Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses

Plant Cell

Volumn 19, Issue 12, 2007, Pages 4061-4076

  Noël, Laurent D ^a,b   Cagna, Giuseppe ^b,c   Stuttmann, Johannes ^a   Wirthmüller, Lennart ^b   Betsuyaku, Shigeyuki ^b   Witte, Claus Peter ^b,d   Bhat, Riyaz ^a,e   Pochon, Nathalie ^a   Colby, Thomas ^b   Parker, Jane E ^b  

^a Centre d'Étude Nucléaire Cadarache   (France)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^c MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

^e Myers Hall 150   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA; NICOTIANA BENTHAMIANA;

EID: 39449086162     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.107.051896     Document Type: Article

References (60)

1. Aarts, N., Metz, M., Holub, E., Staskawicz, B.J., Daniels, M.J., and Parker, J.E. (1998). Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. USA 95: 10306-10311.
2. Austin, M.J., Muskett, P., Kahn, K., Feys, B.J., Jones, J.D., and Parker, J.E. (2002). Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295: 2077-2080.
3. Azevedo, C., Betsuyaku, S., Peart, J., Takahashi, A., Noël, L., Sadanandom, A., Casais, C., Parker, J., and Shirasu, K. (2006). Role of SGT1 in resistance protein accumulation in plant immunity. EMBO J. 25: 2007-2016.
4. Azevedo, C., Sadanandom, A., Kitagawa, K., Freialdenhoven, A., Shirasu, K., and Schulze-Lefert, P. (2002). The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295: 2073-2076.
5. Bansal, P.K., Abdulle, R., and Kitagawa, K. (2004). Sgt1 associates with Hsp90: An initial step of assembly of the core kinetochore complex. Mol. Cell. Biol. 24: 8069-8079.
6. Bhat, R.A., Miklis, M., Schmelzer, E., Schulze-Lefert, P., and Panstruga, R. (2005). Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane micro-domain. Proc. Natl. Acad. Sci. USA 102: 3135-3140.
7. Bieri, S., Mauch, S., Shen, Q.H., Peart, J., Devoto, A., Casais, C., Ceron, F., Schulze, S., Steinbiss, H.H., Shirasu, K., and Schulze-Lefert, P. (2004). RAR1 positively controls steady state levels of barley MLA resistance proteins and enables sufficient MLA6 accumulation for effective resistance. Plant Cell 16: 3480-3495.
8. Bisgrove, S.R., Simonich, M.T., Smith, N.M., Sattler, A., and Innes, R.W. (1994). A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6: 927-933.
9. Boyes, D.C., Nam, J., and Dangl, J.L. (1998). The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. Proc. Natl. Acad. Sci. USA 95: 15849-15854.
10. Brodsky, J.L., and Chiosis, G. (2006). Hsp70 molecular chaperones: Emerging roles in human disease and identification of small molecule modulators. Curr. Top. Med. Chem. 6: 1215-1225.
11. Bukau, B., Weissman, J., and Horwich, A. (2006). Molecular chaperones and protein quality control. Cell 125: 443-451.
12. Catlett, M.G., and Kaplan, K.B. (2006). Sgt1p is a unique co-chaperone that acts as a client adaptor to link Hsp90 to Skp1p. J. Biol. Chem. 281: 33739-33748.
13. Chisholm, S.T., Coaker, G., Day, B., and Staskawicz, B.J. (2006). Host-microbe interactions: Shaping the evolution of the plant immune response. Cell 124: 803-814.
14. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
15. Connell, P., Ballinger, C.A., Jiang, J., Wu, Y., Thompson, L.J., Höhfeld, J., and Patterson, C. (2001). The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins. Nat. Cell Biol. 3: 93-96.
16. Dubacq, C., Guerois, R., Courbeyrette, R., Kitagawa, K., and Mann, C. (2002). Sgt1p contributes to cyclic AMP pathway activity and physically interacts with the adenylyl cyclase Cyr1p/Cdc35p in budding yeast. Eukaryot. Cell 1: 568-582.
17. Erbse, A., Mayer, M.P., and Bukau, B. (2004). Mechanism of substrate recognition by Hsp70 chaperones. Biochem. Soc. Trans. 32: 617-621.
18. Esser, C., Alberti, S., and Hohfeld, J. (2004). Cooperation of molecular chaperones with the ubiquitin/proteasome system. Biochim. Biophys. Acta 1695: 171-188.
