Advertisement

Brassinosteroid Regulated Physiological Process: An Omics Perspective

  • Husna Siddiqui
  • Fareen Sami
  • H. F. JuanEmail author
  • Shamsul Hayat
Chapter

Abstract

Transcriptomes is referred to an entire set of transcripts and their number present in a cell at a particular developmental phase or physiological state. Study of the transcriptome is necessary to identify different genes and their functions, and elucidating various signalling pathways. The key intend of transcriptomics is to index all sort of transcripts (coding and non-coding RNAs) to establish the transcriptional organization of genes. Genes act as blueprint whereas proteins act as a functional unit of cell that is regulated by gene expression/repression. Proteomics is a broad scale analysis of a complete set of proteins (proteome) in a cell, tissue or organ at a particular time. As proteins are final product of a gene they are closer to the function as compared to genes. Hence, this “omics” study will facilitate more rapid advancement in understanding of different biochemical pathways of plants. Brassinosteroids (BRs), a class of plant hormone regulates various developmental and physiological processes. This chapter deal with the application of transcriptomics and proteomics to elucidate the hormonal targets for growth and development of plants.

Keywords

Brassinosteroids Transcriptome Proteome Plant physiology Phytohormones 

References

  1. Ahammed, G., Xia, X. J., Li, X., Shi, K., Yu, J. Q., & Zhou, Y. H. (2015). Role of brassinosteroid in plant adaptation to abiotic stresses and its interplay with other hormones. Current Protein & Peptide Science, 16, 462–473.CrossRefGoogle Scholar
  2. Ahsan, N., Donnart, T., Nouri, M. Z., & Komatsu, S. (2010). Tissue-specific defense and thermo-adaptive mechanisms of soybean seedlings under heat stress revealed by proteomic approach. Journal of Proteome Research, 9, 4189–4204.PubMedCrossRefGoogle Scholar
  3. Alabadí, D., Gil, J., Blázquez, M. A., & García-Martínez, J. L. (2004). Gibberellins repress photomorphogenesis in darkness. Plant Physiology, 134, 1050–1057.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Alfonso, P., Dolado, I., Swat, A., Núñez, A., Cuadrado, A., Nebreda, A. R., & Casal, J. I. (2007). Proteomic analysis of p38α MAP kinase-regulated changes in membrane fractions of Ras-transformed fibroblasts. In Regulation of malignant cell transformation by the stress-activated kinase (Vol. 6, pp. S262–S271).Google Scholar
  5. Allen, G. J., Chu, S. P., Schumacher, K., Shimazaki, C. T., Vafeados, D., Kemper, A., & Chory, J. (2000). Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science, 289, 2338–2342.PubMedCrossRefGoogle Scholar
  6. Bai, M. Y., Shang, J. X., Oh, E., Fan, M., Bai, Y., Zentella, R., & Wang, Z. Y. (2012). Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nature Cell Biology, 14, 810.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bajguz, A. (2009). Isolation and characterization of brassinosteroids from algal cultures of Chlorella vulgaris Beijerinck (Trebouxiophyceae). Journal of Plant Physiology, 166, 1946–1949.PubMedCrossRefGoogle Scholar
  8. 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
  9. Benjamins, R., & Scheres, B. (2008). Auxin: The looping star in plant development. Annual Review of Plant Biology, 59, 443–465.PubMedCrossRefGoogle Scholar
  10. Bernardo-García, S., de Lucas, M., Martínez, C., Espinosa-Ruiz, A., Davière, J. M., & Prat, S. (2014). BR-dependent phosphorylation modulates PIF4 transcriptional activity and shapes diurnal hypocotyl growth. Genes & Development, 28, 1681–1694.CrossRefGoogle Scholar
  11. Biesgen, C., & Weiler, E. W. (1999). Structure and regulation of OPR1 and OPR2, two closely related genes encoding 12-oxophytodienoic acid-10, 11-reductases from Arabidopsis thaliana. Planta, 208, 155–165.PubMedCrossRefGoogle Scholar
  12. Bouquin, T., Meier, C., Foster, R., Nielsen, M. E., & Mundy, J. (2001). Control of specific gene expression by gibberellin and brassinosteroid. Plant Physiology, 127, 450–458.PubMedPubMedCentralCrossRefGoogle Scholar
  13. Burla, B., Pfrunder, S., Nagy, R., Francisco, R. M., Lee, Y., & Martinoia, E. (2013). Vacuolar transport of abscisic acid glucosyl ester is mediated by ATP-binding cassette and proton-antiport mechanisms in Arabidopsis. Plant Physiology, 163, 1446–1458.PubMedPubMedCentralCrossRefGoogle Scholar
