Advertisement

Emerging Trends on Crosstalk of BRS with Other Phytohormones

  • Puja Ohri
  • Renu Bhardwaj
  • Ravinderjit Kaur
  • Shivam Jasrotia
  • Ripu Daman Parihar
  • Anjali Khajuria
  • Nandni Sharma
Chapter

Abstract

Brassinosteroids (BRs), a class of steroidal hormones, play diverse roles in plant growth, development, signaling and defense against various biotic and abiotic stresses. It is broad spectrum key regulator in plants that participates in various molecular processes. Exogenous application of BRs vanish various constrains in the path of agricultural development. The present book chapter highlights the interaction and crosstalk of brassinosteroids with other phytohormones such as auxins, gibberellins, jasmonic acid, abscisic acid, salicylic acid, polyamines, ethylene and strigolactones in regulation of various physiological and developmental processes in plants. Various pathways reveal the versatile role of brassinosteroids in various hormonal interactions.

Keywords

Brassinosteroids Phytohormones Crosstalk Signaling 

References

  1. Ahammed, G. J., Zhou, Y. H., Xia, X. J., Mao, W. H., Shi, K., & Yu, J. Q. (2013). Brassinosteroid regulates secondary metabolism in tomato towards enhanced tolerance to phenanthrene. Biologia Plantarum, 57, 154–158.CrossRefGoogle Scholar
  2. Ahammed, G. J., Xia, X. J., Li, X., Shi, K., Yu, J. Q., & Zhou, Y. H. (2014). Role of brassinosteroid in plant adaptation to abiotic stresses and its interpay with other hormones. Current Protein and Peptide Science, 16, 462–473.CrossRefGoogle Scholar
  3. Ahmad, F., Singh, A., & Kamal, A. (2017). Ameliorative effect of salicylic acid in salinity stressed Pisum sativum by improving growth parameters, activating photosynthesis and enhancing antioxidant defense system. Bioscience Biotechnology Research Communications, 10, 481–490.Google Scholar
  4. Ahmad, F., Singh, A., & Kamal, A. (2018). Crosstalk of brassinosteroids with other phytohormones under various abiotic stresses. Journal of Applied Biology and Biotechnology, 6, 56–62.Google Scholar
  5. Aljbory, Z., & Chen, M. S. (2018). Indirect plant defense against insect herbivores: A review. Insect Sci, 25, 2–23.PubMedCrossRefGoogle Scholar
  6. Andres-Colas, N., Sancenon, V., Rodriguez-Navarro, S., Mayo, S., Thiele, D. J., Ecker, J. R., Puig, S., & Penarrubia, L. (2006). The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots. The Plant Journal, 45, 225–236.PubMedCrossRefGoogle Scholar
  7. Anwar, R., Mattoo, A. K., & Handa, A. K. (2015). Polyamine interactions with plant hormones: Crosstalk at several levels. Polyamines (pp. 267–302). Tokyo: Springer.Google Scholar
  8. Bai, M. Y., Shang, J. X., Oh, E., Fan, M., Bai, Y., Zentella, R., Sun, T. P., & Wang, Z. Y. (2012). Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nature Cell Biology, 14, 810–817.PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bajguz, A. (2010). An enhancing effect of exogenous brassinolide on the growth and antioxidant activity in Chlorella vulgaris cultures under heavy metals stress. Environmental and Experimental Botany, 68, 175–179.CrossRefGoogle Scholar
  10. Bajguz, A., & Hayat, S. (2009). Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiology and Biochemistry, 47, 1–8.PubMedCrossRefGoogle Scholar
  11. Banerjee, A., & Roychoudhury, A. (2018). Interactions of brassinosteroids with major phytohormones: Antagonistic effects. Journal of Plant Growth Regulation, 37(4), 1025–1032.  https://doi.org/10.1007/s00344-018-9828-5.CrossRefGoogle Scholar
