E., Sieprawska, A., Kvasnica, M., Janeczko, A.: Regulation of the membrane structure by brassinosteroids and progesterone in winter wheat seedlings exposed to low temperature. - Steroids 128: 37-45, 2017. Go to original source...
  16. Fujioka, S., Yokota, T.: Biosynthesis and metabolism of brassinosteroids. - Physiol. Plant. 100: 710-715, 1997. Go to original source...
  17. Grove, M.D., Spencer, G.F., Rohwedder, W.K., Mandava, N., Worley, J.F., Warthen, J.D., Jr., Steffens, G.L., Flippen- Anderson, J.L., Cook, J.C., Jr.: Brassinolide, a plant growthpromoting steroid isolated from Brassica napus pollen. - Nature 281: 216-217, 1979. Go to original source...
  18. Hayat, S., Hayat, Q., Alyemeni, M.N., Wani, A.S., Pichtel, J., Ahmad, A.: Role of proline under changing environments: a review. - Plant Signal Behav. 7: 1456-1466, 2012. Go to original source...
  19. He, R.-Y., Wang, G.-J., Wang, X.-S.: Effects of brassinolide on growth and chilling resistance of maize seedlings. - In: Cutler, G.H., Yokota, T, Adam, G. (ed.): Brassinosteroids. Vol. 19. Pp. 220-230. American Chemical Society, Washington 1991. Go to original source...
  20. Henry, R.P.: Multiple roles of carbonic anhydrase in cellular transport and metabolism. - Annu. Rev. Plant Physiol. 58: 523-538, 1996. Go to original source...
  21. Hodges, D. M., DeLong, J.M., Forney, C.F., Prange, R.K.: Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. - Planta 207: 604-611, 1999. Go to original source...
  22. Hörtensteiner, S., Kräutler, B.: Chlorophyll breakdown in higher plants. - BBA Bioenergetics 1807: 977-988, 2011. Go to original source...
  23. Horváth, I., Glatz, A., Nakamoto, H., Mishkind, M.L., Munnik, T., Saidi, Y., Goloubinoff, P., Harwood, J.L., Vigh, L.: Heat shock response in photosynthetic organisms: membrane and lipid connections. - Progr. Lipid Res. 51: 208-220, 2012. Go to original source...
  24. Hu, W.H., Wu, Y., Zeng, J.Z., He, L., Zeng, Q.M.: Chillinduced inhibition of photosynthesis was alleviated by 24-epibrassinolide pretreatment in cucumber during chilling and subsequent recovery. - Photosynthetica 48: 537-544, 2010. Go to original source...
  25. Janeczko, A. (ed): Wystêpowanie, transport i wybrane aspekty aktywno¶ci fizjologicznej brasinosteroidów w ro¶linach uprawnych z rodzin Poaceae I Fabaceae. [Presence, Transport and PhysiologicalAactivity of Brassinosteroids in Crop Plants from Poaceae and Fabaceae family]. - Polish Academy of Sciences, Krakow 2016. [In Polish.]
  26. Janeczko, A., Gruszka, D., Pociecha, E., Dziurka, M., Filek, M., Jurczyk, B., Kalaji, H.M., Kocurek, M., Waligórski, P.: Physiological and biochemical characterisation of watered and drought-stressed barley mutants in the HvDWARF gene encoding C6-oxidase involved in brassinosteroid biosynthesis. - Plant Physiol. Biochem. 99: 126-141, 2016. Go to original source...
  27. Janeczko, A., Gullner, G., Skoczowski, A., Dubert, F., Barna, B.: Effects of brassinosteroid infiltration prior to cold treatment on ion leakage and pigment contents in rape leaves. - Biol. Plant. 51: 355-358, 2007. Go to original source...
  28. Janeczko, A., Hura, K., Skoczowski, A., Idzik, I., Biesaga- Ko¶cielniak, J., Niemczyk, E.: Temperature-dependent impact of 24-epibrassinolide on the fatty acid composition and sugar content in winter oilseed rape callus. - Acta Physiol Plant. 31: 71-79, 2009. Go to original source...