  14. Carter, C., Pan, S., Zouhar, J., Avila, E. L., Girke, T., & Raikhel, N. V. (2004). The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. The Plant Cell, 16, 3285–3303.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Casati, P., Zhang, X., Burlingame, A. L., & Walbot, V. (2005). Analysis of leaf proteome after UV-B irradiation in maize lines differing in sensitivity. Molecular & Cellular Proteomics, 4, 1673–1685.CrossRefGoogle Scholar
  16. 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
  17. Chung, Y., Maharjan, P. M., Lee, O., Fujioka, S., Jang, S., Kim, B., & Park, T. (2011). Auxin stimulates DWARF4 expression and brassinosteroid biosynthesis in Arabidopsis. The Plant Journal, 66, 564–578.PubMedCrossRefGoogle Scholar
  18. Clouse, S. D. (2011). Brassinosteroid signal transduction: From receptor kinase activation to transcriptional networks regulating plant development. The Plant Cell, 23, 1219–1230.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Cockcroft, S. (1998). Phosphatidylinositol transfer proteins: A requirement in signal transduction and vesicle traffic. Bio Essays, 20, 423–432.Google Scholar
  20. Coll-Garcia, D., Mazuch, J., Altmann, T., & Müssig, C. (2004). EXORDIUM regulates brassinosteroid-responsive genes. FEBS Letters, 563, 82–86.PubMedCrossRefGoogle Scholar
  21. Crafts-Brandner, S. J., & Salvucci, M. E. (2002). Sensitivity of photosynthesis in a C4 plant, maize, to heat stress. Plant Physiology, 129, 1773–1780.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Cui, J. X., Zhou, Y. H., Ding, J. G., Xia, X. J., Shi, K. A. I., Chen, S. C., & Yu, J. Q. (2011). Role of nitric oxide in hydrogen peroxide-dependent induction of abiotic stress tolerance by brassinosteroids in cucumber. Plant, Cell and Environment, 34, 347–358.PubMedCrossRefGoogle Scholar
  23. Deng, Z., Zhang, X., Tang, W., Oses-Prieto, J. A., Suzuki, N., Gendron, J. M., & Burlingame, A. L. (2007). A proteomics study of brassinosteroid response in Arabidopsis. Molecular & Cellular Proteomics, 6, 2058–2071.CrossRefGoogle Scholar
  24. Dhaubhadel, S., Chaudhary, S., Dobinson, K. F., & Krishna, P. (1999). Treatment with 24-epibrassinolide, a brassinosteroid, increases the basic thermotolerance of Brassica napus and tomato seedlings. Plant Molecular Biology, 40, 333–342.PubMedCrossRefGoogle Scholar
  25. 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
  26. Divi, U. K., Rahman, T., & Krishna, P. (2016). Gene expression and functional analyses in brassinosteroid-mediated stress tolerance. Plant Biotechnology Journal, 14, 419–432.PubMedCrossRefGoogle Scholar
  27. Du, L., & Poovaiah, B. W. (2005). Ca 2+/calmodulin is critical for brassinosteroid biosynthesis and plant growth. Nature, 437, 741.PubMedCrossRefGoogle Scholar
  28. Fariduddin, Q., Ahmad, A., Hayat, S., & Alvi, S. (2000). The response of chickpea, raised from the seeds pretreated with 28-homobrassinolide. In National seminar on plant physiological paradigm for fostering agro and biotechnology and augmenting environmental productivity in millennium (p. 134).Google Scholar
  29. Fedina, E. O., Karimova, F. G., Tarchevsky, I. A., Toropygin, I. Y., & Khripach, V. A. (2008). Effect of epibrassinolide on tyrosine phosphorylation of the Calvin cycle enzymes. Russian Journal of Plant Physiology, 55(2), 193–200.CrossRefGoogle Scholar
  30. Feng, L., Wang, K., Li, Y., Tan, Y., Kong, J., Li, H., & Zhu, Y. (2007). Overexpression of SBPase enhances photosynthesis against high temperature stress in transgenic rice plants. Plant Cell Reports, 26, 1635–1646.PubMedCrossRefGoogle Scholar
  31. Fujioka, S., & Yokota, T. (2003). Biosynthesis and metabolism of brassinosteroids. Annual Review of Plant Biology, 54, 137–164.PubMedCrossRefGoogle Scholar
  32. Fukuda, H. (1997). Tracheary element differentiation. The Plant Cell, 9, 1147.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Gallego-Bartolomé, J., Minguet, E. G., Grau-Enguix, F., Abbas, M., Locascio, A., Thomas, S. G., & Blázquez, 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
  34. Gendron, J. M., Liu, J. S., Fan, M., Bai, M. Y., Wenkel, S., Springer, P. S., & Wang, Z. Y. (2012). Brassinosteroids regulate organ boundary formation in the shoot apical meristem of Arabidopsis. Proceedings of the National Academy of Sciences, 109, 21152–21157.CrossRefGoogle Scholar
  35. Goda, H., Shimada, Y., Asami, T., Fujioka, S., & Yoshida, S. (2002). Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiology, 130, 1319–1334.PubMedPubMedCentralCrossRefGoogle Scholar
  36. Goda, H., Sawa, S., Asami, T., Fujioka, S., Shimada, Y., & Yoshida, S. (2004). Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiology, 134, 1555–1573.PubMedPubMedCentralCrossRefGoogle Scholar
