Journal of Life Science (생명과학회지)

Korean Society of Life Science (한국생명과학회)
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Update on Phosphorylation-Mediated Brassinosteroid Signaling Pathways

단백질 인산화에 의해 매개되는 브라시노스테로이드 신호전달 연구의 최근 상황

  • Lee, Yew (Division of Biological Science and Technology, Yonsei University) ;
  • Kim, Soo-Hwan (Division of Biological Science and Technology, Yonsei University)
  • 이유 (연세대학교 원주캠퍼스 생명과학기술학부) ;
  • 김수환 (연세대학교 원주캠퍼스 생명과학기술학부)
  • Received : 2011.10.05
  • Accepted : 2011.12.06
  • Published : 2012.03.30
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Abstract

Protein phosphorylation is a universal mechanism that regulates cellular activities. The brassinosteroid (BR) signal transduction pathway is a relay of phosphorylation and dephosphorylation cascades. It starts with the BR-induced activation of the membrane receptor kinase brassinosteroid insensitive 1 (BRI1), resulting in the dephosphorylation of transcription factors such as BZR1/BES2 and BZR2/BES1 followed by BR-induced gene expression. Brassinosteroid signal transduction research has progressed rapidly by identifying the phosphorylation/dephosphorylation site(s) of the BR-regulated kinase and phosphatase substrates with a simultaneous pursuit of mutant phenotypes. Autophosphorylation, transphosphorylation, and serine/threonine and tyrosine phosphorylation of the receptor protein kinases BRI1 and BRI1-associated kinase (BAK1) have increased the understanding of the regulatory role of those kinases during physiological and developmental processes in plants. The phosphorylation event initiated by BR is also found in the regulation of receptor-mediated endocytosis and the subsequent degradation of the receptor. However, the basic molecular links of the BR signal transduction pathway are not well understood regarding this phosphorylation/dephosphorylation event. This review summarizes the current state of BR signal transduction research to uncover the phosphorylation/dephosphorylation networks and suggests directions for future research on steroid signal transduction to gain a more comprehensive understanding of the process.

단백질 인산화는 세포의 활동을 조절하는 보편적인 과정이다. 브라시노스테로이드(brassinostreoid)에 의해 매개되는 신호전달은 브라시노스테로이드에 의해 활성화된 세포막상의 protein kinase 로부터 인산화되어 있는 전사인자들을 탈인산화하는 연속적인 인산화/탈인산화 과정이다. 브라시노스테로이드에 의해 매개되는 신호전달의 연구는 인산화에 관여하는 kinase 기질상의 아미노산을 밝히고, 그와 관련된 돌연변이체의 표현형을 알아봄으로써 급속하게 발전하였다. BRI1과 BAK1의 자기인산화(autophosphorylation), 상호인산화(transphosphorylation), 타이로신 인산화(tyrosine phosphorylation)를 밝힘으로써 그들의 조절작용을 식물의 생리학적, 발생학적 과정을 더 이해할 수 있는 장이 열렸다. 브라시노스테로이드에 의한 인산화는 수용체에 의해 매개되는 세포 내 함입(endocytosis)과 그에 뒤따르는 수용체의 파괴현상에서도 볼 수 있다. 인산화/탈인산화 과정에 관련하여 브라시노스테로이드에 의해 매개되는 신호전달은 더 연구할 여지가 많이 남아 있다. 이 총설은 단백질의 인산화/탈인산화 과정을 통한 브라시노스테로이드의 신호전달 연구의 최근 상황을 기술하였다.

