Agrobacterium counteracts host-induced degradation of its effector F-box protein

Science Signaling

Volumn 4, Issue 195, 2011, Pages

  Magori, Shimpei ^a   Citovsky, Vitaly ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

F BOX PROTEIN; F BOX PROTEIN VIRD5; F BOX PROTEIN VIRF; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR; BACTERIAL PROTEIN; BENZYLOXYCARBONYLLEUCYL LEUCYL LEUCINE ALDEHYDE; BENZYLOXYCARBONYLLEUCYL-LEUCYL-LEUCINE ALDEHYDE; CYSTEINE PROTEINASE INHIBITOR; LEUPEPTIN; PHOTOPROTEIN; PROTEASOME; UBIQUITIN; VEGETABLE PROTEIN;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL NUCLEUS; HOST PATHOGEN INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; RHIZOBIUM; AMINO ACID SEQUENCE; CONFOCAL MICROSCOPY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; PLANT LEAF; PROTEIN BINDING; RHIZOBIUM RADIOBACTER; TOBACCO; UBIQUITINATION;

AGROBACTERIUM; BACTERIA (MICROORGANISMS);

AGROBACTERIUM TUMEFACIENS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CYSTEINE PROTEINASE INHIBITORS; F-BOX PROTEINS; HOST-PATHOGEN INTERACTIONS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LEUPEPTINS; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; PLANT LEAVES; PLANT PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; TOBACCO; UBIQUITIN; UBIQUITINATION; VIRULENCE FACTORS;

EID: 80054765569     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2002124     Document Type: Article

References (43)