  12. Bao, F., Shen, J., Brady, S. R., Muday, G. K., Asami, T., & Yang, Z. (2004). Brassinosteroids interact with auxin to promote lateral root development in Arabidopsis. Plant Physiology, 134, 1624–1631.PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bari, R., & Jones, J. D. G. (2009). Role of plant hormones in plant defence responses. Plant Molecular Biology, 69, 473–488.PubMedCrossRefGoogle Scholar
  14. Benkova, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertova, D., Jurgens, G., & Friml, J. (2003). Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell, 115, 591–602.PubMedCrossRefGoogle Scholar
  15. Bhalerao, R. P., Eklof, J., Ljung, K., Marchant, A., Bennett, M., & Sandberg, G. (2002). Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. The Plant Journal, 29, 325–332.PubMedCrossRefGoogle Scholar
  16. Buer, C. S., Sukumar, P., & Muday, G. K. (2006). Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis. Plant Physiology, 140, 1384–1396.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Campos, M. L., DeAlmeida, M., Rossi, M. L., Martinelli, A. P., Junior, C. G., Figueira, A., Rampelotti-Ferreira, F. T., Vendramim, J. D., Benedito, V. A., & Peres, L. E. (2009). Brassinosteroids interact negatively with jasmonates in the formation of anti-herbivory traits in tomato. Journal of Experimental Botany, 60, 4347–4361.PubMedCrossRefGoogle Scholar
  18. Casimiro, I., Marchant, A., Bhalerao, R. P., Beeckman, T., Dhooge, S., Swarup, R., Graham, N., Inzé, D., Sandberg, G., Casero, P. J., & Bennett, M. (2001). Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell, 13, 843–852.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Chaiwanon, J., & Wang, Z. Y. (2015). Spatiotemporal brassinosteroid signaling and antagonism with auxin pattern stem cell dynamics in Arabidopsis roots. Current Biology, 25, 1031–1042.PubMedCrossRefGoogle Scholar
  20. Choudhary, S. P., Oral, H. V., Bhardwaj, R., Yu, J. Q., & Tran, L. S. P. (2012). Interaction of brassinosteroids and polyamines enhances copper stress tolerance in Raphanus sativus. Journal of Experimental Botany, 63, 5659–5675.PubMedPubMedCentralCrossRefGoogle Scholar
  21. Chung, Y., Maharjan, P. M., Lee, O., Fujioka, S., Jang, S., Kim, B., Takatsuto, S., Tsujimoto, M., Kim, H., Cho, H., Hwang, I., & Choe, S. (2011). Auxin stimulates DWARF4 expression and brassinosteroid biosynthesis in Arabidopsis. The Plant Journal, 66, 564–578.PubMedCrossRefGoogle Scholar
  22. Çoban, O., & Göktürk Baydar, N. (2016). Brassinosteroid effects on some physical and biochemical properties and secondary metabolite accumulation in peppermint (Mentha piperita L.) under salt stress. Industrial Crops and Products, 86, 251–258.CrossRefGoogle Scholar
  23. De Vleesschauwer, D., Buyten, V. E., Satoh, K., Balidion, J., Mauleon, R., Choi, I. I.-R., Vera-Cruz, C., Kikuchi, S., & Hofte, M. (2012). Brassinosteroids antagonize gibberellin– and salicylate-mediated root immunity in rice. Plant Physiology, 158, 1833–1846.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Divi, U. K., Rahman, T., & Krishna, P. (2010). Brassinosteroid mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biology, 10, 151.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Feng, Z., Wu, C., Wang, C., Roh, J., Zhang, L., Chen, J., Zhang, S., Zhang, H., Yang, C., Hu, J., You, X., Liu, X., Yang, X., Guo, X., Zhang, X., Wu, F., Terzaghi, W., Kim, S.