Keywords

References

  1. Aker, J. and S. C. de Vries. 2008. Plasma membrane receptor complexes. Plant Physiol. 147, 1560-1564. https://doi.org/10.1104/pp.108.120501
  2. Albrecht, C., E. Russinova, B. Kemmerling, M., Kwaaitaal, and S. C. de Vries. 2008. Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE proteins serve brassinosteroid-dependent and -independent signaling pathways. Plant Physiol. 148, 611-619. https://doi.org/10.1104/pp.108.123216
  3. Avraham, R. and Y. Yarden. 2011. Feedback regulation of EGFR signaling, decision making by early and delayed loops. Nat. Rev. Mol. Cell Biol. 12, 104-117. https://doi.org/10.1038/nrm3048
  4. Bar, M., M. Sharfman, M. Ron, and A. Avni. 2010. BAK1 is required for the attenuation of ethylene-inducing xylanase (Eix)-induced defense responses by the decoy receptor LeEix1. Plant J. 63, 791-800. https://doi.org/10.1111/j.1365-313X.2010.04282.x
  5. Cano-Delgado, A., Y. Yin, C. Yu, D., Vafeados, S. Mora-García, J. C. Cheng, K. H. Nam, J. Li, and J. Chory. 2004. BRL1 and BRL3 are novel Brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131, 5341-5351. https://doi.org/10.1242/dev.01403
  6. Chinchilla, D., L. Shan, P. He, S. C. de Vries, and B. Kemmerling. 2009. One for all, The receptor-associated kinase BAK1. Trends Plant Sci. 14, 535-541. https://doi.org/10.1016/j.tplants.2009.08.002
  7. Choe, S., R. J. Schmitz, S., Fujioka, S. Takatsuto, M. O. Lee, S. Yoshida, K. A. Feldmann, and F. E. Tax. 2002. Arabidopsis brassinosteroid insensitive dwarf12 mutants are semidominant and defective in a glycogen synthase kinase 3beta-like kinase. Plant Physiol. 130, 1506-1515. https://doi.org/10.1104/pp.010496
  8. Clouse, S. D. 2002. Brassinosteroid signaling, novel downstream components emerge. Curr. Biol. 12, R485-487. https://doi.org/10.1016/S0960-9822(02)00964-8
  9. Clouse, S. D. 2011. Brassinosteroid signal transduction, From receptor kinase activation to transcriptional networks regulating plant development. Plant Cell doi, 10.1105/tpc.111.084475.
  10. Clouse, S. D., M. Langford, and T. C. McMorris. 1996. A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol. 111, 671-678. https://doi.org/10.1104/pp.111.3.671
  11. Clouse, S. D. and J. M. Sasse. 1998. BRASSINOSTEROIDS, Essential Regulators of Plant Growth and Development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 427-451. https://doi.org/10.1146/annurev.arplant.49.1.427
  12. Colcombet, J., A. Boisson-Dernier, R. Ros-Palau, C. E. Vera, and J. I. Schroeder. 2005. Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17, 3350-3361. https://doi.org/10.1105/tpc.105.036731
  13. Deng, Z., X. Zhang, W. Tang, J. A. Oses-Prieto, and N. Suzuki. 2007. A proteomics study of brassinosteroid response in Arabidopsis. Mol. Cell Proteomics 6, 2058-2071. https://doi.org/10.1074/mcp.M700123-MCP200
  14. Di Rubbo, S., N. G. Irani, and E. Russinova. 2011. PP2A Phosphatases, The "On-Off" Regulatory Switches of Brassinosteroid Signaling. Sci. Signal. 4, pe25. https://doi.org/10.1126/scisignal.2002046
  15. Eden, E. R., I. J. White, and C. E. Futter. 2009, Down-regulation of epidermal growth factor receptor signaling within multivesicular bodies. Biochem. Soc. Trans. 37, 173-177. https://doi.org/10.1042/BST0370173
  16. Ehsan, H., W. K. Ray, B. Phinney, X. Wang, S. C. Huber, and S. D. Clouse. 2005. Interaction of Arabidopsis BRASSINOSTEROID-INSENSITIVE 1 receptor kinase with a homolog of mammalian TGF-beta receptor interacting protein. Plant J. 43, 251-261. https://doi.org/10.1111/j.1365-313X.2005.02448.x