1. B. Lacroix, T. Tzfira, A. Vainstein, V. Citovsky, A case of promiscuity: Agrobacterium's endless hunt for new partners. Trends Genet. 22, 29-37 (2006).
2. S. B. Gelvin, Agrobacterium and plant genes involved in T-DNA transfer and integration. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 223-256 (2000).
3. V. Citovsky, S. V. Kozlovsky,B. Lacroix,A.Zaltsman, M. Dafny-Yelin,S. Vyas, A. Tovkach, T. Tzfira, Biological systems of the host cell involved in Agrobacteriuminfection. Cell. Microbiol. 9, 9-20 (2007).
4. B. Lacroix, A. Loyter, V. Citovsky, Association of the Agrobacterium T-DNA-protein complex with plant nucleosomes. Proc. Natl. Acad. Sci. U.S.A. 105, 15429-15434 (2008).
5. T. Tzfira, M. Vaidya, V. Citovsky, VIP1, an Arabidopsis protein that interacts with Agrobacterium VirE2, is involved in VirE2 nuclear import and Agrobacterium infectivity. EMBO J. 20, 3596-3607 (2001).
6. J. Li, A. Krichevsky, M. Vaidya, T. Tzfira, V. Citovsky, Uncoupling of the functions of the Arabidopsis VIP1 protein in transient and stable plant genetic transformation by Agrobacterium. Proc. Natl. Acad. Sci. U.S.A. 102, 5733-5738 (2005).
7. A. Djamei, A. Pitzschke, H. Nakagami, I. Rajh, H. Hirt, Trojan horse strategy in Agrobacterium transformation: Abusing MAPK defense signaling. Science 318, 453-456 (2007).
8. A. Pitzschke, A. Djamei, M. Teige, H. Hirt, VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression. Proc. Natl. Acad. Sci. U.S.A. 106, 18414-18419 (2009).
9. T. Tzfira, M. Vaidya, V. Citovsky, Involvement of targeted proteolysis in plant genetic transformation by Agrobacterium. Nature 431, 87-92 (2004).
10. B. Schrammeijer, E. Risseeuw, W. Pansegrau, T. J. Regensburg-Tuïnk, W. L. Crosby, P. J. Hooykaas, Interaction of the virulence protein VirF of Agrobacterium tumefaciens with plant homologs of the yeast Skp1 protein. Curr. Biol. 11, 258-262 (2001).
11. L. S. Melchers, M. J. Maroney, A. den Dulk-Ras, D. V. Thompson, H. A. van Vuuren, R. A. Schilperoort, P. J. Hooykaas, Octopine and nopaline strains of Agrobacterium tumefaciens differ in virulence; molecular characterization of the virF locus. Plant Mol. Biol. 14, 249-259 (1990).
12. A. J. Regensburg-Tuïnk, P. J. Hooykaas, Transgenic N. glauca plants expressing bacterial virulence gene virF are converted into hosts for nopaline strains of A. tumefaciens. Nature 363, 69-71 (1993).
13. M. N. Aronson, A. D. Meyer, J. Gyorgyey, L. Katul, H. J. Vetten, B. Gronenborn, T. Timchenko, Clink, a nanovirus-encoded protein, binds both pRB and SKP1. J. Virol. 74, 2967-2972 (2000).
14. N. Baumberger, C. H. Tsai, M. Lie, E. Havecker, D. C. Baulcombe, The Polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr. Biol. 17, 1609-1614 (2007).
15. D. Bortolamiol, M. Pazhouhandeh, K. Marrocco, P. Genschik, V. Ziegler-Graff, The Polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Curr. Biol. 17, 1615-1621 (2007).
16. A. Angot, N. Peeters, E. Lechner, F. Vailleau, C. Baud, L. Gentzbittel, E. Sartorel, P. Genschik, C. Boucher, S. Genin, Ralstonia solanacearum requires F-box-like domain-containing type III effectors to promote disease on several host plants. Proc. Natl. Acad. Sci. U.S.A. 103, 14620-14625 (2006).
17. C. T. Price, S. Al-Khodor, T. Al-Quadan, M. Santic, F. Habyarimana, A. Kalia, Y. A. Kwaik, Molecular mimicry by an F-box effector of Legionella pneumophila hijacks a conserved polyubiquitination machinery within macrophages and protozoa. PLoS Pathog. 5, e1000704 (2009).
18. M. Lomma, D. Dervins-Ravault, M. Rolando, T. Nora, H. J. Newton, F. M. Samson, T. Sahr, L. Gomez-Valero, M. Jules, E. L. Hartland, C. Buchrieser, The Legionella pneumophila F-box protein Lpp2082 (AnkB) modulates ubiquitination of the host protein parvin B and promotes intracellular replication. Cell. Microbiol. 12, 1272-1291 (2010).
19. P. Zhou, P. M. Howley, Ubiquitination and degradation of the substrate recognition subunits of SCF ubiquitin-protein ligases. Mol. Cell 2, 571-580 (1998).
20. J. M. Galan, M. Peter, Ubiquitin-dependent degradation of multiple F-box proteins by an autocatalytic mechanism. Proc. Natl. Acad. Sci. U.S.A. 96, 9124-9129 (1999).
21. N. G. Ayad, S. Rankin, M. Murakami, J. Jebanathirajah, S. Gygi, M. W. Kirschner, Tome-1, a trigger of mitotic entry, is degraded during G1 via the APC. Cell 113, 101-113 (2003).
22. βTrCP/Slimb ubiquitin ligase activates the anaphase promoting complex to allow progression beyond prometaphase. Dev. Cell 4, 813-826 (2003).