-K., Jiang, L., & Wan, J. (2016). SLG controls grain size and leaf angle by modulating brassinosteroid homeostasis in rice. Journal of Experimental Botany, 67, 4241–4253.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Ferguson, B. J., Ross, J. J., & Reid, J. B. (2005). Nodulation phenotypes of gibberellin and brassinosteroid mutants of pea. Plant Physiology, 138, 2396–2405.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Finkelstein, R., Reeves, W., Ariizumi, T., & Steber, C. (2008). Molecular aspects of seed dormancy. Annual Review of Plant Biology, 59, 387–415.PubMedCrossRefGoogle Scholar
  28. Foo, E., & Davies, N. W. (2011). Strigolactones promote nodulation in pea. Planta, 234, 1073–1081.PubMedCrossRefGoogle Scholar
  29. Foo, E., Ferguson, B. J., & Reid, J. B. (2014). The potential roles of strigolactones and brassinosteroids in the autoregulation of nodulation pathway. Annals of Botany, 113, 1037–1045.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Gallego-Bartolome, J., Minguet, E. G., Grau-Enguix, F., Abbas, M., Locascio, A., Thomas, S. G., Alabadi, D., & Blazquez, M. A. (2012). Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proceedings of the National Academy of Sciences, 109, 13446–13451.CrossRefGoogle Scholar
  31. Hao, J., Yin, Y., & Fei, S.-Z. (2013). Brassinosteroid signaling network: Implications on yield and stress tolerance. Plant Cell Reports, 32, 1017–1030.PubMedCrossRefGoogle Scholar
  32. He, Y., Zhang, H., Sun, Z., Li, J., Hong, G., Zhu, Q., Zhou, X., MacFarlane, S., Yan, F., & Chen, J. (2017). Jasmonic acid-mediated defense suppresses brassinosteroid-mediated susceptibility to rice black streaked dwarf virus infection in rice. The New Phytologist, 214, 388–399.PubMedCrossRefGoogle Scholar
  33. 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, 4394–4408.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Hu, S., Wang, C., Sanchez, D. L., Lipka, A. E., Liu, P., Yin, Y., Blanco, M., & Lubberstedt, T. (2017). Gibberellins promote brassinosteroids action and both increase heterosis for plant height in maize (Zea mays L.). Frontiers in Plant Science, 8, 1039.PubMedPubMedCentralCrossRefGoogle Scholar
  35. Huangfu, J., Li, J., Li, R., Ye, M., Kuai, P., Zhang, T., & Lou, Y. (2016). The transcription factor OsWRKY45 negatively modulates the resistance of rice to the brown plant hopper Nilaparvata lugens. International Journal of Molecular Sciences, 17, 697.PubMedCentralCrossRefPubMedGoogle Scholar
  36. Kim, T. W., Guan, S., Burlingame, A. L., & Wang, Z. Y. (2011). The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2. Molecular Cell, 43, 561–571.PubMedPubMedCentralCrossRefGoogle Scholar
  37. Kim, T. W., Michniewicz, M., Bergmann, D. C., & Wang, Z. Y. (2012). Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature, 482, 419.PubMedPubMedCentralCrossRefGoogle Scholar
  38. Kim, B., Fujioka, S., Kwon, M., Jeon, J., & Choe, S. (2013). Arabidopsis brassinosteroid-overproducing gulliver3-D/dwarf4-D mutants exhibit altered responses to jasmonic acid and pathogen. Plant Cell Reports, 32, 1139–1149.PubMedCrossRefGoogle Scholar
  39. Kim, J., Dotson, B., Rey, C., Lindsey, J., Bleecker, A. B., Binder, B. M., & Patterson, S. E. (2018). New clothes for the jasmonic acid receptor COI1: Delayed abscission, meristem arrest and apical dominance. PLoS One, 8, e60505.CrossRefGoogle Scholar