  37. Griffin, T. J., Gygi, S. P., Ideker, T., Rist, B., Eng, J., Hood, L., & Aebersold, R. (2002). Complementary profiling of gene expression at the transcriptome and proteome levels in Saccharomyces cerevisiae. Molecular & Cellular Proteomics, 1, 323–333.CrossRefGoogle Scholar
  38. Guilfoyle, T. J., & Hagen, G. (2007). Auxin response factors. Current Opinion in Plant Biology, 10, 453–460.PubMedCrossRefGoogle Scholar
  39. Guo, H., Li, L., Ye, H., Yu, X., Algreen, A., & Yin, Y. (2009). Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, 106, 7648–7653.CrossRefGoogle Scholar
  40. Han, F., Chen, H., Li, X. J., Yang, M. F., Liu, G. S., & Shen, S. H. (2009). A comparative proteomic analysis of rice seedlings under various high-temperature stresses. Biochimica et Biophysica Acta, Proteins and Proteomics, 1794, 1625–1634.CrossRefGoogle Scholar
  41. Harrison, E. P., Willingham, N. M., Lloyd, J. C., & Raines, C. A. (1997). Reduced sedoheptulose-1, 7-bisphosphatase levels in transgenic tobacco lead to decreased photosynthetic capacity and altered carbohydrate accumulation. Planta, 204, 27–36.CrossRefGoogle Scholar
  42. Hayat, S., Ali, B., Hasan, S. A., & Ahmad, A. (2007). Brassinosteroid enhanced the level of antioxidants under cadmium stress in Brassica juncea. Environmental and Experimental Botany, 60, 33–41.CrossRefGoogle Scholar
  43. Hayat, S., Hasan, S. A., Hayat, Q., & Ahmad, A. (2010). Brassinosteroids protect Lycopersicon esculentum from cadmium toxicity applied as shotgun approach. Protoplasma, 239, 3–14.PubMedCrossRefGoogle Scholar
  44. He, J. X., Gendron, J. M., Sun, Y., Gampala, S. S., Gendron, N., Sun, C. Q., & Wang, Z. Y. (2005). BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science, 307, 1634–1638.PubMedPubMedCentralCrossRefGoogle Scholar
  45. Hou, Y., Qiu, J., Wang, Y., Li, Z., Zhao, J., Tong, X., et al. (2017). A quantitative proteomic analysis of Brassinosteroid-induced protein phosphorylation in Rice (Oryza sativa L.). Frontiers in Plant Science, 8, 514.PubMedPubMedCentralGoogle Scholar
  46. Howe, G. A., & Ryan, C. A. (1999). Suppressors of systemin signaling identify genes in the tomato wound response pathway. Genetics, 153, 1411–1421.PubMedPubMedCentralGoogle Scholar
  47. Hu, M. Y., Ming, L. U. O., Xiao, Y. H., Li, X. B., Tan, K. L., Lei, H. O. U., & Zang, Z. L. (2011). Brassinosteroids and auxin down-regulate DELLA genes in fiber initiation and elongation of cotton. Agricultural Sciences in China, 10, 1168–1176.CrossRefGoogle Scholar
  48. Huang, B., Chu, C. H., Chen, S. L., Juan, H. F., & Chen, Y. M. (2006). A proteomics study of the mung bean epicotyl regulated by brassinosteroids under conditions of chilling stress. Cellular & Molecular Biology Letters, 11(2), 264.CrossRefGoogle Scholar
  49. Huang, D., Wu, W., Abrams, S. R., & Cutler, A. J. (2008). The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. Journal of Experimental Botany, 59, 2991–3007.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Huber, M., Bahr, I., Krätzschmar, J. R., Becker, A., Müller, E. C., Donner, P., & Sommer, A. (2004). Comparison of proteomic and genomic analyses of the human breast cancer cell line T47D and the antiestrogen-resistant derivative T47D-r. Molecular & Cellular Proteomics, 3, 43–55.CrossRefGoogle Scholar
  51. Ideker, T., Thorsson, V., Ranish, J. A., Christmas, R., Buhler, J., Eng, J. K., & Hood, L. (2001). Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science, 292, 929–934.PubMedCrossRefGoogle Scholar
  52. Iliev, E. A., Xu, W., Polisensky, D. H., Oh, M. H., Torisky, R. S., Clouse, S. D., & Braam, J. (2002). Transcriptional and posttranscriptional regulation of Arabidopsis TCH4 expression by diverse stimuli. Roles of cis regions and brassinosteroids. Plant Physiology, 130, 770–783.PubMedPubMedCentralCrossRefGoogle Scholar
  53. Im, K. H., Cosgrove, D. J., & Jones, A. M. (2000). Subcellular localization of expansin mRNA in xylem cells. Plant Physiology, 123, 463–470.PubMedPubMedCentralCrossRefGoogle Scholar
  54. Ishiguro, S., Watanabe, Y., Ito, N., Nonaka, H., Takeda, N., Sakai, T., & Okada, K. (2002). SHEPHERD is the Arabidopsis GRP94 responsible for the formation of functional CLAVATA proteins. The EMBO Journal, 21, 898–908.PubMedPubMedCentralCrossRefGoogle Scholar
  55. Kolkman, A., Dirksen, E. H., Slijper, M., & Heck, A. J. (2005). Double standards in quantitative proteomics direct comparative assessment of difference in gel electrophoresis and metabolic stable isotope labeling. Molecular & Cellular Proteomics, 4, 255–266.CrossRefGoogle Scholar