23. D. Guardavaccaro, Y. Kudo, J. Boulaire, M. Barchi, L. Busino, M. Donzelli, F. Margottin-Goguet, P. K. Jackson, L. Yamasaki, M. Pagano, Control of meiotic and mitotic progression by the F box protein b-Trcp1 in vivo. Dev. Cell 4, 799-812 (2003).
24. A. C. Vergunst, M. C. van Lier, A. den Dulk-Ras, T. A. Stuve, A. Ouwehand, P. J. Hooykaas, Positive charge is an important feature of the C-terminal transport signal of the VirB/D4-translocated proteins of Agrobacterium. Proc. Natl. Acad. Sci. U.S.A. 102, 832-837 (2005).
25. S. G. Porter, M. F. Yanofsky, E. W. Nester, Molecular characterization of the virD operon from Agrobacterium tumefaciens. Nucleic Acids Res. 15, 7503-7517 (1987).
26. Z. Koukolíkova-Nicola, D. Raineri, K. Stephens, C. Ramos, B. Tinland, E. W. Nester, B. Hohn, Genetic analysis of the virD operon of Agrobacterium tumefaciens: A search for functions involved in transport of T-DNA into the plant cell nucleus and in T-DNA integration. J. Bacteriol. 175, 723-731 (1993).
27. T. S. Lin, C. I. Kado, The virD4 gene is required for virulence while virD3 and orf5 are not required for virulence of Agrobacterium tumefaciens. Mol. Microbiol. 9, 803-812 (1993).
28. V. S. Kalogeraki, J. Zhu, J. L. Stryker, S. C. Winans, The right end of the vir region of an octopine-type Ti plasmid contains four new members of the vir regulon that are not essential for pathogenesis. J. Bacteriol. 182, 1774-1778 (2000).
29. A. C. Vergunst, B. Schrammeijer, A. den Dulk-Ras, C. M. de Vlaam, T. J. Regensburg-Tuïnk, P. J. Hooykaas, VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290, 979-982 (2000).
30. V. Citovsky, Y. Gafni, T. Tzfira, Localizing protein-protein interactions by bimolecular fluorescence complementation in planta. Methods 45, 196-206 (2008).
31. A. Zaltsman, A. Krichevsky, A. Loyter, V. Citovsky, Agrobacterium induces expression of a host F-box protein required for tumorigenicity. Cell Host Microbe 7, 197-209 (2010).
32. J. M. Gagne, B. P. Downes, S. H. Shiu, A. M. Durski, R. D. Vierstra, The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 99, 11519-11524 (2002).
33. H. C. Yen, S. J. Elledge, Identification of SCF ubiquitin ligase substrates by global protein stability profiling. Science 322, 923-929 (2008).
34. J. A. Díaz-Pendón, S. W. Ding, Direct and indirect roles of viral suppressors of RNA silencing in pathogenesis. Annu. Rev. Phytopathol. 46, 303-326 (2008).
35. V. Vance, H. Vaucheret, RNA silencing in plants - Defense and counterdefense. Science 292, 2277-2280 (2001).
36. D. Hermand, F-box proteins: More than baits for the SCF? Cell Div. 1, 30 (2006).
37. R. F. Ditt, K. F. Kerr, P. de Figueiredo, J. Delrow, L.Comai, E. W. Nester, The Arabidopsis thaliana transcriptome in response to Agrobacterium tumefaciens. Mol. Plant Microbe Interact. 19, 665-681 (2006).
38. V. Citovsky, A. Zaltsman, S. V. Kozlovsky, Y. Gafni, A. Krichevsky, Proteasomal degradation in plant-pathogen interactions. Semin. Cell Dev. Biol. 20, 1048-1054 (2009).
39. B. Lacroix, M. Vaidya, T. Tzfira, V. Citovsky, The VirE3 protein of Agrobacterium mimics a host cell function required for plant genetic transformation. EMBO J. 24, 428-437 (2005).
40. T. Tzfira, G. W. Tian, B. Lacroix, S. Vyas, J. Li, Y. Leitner-Dagan, A. Krichevsky, T. Taylor, A. Vainstein, V. Citovsky, pSAT vectors: A modular series of plasmids for autofluorescent protein tagging and expression of multiple genes in plants. Plant Mol. Biol. 57, 503-516 (2005).
41. I. J.Goderis, M. F. De Bolle, I. E. François, P. F.Wouters, W. F. Broekaert, B. P. Cammue, A set of modular plant transformation vectors allowing flexible insertion of up to six expression units. Plant Mol. Biol. 50, 17-27 (2002).
42. P. Más, W. Y. Kim, D. E. Somers, S. A. Kay, Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426, 567-570 (2003).
43. Acknowledgments: We thank S. C. Winans (Cornell University) for the gift of the Agrobacterium strain VIK36. We also thank A. Zaltsman for technical assistance with tomato tumor assay. Funding: Supported by grants from the United States Department of Agriculture National Institute of Food and Agriculture, NIH, NSF, and United States-Israel Binational Agricultural Research and Development Fund to V.C. and by Grant-in-Aid for Japan Society for the Promotion of Science Fellows to S.M. Author contributions: S.M. designed the research, performed the experiments, and wrote the manuscript. V.C. commented on and edited the manuscript. Competing interests: The authors declare that they have no competing financial interests.