Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs

Plant Journal

Volumn 59, Issue 3, 2009, Pages 387-399

  Meiri, David ^a   Breiman, Adina ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

AtFKBP62; HsfA2; HSP90; Immunophilins; ROF1; Thermotolerance

Indexed keywords

ARABIDOPSIS PROTEIN; DNA BINDING PROTEIN; FK 506 BINDING PROTEIN; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 90; HEAT STRESS TRANSCRIPTION FACTORS; HSP90 1 PROTEIN, ARABIDOPSIS; HSP90-1 PROTEIN, ARABIDOPSIS; PLANT RNA; ROF1 PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; HEAT; METABOLISM; PHYSIOLOGY; PROTEIN BINDING; TRANSGENIC PLANT; TWO HYBRID SYSTEM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, PLANT; GENE KNOCKOUT TECHNIQUES; HEAT-SHOCK PROTEINS; HOT TEMPERATURE; HSP90 HEAT-SHOCK PROTEINS; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROTEIN BINDING; RNA, PLANT; TACROLIMUS BINDING PROTEINS; TRANSCRIPTION FACTORS; TWO-HYBRID SYSTEM TECHNIQUES;

ARABIDOPSIS;

EID: 67651216183     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2009.03878.x     Document Type: Article

References (67)

1. Aviezer-Hagai, K., Skovorodnikova, J., Galigniana, M., Farchi-Pisanty, O., Maayan, E., Bocovza, S., Efrat, Y., von Koskull-Doring, P., Ohad, N. Breiman, A. (2007) Arabidopsis immunophilins ROF1 (AtFKBP62) and ROF2 (AtFKBP65) exhibit tissue specificity, are heat-stress induced, and bind HSP90. Plant Mol. Biol. 63, 237 255.
2. Banerjee, A., Periyasamy, S., Wolf, I.M., Hinds, T.G., Yong, W., Shou, W. Sanchez, E.R. (2008) Control of glucocorticoid and progesterone receptor subcellular localization by the ligand-binding domain is mediated by distinct interactions with tetratricopeptide repeat proteins. Biochemistry 39, 10471 10480.
3. Baniwal, S.K., Bharti, K., Chan, K.Y. et al. (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J. Biosci. 29, 471 487.
4. Bechtold, N. Pelletier, G. (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol. Biol. 82, 259 266.
5. Bechtold, N., Ellis, J. Pelletier, G. (1993) In planta Agrobacterium-mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C R Acad. Sci. Paris, 316, 1194 1199.
6. Blecher, O., Erel, N., Callebaut, I., Aviezer, K. Breiman, A. (1996) A novel plant peptidyl-prolyl-cis-trans-isomerase (PPIase): cDNA cloning, structural analysis, enzymatic activity and expression. Plant Mol. Biol. 32, 493 504.
7. Boellman, F., Guettouche, T., Guo, J., Fenna, M., Mnayer, L. Voellmy, R. (2004) Daxx interacts with heat shock factor 1 during stress activation and enhances its transcriptional activity. Proc. Natl Acad. Sci. USA 101, 4100 4105.
8. Boter, M., Amigues, B., Peart, J. et al. (2007) Structural and functional analysis of SGT1 reveals that its interaction with HSP90 is required for the accumulation of Rx, an R protein involved in plant immunity. Plant Cell 19, 3791 3804.
9. Bracha-Drori, K., Shichrur, K., Katz, A., Oliva, M., Angelovici, R., Yalovsky, S. Ohad, N. (2004) Detection of protein-protein interactions in plants using bimolecular fluorescence complementation. Plant J. 40, 419 427.
10. Busch, W., Wunderlich, M. Schoffl, F. (2005) Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J. 41, 1 14.
11. Charng, Y.Y., Liu, H.C., Liu, N.Y., Hsu, F.C. Ko, S.S. (2006) Arabidopsis Hsa32, a novel heat shock protein, is essential for acquired thermotolerance during long recovery after acclimation. Plant Physiol. 140, 1297 1305.