  40. Kitanaga, Y., Jian, C., Hasegawa, M., Yazaki, J., Kishimoto, N., Kikuchi, S., Nakamura, H., Ichikawa, H., Asami, T., 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. Bioscience, Biotechnology, and Biochemistry, 70, 2410–2419.PubMedCrossRefGoogle Scholar
  41. Kohli, S. K., Handa, N., Sharma, A., Gautam, V., Arora, S., Bhardwaj, R., Nasser, M., Alyemeni, Wijaya, L., & Ahmad, P. (2018). Combined effect of 24-epibrassinolide and salicylic acid mitigates lead (Pb) toxicity by modulating various metabolites in Brassica juncea L. seedlings. Protoplasma, 255, 11–24.PubMedCrossRefGoogle Scholar
  42. Li, Q.-F., & He, J.-X. (2013). Mechanisms of signaling crosstalk between brassinosteroids and gibberellins. Digestive Plant Signal Behavior, 8, e24686.CrossRefGoogle Scholar
  43. Li, Q.-F., Wang, C., Jiang, L., Li, S., Sun, S. S., & He, J.-X. (2012). An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in Arabidopsis. Science Signaling, 5, ra72.PubMedGoogle Scholar
  44. Li, X., Ahammed, G. J., Li, Z.-X., Zhang, L., Wei, J.-P., Shen, C., Yan, P., Zhang, L.-P., & Han, W.-Y. (2016). Brassinosteroids improve quality of summer tea (Camellia sinensis L.) by balancing biosynthesis of polyphenols and amino acids. Frontiers in Plant Science, 7, 1–9.Google Scholar
  45. Li, X., Zhang, L., Ahammed, G. J., Li, Z.-X., Wei, J.-P., Shen, C., Yan, P., Zhang, L.-P., & Han, W.-Y. (2017). Nitric oxide mediates brassinosteroid-induced flavonoid biosynthesis in Camellia sinensis L. Journal of Plant Physiology, 214, 145–151.PubMedCrossRefGoogle Scholar
  46. Li, Q.-F., Lu, J., Yu, J. W., Zhang, C.-Q., He, J.-X., & Liu, Q.-Q. (2018a). The brassinosteroid-regulated transcription factors BZR1/BES1 function as a coordinator in multisignal-regulated plant growth. Biochimica et Biophysica Acta-Gene Regulatory Mechanisms, 1861, 561–571.PubMedCrossRefGoogle Scholar
  47. Li, W., Nishiyama, R., Watanabe, Y., Ha, C. V., Kojima, M., An, P., Tian, L., Tian, C., Sakakibara, H., & Tran, L.-S. P. (2018b). Effects of overproduced ethylene on the contents of other phytohormones and expression of their key biosynthetic genes. Plant Physiology and Biochemistry, 128, 170–177.PubMedCrossRefGoogle Scholar
  48. Liu, J., Lovisolo, C., Schubert, A., & Cardinale, F. (2013). Signaling role of strigolactones at the interface between plants, (micro) organisms, and a changing environment. Journal of Plant Interactions, 8, 17–33.CrossRefGoogle Scholar
  49. López-Gómez, M., Castellanos, J. H., Lluch, C., & Herrera-Cervera, J. A. (2016). 24-Epibrassinolide ameliorates salt stress effects in the symbiosis Medicago truncatula-Sinorhizobium meliloti and regulates the nodulation in cross-talk with polyamines. Plant Physiology and Biochemistry, 108, 212–221.PubMedCrossRefGoogle Scholar
  50. Maharjan, P. M., Schulz, B., & Choe, S. (2011). BIN2/DWF12 antagonistically transduces brassinosteroid and auxin signals in the roots of Arabidopsis. Journal of Plant Biology, 54, 126–134.CrossRefGoogle Scholar
  51. Mazorra, L. M., Oliveira, M. G., Souza, A. F., da Silva, W. B., dos Santos, G. M., da Silva, L. R. A., da Silva, M. G., Bartoli, C. G., & de Oliveira, G. (2013). Involvement of brassinosteroids and ethylene in the control of mitochondrial electron transport chain in postharvest papaya fruit. Theoretical and Experimental Plant Physiology, 25, 203–212.CrossRefGoogle Scholar
  52. Mouchel, C. F., Osmont, K. S., & Hardtke, C. S. (2006). BRX mediates feedback between brassinosteroid levels and auxin signaling in root growth. Nature, 443, 458–461.PubMedCrossRefGoogle Scholar