  17. Friedrichsen, D. M., C. A. Joazeiro, J. Li, T. Hunter, and J. Chory. 2000. Brassinosteroid-insensitive-1 is a ubiquitously expressed leucine rich repeat receptor serine/threonine kinase. Plant Physiol. 123, 1247-1256. https://doi.org/10.1104/pp.123.4.1247
  18. Fujioka, S. and T. Yokota. 2003. Biosynthesis and metabolism of brassinosteroids. Annu. Rev. Plant Biol. 54, 137-164. https://doi.org/10.1146/annurev.arplant.54.031902.134921
  19. Gampala, S. S., T. W. Kim, J. X. He, W. Tang, Z. Deng, M. Y. Bai, S. Guan, S. Lalonde, Y. Sun, J. M. Gendron, H. Chen, N. Shibagaki, R. J. Ferl, D. Ehrhardt, K. Chong, A. L. Burlingame, and Z. Y. Wang. 2007. An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev. Cell 13, 177-189. https://doi.org/10.1016/j.devcel.2007.06.009
  20. He, J. X., J. M. Gendron, Y. Yang, J. Li, and Z. Y. Wang. 2002. The GSK3- like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proc. Natl. Acad. Sci. USA 99, 10185-10190. https://doi.org/10.1073/pnas.152342599
  21. He, K., X. Gou, R. A. Powell, H. Yang, T. Yuan, Z. Guo, and J. Li. 2008. Receptor-like protein kinases, BAK1 and BKK1, regulate a light-dependent cell-death control pathway. Plant Signal. Behav. 3, 813-815. https://doi.org/10.4161/psb.3.10.5890
  22. He, K., X. Gou, T., Yuan, H. Lin, T. Asami, S. Yoshida, S. D. Russell, and J. Li. 2007. BAK1 and BKK1 regulate brassinosteroid- dependent growth and brassinosteroid-independent cell-death pathways. Curr. Biol. 17, 1109-1115. https://doi.org/10.1016/j.cub.2007.05.036
  23. Hecht, V., J. P. Vielle-Calzada, M. V. Hartog, E. D. Schmidt, K. Boutilier, U. Grossniklaus, and S. C. de Vries. 2001. The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol. 127, 803-816. https://doi.org/10.1104/pp.010324
  24. Heese, A., D. R. Hann, S. Gimenez-Ibanez, A. M. Jones, K. He, J. Li, J. I. Schroeder, S. C. Peck, and J. P. Rathjen. 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl. Acad. Sci. USA 104, 12217-12222. https://doi.org/10.1073/pnas.0705306104
  25. Jaillais, Y., M. Hothorn, Y. Belkhadir, T. Dabi, Z. L. Nimchuk, E. M. Meyerowitz, and J. Chory. 2011. Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor. Genes Dev. 25, 232-237. https://doi.org/10.1101/gad.2001911
  26. Janssens, V., S. Longin, and J. Goris. 2008. PP2A holoenzyme assembly, In cauda venenum (the sting is in the tail). Trends Biochem. Sci. 33, 113-121. https://doi.org/10.1016/j.tibs.2007.12.004
  27. Karlova, R., S. Boeren, E. Russinova, J. Aker, J. Vervoort, and S. C. de Vries. 2006. The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE1 protein complex includes BRASSINOSTEROID- INSENSITIVE1. Plant Cell 18, 626-638. https://doi.org/10.1105/tpc.105.039412
  28. Karlova, R., S. Boeren, W. van Dongen, M. Kwaaitaal, and J. Aker. 2009. Identification of in vitro phosphorylation sites in the Arabidopsis thaliana somatic embryogenesis receptor-like kinases. Proteomics 9, 368-379. https://doi.org/10.1002/pmic.200701059
  29. Kemmerling, B., A. Schwedt, P. Rodriguez, S. Mazzotta, M. Frank, S. A. Qamar, T. Mengiste, S., Parker, J. E. Betsuyaku, C. Mussig, B. P. Thomma, C. Albrecht, S. C. de Vries, H. Hirt, and T. Nurnberger. 2007. The BRI1-associated kinase 1, BAK1, has a brassinolide independent role in plant cell-death control. Curr. Biol. 17, 1116-1122. https://doi.org/10.1016/j.cub.2007.05.046
  30. Kim, T. W., S. Guan, A. L. Burlingame, and Z. Y. Wang. 2011. The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK-3-like kinase BIN2. Mol. Cell 43, 561-571. https://doi.org/10.1016/j.molcel.2011.05.037