  29. Janeczko, A., Okle¹»ková, J., Pociecha, E., Ko¶cielniak, J., Mirek, M.: Physiological effects and transport of 24-epibrassinolide in heat-stressed barley. - Acta Physiol. Plant. 33: 1249-1259, 2011. Go to original source...
  30. Jiang, Y.-P., Huang, L.-F., Cheng, F., Zhou, Y.-H., Xia, X.-J., Mao, W.-H., Shi, K., Yu, J.-Q.: 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, 2013. Go to original source...
  31. Jin, S.H., Li, X.Q., Wang, G.G., Zhu, X.T.: Brassinosteroids alleviate high-temperature injury in Ficus concinna seedlings via maintaining higher antioxidant defence and glyoxalase systems. - AoB Plants 7: plv009, 2015. Go to original source...
  32. Johnson, G., Williams, J.P.: Effect of growth temperature on the biosynthesis of chloroplastic galactosyldiacylglycerol molecular species in Brassica napus leaves. - Plant Physiol. 91: 924-929, 1989. Go to original source...
  33. Kagale, S., Divi, U.K., Krochko, J.E., Keller, W.A., Krishna, P.: Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. - Planta 225: 353-364, 2007. Go to original source...
  34. Kim, T.-W., Chang, S.C.. Lee, J.S, Takatsuto, S., Yokota, T., Kim, S.-K.: Novel biosynthetic pathway of castasterone from cholesterol in tomato. - Plant Physiol. 135: 1231-1242, 2004. Go to original source...
  35. Kim, Y.-S., Joo, S.-H., Hwang, J.-Y., Park, C.H., Kim, S.-K.: Characterization of C29-brassinosteroids and their biosynthetic precursors in immature seeds of Phaseolus vulgaris. - Bull. korean chem. Soc. 27: 1117-1118, 2006. Go to original source...
  36. Kreslavski, V.D., Los, D.A., Allakhverdiev, S.I., Kuznetsov, V.V.: Signaling role of reactive oxygen species in plants under stress.-Russ. J Plant Physiol. 59: 141-154, 2012. Go to original source...
  37. Krishna, P.: Brassinosteroid-mediated stress responses. - J. Plant Growth Regul. 22: 289-297, 2003. Go to original source...
  38. Lafuente, M.T., Zacarias, L., Martinez-Téllez, M.A., Sanchez- Ballesta, M.T., Granell, A.: Phenylalanine ammonia-lyase and ethylene in relation to chilling injury as affected by fruit age in citrus. - Postharvest Biol. Technol. 29: 308-317, 2003. Go to original source...
  39. Li, B., Zhang, C., Cao, B., Qin, G., Wang, W., Tian, S.: Brassinolide enhances cold stress tolerance of fruit by regulating plasma membrane proteins and lipids. - Amino Acids 43: 2469-2480, 2012. Go to original source...
  40. Li, J.M., Jin, H.: The regulation of brassinosteroids signaling. - Trends Plant Sci. 12: 37-41, 2007. Go to original source...
  41. Li, H., Ye, K., Shi, Y., Cheng, J., Zhang, X., Yang, S.: BZR1 positively regulates freezing tolerance via CBF-dependent and CBF-independent pathways in Arabidopsis. - Mol. Plants 10: 545-559, 2017. Go to original source...
  42. Liu, Y., Jiang, H., Zhao, Z., An, L.: Abscisic acid is involved in brassinosteroids-induced chilling tolerance in the suspension cultured cells from Chorispora bungeana. - J. Plant Physiol. 168: 853-862, 2011. Go to original source...
  43. Liu, Y., Zhao, Z., Si, J., Di, C., Han, J., An, L.: Brassinosteroids alleviate chilling-induced oxidative damage by enhancing antioxidant defense system in suspension cultured cells of Chorispora bungeana. - Plant Growth Regul. 25: 207-214, 2009. Go to original source...
