Molecular evidence of the involvement of heat shock protein 90 in brassinosteroid signaling in Arabidopsis T87 cultured cells

Plant Cell Reports

Volumn 33, Issue 3, 2014, Pages 499-510

  Shigeta, Tomoaki ^a   Zaizen, Yuichi ^a   Asami, Tadao ^b   Yoshida, Shigeo ^c   Nakamura, Yasushi ^d   Okamoto, Shigehisa ^a   Matsuo, Tomoaki ^a   Sugimoto, Yasushi ^a  

^a KAGOSHIMA UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c YOKOHAMA CITY UNIVERSITY   (Japan)

^d KYOTO PREFECTURAL UNIVERSITY   (Japan)

Author keywords

BES1; Brassinosteroid; CPD; DWF4; Geldanamycin; HSP90.3

Indexed keywords

ARABIDOPSIS PROTEIN; BRASSINOLIDE; BRASSINOSTEROID; HEAT SHOCK PROTEIN; HETEROCYCLIC STEROID;

ARABIDOPSIS; ARTICLE; GENE EXPRESSION REGULATION; METABOLISM; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRASSINOSTEROIDS; GENE EXPRESSION REGULATION, PLANT; HEAT-SHOCK PROTEINS; SIGNAL TRANSDUCTION; STEROIDS, HETEROCYCLIC;

EID: 84893957157     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-013-1550-y     Document Type: Article

References (37)