  31. Kim, T. W., S. Guan, Y. Sun, Z. Deng, W. Tang, J. X. Shang, Y. Sun, A. L., Burlingame, and Z. Y. Wang. 2009. Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nature Cell Biol. 11, 1254-1262. https://doi.org/10.1038/ncb1970
  32. Kim, T. W. and Z. Y. Wang. 2010. Brassinosteroid signal transduction from receptor kinases to transcription factors. Ann. Rev. Plant Biol. 61, 681-704. https://doi.org/10.1146/annurev.arplant.043008.092057
  33. Kinoshita, T., A. Cãno-Delgado, H. Seto, S. Hiranuma, S. Fujioka, S. Yoshida, and J. Chory. 2005. Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433, 167-171. https://doi.org/10.1038/nature03227
  34. Li, J. and J. Chory. 1997. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90, 929-938. https://doi.org/10.1016/S0092-8674(00)80357-8
  35. Li, J. and K. H. Nam. 2002. Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science 295: 1299-1301.
  36. Li, J., J. Wen, K. A. Lease, J. T. Doke, F. E. Tax, and J. C. Walker. 2002. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110, 213-222. https://doi.org/10.1016/S0092-8674(02)00812-7
  37. Liu, T. and Z. H. Feng. 2010, Regulation of TGF-beta signaling by protein phosphatases. Biochem. J. 430, 191-198. https://doi.org/10.1042/BJ20100427
  38. Mora-Garcia, S., G. Vert, Y. Yin, A. Cãno-Delgado, H. Cheong, and J. Chory. 2004. Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis. Genes Dev. 18, 448-460. https://doi.org/10.1101/gad.1174204
  39. Muto, H., N. Yabe, T. Asami, K. Hasunuma, and K. T. Yamamoto. 2004. Overexpression of constitutive differential growth 1 gene, which encodes a RLCKVII-subfamily protein kinase, causes abnormal differential and elongation growth after organ differentiation in Arabidopsis. Plant Physiol. 136, 3124-3133. https://doi.org/10.1104/pp.104.046805
  40. Nam, K. H. and J. Li. 2002. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110, 203-212. https://doi.org/10.1016/S0092-8674(02)00814-0
  41. Nam, K. H. and J. Li. 2004. The Arabidopsis transthyretin-like protein is a potential substrate of BRASSINOSTEROIDINSENSITIVE 1. Plant Cell 16, 2406-2417. https://doi.org/10.1105/tpc.104.023903
  42. Oh, M. H., S. D. Clouse, and S. C. Huber. 2009a. Tyrosine phosphorylation in brassinosteroid signaling. Plant Signal. Behav. 4, 1182-1185. https://doi.org/10.4161/psb.4.12.10046
  43. Oh, M. H., W. K. Ray, S. C. Huber, J. M. Asara, D. A. Gage, and S. D. Clouse. 2000. Recombinant brassinosteroid insensitive 1 receptor-like kinase autophosphorylates on serine and threonine residues and phosphorylates a conserved peptide motif in vitro. Plant Physiol. 124, 751-766. https://doi.org/10.1104/pp.124.2.751
  44. Oh, M. H., X. Wang, U. Kota, M. B. Goshe, S. D. Clouse, and S. C. Huber. 2009b. Tyrosine phosphorylation of the BRI1 receptor kinase emerges as a component of brassinosteroid signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA 106, 658-663. https://doi.org/10.1073/pnas.0810249106
  45. Perez-Perez, J. M., M. R. Ponce, and J. L. Micol. 2002. The UCU1 Arabidopsis gene encodes a SHAGGY/GSK3-like kinase required for cell expansion along the proximodistal axis. Dev. Biol. 242, 161-173. https://doi.org/10.1006/dbio.2001.0543
  46. Postel, S., I. Küfner, C. Beuter, S. Mazzotta, A. Schwedt, A. Borlotti, T. Halter, B. Kemmerling, and T. Nürnberger. 2010. The multifunctional leucine-rich repeat receptor kinase BAK1 is implicated in Arabidopsis development and immunity. Eur. J. Cell Biol. 89, 169-174. https://doi.org/10.1016/j.ejcb.2009.11.001