  44. Mazorra, L.M., Holton, N., Bishop, G.J., Núñez, M.: Heat shock response in tomato brassinosteroid mutants indicates that thermotolerance is independent of brassinosteroid homeostasis. - Plant Physiol. Biochem. 49: 1420-1428, 2011. Go to original source...
  45. Micheli, F.: Pectin methylesterases: cell wall enzymes with important roles in plant physiology. - Trends Plant Sci. 6: 414-419, 2001. Go to original source...
  46. Mitchell, J.W., Mandava, N., Worley, J.F., Plimmer, J.R., Smith, M.V.: Brassins - a new family of plant hormones from rape pollen. - Nature 225: 1065-1066, 1970. Go to original source...
  47. Morillon, R., Catterou, M., Sangwan, R.S., Sangwan, B.S., Lassalles, J.P.: Brassinolide may control aquaporin activities in Arabidopsis thaliana. - Planta 212: 199-204, 2001. Go to original source...
  48. Parthier, B.: The role of phytohormones (cytokinins). III Chloroplast development. - Biochem. Physiol. Pflanz. 174: 173-214, 1979. Go to original source...
  49. Park, S.C., Kim, T.-W., Kim, S.-K.: Identification of brassinosteroids with 24R-methyl in immature seeds of Phaseolus vulgaris. - Bull. korean chem. Soc. 21: 1274-1276, 2000. Go to original source...
  50. Pociecha, E., Dziurka, M., Oklestkova, J., Janeczko, A.: Brassinosteroids increase winter survival of winter rye (Secale cereale L.) by affecting photosynthetic capacity and carbohydrate metabolism during the cold acclimation process. - Plant Growth Regul. 80: 127-135, 2016. Go to original source...
  51. Pociecha, E., Dziurka, M., Waligórski, P., Krêpski, T., Janeczko, A.: 24-Epibrassinolide pre-treatment modifies cold-induced photosynthetic acclimation mechanisms and phytohormone response of perennial ryegrass in cultivardependent manner. - J. Plant Growth. Regul. 36:618-628, 2017. Go to original source...
  52. Qu, T., Liu, R., Wang, W., An, L., Chen, T., Liu, G., Zhao, Z.: Brassinosteroids regulate pectin methylesterase activity and AtPME41 expression in Arabidopsis under chilling stress. - Cryobiology 63: 111-117, 2011. Go to original source...
  53. Samakovli, D., Margaritopoulou, T., Prassinos, C., Milioni, D., Hatzopoulos, P.: Brassinosteroid nuclear signaling recruits HSP90 activity. - New Phytol. 203: 743-757, 2014. Go to original source...
  54. Sakuraba, Y., Lee, S.H., Kim, Y.S., Park, O.K., Hörtensteiner, S., Paek, N.C.: Delayed degradation of chlorophylls and photosynthetic proteins in Arabidopsis autophagy mutants during stress-induced leaf yellowing. - J. exp. Bot. 65: 3915-3925, 2014. Go to original source...
  55. Schaller, H.: The role of sterols in plant growth and development. - Progr. Lipid Res. 42: 163-175, 2003. Go to original source...
  56. Senaratna, T., Mackay, C.E., McKersie, B.D., Fletcher, R.A.: Uniconazole-induced chilling tolerance in tomato and its relationship to antioxidant content. - J. Plant Physiol. 133: 56-61, 1988. Go to original source...
  57. Shu, H.M., Guo, S.Q., Gong, Y.Y., Jiang, J.W., Ni, W.C.: RNA-seq analysis reveals a key role of brassinolideregulated pathways in NaCl-stressed cotton. - Biol. Plant. 61: 667-674, 2017. Go to original source...
  58. Singh, I., Kumar, U., Singh, S.K., Gupta, C., Singh, M., Kushwaha, S.R.: Physiological and biochemical effect of 24-epibrassinoslide on cold tolerance in maize seedlings. - Physiol. mol. Biol. Plants 18: 229-236, 2012. Go to original source...