  56. Konishi, H., & Komatsu, S. (2003). A proteomics approach to investigating promotive effects of brassinolide on lamina inclination and root growth in rice seedlings. Biological & Pharmaceutical Bulletin, 26, 401–408.CrossRefGoogle Scholar
  57. Kurepin, L. V., Qaderi, M. M., Back, T. G., Reid, D. M., & Pharis, R. P. (2008). A rapid effect of applied brassinolide on abscisic acid concentrations in Brassica napus leaf tissue subjected to short-term heat stress. Plant Growth Regulation, 55, 165–167.CrossRefGoogle Scholar
  58. Kwon, S. I., Cho, H. J., Jung, J. H., Yoshimoto, K., Shirasu, K., & Park, O. K. (2010). The Rab GTPase RabG3b functions in autophagy and contributes to tracheary element differentiation in Arabidopsis. The Plant Journal, 64, 151–164.PubMedGoogle Scholar
  59. Lee, M. W., Qi, M., & Yang, Y. (2001). A novel jasmonic acid-inducible rice myb gene associates with fungal infection and host cell death. Molecular Plant-Microbe Interactions, 14, 527–535.PubMedCrossRefGoogle Scholar
  60. Lee, D. G., Ahsan, N., Lee, S. H., Kang, K. Y., Bahk, J. D., Lee, I. J., & Lee, B. H. (2007). A proteomic approach in analyzing heat-responsive proteins in rice leaves. Proteomics, 7, 3369–3383.PubMedCrossRefGoogle Scholar
  61. Li, Q. F., & He, J. X. (2013). Mechanisms of signaling crosstalk between brassinosteroids and gibberellins. Plant Signaling & Behavior, 8, e24686.CrossRefGoogle Scholar
  62. Li, L., Staden, J. V., & Jäger, A. K. (1998). Effects of plant growth regulators on the antioxidant system in seedlings of two maize cultivars subjected to water stress. Plant Growth Regulation, 25, 81–87.CrossRefGoogle Scholar
  63. Li, X., Xie, Z., & Bankaitis, V. A. (2000). Phosphatidylinositol/phosphatidylcholine transfer proteins in yeast. Biochimica et Biophysica Acta, Molecular and Cell Biology of Lipids, 1486, 55–71.CrossRefGoogle Scholar
  64. Li, Y., Darley, C. P., Ongaro, V., Fleming, A., Schipper, O., Baldauf, S. L., & McQueen-Mason, S. J. (2002). Plant expansins are a complex multigene family with an ancient evolutionary origin. Plant Physiology, 128(3), 854–864.PubMedPubMedCentralCrossRefGoogle Scholar
  65. Li, C., Liu, G., Xu, C., Lee, G. I., Bauer, P., Ling, H. Q., & Howe, G. A. (2003). The tomato suppressor of prosystemin-mediated responses2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression. The Plant Cell, 15, 1646–1661.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Li, L., Xu, J., Xu, Z. H., & Xue, H. W. (2005). Brassinosteroids stimulate plant tropisms through modulation of polar auxin transport in Brassica and Arabidopsis. The Plant Cell, 17(10), 2738–2753.PubMedPubMedCentralCrossRefGoogle Scholar
  67. Li, Z. Y., Xu, Z. S., He, G. Y., Yang, G. X., Chen, M., Li, L. C., & Ma, Y. Z. (2012). A mutation in Arabidopsis BSK5 encoding a brassinosteroid-signaling kinase protein affects responses to salinity and abscisic acid. Biochemical and Biophysical Research Communications, 426, 522–527.PubMedCrossRefGoogle Scholar
  68. Li, J., Yang, P., Kang, J., Gan, Y., Yu, J., Calderón-Urrea, A., & Xie, J. (2016). Transcriptome analysis of pepper (Capsicum annuum) revealed a role of 24-epibrassinolide in response to chilling. Frontiers in Plant Science, 7, 1281.PubMedPubMedCentralGoogle Scholar
  69. Lin, L. L., Wu, C. C., Huang, H. C., Chen, H. J., Hsieh, H. L., & Juan, H. F. (2013). Identification of microRNA 395a in 24-epibrassinolide-regulated root growth of Arabidopsis thaliana using microRNA arrays. International Journal of Molecular Sciences, 14, 14270–14286.PubMedPubMedCentralCrossRefGoogle Scholar
  70. Lin, L. L., Hsu, C. L., Hu, C. W., Ko, S. Y., Hsieh, H. L., Huang, H. C., & Juan, H. F. (2015). Integrating phosphoproteomics and bioinformatics to study brassinosteroid-regulated phosphorylation dynamics in Arabidopsis. BMC Genomics, 16, 533.PubMedPubMedCentralCrossRefGoogle Scholar
  71. Lisso, J., Steinhauser, D., Altmann, T., Kopka, J., & Müssig, C. (2005). Identification of brassinosteroid-related genes by means of transcript co-response analyses. Nucleic Acids Research, 33(8), 2685–2696.PubMedPubMedCentralCrossRefGoogle Scholar
  72. Liu, G. T., Ma, L., Duan, W., Wang, B. C., Li, J. H., Xu, H. G., & Wang, L. J. (2014). Differential proteomic analysis of grapevine leaves by iTRAQ reveals responses to heat stress and subsequent recovery. BMC Plant Biology, 14, 110.PubMedPubMedCentralCrossRefGoogle Scholar