  47. Rahimi, R. A. and E. B. Leof, 2007. TGF-beta signaling: a tale of two responses. J. Biol. Chem. 102, 593-608.
  48. Russinova, E., J. W. Borst, M. Kwaaitaal, A. Cãno-Delgado, Y. Yin, Chory, J., and S. C. de Vries. 2004. Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16, 3216-3229. https://doi.org/10.1105/tpc.104.025387
  49. Ryu, H., K. Kim, H. Cho, J. Park, S. Choe, and I. Hwang. 2007. Nucleocytoplasmic shuttling of BZR1 mediated by phosphorylation is essential in Arabidopsis brassinosteroid signaling. Plant Cell 19, 2749-2762. https://doi.org/10.1105/tpc.107.053728
  50. Shah, K., E. Russinova, T. W. Jr. Gadella, J. Willemse, and S. C. de Vries. 2002. The Arabidopsis kinase associated protein phosphatase controls internalization of the somatic embryogenesis receptor kinase 1. Genes Dev. 16, 1707-1720. https://doi.org/10.1101/gad.220402
  51. Shan, L., P. He, J. Li, A. Heese, S. C. Peck, T. Nurnberger, G. B. Martin, and J. Sheen. 2008. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4, 17-27. https://doi.org/10.1016/j.chom.2008.05.017
  52. Shiu, S. H., W. M. Karlowski, R. Pan, Y. H. Tzeng, K. F. Mayer, and W. H. Li. 2004. Comparative analysis of the receptor- like kinase family in Arabidopsis and rice. Plant Cell 16, 1220-1234. https://doi.org/10.1105/tpc.020834
  53. Schlessinger, J. 2002. Ligand-induced, receptor-mediated dimerization and activation of EGF receptor. Cell 110, 669-672. https://doi.org/10.1016/S0092-8674(02)00966-2
  54. Schulze, B., T. Mentzel, A. K. Jehle, K. Mueller, S. Beeler, T. Boller, G. Felix, and D. Chinchilla. 2010. Rapid heterodimerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J. Biol. Chem. 285, 9444-9451. https://doi.org/10.1074/jbc.M109.096842
  55. Stanevich, V., L. Jiang, K. A. Satyshur, Y. Li, P. D. Jeffrey, Z. Li, P. Menden, M. F. Semmelhack, and Y. Xing. 2011. The structural basis for tight control of PP2A methylation and function by LCMT-1. Mol. Cell 41, 331-342. https://doi.org/10.1016/j.molcel.2010.12.030
  56. Tang, W., T. W. Kim, J. A. Oses-Prieto, Y. Sun, Z. Deng, S. Zhu, R. Wang, A. L. Burlingame, and Z. Y. Wang. 2008. BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321, 557-560. https://doi.org/10.1126/science.1156973
  57. Tang, W., M. Yuan, R. Wang, Y. Yang, C. Wang, J. A. Oses-Prieto, T. W. Kim, H. W. Zhou, Z. Deng, S. S. Gampala, J. M. Gendron, E. M. Jonassen, C. Lillo, A. DeLong, A. L. Burlingame, Y. Sun, and Z. Y. Wang. 2011. PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat. Cell Biol. 13, 124-131. https://doi.org/10.1038/ncb2151
  58. Vert, G. and J. Chory. 2006. Downstream nuclear events in brassinosteroid signalling. Nature 441, 96-100. https://doi.org/10.1038/nature04681
  59. Vert, G., J. L. Nemhauser, N. Geldner, F. Hong, and J. Chory. 2005. Molecular mechanisms of steroid hormone signaling in plants. Ann. Rev. Cell Dev. Biol. 21, 177-201. https://doi.org/10.1146/annurev.cellbio.21.090704.151241
  60. Wang, X. and J. Chory. 2006. Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, form the plasma membrane. Science 313, 1118-1122. https://doi.org/10.1126/science.1127593