  59. Singh, I., Shono, M.: Effect of 24-epibrassinolide on pollen viability during heat-stress in tomato. - Indian J. exp. Biol. 41: 174-176, 2003.
  60. Song, Y.L., Dong, Y.J., Tian, X.Y., Kong, J., Bai, X.Y., Xu, L.L., He, Z.L.: Role of foliar application of 24-epibrassinolide in response of peanut seedlings to iron deficiency. - Biol. Plant. 60: 329-342, 2016. Go to original source...
  61. Takatsuto, S., Kosuga, N., Abe, B-I., Noguchi, T., Fujioka, S., Yokota, T.: Occurrence of potential brassinosteroid precursor steroids in seeds of wheat and foxtail millet. - J. Plant Res. 112: 27-33, 1999. Go to original source...
  62. Thussagunpanit, J., Jutamanee, K., Kaveeta, L., Chai-arree, W., Pankean, P., Homvisasevongsa, S., Suksamrarn, A.: Comparative effects of brassinosteroid and brassinosteroid mimic on improving photosynthesis, lipid peroxidation and rice seed set under heat stress. - J. Plant Growth Regul. 34: 320-331, 2015b. Go to original source...
  63. Thussagunpanit, J., Jutamanee, K., Sonjaroon, W., Kaveeta, L., Chai-arree, W., Pankean, P., Suksamrarn, A.: Effects of brassinosteroid and brassinosteroid mimic on photosynthetic efficiency and rice yield under heat stress. - Photosynthetica 53: 312-320, 2015a. Go to original source...
  64. Tomashow, M.F.: Role of cold-responsive genes in plant freezing tolerance. - Plant Physiol. 118: 1-7, 1998. Go to original source...
  65. Wang, Q., Ding, T., Gao, L., Pang, J., Yang, N.: Effect of brassinolide on chilling injury of green bell pepper in storage. - Sci. Hort. 144: 195-200, 2012. Go to original source...
  66. Wang, W., Bai, M.Y., Wang, Z.Y.: The brassinosteroid signalling network - a paradigm of signal transduction. - Curr. Opin. Plant Biol. 21: 147-153, 2014. Go to original source...
  67. Wang, Z.Y., Wang, Q.M., Chong, K., Wang, L., Bai., M.Y., Jia, C.G.: The brassinosteroid signal transduction pathway. - Cell Res. 16: 427-434, 2006. Go to original source...
  68. Weiss, D., Ori, N.: Mechanisms of cross talk between gibberellin and other hormones. - Plant Physiol. 144: 1240-1246, 2007. Go to original source...
  69. Wilen, R., Sacco, W., Gusta, M. L. V., Krishna, P.: Effects of 24-epibrassinolide on freezing and thermotolerance of bromegrass (Bromus inermis) cell cultures. - Physiol. Plant. 95: 195-202, 1995. Go to original source...
  70. Winter, J., Schneider, B., Meyenburg, S., Strack, D., Adam, G.: Monitoring brassinosteroid biosynthetic enzymes by fluorescent tagging and HPLC analysis of their substrates and products. - Phytochemistry 51: 237-242, 1999. Go to original source...
  71. Wu, X., Yao, X., Chen, J., Zhu, Z., Zhang, H., Zha, D.: Brassinosteroids protect photosynthesis and antioxidant system of eggplant seedlings from high-temperature stress. - Acta Physiol Plant. 36: 251-261, 2014b. Go to original source...
  72. Wu, X.X., He, J., Zhu, Z.W., Yang, S.J., Zha, D.S.: Protection of photosynthesis and antioxidative system by 24-epibrassinolide in Solanum melongena under cold stress. - Biol. Plant. 58: 185-188, 2014a. Go to original source...
  73. Xia, X.-J., Huang, L.F., Zhou, Y.H., Mao, W.H., Shi, K., Wu, J.X., Asami, T., Chen, Z., Yu, J.Q.: Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. - Planta 230: 1185-1196, 2009b. Go to original source...