12. Charng, Y.Y., Liu, H.C., Liu, N.Y., Chi, W.T., Wang, C.N., Chang, S.H. Wang, T.T. (2007) A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol. 143, 251 262.
13. Clough, S.J. Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735 743.
14. Dafny-Yelin, M., Tzfira, T., Vainstein, A. Adam, Z. (2008) Non-redundant functions of sHSP-CIs in acquired thermotolerance and their role in early seed development in Arabidopsis. Plant Mol. Biol. 67, 363 373.
15. Davies, T.H., Ning, Y.M. Sanchez, E.R. (2005) Differential control of glucocorticoid receptor hormone-binding function by tetratricopeptide repeat (TPR) proteins and the immunosuppressive ligand FK506. Biochemistry 44, 2030 2038.
16. Duncan, R. (2005) Inhibition of Hsp90 function delays and impairs recovery from heat shock. FEBS J. 272, 5244 5256.
17. Eckhoff, A., Granzin, J., Kamphausen, T., Buldt, G., Schulz, B. Weiergraber, O.H. (2005) Crystallization and preliminary X-ray analysis of immunophilin-like FKBP42 from Arabidopsis thaliana. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61, 363 365.
18. Galat, A. (2003) Peptidylprolyl cis/trans isomerases (immunophilins): biological diversity - targets - functions. Curr. Top. Med. Chem. 3, 1315 1347.
19. Galat, A. (2004) A note on clustering the functionally-related paralogues and orthologues of proteins: a case of the FK506-binding proteins (FKBPs). Comput. Biol. Chem. 28, 129 140.
20. Geisler, M., Kolukisaoglu, H.U., Bouchard, R. et al. (2003) TWISTED DWARF1, a unique plasma membrane-anchored immunophilin-like protein, interacts with Arabidopsis multidrug resistance-like transporters AtPGP1 and AtPGP19. Mol. Biol. Cell 14, 4238 4249.
21. Geisler, M., Girin, M., Brandt, S. et al. (2004) Arabidopsis immunophilin-like TWD1 functionally interacts with vacuolar ABC transporters. Mol. Biol. Cell 15, 3393 3405.
22. Goebl, M. Yanagida, M. (1991) The TPR snap helix: a novel protein repeat motif from mitosis to transcription. Trends Biochem. Sci. 16, 173 177.
23. Guo, Y., Guettouche, T., Fenna, M., Boellmann, F., Pratt, W.B., Toft, D.O., Smith, D.F. Voellmy, R. (2001) Evidence for a mechanism of repression of HSF1 transcriptional activity by a multichaperone complex. J. Biol. Chem. 276, 45791 45799.
24. Haralampidis, K., Milioni, D., Rigas, S. Hatzopoulos, P. (2002) Combinatorial interaction of cis elements specifies the expression of the Arabidopsis AtHsp90-1 gene. Plant Physiol. 129, 1138 1149.
25. Harrar, Y., Bellec, Y., Bellini, C. Faure, J.D. (2003) Hormonal control of cell proliferation requires PASTICCINO genes. Plant Physiol. 132, 1217 1227.
26. Harrell, J.M., Kurek, I., Breiman, A., Radanyi, C., Renoir, J.M., Pratt, W.B. Galigniana, M.D. (2002) All of the protein interactions that link steroid receptor hsp90 immunophilin heterocomplexes to cytoplasmic dynein are common to plant and animal cells. Biochemistry 41, 5581 5587.
27. He, Z., Li, L. Luan, S. (2004) Immunophilins and parvulins. Superfamily of peptidyl prolyl isomerases in Arabidopsis. Plant Physiol. 134, 1248 1267.
28. Heerklotz, D., Doring, P., Bonzelius, F., Winkelhaus, S. Nover, L. (2001) The balance of nuclear import and export determines the intracellular distribution and function of tomato heat stress transcription factor HsfA2. Mol. Cell. Biol. 21, 1759 1768.
29. Hubert, D.A., Tornero, P., Belkhadir, Y., Krishna, P., Takahashi, A., Shirasu, K. Dangl, J.L. (2003) Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J. 22, 5679 5689.