  61. Wang, X., M. B. Goshe, E. J. Soderblom, B. S. Phinney, J. A. Kuchar, J. Li, T. Asami, S. Yoshida, S. C. Huber, and S. D. Clouse. 2005a. Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROID-INSENSTIVE1 receptor kinase. Plant Cell 17, 1685-1703. https://doi.org/10.1105/tpc.105.031393
  62. Wang, X., U. Kota, K. He, K. Blackburn, J. Li, M.B. Goshe, S. C. Huber, and S. D. Clouse. 2008. Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev. Cell 15, 220-235. https://doi.org/10.1016/j.devcel.2008.06.011
  63. Wang, X., X. Li, J. Meisenhelder, T. Hunter, S. Yoshida, T. Asami, and J. Chory. 2005b. Autoregulation and homodimerization are involved in the activation of the plant steroid receptor BRI1. Dev. Cell 8, 855-865. https://doi.org/10.1016/j.devcel.2005.05.001
  64. Wang, Z. Y., T. Nakano, J. Gendron, J. He, M. Chen, D. Vafeados, Y. Yang, S. Fujioka, S. T. Asami, and J. Chory. 2002. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell 2, 505-513. https://doi.org/10.1016/S1534-5807(02)00153-3
  65. White, R. and M. G. Parker. 1998. Molecular mechanisms of steroid hormone action. Endocrine-Related Cancer 5, 1-14. https://doi.org/10.1677/erc.0.0050001
  66. Wu, D. and W. Pan. 2010, GSK3: multifaceted kinase in Wnt signaling. Trends Biochem. Sci. 35, 161-168. https://doi.org/10.1016/j.tibs.2009.10.002
  67. Wu, G., X. Wang, X. Li, Y. Kamiya, M. S. Otegui, and J. Chory. 2011. Methylation of a phosphatase specifies dephosphorylation and degradation of activated brassinosteroid receptors. Sci. Signal. 4, ra29. https://doi.org/10.1126/scisignal.2001258
  68. Yang, C. J., C. Zhang, Y. N. Lu, J. Q. Jin, and X. L. Wang. 2011. The mechanism of Brassinosteroids' Action, From signal transduction to plant development. Mol. Plant doi, 10.1093/mp/ssr020.
  69. Ye, H., L. Li, and Y. Yin. 2011. Recent advances in the regulation of brassinosteroid signaling and biosynthesis pathway. J. Integr. Plant Biol. 53, 455-468. https://doi.org/10.1111/j.1744-7909.2011.01046.x
  70. Yin, Y., D. Vafeados, Y. Tao, T. Yokoda, T. Asami, and J. Chory. 2005. A new class of transcription factors mediate brassinosteroid-regulated gene expression in Arabidopsis. Cell 120, 249-259. https://doi.org/10.1016/j.cell.2004.11.044
  71. Yin, Y., Z. Y. Wang, S. Mora-Garcia, J. Li, S. Yoshida, T. Asami, and J. Chory. 2002. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109, 181-191. https://doi.org/10.1016/S0092-8674(02)00721-3
  72. Yun, H. S., Y. H. Bae, Y. J. Lee, S. C. Chang, and S. K. Kim. 2009. Analysis of phosphorylation of the BRI1/BAK1 complex in Arabidopsis reveals amino acid residues critical for receptor formation and activation of BR signaling. Mol. Cell 27, 183-190. https://doi.org/10.1007/s10059-009-0023-1
  73. Zhou, A., H. Wang, J. C. Walker, and J. Li. 2004. BRL1, a leucine-rich repeat receptor-like protein kinase, is functionally redundant with BRI1 in regulating Arabidopsis brassinosteroid signaling. Plant J. 40, 399-409. https://doi.org/10.1111/j.1365-313X.2004.02214.x