  73. Logan, D. C., Domergue, O., de la Serve, B. T., & Rossignol, M. (1997). A new family of plasma membrane polypeptides differentially regulated during plant development. IUBMB Life, 43, 1051–1062.CrossRefGoogle Scholar
  74. Maharjan, P. M., & Choe, S. (2011). High temperature stimulates DWARF4 (DWF4) expression to increase hypocotyl elongation in Arabidopsis. Journal of Plant Biology, 54, 425.CrossRefGoogle Scholar
  75. 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
  76. Majoul-Haddad, T., Bancel, E., Martre, P., Triboi, E., & Branlard, G. (2013). Effect of short heat shocks applied during grain development on wheat (Triticum aestivum L.) grain proteome. Journal of Cereal Science, 57, 486–495.CrossRefGoogle Scholar
  77. Marino, D., Dunand, C., Puppo, A., & Pauly, N. (2012). A burst of plant NADPH oxidases. Trends in Plant Science, 17, 9–15.PubMedCrossRefGoogle Scholar
  78. Marmagne, A., Rouet, M. A., Ferro, M., Rolland, N., Alcon, C., Joyard, J., & Ephritikhine, G. (2004). Identification of new intrinsic proteins in Arabidopsis plasma membrane proteome. Molecular & Cellular Proteomics, 3, 675–691.CrossRefGoogle Scholar
  79. Mei, C., Qi, M., Sheng, G., & Yang, Y. (2006). Inducible overexpression of a rice allene oxide synthase gene increases the endogenous jasmonic acid level, PR gene expression, and host resistance to fungal infection. Molecular Plant-Microbe Interactions, 19, 1127–1137.PubMedCrossRefGoogle Scholar
  80. Mouchel, C. F., Osmont, K. S., & Hardtke, C. S. (2006). BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature, 443, 458.PubMedCrossRefGoogle Scholar
  81. Muday, G. K., Rahman, A., & Binder, B. M. (2012). Auxin and ethylene: Collaborators or competitors? Trends in Plant Science, 17, 181–195.PubMedCrossRefGoogle Scholar
  82. Müssig, C., & Altmann, T. (2003). Genomic brassinosteroid effects. Journal of Plant Growth Regulation, 22, 313–324.PubMedCrossRefGoogle Scholar
  83. Müssig, C., Biesgen, C., Lisso, J., Uwer, U., Weiler, E. W., & Altmann, T. (2000). A novel stress-inducible 12-oxophytodienoate reductase from Arabidopsis thaliana provides a potential link between brassinosteroid-action and jasmonic-acid synthesis. Journal of Plant Physiology, 157, 143–152.CrossRefGoogle Scholar
  84. 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
  85. 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 Physiology, 140(2), 580–590.PubMedPubMedCentralCrossRefGoogle Scholar
  86. Nelson, C. J., Hegeman, A. D., Harms, A. C., & Sussman, M. R. (2006). A quantitative analysis of Arabidopsis plasma membrane using trypsin-catalyzed 18O labeling. Molecular & Cellular Proteomics, 5, 1382–1395.CrossRefGoogle Scholar
  87. Nemhauser, J. L., Mockler, T. C., & Chory, J. (2004). Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biology, 2, e258.PubMedPubMedCentralCrossRefGoogle Scholar
  88. Nie, S., Huang, S., Wang, S., Cheng, D., Liu, J., Lv, S., & Wang, X. (2017). Enhancing brassinosteroid signaling via overexpression of tomato (Solanum lycopersicum) SlBRI1 improves major agronomic traits. Frontiers in Plant Science, 8, 1386.PubMedPubMedCentralCrossRefGoogle Scholar
  89. O’Farrell, P. H. (1975). High resolution two-dimensional electrophoresis of proteins. The Journal of Biological Chemistry, 250, 4007–4021.PubMedPubMedCentralGoogle Scholar
  90. Oh, E., Zhu, J. Y., & Wang, Z. Y. (2012). Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nature Cell Biology, 14, 802.PubMedPubMedCentralCrossRefGoogle Scholar
  91. Ohashi-Ito, K., & Fukuda, H. (2010). Transcriptional regulation of vascular cell fates. Current Opinion in Plant Biology, 13, 670–676.PubMedCrossRefGoogle Scholar
  92. Ohashi-Ito, K., Kubo, M., Demura, T., & Fukuda, H. (2005). Class III homeodomain leucine-zipper proteins regulate xylem cell differentiation. Plant and Cell Physiology, 46, 1646–1656.PubMedCrossRefGoogle Scholar
  93. Paparella, S., Araújo, S. S., Rossi, G., Wijayasinghe, M., Carbonera, D., & Balestrazzi, A. (2015). Seed priming: State of the art and new perspectives. Plant Cell Reports, 34, 1281–1293.PubMedCrossRefGoogle Scholar
  94. 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 Biotechnology Journal, 9, 747–758.PubMedCrossRefGoogle Scholar
  95. Penfield, S., Rylott, E. L., Gilday, A. D., Graham, S., Larson, T. R., & Graham, I. A. (2004). Reserve mobilization in the Arabidopsis endosperm fuels hypocotyl elongation in the dark, is independent of abscisic acid, and requires PHOSPHOENOLPYRUVATE CARBOXYKINASE1. The Plant Cell, 16, 2705–2718.PubMedPubMedCentralCrossRefGoogle Scholar