30. Kohler, C., Hennig, L., Bouveret, R., Gheyselinck, J., Grossniklaus, U. Gruissem, W. (2003) Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development. EMBO J. 22, 4804 4814.
31. von Koskull-Doring, P., Scharf, K.D. Nover, L. (2007) The diversity of plant heat stress transcription factors. Trends Plant Sci. 12, 452 457.
32. Kotak, S., Larkindale, J., Lee, U., von Koskull-Doring, P., Vierling, E. Scharf, K.D. (2007) Complexity of the heat stress response in plants. Curr. Opin. Plant Biol. 10, 310 316.
33. Krishna, P. Gloor, G. (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6, 238 246.
34. Krishna, P., Reddy, R., Sacco, M., Frappier, J. Felsheim, R. (1997) Analysis of the native forms of the 90 kDa heat shock protein (hsp90) in plant cytosolic extracts. Plant Mol. Biol. 33, 457 466.
35. Kurek, I., Aviezer, K., Erel, N., Herman, E. Breiman, A. (1999) The wheat peptidyl prolyl cis-trans-isomerase FKBP77 is heat induced and developmentally regulated. Plant Physiol. 119, 693 704.
36. Kurek, I., Pirkl, F., Fischer, E., Buchner, J. Breiman, A. (2002) Wheat FKBP73 functions in vitro as a molecular chaperone independently of its peptidyl prolyl cis-trans isomerase activity. Planta 215, 119 126.
37. Larkindale, J. Huang, B. (2004) Thermotolerance and antioxidant systems in Agrostis stolonifera: involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. J. Plant Physiol. 161, 405 413.
38. Larkindale, J. Vierling, E. (2008) Core genome responses involved in acclimation to high temperature. Plant Physiol. 146, 748 761.
39. Larkindale, J., Hall, J.D., Knight, M.R. Vierling, E. (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol. 138, 882 897.
40. Liu, Y., Burch-Smith, T., Schiff, M., Feng, S. Dinesh-Kumar, S.P. (2004) Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J. Biol. Chem. 279, 2101 2108.
41. Mishra, S.K., Tripp, J., Winkelhaus, S., Tschiersch, B., Theres, K., Nover, L. Scharf, K.D. (2002) In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev. 16, 1555 1567.
42. Nair, S.C., Toran, E.J., Rimerman, R.A., Hjermstad, S., Smithgall, T.E. Smih, D.F. (1996) A pathway of multichaperones interactions common to diverse regulatory proteins: estrogen receptor, FES tyrosine kinase, heat shock transcriprion factor 1, and the aryl hydrocarbon receptor. Cell Stress Chaperones 1, 237 250.
43. Nishizawa, A., Yabuta, Y., Yoshida, E., Maruta, T., Yoshimura, K. Shigeoka, S. (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J. 48, 535 547.
44. Ogawa, D., Yamaguchi, K. Nishiuchi, T. (2007) High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth. J. Exp. Bot. 58, 3373 3383.
45. Perez-Perez, J.M., Ponce, M.R. Micol, J.L. (2004) The ULTRACURVATA2 gene of Arabidopsis encodes an FK506-binding protein involved in auxin and brassinosteroid signaling. Plant Physiol. 134, 101 117.
46. Picard, D. (2002) Heat-shock protein 90, a chaperone for folding and regulation. Cell. Mol. Life Sci. 59, 1640 1648.
47. Port, M., Tripp, J., Zielinski, D., Weber, C., Heerklotz, D., Winkelhaus, S., Bublak, D. Scharf, K.D. (2004) Role of Hsp17.4-CII as coregulator and cytoplasmic retention factor of tomato heat stress transcription factor HsfA2. Plant Physiol. 135, 1457 1470.
48. Pratt, W.B., Galigniana, M.D., Harrell, J.M. DeFranco, D.B. (2004) Role of hsp90 and the hsp90-binding immunophilins in signaling protein movement. Cell. Signal. 16, 857 872.
49. Pratt, W.B., Morishima, Y., Murphy, M. Harrell, M. (2006) Chaperoning of glucocorticoid receptors. Handb. Exp. Pharmacol. 172, 111 138.