  53. Nahar, K., Kyndt, T., Hause, B., Höfte, M., & Gheysen, G. (2013). Brassinosteroids suppress rice defense against root-knot nematodes through antagonism with the jasmonate pathway. Molecular Plant-Microbe Interactions, 26, 106–115.PubMedCrossRefGoogle Scholar
  54. Nakashita, H., Yasuda, M., Nitta, T., Asami, T., Fujioka, S., Arai, Y., Sekimata, K., Takatsuto, S., Yamaguchi, I., & Yoshida, S. (2003). Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. The Plant Journal, 33, 887–898.PubMedCrossRefGoogle Scholar
  55. Nemhauser, J. L., Hong, F., & Chory, J. (2006). Different plant hormones regulate similar processes through largely non overlapping transcriptional responses. Cell, 126, 467–475.PubMedCrossRefGoogle Scholar
  56. Oh, E., Zhu, J. Y., Bai, M. Y., Arenhart, R. A., Sun, Y., & Wang, Z. Y. (2014). Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. eLife, 3, e03031.PubMedCentralCrossRefPubMedGoogle Scholar
  57. Ohri, P., Bhardwaj, R., Bali, S., Kaur, R., Jasrotia, S., Khajuria, A., & Parihar, R. D. (2015). The common molecular players in plant hormone crosstalk and signaling. Current Protein & Peptide Science, 16, 369–388.CrossRefGoogle Scholar
  58. Pál Magda, C. G., Szalai, G., Oláh, T., Khalil, R., Yordanova, R., Gell, G., Birinyi, Z., Németh, E., & Janda, T. (2017). Polyamines may influence phytochelatin synthesis during Cd stress in rice. Journal of Hazardous Materials, 340, 272–280.PubMedCrossRefGoogle Scholar
  59. Pan, G., Liu, Y., Ji, L., Zhang, X., He, J., Huang, J., Qiu, Z., Liu, D., Sun, Z., Xu, T., Liu, L., Wang, C., Jiang, L., Cheng, X., & Wan, J. (2018). Brassinosteroids mediate susceptibility to brown planthopper by integrating with the salicylic acid and jasmonic acid pathways in rice. Journal of Experimental Botany, 69, 4433–4442.PubMedPubMedCentralCrossRefGoogle Scholar
  60. Peng, Z., Han, C., Yuan, L., Zhang, K., Huang, H., & Ren, C. (2011). Brassinosteroid enhances jasmonate-induced anthocyanin accumulation in Arabidopsis seedlings. Journal of Integrative Plant Biology, 53, 632–640.PubMedCrossRefGoogle Scholar
  61. Per, T. S., Khan, M. I. R., Anjum, N. A., Masood, A., Hussain, S. J., & Khan, N. A. (2018). Jasmonates in plants under abiotic stresses: Crosstalk with other phytohormones matters. Environmental and Experimental Botany, 145, 104–120.CrossRefGoogle Scholar
  62. Ren, C., Han, W., Peng, Y., Huang, Z., Peng, X., Xiong, Q., Zhu, B., Gao, D., & Xie, A. (2009). Leaky mutation in DWARF4 reveals an antagonistic role of brassinosteroid in the inhibition of root growth by jasmonate in Arabidopsis. Plant Physiology, 151, 1412–1420.PubMedPubMedCentralCrossRefGoogle Scholar
  63. Ryu, H., Cho, H., Bae, W., & Hwang, I. (2014). Control of early seedling development by BES1/TPL/HDA19-mediated epigenetic regulation of ABI3. Nature Communications, 5, 4138.PubMedCrossRefGoogle Scholar
  64. Saini, S., Sharma, I., Kaur, N., & Pati, P. K. (2013). Auxin: A master regulator in plant root development. Plant Cell Reports, 32, 741–757.PubMedCrossRefGoogle Scholar
  65. Saini, S., Sharma, I., & Pati, P. K. (2015). Versatile roles of brassinosteroid in plants in the context of its homoeostasis, signaling and crosstalks. Frontiers in Plant Science, 6, 950.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Sharma, I., Bhardwaj, R., & Pati, P. K. (2015). Exogenous application of 28- Homobrassinolide modulates the dynamics of salt and pesticides induced stress responses in an elite rice variety Pusa Basmati-1. Journal of Plant Growth Regulation, 34, 509–518.CrossRefGoogle Scholar
