The E3 ubiquitin ligase activity of Arabidopsis PLANT U-BOX17 and its functional tobacco homolog ACRE276 are required for cell death and defense

Plant Cell

Volumn 18, Issue 4, 2006, Pages 1084-1098

  Yang, Cheng Wei ^a   González Lamothe, Rocío ^b   Ewan, Richard A ^a   Rowland, Owen ^b,c   Yoshioka, Hirofumi ^b,d   Shenton, Matt ^a   Ye, Heng ^a   O'Donnell, Elizabeth ^a   Jones, Jonathan D G ^b   Sadanandom, Ari ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b JOHN INNES CENTRE   (United Kingdom)

^c CARLETON UNIVERSITY   (Canada)

^d NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; GENES; PLANTS (BOTANY); RNA; TOBACCO;

ACRE276; CLADOSPORIUM FULVUM LEAVES; TOBACCO ACRE276; U-BOX17;

PROTEINS;

CELLS; GENES; NUCLEIC ACIDS; PLANTS; PROTEINS; TOBACCO;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICA NAPUS; BRASSICACEAE; CLADOSPORIUM; CLADOSPORIUM FULVUM; LYCOPERSICON ESCULENTUM; MAGNOLIOPHYTA; NICOTIANA TABACUM; PSEUDOMONAS SYRINGAE; SOLANACEAE; TOBACCO MOSAIC VIRUS;

EID: 33745449581     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.105.039198     Document Type: Article

References (65)