  74. Xia, X.-J., Wang, Y.-J., Zhou, Y.-H., Tao, Y., Mao, W.-H., Shi, K., Asami, T., Chen, Z., Yu, J.-Q.: Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. - Plant Physiol. 150: 801-814, 2009a. Go to original source...
  75. Xia, X.-J., Zhou, Y.-H., Shi, K., Zhou, J., Foyer, C.H., Yu, J. -, Q.: Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. - J. exp. Bot. 66: 2839-2856, 2015. Go to original source...
  76. Xia, X.-J., Fang, P.-P., Guo, X., Qian, X.-J., Zhou, J., Shi, K., Zhou, Y.-H., Yu, J.-Q.: Brassinosteroid-mediated apoplastic H2O2-glutaredoxin 12/14 cascade regulates antioxidant capacity in response to chilling in tomato. - Plant Cell Environ. 2017: 1-13, 2017. Go to original source...
  77. Yang, G, Komatsu, S.: Microarray and proteomic analysis of brassinosteroid - and gibberellin-regulated gene and protein expression in rice. - Genomics Proteomics Bioinfor. 2: 77-83, 2004. Go to original source...
  78. Yang, C.-J., Zhang, C., Lu, Y.-N., Jin, J.-Q., Wang, X.-L.: The mechanisms of brassinosteroids' action: from signal transduction to plant development. - Mol. Plants 4: 588-600, 2011. Go to original source...
  79. Yang, S., Maeshima, M., Tanaka, Y., Komatsu, S.: Modulation of vacuolar H+ -pumps and aquaporin by phytohormones in rice seedling leaf sheaths. - Biol. pharmacol. Bull. 26: 88-92, 2003. Go to original source...
  80. Yokota, T., Ogino, Y., Takahashi, N., Saimoto, H., Fujioka, S., Sakurai, A.: Brassinolide is biosynthesized from castasterone in Catharanthus roseus crown gall cells. - Agr. Biol. Chem. 54: 1107-1108, 1990. Go to original source...
  81. Yoshizawa, E., Kaizuka, M., Yamagami, A., Higuchi-Takeuchi, M., Matsui, M., Kakei, Y., Shimada, Y., Sakuta, M., Osada, H., Asami, T., Nakano, T.: BPG3 is a novel chloroplast protein that involves the greening of leaves and related to brassinosteroid signaling. - Biosci. Biotechnol. Biochem. 78: 420-429, 2014. Go to original source...
  82. Yu, J.Q., Huang, L.F., Hu, W.H., Zhou, Y.H., Mao, W.H., Ye, S.F., Nogués, S.: A role for brassinosteroids in the regulation of photosynthesis in Cucumis sativus. - J. exp. Bot. 55: 1135-1143, 2004. Go to original source...
  83. Yuan, L., Shu, S., Sun, J., Guo, S., Tezuka, T.: Effects of 24-epibrassinolide on the photosynthetic characteristics, antioxidant system, and chloroplast ultrastructure in Cucumis sativus L. under Ca(NO3)2 stress. - Photosynth. Res. 112: 205-214, 2012. Go to original source...
  84. Zhang, S., Wei, Y., Lu, Y., Wang, X.: Mechanisms of brassinosteroids interacting with multiple hormones. - Plant Signal. Behav. 4: 1117-1120, 2009. Go to original source...
  85. Zhang, Y.P., He, J., Yang, S.J., Chen, Y.Y.: Exogenous 24-epibrassinolide ameliorates high temperature-induced inhibition of growth and photosynthesis in Cucumis melo. - Biol. Plant. 58: 311-318, 2014. Go to original source...
  86. Zhang, Y.P., Zhu, X.H., Ding, H.D., Yang, S.J., Chen, Y.Y.: Foliar application of 24-epibrassinolide alleviates hightemperature- induced inhibition of photosynthesis in seedlings of two melon cultivars. - Photosynthetica 51: 341-349, 2013. Go to original source...