Proteasome-Mediated Turnover of the Transcription Coactivator NPR1 Plays Dual Roles in Regulating Plant Immunity

Cell

Volumn 137, Issue 5, 2009, Pages 860-872

  Spoel, Steven H ^a   Mou, Zhonglin ^a   Tada, Yasuomi ^a   Spivey, Natalie W ^a   Genschik, Pascal ^b   Dong, Xinnian ^a  

^a DUKE UNIVERSITY   (United States)

^b CNRS   (France)

Author keywords

SIGNALING

Indexed keywords

CULLIN; NONEXPRESSOR OF PATHOGENESIS RELATED PR PROTEIN; NUCLEAR PROTEIN; PROTEASOME; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS; GENE ACTIVATION; GENE TARGETING; GENETIC TRANSCRIPTION; IMMUNE RESPONSE; IMMUNOREGULATION; NONHUMAN; PHYTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SYSTEMIC ACQUIRED RESISTANCE; TRANSCRIPTION REGULATION;

EID: 65849096454     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2009.03.038     Document Type: Article

References (42)

1. Cao H., Bowling S.A., Gordon A.S., and Dong X. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6 (1994) 1583-1592
2. Cao H., Glazebrook J., Clarke J.D., Volko S., and Dong X. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88 (1997) 57-63
3. Chi Y., Huddleston M.J., Zhang X., Young R.A., Annan R.S., Carr S.A., and Deshaies R.J. Negative regulation of Gcn4 and Msn2 transcription factors by Srb10 cyclin-dependent kinase. Genes Dev. 15 (2001) 1078-1092
4. Collins G.A., and Tansey W.P. The proteasome: a utility tool for transcription?. Curr. Opin. Genet. Dev. 16 (2006) 197-202
5. Delaney T.P., Friedrich L., and Ryals J.A. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc. Natl. Acad. Sci. USA 92 (1995) 6602-6606
6. Després C., Chubak C., Rochon A., Clark R., Bethune T., Desveaux D., and Fobert P.R. The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell 15 (2003) 2181-2191
7. Després C., DeLong C., Glaze S., Liu E., and Fobert P.R. The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell 12 (2000) 279-290
8. Dieterle M., Thomann A., Renou J.P., Parmentier Y., Cognat V., Lemonnier G., Muller R., Shen W.H., Kretsch T., and Genschik P. Molecular and functional characterization of Arabidopsis Cullin 3A. Plant J. 41 (2005) 386-399
9. Durrant W.E., and Dong X. Systemic acquired resistance. Annu. Rev. Phytopathol. 42 (2004) 185-209
10. Fan W., and Dong X. In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis. Plant Cell 14 (2002) 1377-1389
11. Figueroa P., Gusmaroli G., Serino G., Habashi J., Ma L., Shen Y., Feng S., Bostick M., Callis J., Hellmann H., et al. Arabidopsis has two redundant Cullin3 proteins that are essential for embryo development and that interact with RBX1 and BTB proteins to form multisubunit E3 ubiquitin ligase complexes in vivo. Plant Cell 17 (2005) 1180-1195
12. Hayden M.S., and Ghosh S. Signaling to NF-κB. Genes Dev. 18 (2004) 2195-2224
13. Heidel A.J., Clarke J.D., Antonovics J., and Dong X. Fitness costs of mutations affecting the systemic acquired resistance pathway in Arabidopsis thaliana. Genetics 168 (2004) 2197-2206
14. Johnson C., Boden E., and Arias J. Salicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis. Plant Cell 15 (2003) 1846-1858
15. Karin M., and Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu. Rev. Immunol. 18 (2000) 621-663
16. Kim S.Y., Herbst A., Tworkowski K.A., Salghetti S.E., and Tansey W.P. Skp2 regulates Myc protein stability and activity. Mol. Cell 11 (2003) 1177-1188
17. Kinkema M., Fan W., and Dong X. Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12 (2000) 2339-2350
18. Kodadek T., Sikder D., and Nalley K. Keeping transcriptional activators under control. Cell 127 (2006) 261-264
19. Lebel E., Heifetz P., Thorne L., Uknes S., Ryals J., and Ward E. Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis. Plant J. 16 (1998) 223-233
20. Liao S.M., Zhang J., Jeffery D.A., Koleske A.J., Thompson C.M., Chao D.M., Viljoen M., van Vuuren H.J.J., and Young R.A. A kinase-cyclin pair in the RNA polymerase II holoenzyme. Nature 374 (1995) 193-196
21. Lipford J.R., Smith G.T., Chi Y., and Deshaies R.J. A putative stimulatory role for activator turnover in gene expression. Nature 438 (2005) 113-116