1. Aebersold, D.M., Shaul, Y.D., Yung, Y., Yarom, N., Yao, Z., Hanoch, T., and Seger, R. (2004). Extracellular signal-regulated kinase 1c (ERK1c), a novel 42-kilodalton ERK, demonstrates unique modes of regulation, localization, and function. Mol. Cell. Biol. 24, 10000-10015.
2. Amador, V., Monte, E., Garcia-Martinez, J.L., and Prat, S. (2001). Gibberellins signal nuclear import of PHOR1, a photoperiod-responsive protein with homology to Drosophila armadillo. Cell 106, 343-354.
3. Andrews, E.A., Palecek, J., Sergeant, J., Taylor, E., Lehmann, A.R., and Watts, F.Z. (2005). Nse2, a component of the Smc5-6 complex, is a SUMO ligase required for the response to DNA damage. Mol. Cell. Biol. 25, 185-196.
4. Aravind, L., and Koonin, E.V. (2000). The U box is a modified RING finger-A common domain in ubiquitination. Curr. Biol. 10, R132-R134.
5. Ausubel, F.M. (2005). Are innate immune signaling pathways in plants and animals conserved? Nat. Immunol. 6, 973-979.
6. Azevedo, C., Santos-Rosa, M.J., and Shirasu, K. (2001). The U-box protein family in plants. Trends Plant Sci. 6, 354-358.
7. Bower, M.S., Matias, D.D., Fernandes-Carvalho, E., Mazzurco, M., Gu, T., Rothstein, S.J., and Goring, D.R. (1996). Two members of the thioredoxin-h family interact with the kinase domain of a Brassica S locus receptor kinase. Plant Cell 8, 1641-1650.
8. Cabrillac, D., Cock, J.M., Dumas, C., and Gaude, T. (2001). The S-locus receptor kinase is inhibited by thioredoxins and activated by pollen coat proteins. Nature 410, 220-223.
9. Callis, J., and Vierstra, R.D. (2000). Protein degradation in signaling. Curr. Opin. Plant Biol. 3, 381-386.
10. Ciechanover, A. (1998). The ubiquitin-proteasome pathway. On protein death and cell life. EMBO J. 17, 7151-7160.
11. Dangl, J.L., and Jones, J.D. (2001). Plant pathogens and integrated defence responses to infection. Nature 411, 826-833.
12. Dorey, S., Kopp, M., Geoffroy, P., Fritig, B., and Kauffmann, S. (1999). Hydrogen peroxide from the oxidative burst is neither necessary nor sufficient for hypersensitive cell death induction, phenylalanine ammonia lyase stimulation, salicylic acid accumulation, or scopoletin consumption in cultured tobacco cells treated with elicitin. Plant Physiol. 121, 163-172.
13. Durrant, W.E., Rowland, O., Piedras, P., Hammond-Kosack, K.E., and Jones, J.D. (2000). cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles. Plant Cell 12, 963-977.
14. Erickson, F.L., Holzberg, S., Calderon-Urrea, A., Handley, V., Axtell, M., Corr, C., and Baker, B. (1999). The helicase domain of the TMV replicase proteins induces the N-mediated defence response in tobacco. Plant J. 18, 67-75.
15. González-Lamothe, R., Tsitsigiannis, D.I., Ludwig, A.A., Panicot, M., Shirasu, K., and Jones, J.D.G. (2006). The U-box protein CMPG1 is required for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato. Plant Cell 18, 1067-1083.
16. Grant, J.J., and Loake, G.J. (2000). Role of reactive oxygen intermediates and cognate redox signalling in disease resistance. Plant Physiol. 124, 21-29.
17. Gu, T., Mazzurco, M., Sulaman, W., Matias, D.D., and Goring, D.R. (1998). Binding of an arm repeat protein to the kinase domain of the S-locus receptor kinase. Proc. Natl. Acad. Sci. USA 95, 382-387.
18. Hammond-Kosack, K.E., and Jones, J.D. (1997). Plant disease resistance genes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 575-607.
19. Hammond-Kosack, K.E., Tang, S., Harrison, K., and Jones, J.D. (1998). The tomato Cf-9 disease resistance gene functions in tobacco and potato to confer responsiveness to the fungal avirulence gene product avr 9. Plant Cell 10, 1251-1266.
20. Hardtke, C.S., Okamoto, H., Stoop-Myer, C., and Deng, X.W. (2002). Biochemical evidence for ubiquitin ligase activity of the Arabidopsis COP1 interacting protein 8 (CIP8). Plant J. 30, 385-394.
21. Hatakeyama, S., Yada, M., Matsumoto, M., Ishida, N., and Nakayama, K.I. (2001). U box proteins as a new family of ubiquitin-protein ligases. J. Biol. Chem. 276, 33111-33120.