  96. Peng, H., Zhao, J., & Neff, M. M. (2015). ATAF2 integrates Arabidopsis brassinosteroid inactivation and seedling photomorphogenesis. Development, 142, 4129–4138.PubMedCrossRefGoogle Scholar
  97. Peterman, T. K., Ohol, Y. M., McReynolds, L. J., & Luna, E. J. (2004). Patellin1, a novel Sec14-like protein, localizes to the cell plate and binds phosphoinositides. Plant Physiology, 136, 3080–3094.PubMedPubMedCentralCrossRefGoogle Scholar
  98. Phillips, S. E., Vincent, P., Rizzieri, K. E., Schaaf, G., Bankaitis, V. A., & Gaucher, E. A. (2006). The diverse biological functions of phosphatidylinositol transfer proteins in eukaryotes. Critical Reviews in Biochemistry and Molecular Biology, 41, 21–49.PubMedCrossRefGoogle Scholar
  99. Polko, J. K., Pierik, R., van Zanten, M., Tarkowská, D., Strnad, M., Voesenek, L. A., & Peeters, A. J. (2013). Ethylene promotes hyponastic growth through interaction with ROTUNDIFOLIA3/CYP90C1 in Arabidopsis. Journal of Experimental Botany, 64, 613–624.PubMedPubMedCentralCrossRefGoogle Scholar
  100. Raines, C. A. (2011). Increasing photosynthetic carbon assimilation in C3 plants to improve crop yield: Current and future strategies. Plant Physiology, 155, 36–42.PubMedCrossRefGoogle Scholar
  101. Rokka, A., Zhang, L., & Aro, E. M. (2001). Rubisco activase: An enzyme with a temperature-dependent dual function? The Plant Journal, 25, 463–471.PubMedCrossRefGoogle Scholar
  102. Rossignol, M., Peltier, J.-B., Mock, H.-P., Matros, A., Maldonado, A. M., & Jorrín, J. V. (2006). Plant proteome analysis: A 2004–2006 update. Proteomics, 6, 5529–5548.PubMedCrossRefGoogle Scholar
  103. Routt, S. M., & Bankaitis, V. A. (2004). Biological functions of phosphatidylinositol transfer proteins. Biochemistry and Cell Biology, 82, 254–262.PubMedCrossRefGoogle Scholar
  104. Rylott, E. L., Gilday, A. D., & Graham, I. A. (2003). The gluconeogenic enzyme phosphoenolpyruvate carboxykinase in Arabidopsis is essential for seedling establishment. Plant Physiology, 131, 1834–1842.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 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
  106. Salvucci, M. E., & Crafts-Brandner, S. J. (2004). Relationship between the heat tolerance of photosynthesis and the thermal stability of rubisco activase in plants from contrasting thermal environments. Plant Physiology, 134, 1460–1470.PubMedPubMedCentralCrossRefGoogle Scholar
  107. Sano, N., Kim, J. S., Onda, Y., Nomura, T., Mochida, K., Okamoto, M., & Seo, M. (2017). RNA-Seq using bulked recombinant inbred line populations uncovers the importance of brassinosteroid for seed longevity after priming treatments. Scientific Reports, 7, 8095.PubMedPubMedCentralCrossRefGoogle Scholar
  108. Sasse, J. (1999). Physiological actions of brassinosteroids. Brassinosteroids-Steroidal Plant Hormones, 1, 137–161.Google Scholar
  109. Sazer, S., & Dasso, M. (2000). The ran decathlon: Multiple roles of ran. Journal of Cell Science, 113, 1111–1118.PubMedGoogle Scholar
  110. Scafaro, A. P., Haynes, P. A., & Atwell, B. J. (2009). Physiological and molecular changes in Oryza meridionalis Ng., a heat-tolerant species of wild rice. Journal of Experimental Botany, 61, 191–202.PubMedCentralCrossRefPubMedGoogle Scholar
  111. Schomburg, F. M., Bizzell, C. M., Lee, D. J., Zeevaart, J. A., & Amasino, R. M. (2003). Overexpression of a novel class of gibberellin 2-oxidases decreases gibberellin levels and creates dwarf plants. The Plant Cell, 15, 151–163.PubMedPubMedCentralCrossRefGoogle Scholar
  112. Sechet, J., Frey, A., Effroy-Cuzzi, D., Berger, A., Perreau, F., Cueff, G., & Marion-Poll, A. (2016). Xyloglucan metabolism differentially impacts the cell wall characteristics of the endosperm and embryo during Arabidopsis seed germination. Plant Physiology, 170, 1367–1380.PubMedPubMedCentralGoogle Scholar
  113. Sharmin, S. A., Alam, I., Rahman, M. A., Kim, K. H., Kim, Y. G., & Lee, B. H. (2013). Mapping the leaf proteome of Miscanthus sinensis and its application to the identification of heat-responsive proteins. Planta, 238, 459–474.PubMedCrossRefGoogle Scholar
  114. Shigeyama, T., Watanabe, A., Tokuchi, K., Toh, S., Sakurai, N., Shibuya, N., & Kawakami, N. (2016). α-Xylosidase plays essential roles in xyloglucan remodelling, maintenance of cell wall integrity, and seed germination in Arabidopsis thaliana. Journal of Experimental Botany, 6719, 5615–5629.CrossRefGoogle Scholar
  115. Siddiqui, H., Hayat, S., & Bajguz, A. (2018a). Regulation of photosynthesis by brassinosteroids in plants. Acta Physiologiae Plantarum, 40, 59.CrossRefGoogle Scholar