1. Basso AD, Solit DB, Chiosis G, Giri B, Tsichlis P, Rosen N (2002) Akt forms an intracellular complex with heat shock protein 90 (Hsp90) and Cdc37 and is destabilized by inhibitors of Hsp90 function. J Biol Chem 277: 39858-39866.
2. Bekh-Ochir D, Shimada S, Yamagami A, Kanda S, Ogawa K, Nakazawa M, Matsui M, Sakuta M, Osada H, Asami T, Nakano T (2013) A novel mitochondrial DnaJ/Hsp40 family protein BIL2 promotes plant growth and resistance against environmental stress in brassinosteroid signaling. Planta 237: 1509-1525.
3. Chiu W, Niwa Y, Zeng W, Hirano T, Kobayashi H, Sheen J (1996) Engineered GFP as a vital reporter in plants. Curr Biol 6: 325-330.
4. Clément M, Leonhardt N, Droillard MJ, Reiter I, Montillet JL, Genty B, Laurière C, Nussaume L, Noël LD (2011) The cytosolic/nuclear HSC70 and HSP90 molecular chaperones are important for stomatal closure and modulate abscisic acid-dependent physiological responses in Arabidopsis. Plant Physiol 156: 1481-1492.
5. Clouse S, Sasse J (1998) BRASSINOSTEROIDS: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49: 427-451.
6. Divi UK, Krishna P (2009) Brassinosteroid: a biotechnological target for enhancing crop yield and stress tolerance. N Biotechnol 26: 131-136.
7. Fang S, Fu J, Yuan X, Han C, Shi L, Xin Y, Luo L, Yin Z (2009) Heat shock protein 90 regulates the stability of MEKK3 in HEK293 cells. Cell Immunol 259: 49-55.
8. He JX, Gendron JM, Sun Y, Gampala SS, Gendron N, Sun CQ, Wang ZY (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307: 1634-1638.
9. Kadota Y, Shirasu K (2012) The HSP90 complex of plants. Biochim Biophys Acta 1823: 689-697.
10. Kamphausen T, Fanghänel J, Neumann D, Schulz B, Rahfeld JU (2002) Characterization of Arabidopsis thaliana AtFKBP42 that is membrane-bound and interacts with Hsp90. Plant J 32: 263-276.
11. Kim TW, Wang ZY (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 61: 681-704.
12. Krishna P, Gloor G (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6: 238-246.
13. Lachowiec J, Lemus T, Thomas JH, Murphy PJ, Nemhauser JL, Queitsch C (2013) The protein chaperone HSP90 can facilitate the divergence of gene duplicates. Genetics 193: 1269-1277.
14. Li L, Yu X, Thompson A, Guo M, Yoshida S, Asami T, Chory J, Yin Y (2009) Arabidopsis MYB30 is a direct target of BES1 and cooperates with BES1 to regulate brassinosteroid-induced gene expression. Plant J 58: 275-286.
15. Li L, Ye H, Guo H, Yin Y (2010) Arabidopsis IWS1 interacts with transcription factor BES1 and is involved in plant steroid hormone brassinosteroid regulated gene expression. Proc Natl Acad Sci USA 107: 3918-3923.
16. Nemoto K, Seto T, Takahashi H, Nozawa A, Seki M, Shinozaki K, Endo Y, Sawasaki T (2011) Autophosphorylation profiling of Arabidopsis protein kinases using the cell-free system. Phytochemistry 72: 1136-1144.
17. Obermann WM, Sondermann H, Russo AA, Pavletich NP, Hartl FU (1998) In vivo function of Hsp90 is dependent on ATP binding and ATP hydrolysis. J Cell Biol 143: 901-910.
18. Ogawa Y, Dansako T, Yano K, Sakurai N, Suzuki H, Aoki K, Noji M, Saito K, Shibata D (2008) Efficient and high-throughput vector construction and Agrobacterium-mediated transformation of Arabidopsis thaliana suspension-cultured cells for functional genomics. Plant Cell Physiol 49: 242-250.
19. Pérez-Pérez JM, Ponce MR, Micol JL (2004) The ULTRACURVATA2 gene of Arabidopsis encodes an FK506-binding protein involved in auxin and brassinosteroid signaling. Plant Physiol 134: 101-117.
20. Ryu H, Cho H, Kim K, Hwang I (2010) Phosphorylation dependent nucleocytoplasmic shuttling of BES1 is a key regulatory event in brassinosteroid signaling. Mol Cells 29: 283-290.
21. Sangster TA, Queitsch C (2005) The HSP90 chaperone complex, an emerging force in plant development and phenotypic plasticity. Curr Opin Plant Biol 8: 86-92.
22. Sangster TA, Bahrami A, Wilczek A, Watanabe E, Schellenberg K, McLellan C, Kelley A, Kong SW, Queitsch C, Lindquist S (2007) Phenotypic diversity and altered environmental plasticity in Arabidopsis thaliana with reduced Hsp90 levels. PLoS One 2: e648.
23. Sekimata K, Kimura T, Kaneko I, Nakano T, Yoneyama K, Takeuchi Y, Yoshida S, Asami T (2001) A specific brassinosteroid biosynthesis inhibitor, Brz 2001: evaluation of its effects on Arabidopsis, cress, tobacco, and rice. Planta 213: 716-721.
24. Shigeta T, Yasuda D, Mori T, Yoshimitsu Y, Nakamura Y, Yoshida S, Asami T, Okamoto S, Matsuo T (2011) Characterization of brassinosteroid-regulated proteins in a nuclear-enriched fraction of Arabidopsis suspension-cultured cells. Plant Physiol Biochem 49: 985-995.
25. Sun Y, Fan XY, Cao DM, Tang W, He K, Zhu JY, He JX, Bai MY, Zhu S, Oh E, Patil S, Kim TW, Ji H, Wong WH, Rhee SY, Wang ZY (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 19: 765-777.
26. Taipale M, Jarosz DF, Lindquist S (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11: 515-528.
27. Taipale M, Krykbaeva I, Koeva M, Kayatekin C, Westover KD, Karras GI, Lindquist S (2012) Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition. Cell 150: 987-1001.
28. Takahashi H, Takahashi C, Moreland NJ, Chang YT, Sawasaki T, Ryo A, Vasudevan SG, Suzuki Y, Yamamoto N (2012) Establishment of a robust dengue virus NS3-NS5 binding assay for identification of protein-protein interaction inhibitors. Antiviral Res 96: 305-314.
29. Tanaka K, Asami T, Yoshida S, Nakamura Y, Matsuo T, Okamoto S (2005) Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. Plant Physiol 138: 1117-1125.
30. Tang W, Yuan M, Wang R, Yang Y, Wang C, Oses-Prieto JA, Kim TW, Zhou HW, Deng Z, Gampala SS, Gendron JM, Jonassen EM, Lillo C, DeLong A, Burlingame AL, Sun Y, Wang ZY (2011) PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat Cell Biol 13: 124-131.
31. Vert G, Chory J (2006) Downstream nuclear events in brassinosteroid signalling. Nature 441: 96-100.
32. Wayne N, Bolon DN (2007) Dimerization of Hsp90 is required for in vivo function. Design and analysis of monomers and dimers. J Biol Chem 282: 35386-35395.
33. Yan Z, Zhao J, Peng P, Chihara RK, Li J (2009) BIN2 functions redundantly with other Arabidopsis GSK3-like kinases to regulate brassinosteroid signaling. Plant Physiol 150: 710-721.
34. Ye H, Li L, Guo H, Yin Y (2012) MYBL2 is a substrate of GSK3-like kinase BIN2 and acts as a corepressor of BES1 in brassinosteroid signaling pathway in Arabidopsis. Proc Natl Acad Sci USA 109: 20142-20147.
35. 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.
36. Yu X, Li L, Guo M, Chory J, Yin Y (2008) Modulation of brassinosteroid-regulated gene expression by Jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis. Proc Natl Acad Sci USA 105: 7618-7623.
37. Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, Guo H, Anderson S, Aluru S, Liu P, Rodermel S, Yin Y (2011) A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J 65: 634-646.