22. Hershko, A., Heller, H., Elias, S., and Ciechanover, A. (1983). Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown. J. Biol. Chem. 258, 8206-8214.
23. Hochstrasser, M. (2001). SP-RING for SUMO: New functions bloom for a ubiquitin-like protein. Cell 107, 5-8.
24. Horsch, R.B., Rogers, S.G., and Fraley, R.T. (1985). Transgenic plants. Cold Spring Harb. Symp. Quant. Biol. 50, 433-437.
25. Jiang, J., Ballinger, C.A., Wu, Y., Dai, Q., Cyr, D.M., Hohfeld, J., and Patterson, C. (2001). CHIP is a U-box-dependent E3 ubiquitin ligase: Identification of Hsc70 as a target for ubiquitylation. J. Biol. Chem. 276, 42938-42944.
26. Jones, D.T., Taylor, W.R., and Thornton, J.M. (1992). The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8, 275-282.
27. Joosten, M.H., Cozijnsen, T.J., and De Wit, P.J. (1994). Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature 367, 384-386.
28. Kirsch, C., Logemann, E., Lippok, B., Schmelzer, E., and Hahlbrock, K. (2001). A highly specific pathogen-responsive promoter element from the immediate-early activated CMPG1 gene in Petroselinum crispum. Plant J. 26, 217-227.
29. Kumar, S., Tamura, K., and Nei, M. (2004). MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief. Bioinform. 5, 150-163.
30. Lee, Y.H., Kolade, O.O., Nomura, K., Arvidson, D.N., and He, S.Y. (2005). Use of dominant-negative HrpA mutants to dissect Hrp pilus assembly and type III secretion in Pseudomonas syringae pv. tomato. J. Biol. Chem. 280, 21409-21417.
31. Letunic, I., Copley, R.R., Schmidt, S., Ciccarelli, F.D., Doerks, T., Schultz, J., Ponting, C.P., and Bork, P. (2004). SMART 4.0: Towards genomic data integration. Nucleic Acids Res. 32, D142-D144.
32. Liu, Y., Schiff, M., and Dinesh-Kumar, S.P. (2002a). Virus-induced gene silencing in tomato. Plant J. 31, 777-786.
33. Liu, Y., Schiff, M., Serino, G., Deng, X.W., and Dinesh-Kumar, S.P. (2002b). 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.
34. Lorick, K.L., Jensen, J.P., Fang, S., Ong, A.M., Hatakeyama, S., and Weissman, A.M. (1999). RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc. Natl. Acad. Sci. USA 96, 11364-11369.
35. Miki, D., Itoh, R., and Shimamoto, K. (2005). RNA silencing of single and multiple members in a gene family of rice. Plant Physiol. 138, 1903-1913.
36. Murata, S., Minami, Y., Minami, M., Chiba, T., and Tanaka, K. (2001). CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Rep. 2, 1133-1138.
37. Muratani, M., and Tansey, W.P. (2003). How the ubiquitin-proteasome system controls transcription. Nat. Rev. Mol. Cell Biol. 4, 192-201.
38. Muskett, P., and Parker, J. (2003). Role of SGT1 in the regulation of plant R gene signalling. Microbes Infect. 5, 969-976.
39. Navarro, L., Zipfel, C., Rowland, O., Keller, I., Robatzek, S., Boller, T., and Jones, J.D. (2004). The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol. 135, 1113-1128.
40. Nei, M., and Kumar, S. (2000). Molecular Evolution and Phylogenetics. (Oxford, UK: Oxford University Press).
41. Ohi, M.D., Vander Kooi, C.W., Hosenberg, J.A., Chazin, W.J., and Gould, K.L (2003). Structural insights into the U-box, a domain associated with multi-ubiquitination. Nat. Struct. Biol. 10, 250-255.
42. Ohi, M.D., Vander Kooi, C.W., Rosenberg, J.A., Ren, L., Hirsch, J.P., Chazin, W.J., Walz, T., and Gould, K.L. (2005). Structural and functional analysis of essential pre-mRNA splicing factor Prp19p. Mol. Cell. Biol. 25, 451-460.
43. Okui, M., Yamaki, A., Takayanagi, A., Kudoh, J., Shimizu, N., and Shimizu, Y. (2005). Transcription factor single-minded 2 (SIM2) is ubiquitinated by the RING-IBR-RING-type E3 ubiquitin ligases. Exp. Cell Res. 309, 220-228.
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. Piedras, P., Hammond-Kosack, K.E., Harrison, K., and Jones, J.D. (1998). Rapid, Cf-9- and Avr9-dependent production of active oxygen species in tobacco suspension cultures. Mol. Plant Microbe Interact. 11, 1155-1166.