  116. Siddiqui, H., Ahmed, K. B. M., & Hayat, S. (2018b). Comparative effect of 28-homobrassinolide and 24-epibrassinolide on the performance of different components influencing the photosynthetic machinery in Brassica juncea L. Plant Physiology and Biochemistry, 29, 198–212.CrossRefGoogle Scholar
  117. Singh, A., Breja, P., Khurana, J. P., & Khurana, P. (2016). Wheat Brassinosteroid-Insensitive1 (TaBRI1) interacts with members of TaSERK gene family and cause early flowering and seed yield enhancement in Arabidopsis. PLoS One, 11, e0153273.PubMedPubMedCentralCrossRefGoogle Scholar
  118. Steber, C. M., & McCourt, P. (2001). A role for brassinosteroids in germination in Arabidopsis. Plant Physiology, 125, 763–769.PubMedPubMedCentralCrossRefGoogle Scholar
  119. 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
  120. Sun, Y., Fan, X. Y., Cao, D. M., Tang, W., He, K., Zhu, J. Y., & Patil, S. (2010). Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Developmental Cell, 19, 765–777.PubMedPubMedCentralCrossRefGoogle Scholar
  121. Szekeres, M. (2003). Brassinosteroid and systemin: Two hormones perceived by the same receptor. Trends in Plant Science, 8, 102–104.PubMedCrossRefGoogle Scholar
  122. Szekeres, M., Németh, K., Koncz-Kálmán, Z., Mathur, J., Kauschmann, A., Altmann, T., & Koncz, C. (1996). Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell, 85, 171–182.PubMedCrossRefGoogle Scholar
  123. Tanaka, K., Nakamura, Y., Asami, T., Yoshida, S., Matsuo, T., & Okamoto, S. (2003). Physiological roles of brassinosteroids in early growth of Arabidopsis: Brassinosteroids have a synergistic relationship with gibberellin as well as auxin in light-grown hypocotyl elongation. Journal of Plant Growth Regulation, 22, 259–271.CrossRefGoogle Scholar
  124. 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(2), 1117–1125.PubMedPubMedCentralCrossRefGoogle Scholar
  125. Tang, W., Deng, Z., Oses-Prieto, J. A., Suzuki, N., Zhu, S., Zhang, X., et al. (2008). Proteomics studies of brassinosteroid signal transduction using prefractionation and two-dimensional DIGE. Molecular & Cellular Proteomics, 7(4), 728–738.CrossRefGoogle Scholar
  126. Tian, Q., Stepaniants, S. B., Mao, M., Weng, L., Feetham, M. C., Doyle, M. J., & Goodlett, D. (2004). Integrated genomic and proteomic analyses of gene expression in mammalian cells. Molecular & Cellular Proteomics, 3, 960–969.CrossRefGoogle Scholar
  127. Todd, J., Post-Beittenmiller, D., & Jaworski, J. G. (1999). KCS1 encodes a fatty acid elongase 3-ketoacyl-CoA synthase affecting wax biosynthesis in Arabidopsis thaliana. The Plant Journal, 17, 119–130.PubMedCrossRefGoogle Scholar
  128. Tong, H., Xiao, Y., Liu, D., Gao, S., Liu, L., Yin, Y., & Chu, C. (2014). Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice. The Plant Cell, 26, 4376–4393.PubMedPubMedCentralCrossRefGoogle Scholar
  129. Tonge, R., Shaw, J., Middleton, B., Rowlinson, R., Rayner, S., Young, J., & Davison, M. (2001). Validation and development of fluorescence two-dimensional differential gel electrophoresis proteomics technology. Proteomics: International Education, 1, 377–396.CrossRefGoogle Scholar
  130. Tzivion, G., & Avruch, J. (2002). 14-3-3 proteins: Active cofactors in cellular regulation by serine/threonine phosphorylation. The Journal of Biological Chemistry, 277, 3061–3064.PubMedCrossRefGoogle Scholar
  131. Ünlü, M., Morgan, M. E., & Minden, J. S. (1997). Difference gel electrophoresis. A single gel method for detecting changes in protein extracts. Electrophoresis, 18, 2071–2077.PubMedCrossRefGoogle Scholar
  132. 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
  133. Varier, A., Vari, A. K., & Dadlani, M. (2010). The subcellular basis of seed priming. Current Science, 99, 450–456.Google Scholar
  134. Vert, G., Walcher, C. L., Chory, J., & Nemhauser, J. L. (2008). Integration of auxin and brassinosteroid pathways by Auxin Response Factor 2. Proceedings of the National Academy of Sciences, 105, 9829–9834.CrossRefGoogle Scholar
  135. Wang, Z. Y., & He, J. X. (2004). Brassinosteroid signal transduction–choices of signals and receptors. Trends in Plant Science, 9, 91–96.PubMedCrossRefGoogle Scholar
  136. Wang, Z. Y., Nakano, T., Gendron, J., He, J., Chen, M., Vafeados, D., & Chory, J. (2002). Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Developmental Cell, 2, 505–513.PubMedCrossRefGoogle Scholar
  137. Wang, K. L. C., Yoshida, H., Lurin, C., & Ecker, J. R. (2004). Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature, 428, 945.PubMedCrossRefGoogle Scholar