22. Lonard D.M., Nawaz Z., Smith C.L., and O'Malley B.W. The 26S proteasome is required for estrogen receptor-alpha and coactivator turnover and for efficient estrogen receptor-alpha transactivation. Mol. Cell 5 (2000) 939-948
23. Luke-Glaser S., Roy M., Larsen B., Le Bihan T., Metalnikov P., Tyers M., Peter M., and Pintard L. CIF-1, a shared subunit of the COP9/signalosome and eukaryotic initiation factor 3 complexes, regulates MEL-26 levels in the Caenorhabditis elegans embryo. Mol. Cell. Biol. 27 (2007) 4526-4540
24. Mou Z., Fan W., and Dong X. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113 (2003) 935-944
25. Muratani M., Kung C., Shokat K.M., and Tansey W.P. The F box protein Dsg1/Mdm30 is a transcriptional coactivator that stimulates Gal4 turnover and cotranscriptional mRNA processing. Cell 120 (2005) 887-899
26. Petroski M.D., and Deshaies R.J. Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 6 (2005) 9-20
27. Pintard L., Willis J.H., Willems A., Johnson J.L., Srayko M., Kurz T., Glaser S., Mains P.E., Tyers M., Bowerman B., et al. The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitin-ligase. Nature 425 (2003) 311-316
28. Reid G., Hubner M.R., Metivier R., Brand H., Denger S., Manu D., Beaudouin J., Ellenberg J., and Gannon F. Cyclic, proteasome-mediated turnover of unliganded and liganded ERα on responsive promoters is an integral feature of estrogen signaling. Mol. Cell 11 (2003) 695-707
29. Rochon A., Boyle P., Wignes T., Fobert P.R., and Després C. The coactivator function of Arabidopsis NPR1 requires the core of its BTB/POZ domain and the oxidation of C-terminal cysteines. Plant Cell 18 (2006) 3670-3685
30. Ryals J., Weymann K., Lawton K., Friedrich L., Ellis D., Steiner H.Y., Johnson J., Delaney T.P., Jesse T., Vos P., et al. The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor IκB. Plant Cell 9 (1997) 425-439
31. Salghetti S.E., Muratani M., Wijnen H., Futcher B., and Tansey W.P. Functional overlap of sequences that activate transcription and signal ubiquitin-mediated proteolysis. Proc. Natl. Acad. Sci. USA 97 (2000) 3118-3123
32. Smalle J., and Vierstra R.D. The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55 (2004) 555-590
33. Szutorisz H., Georgiou A., Tora L., and Dillon N. The proteasome restricts permissive transcription at tissue-specific gene loci in embryonic stem cells. Cell 127 (2006) 1375-1388
34. Tada Y., Spoel S.H., Pajerowska-Mukhtar K., Mou Z., Song J., and Dong X. S-nitrosylation and thioredoxins regulate conformational changes of NPR1 in plant innate immunity. Science 321 (2008) 952-956
35. Thomann A., Brukhin V., Dieterle M., Gheyeselinck J., Vantard M., Grossniklaus U., and Genschik P. Arabidopsis CUL3A and CUL3B genes are essential for normal embryogenesis. Plant J. 43 (2005) 437-448
36. van Hulten M., Pelser M., van Loon L.C., Pieterse C.M.J., and Ton J. Costs and benefits of priming for defense in Arabidopsis. Proc. Natl. Acad. Sci. USA 103 (2006) 5602-5607
37. von der Lehr N., Johansson S., Wu S., Bahram F., Castell A., Cetinkaya C., Hydbring P., Weidung I., Nakayama K., Nakayama K.I., et al. The F-box protein Skp2 participates in c-Myc proteosomal degradation and acts as a cofactor for c-Myc-regulated transcription. Mol. Cell 11 (2003) 1189-1200
38. Wang D., Amornsiripanitch N., and Dong X. A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog. 2 (2006) e123 10.1371/journal.ppat.0020123
39. Wang D., Weaver N.D., Kesarwani M., and Dong X. Induction of protein secretory pathway is required for systemic acquired resistance. Science 308 (2005) 1036-1040
40. Wu R.C., Feng Q., Lonard D.M., and O'Malley B.W. SRC-3 coactivator functional lifetime is regulated by a phospho-dependent ubiquitin time clock. Cell 129 (2007) 1125-1140
41. Zhang Y., Fan W., Kinkema M., Li X., and Dong X. Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc. Natl. Acad. Sci. USA 96 (1999) 6523-6528
42. Zhou J.M., Trifa Y., Silva H., Pontier D., Lam E., Shah J., and Klessig D.F. NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol. Plant Microbe Interact. 13 (2000) 191-202