46. Prag, G., Misra, S., Jones, E.A., Ghirlando, R., Davies, B.A., Horazdovsky, B.F., and Hurley, J.H. (2003). Mechanism of ubiquitin recognition by the CUE domain of Vps9p. Cell 113, 609-620.
47. Pringa, E., Martinez-Noel, G., Muller, U., and Harbers, K. (2001). Interaction of the ring finger-related U-box motif of a nuclear dot protein with ubiquitin-conjugating enzymes. J. Biol. Chem. 276, 19617-19623.
48. Rivas, S., Rougon-Cardoso, A., Smoker, M., Schauser, L., Yoshioka, H., and Jones, J.D. (2004). CITRX thioredoxin interacts with the tomato Cf-9 resistance protein and negatively regulates defence. EMBO J. 23, 2156-2165.
49. Rivas, S., and Thomas, C.M. (2005). Molecular interactions between tomato and the leaf mold pathogen Cladosporium fulvum. Annu. Rev. Phytopathol. 43, 395-436.
50. Rowland, O., Ludwig, A.A., Merrick, C.J., Baillieul, F., Tracy, F.E., Durrant, W.E., Fritz-Laylin, L., Nekrasov, V., Sjolander, K., Yoshioka, H., and Jones, J.D. (2005). Functional analysis of Avr9/Cf-9 rapidly elicited genes identifies a protein kinase, ACIK1, that is essential for full Cf-9-dependent disease resistance in tomato. Plant Cell 17, 295-310.
51. Ruiz, M.T., Voinnet, O., and Baulcombe, D.C. (1998). Initiation and maintenance of virus-induced gene silencing. Plant Cell 10, 937-946.
52. Scherer, D.C., Brockman, J.A., Chen, Z., Maniatis, T., and Ballard, D.W. (1995). Signal-induced degradation of I kappa B alpha requires site-specific ubiquitination. Proc. Natl. Acad. Sci. USA 92, 11259-11263.
53. Schultz, J., Milpetz, F., Bork, P., and Ponting, C.P. (1998). SMART, a simple modular architecture research tool: Identification of signaling domains. Proc. Natl. Acad. Sci. USA 95, 5857-5864.
54. Sharma, P.C., Ito, A., Shimizu, T., Terauchi, R., Kamoun, S., and Saitoh, H. (2003). Virus-induced silencing of WIPK and SIPK genes reduces resistance to a bacterial pathogen, but has no effect on the INF1-induced hypersensitive response (HR) in Nicotiana benthamiana. Mol. Genet. Genomics 269, 583-591.
55. Stone, S.L., Anderson, E.M., Mullen, R.T., and Goring, D.R. (2003). ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell 15, 885-898.
56. Thomas, C.M., Jones, D.A., Parniske, M., Harrison, K., Balint-Kurti, P.J., Hatzixanthis, K., and Jones, J.D. (1997). Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell 9, 2209-2224.
57. Thomas, S.G., and Franklin-Tong, V.E. (2004). Self-incompatibility triggers programmed cell death in Papaver pollen. Nature 429, 305-309.
58. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997). The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882.
59. Uknes, S., Mauch-Mani, B., Moyer, M., Potter, S., Williams, S., Dincher, S., Chandler, D., Slusarenko, A., Ward, E., and Ryals, J. (1992). Acquired resistance in Arabidopsis. Plant Cell 4, 645-656.
60. Vierstra, R.D. (2003). The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci. 8, 135-142.
61. Villalobo, E., Morin, L., Moch, C., Lescasse, R., Hanna, M., Xiao, W., and Baroin-Tourancheau, A. (2002). A homologue of CROC-1 in a ciliated protist (Sterkiella histriomuscorum) testifies to the ancient origin of the ubiquitin-conjugating enzyme variant family. Mol. Biol. Evol. 19, 39-48.
62. Wesley, S.V., et al. (2001). Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J. 27, 581-590.
63. Yan, J., Wang, J., Li, Q., Hwang, J.R., Patterson, C., and Zhang, H. (2003). AtCHIP, a U-box-containing E3 ubiquitin ligase, plays a critical role in temperature stress tolerance in Arabidopsis. Plant Physiol. 132, 861-869.
64. Zeng, L.R., Qu, S., Bordeos, A., Yang, C., Baraoidan, M., Yan, H., Xie, Q., Nahm, B.H., Leung, H., and Wang, G.L. (2004). Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16, 2795-2808.
65. Zhang, Y., Higashide, W., Dai, S., Sherman, D.M., and Zhou, D. (2005). Recognition and ubiquitination of Salmonella type III effector SopA by a ubiquitin E3 ligase, HsRMA1. J. Biol. Chem. 280, 38682-38688.