  138. Wang, F., Bai, M. Y., Deng, Z., Oses-Prieto, J. A., Burlingame, A. L., Lu, T., & Wang, Z. Y. (2010). Proteomic study identifies proteins involved in brassinosteroid regulation of rice growth. Journal of Integrative Plant Biology, 52, 1075–1085.PubMedCrossRefGoogle Scholar
  139. Wang, X., Dinler, B. S., Vignjevic, M., Jacobsen, S., & Wollenweber, B. (2015). Physiological and proteome studies of responses to heat stress during grain filling in contrasting wheat cultivars. Plant Science, 230, 33–50.PubMedCrossRefGoogle Scholar
  140. Xia, X. J., Huang, L. F., Zhou, Y. H., Mao, W. H., Shi, K., Wu, J. X., & Yu, J. Q. (2009). Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. Planta, 230, 1185.PubMedCrossRefGoogle Scholar
  141. Xu, C., & Huang, B. (2010). Differential proteomic response to heat stress in thermal Agrostis scabra and heat-sensitive Agrostis stolonifera. Physiologia Plantarum, 139, 192–204.PubMedCrossRefGoogle Scholar
  142. Xu, W., Purugganan, M. M., Polisensky, D. H., Antosiewicz, D. M., Fry, S. C., & Braam, J. (1995). Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase. The Plant Cell, 7, 1555–1567.PubMedPubMedCentralCrossRefGoogle Scholar
  143. Yamamuro, C., Ihara, Y., Wu, X., Noguchi, T., Fujioka, S., Takatsuto, S., et al. (2000). Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. The Plant Cell, 12(9), 1591–1605.PubMedPubMedCentralCrossRefGoogle Scholar
  144. Yan, A., Wu, M., Yan, L., Hu, R., Ali, I., & Gan, Y. (2014). AtEXP2 is involved in seed germination and abiotic stress response in Arabidopsis. PLoS One, 9, e85208.PubMedPubMedCentralCrossRefGoogle Scholar
  145. Yang, G., & Komatsu, S. (2004). Microarray and proteomic analysis of brassinosteroid-and gibberellin-regulated gene and protein expression in rice. Genomics, Proteomics & Bioinformatics, 2(2), 77–83.CrossRefGoogle Scholar
  146. Yi, H. C., Joo, S., Nam, K. H., Lee, J. S., Kang, B. G., & Kim, W. T. (1999). Auxin and brassinosteroid differentially regulate the expression of three members of the 1-aminocyclopropane-1-carboxylate synthase gene family in mung bean (Vigna radiata L.). Plant Molecular Biology, 41, 443–454.PubMedCrossRefGoogle Scholar
  147. Yin, Y., Vafeados, D., Tao, Y., Yoshida, S., Asami, T., & Chory, J. (2005). A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell, 120, 249–259.PubMedCrossRefGoogle Scholar
  148. Yu, X., Li, L., Zola, J., Aluru, M., Ye, H., Foudree, A., & Rodermel, S. (2011). A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. The Plant Journal, 65, 634–646.PubMedCrossRefGoogle Scholar
  149. Yuan, T., Fujioka, S., Takatsuto, S., Matsumoto, S., Gou, X., He, K., & Li, J. (2007). BEN1, a gene encoding a dihydroflavonol 4-reductase (DFR)-like protein, regulates the levels of brassinosteroids in Arabidopsis thaliana. The Plant Journal, 51, 220–233.PubMedCrossRefGoogle Scholar
  150. Zhang, A., Zhang, J., Zhang, J., Ye, N., Zhang, H., Tan, M., & Jiang, M. (2010a). Nitric oxide mediates brassinosteroid-induced ABA biosynthesis involved in oxidative stress tolerance in maize leaves. Plant and Cell Physiology, 52, 181–192.PubMedCrossRefGoogle Scholar
  151. Zhang, M., Li, G., Huang, W., Bi, T., Chen, G., Tang, Z., Su, W., & Sun, W. (2010b). Proteomic study of Carissa spinarum in response to combined heat and drought stress. Proteomics, 10, 3117–3129.PubMedCrossRefGoogle Scholar
  152. Zhang, Z., Xu, Y., Xie, Z., Li, X., He, Z. H., & Peng, X. X. (2016). Association–dissociation of glycolate oxidase with catalase in rice: A potential switch to modulate intracellular H2O2 levels. Molecular Plant, 9, 737–748.PubMedCrossRefGoogle Scholar
  153. Zhou, J., Wang, J., Li, X., Xia, X. J., Zhou, Y. H., Shi, K., & 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
  154. Zúñiga-Sánchez, E., Soriano, D., Martínez-Barajas, E., Orozco-Segovia, A., & Gamboa-deBuen, A. (2014). BIIDXI, the At4g32460 DUF642 gene, is involved in pectin methyl esterase regulation during Arabidopsis thaliana seed germination and plant development. BMC Plant Biology, 14, 338.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Husna Siddiqui
    • 1
  • Fareen Sami
    • 1
  • H. F. Juan
    • 2
    Email author
  • Shamsul Hayat
    • 1
  1. 1.Plant Physiology Section, Department of BotanyAligarh Muslim UniversityAligarhIndia
  2. 2.Department of Life Science, Graduate Institute of Biomedical Electronics and BioinformaticsNational Taiwan UniversityTaipeiTaiwan

Personalised recommendations