19. Falk, A., Feys, B.J., Frost, L.N., Jones, J.D., Daniels, M.J., and Parker, J.E. (1999). EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc. Natl. Acad. Sci. USA 96: 3292-3297.
20. Feys, B.J., Wiermer, M., Bhat, R.A., Moisan, L.J., Medina-Escobar, N., Neu, C., Cabral, A., and Parker, J.E. (2005). Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 17: 2601-2613.
21. Garcia-Ranea, J.A., Mirey, G., Camonis, J., and Valencia, A. (2002). p23 and HSP20/alpha-crystallin proteins define a conserved sequence domain present in other eukaryotic protein families. FEBS Lett. 529: 162-167.
22. Glazebrook, J., Zook, M., Mert, F., Kagan, I., Rogers, E.E., Crute, I.R., Holub, E.B., Hammerschmidt, R., and Ausubel, F.M. (1997). Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics 146: 381-392.
23. Gray, W.M., Muskett, P.R., Chuang, H.W., and Parker, J.E. (2003). Arabidopsis SGT1b is required for SCFTIR1-mediated auxin response. Plant Cell 15: 1310-1319.
24. Hernandez, M.P., Sullivan, W.P., and Toft, D.O. (2002). The assembly and intermolecular properties of the hsp70-Hop-hsp90 molecular chaperone complex. J. Biol. Chem. 277: 38294-38304.
25. Holt, B.F., III, Belkhadir, Y., and Dangl, J.L. (2005). Antagonistic control of disease resistance protein stability in the plant immune system. Science 309: 929-932.
26. Hubert, D.A., Tornero, P., Belkhadir, Y., Krishna, P., Takahashi, A., Shirasu, K., and Dangl, J.L. (2003). Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J. 22: 5679-5689.
27. Iordanskiy, S., Zhao, Y., Dubrovsky, L., Iordanskaya, T., Chen, M., Liang, D., and Bukrinsky, M. (2004). Heat shock protein 70 protects cells from cell cycle arrest and apoptosis induced by human immunodeficiency virus type 1 viral protein R. J. Virol. 78: 9697-9704.
28. Jefferson, R.A. (1987). Assaying chimeric genes in plants: The GUS fusion system. Plant Mol. Biol. Rep. 5: 387-405.
29. Kitagawa, K., Skowyra, D., Elledge, S.J., Harper, J.W., and Heiter, P. (1999). SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a subunit of the SCF ubiquitin ligase complex. Mol. Cell 4: 21-33.
30. Krobitsch, S., and Lindquist, S. (2000). Aggregation of huntingtin in yeast varies with the length of the polyglutamine expansion and the expression of chaperone proteins. Proc. Natl. Acad. Sci. USA 97: 1589-1594.
31. Lee, Y.T., Jacob, J., Michowski, W., Nowotny, M., Kuznicki, J., and Chazin, W.J. (2004). Human Sgt1 binds HSP90 through the CHORD-Sgt1 domain and not the tetratricopeptide repeat domain. J. Biol. Chem. 279: 16511-16517.
32. Leister, R.T., Dahlbeck, D., Day, B., Li, Y., Chesnokova, O., and Staskawicz, B.J. (2005). Molecular genetic evidence for the role of SGT1 in the intramolecular complementation of Bs2 protein activity in Nicotiana benthamiana. Plant Cell 17: 1268-1278.
33. Lin, B.L., Wang, J.S., Liu, H.C., Chen, R.W., Meyer, Y., Barakat, A., and Delseny, M. (2001). Genomic analysis of the Hsp70 superfamily in Arabidopsis thaliana. Cell Stress Chaperones 6: 201-208.
34. Lingelbach, L.B., and Kaplan, K.B. (2004). The interaction between Sgt1p and Skp1p is regulated by HSP90 chaperones and is required for proper CBF3 assembly. Mol. Cell. Biol. 24: 8938-8950.
35. Lipka, V., et al. (2005). Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310: 1180-1183.
36. Liu, Y., Schiff, M., Serino, G., Deng, X.W., and Dinesh-Kumar, S.P. (2002a). Role of SCF ubiquitin-ligase and the COP9 signalosome in the N gene-mediated resistance response to Tobacco mosaic virus. Plant Cell 14: 1483-1496.
37. Liu, Y.L., Burch-Smith, T., Schiff, M., Feng, S.H., and 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.
38. Liu, Y.L., Schiff, M., Marathe, R., and Dinesh-Kumar, S.P. (2002b). Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J. 30: 415-429.
39. Lu, R., Malcuit, I., Moffett, P., Ruiz, M.T., Peart, J., Wu, A.J., Rathjen, J.P., Bendahmane, A., Day, L., and Baulcombe, D.C. (2003). High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J. 22: 5690-5699.