50. Queitsch, C., Sangster, T.A. Lindquist, S. (2002) Hsp90 as a capacitor of phenotypic variation. Nature 417, 618 624.
51. Reddy, R.K., Kurek, I., Silverstein, A.M., Chinkers, M., Breiman, A. Krishna, P. (1998) High-molecular-weight FK506-binding proteins are components of heat-shock protein 90 heterocomplexes in wheat germ lysate. Plant Physiol. 118, 1395 1401.
52. Romano, P., Gray, J., Horton, P. Luan, S. (2005) Plant immunophilins: functional versatility beyond protein maturation. New Phytol. 166, 753 769.
53. Sangster, T.A., Bahrami, A., Wilczek, A., Watanabe, E., Schellenberg, K., McLellan, C., Kelley, A., Kong, S.W., Queitsch, C. Lindquist, S. (2007) Phenotypic diversity and altered environmental plasticity in Arabidopsis thaliana with reduced Hsp90 levels. PLoS ONE 2, e648.
54. Scharf, K.D., Heider, H., Hohfeld, I., Lyck, R., Schmidt, E. Nover, L. (1998) The tomato Hsf system: HsfA2 needs interaction with HsfA1 for efficient nuclear import and may be localized in cytoplasmic heat stress granules. Mol. Cell. Biol. 18, 2240 2251.
55. Schramm, F., Ganguli, A., Kiehlmann, E., Englich, G., Walch, D. von Koskull-Doring, P. (2006) The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Mol. Biol. 60, 759 772.
56. Smith, D.F., Baggenstoss, B.A., Marion, T.N. Rimerman, R.A. (1993) Two FKBP-related proteins are associated with progesterone receptor complexes. J. Biol. Chem. 268, 18365 18371.
57. Smyczynski, C., Roudier, F., Gissot, L., Vaillant, E., Grandjean, O., Morin, H., Masson, T., Bellec, Y., Geelen, D. Faure, J.D. (2006) The C terminus of the immunophilin PASTICCINO1 is required for plant development and for interaction with a NAC-like transcription factor. J. Biol. Chem. 281, 25475 25484.
58. Standaert, R.F., Galat, A., Verdine, G.L. Schreiber, S.L. (1990) Molecular cloning and overexpression of the human FK506-binding protein FKBP. Nature 346, 671 674.
59. Takahashi, A., Casais, C., Ichimura, K. Shirasu, K. (2003) HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc. Natl Acad. Sci. USA 100, 11777 11782.
60. Vierling, E. Kimpel, J.A. (1992) Plant responses to environmental stress. Curr. Opin. Biotechnol. 3, 164 170.
61. Vittorioso, P., Cowling, R., Faure, J.D., Caboche, M. Bellini, C. (1998) Mutation in the Arabidopsis PASTICCINO1 gene, which encodes a new FK506-binding protein-like protein, has a dramatic effect on plant development. Mol. Cell. Biol. 18, 3034 3043.
62. Voellmy, R. (2004) On mechanisms that control heat shock transcription factor activity in metazoen cells. Cell Stress Chaperones, 9, 122 133.
63. Weiergraber, O.H., Eckhoff, A. Granzin, J. (2006) Crystal structure of a plant immunophilin domain involved in regulation of MDR-type ABC transporters. FEBS Lett. 580, 251 255.
64. Wochnik, G.M., Ruegg, J., Abel, G.A., Schmidt, U., Holsboer, F. Rein, T. (2005) FK506-binding proteins 51 and 52 differentially regulate dynein interaction and nuclear translocation of the glucocorticoid receptor in mammalian cells. J. Biol. Chem. 280, 4609 4616.
65. Yamada, K., Fukao, Y., Hayashi, M., Fukazawa, M., Suzuki, I. Nishimura, M. (2007) Cytosolic HSP90 regulates the heat shock response that is responsible for heat acclimation in Arabidopsis thaliana. J. Biol. Chem. 282, 37794 37804.
66. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L. Gruissem, W. (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621 2632.
67. Zimmermann, P., Hennig, L. Gruissem, W. (2005) Gene-expression analysis and network discovery using Genevestigator. Trends Plant Sci. 10, 407 409.