  67. Soto, M. J., Fernandez-Aparicio, M., Castellanos-Morales, V., Garcia-Garrido, J. A., Delgado, M. J., & Vierheilig, H. (2010). First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biology and Biochemistry, 42, 383–385.CrossRefGoogle Scholar
  68. Sreeramulu, S., Mostizky, Y., Sunitha, S., Shani, E., Nahum, H., Salomon, D., Hayun, L. B., Gruetter, C., Rauh, D., Ori, N., & Sessa, G. (2013). BSKs are partially redundant positive regulators of brassinosteroid signaling in Arabidopsis. The Plant Journal, 74, 905–919.PubMedCrossRefGoogle Scholar
  69. Steber, C. M., & McCourt, P. (2001). A role for brassinosteroids in germination in Arabidopsis. Plant Physiology, 125, 763–769.PubMedPubMedCentralCrossRefGoogle Scholar
  70. Stewart Lilley, J. L., Gan, Y., Graham, I. A., & Nemhauser, J. L. (2013). The effect of DELLAs on growth change with developmental stage and brassinosteroid levels. The Plant Journal, 76, 165–173.PubMedGoogle Scholar
  71. Sun, T. P. (2011). The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Current Biology, 21, R338–R345.PubMedCrossRefGoogle Scholar
  72. Sun, Y., Fan, X. Y., Cao, D. M., Tang, W., He, K., Zhu, J. Y., He, J.-X., Bai, M.-Y., Zhu, S., Oh, E., Patil, S., Kim, T.-W., Ji, H., Wong, W. H., Rhee, S. Y., & Wang, Z.-Y. (2010). Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Developmental Cell, 19, 765–777.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 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 Physiology, 138, 1117–1125.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 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, 4376–4393.PubMedPubMedCentralCrossRefGoogle Scholar
  75. Ueguchi-Tanaka, M., Nakajima, M., Motoyuki, A., & Matsuoka, M. (2007). Gibberellin receptor and its role in gibberellin signaling in plants. Annual Review of Plant Biology, 58, 183–198.PubMedCrossRefGoogle Scholar
  76. Unterholzner, S. J., Rozhon, W., & Papacek, M. (2015). Brassinosteroids are master regulators of gibberellin biosynthesis in Arabidopsis. Plant Cell, 27, 2261–2272.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Vandenbussche, F., Callebert, P., Zadnikova, P., Benkova, E., & Van Der Straeten, D. (2013). Brassinosteroid control of shoot gravitropism interacts with ethylene and depends on auxin signaling components. American Journal of Botany, 100, 215–225.PubMedCrossRefGoogle Scholar
  78. Vanlerberghe, G. C. (2013). Alternative oxidase: A mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. International Journal of Molecular Sciences, 14, 6805–6847.PubMedPubMedCentralCrossRefGoogle Scholar
  79. Vanstraelen, M., & Benkova, E. (2012). Hormonal interactions in the regulation of plant development. Annual Review of Cell and Developmental Biology, 28, 463–487.PubMedCrossRefGoogle Scholar
  80. Vert, G., Walcher, C. L., Chory, J., & Nemhauser, J. L. (2008). Integration of auxin and brassinosteroid pathways by Auxin response factor2. Proceedings of the National Academy of Sciences, 105, 9829–9834.CrossRefGoogle Scholar
  81. Vukašinović, N., & Russinova, E. (2018). BRexit: Possible brassinosteroid export and transport routes. Trends in Plant Science, 23, 285–292.PubMedCrossRefGoogle Scholar
  82. Wang, Y., Sun, S., Zhu, W., Jia, K., Yang, H., & Wang, X. (2013). Strigolactone/MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. Developmental Cell, 27, 681–688.PubMedCrossRefGoogle Scholar