40. Lyapina, S., Cope, G., Shevchenko, A., Serino, G., Tsuge, T., Zhou, C.S., Wolf, D.A., Wei, N., and Deshaies, R.J. (2001). Promotion of NEDD8-CUL1 conjugate cleavage by COP9 signalosome. Science 292: 1382-1385.
41. Muskett, P., and Parker, J. (2003). Role of SGT1 in the regulation of plant R gene signalling. Microbes Infect. 5: 969-976.
42. Muskett, P.R., Kahn, K., Austin, M.J., Moisan, L.J., Sadanandom, A., Shirasu, K., Jones, J.D.G., and Parker, J.E. (2002). Arabidopsis RAR1 exerts rate-limiting control of R gene-mediated defenses against multiple pathogens. Plant Cell 14: 979-992.
43. Parker, J.E., Holub, E.B., Frost, L.N., Falk, A., Gunn, N.D., and Daniels, M.J. (1996). Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell 8: 2033-2046.
44. Peart, J.R., et al. (2002). Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proc. Natl. Acad. Sci. USA 99: 10865-10869.
45. Pratt, W.B., Galigniana, M.D., Morishima, Y., and Murphy, P.J. (2004). Role of molecular chaperones in steroid receptor action. Essays Biochem. 40: 41-58.
46. Rizzo, M.A., Springer, G.H., Granada, B., and Piston, D.W. (2004). An improved cyan fluorescent protein variant useful for FRET. Nat. Biotechnol. 22: 445-449.
47. Rudiger, S., Germeroth, L., Schneider-Mergener, J., and Bukau, B. (1997). Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J. 16: 1501-1507.
48. Shah, K., Russinova, E., Gadella, T.W.J., Willemse, J., and de Vries, S.C. (2002). The Arabidopsis kinase-associated protein phosphatase controls internalization of the somatic embryogenesis receptor kinase 1. Genes Dev. 16: 1707-1720.
49. Shevchenko, A., Chernushevich, I., Wilm, M., and Mann, M. (2000). De novo peptide sequencing by nanoelectrospray tandem mass spectrometry using triple quadrupole and quadrupole/time-of-flight instruments. Methods Mol. Biol. 146: 1-16.
50. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996). Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. Anal. Chem. 68: 850-858.
51. Shirasu, K., Lahaye, T., Tan, M.W., Zhou, F., Azevedo, C., and Schulze-Lefert, P. (1999). A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell 99: 355-366.
52. Shirasu, K., and Schulze-Lefert, P. (2003). Complex formation, promiscuity and multi-functionality: Protein interactions in disease-resistance pathways. Trends Plant Sci. 8: 252-258.
53. Spiechowicz, M., Zylicz, A., Bieganowski, P., Kuznicki, J., and Filipek, A. (2007). Hsp70 is a new target of Sgt1 - An interaction modulated by S100A6. Biochem. Biophys. Res. Commun. 357: 1148-1153.
54. Sung, D.Y., and Guy, C.L. (2003). Physiological and molecular assessment of altered expression of Hsc70-1 in Arabidopsis. Evidence for pleiotropic consequences. Plant Physiol. 132: 979-987.
55. Takahashi, A., Casais, C., Ichimura, K., and 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.
56. Tor, M., Gordon, P., Cuzick, A., Eulgem, T., Sinapidou, E., Mert-Turk, F., Can, C., Dangl, J.L., and Holub, E.B. (2002). Arabidopsis SGT1b is required for defense signaling conferred by several downy mildew resistance genes. Plant Cell 14: 993-1003.
57. Tornero, P., Merritt, P., Sadanandom, A., Shirasu, K., Innes, R.W., and Dangl, J.L. (2002). RAR1 and NDR1 contribute quantitatively to disease resistance in Arabidopsis, and their relative contributions are dependent on the R gene assayed. Plant Cell 14: 1005-1015.
58. Witte, C.P., Noël, L.D., Gielbert, J., Parker, J.E., and Romeis, T. (2004). Rapid one-step protein purification from plant material using the eight-amino acid StrepII epitope. Plant Mol. Biol. 55: 135-147.
59. Young, J.C., Barral, J.M., and Ulrich Hartl, F. (2003). More than folding: Localized functions of cytosolic chaperones. Trends Biochem. Sci. 28: 541-547.
60. Zhao, R., et al. (2005). Navigating the chaperone network: An integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 120: 715-727.