  83. Wang, H., Tang, J., Liu, J., Hu, J., Liu, J., Chen, Y., Cai, Z., & Wang, X. (2018). Abscisic acid signaling inhibits brassinosteroid signaling through dampening the dephosphorylation of BIN2 by ABI1 and ABI2. Molecular Plant, 11, 315–325.PubMedCrossRefGoogle Scholar
  84. Yang, C. J., Zhang, C., Lu, Y. N., Jin, J. Q., & Wang, X. L. (2011). The mechanisms of brassinosteroids’ action: From signal transduction to plant development. Molecular Plant, 4, 588–600.PubMedCrossRefGoogle Scholar
  85. 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 & Environment, 39, 1994–2003.CrossRefGoogle Scholar
  86. Ye, H., Li, L., & Yin, Y. (2011). Recent advances in the regulation of brassinosteroid signaling and biosynthesis pathways. Journal of Integrative Plant Biology, 53, 455–468.PubMedCrossRefGoogle Scholar
  87. Yin, Y., Wang, Z. Y., Mora-Garcia, S., Li, J., Yoshida, S., Asami, T., & Chory, J. (2002). BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell, 109, 181–191.PubMedCrossRefGoogle Scholar
  88. Yoshimitsu, Y., Tanaka, K., Fukuda, W., Asami, T., Yoshida, S., Hayashi, K., Kamiya, Y., Jikumaru, Y., Shigeta, T., Nakamura, Y., & Matsuo, T. (2011). Transcription of DWARF4 plays a crucial role in auxin regulated root elongation in addition to brassinosteroid homeostasis in Arabidopsis thaliana. PLoS One, 6, e23851.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Youn, J. H., Kim, M. K., Kim, E. J., Son, S. H., Lee, J. E., Jang, M. S., Kim, T. W., & Kim, S. K. (2016). ARF7 increases the endogenous contents of castasterone through suppression of BAS1 expression in Arabidopsis thaliana. Phytochemistry, 122, 34–44.PubMedCrossRefGoogle Scholar
  90. Youn, J. H., Kim, T. W., Joo, S. H., Son, S. H., Roh, J., Kim, S., Kim, T. W., & Kim, S. K. (2018). Function and molecular regulation of DWARF1 as a C-24 reductase in brassinosteroid biosynthesis in Arabidopsis. Journal of Experimental Botany, 69, 1873–1886.PubMedPubMedCentralCrossRefGoogle Scholar
  91. Zhang, S., Cai, Z., & Wang, X. (2009). The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling. Proceedings of the National Academy of Sciences, 106, 4543–4548.CrossRefGoogle Scholar
  92. Zhou, J., Wang, J., Li, X., Xia, X.-J., Zhou, Y.-H., Shi, K., Chen, Z., & Yu, J.-Q. (2014). H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses. Journal of Experimental Botany, 65, 4371–4383.PubMedPubMedCentralCrossRefGoogle Scholar
  93. Zhu, T., Deng, X., Zhou, X., Zhu, L., Zou, L., Li, P., Zhang, D., & Lin, H. (2016). Ethylene and hydrogen peroxide are involved in brassinosteroids-induced salt tolerance in tomato. Scientific Reports, 6, 35392.PubMedPubMedCentralCrossRefGoogle Scholar
  94. Zhu, X. F., Yuan, D., Zhang, C., Li, T. Y., & Xuan, Y. H. (2018). RAVL1, an upstream component of brassinosteroid signaling and biosynthesis, regulates ethylene signaling via activation of EIL1 in rice. Plant Biotechnology Journal, 16, 1399–1401.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Puja Ohri
    • 1
  • Renu Bhardwaj
    • 2
  • Ravinderjit Kaur
    • 3
  • Shivam Jasrotia
    • 1
  • Ripu Daman Parihar
    • 4
  • Anjali Khajuria
    • 1
  • Nandni Sharma
    • 1
  1. 1.Department of ZoologyGuru Nanak Dev UniversityAmritsarIndia
  2. 2.Department of Botanical and Environmental SciencesGuru Nanak Dev UniversityAmritsarIndia
  3. 3.Department of ZoologySR Government College for GirlsAmritsarIndia
  4. 4.Department of ZoologyDAV UniversityJalandharIndia

Personalised recommendations