mADP-RTs: Versatile virulence factors from bacterial pathogens of plants and mammals

Frontiers in Plant Science

Volumn 3, Issue JUN, 2012, Pages

  Wirthmueller, Lennart ^a   Banfield, Mark J ^a  

^a JOHN INNES CENTRE   (United Kingdom)

Author keywords

Crystal structure; Mono ADP ribosyltransferase; Pathogen effector; Plant innate immunity

Indexed keywords

EID: 84888016483     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2012.00142     Document Type: Review

References (38)

1. Axtell, M. J., and Staskawicz, B. J. (2003). Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112, 369-377.
2. Bell, C. E., and Eisenberg, D. (1996). Crystal structure of diphtheria toxin bound to nicotinamide adenine dinucleotide. Biochemistry 35, 1137-1149.
3. Bennett, M. J., and Eisenberg, D. (1994). Refined structure of monomeric diphtheria toxin at 2.3Å resolution. Protein Sci. 3, 1464-1475.
4. Cassel, D., and Pfeuffer, T. (1978). Mechanism of cholera toxin action: covalent modification of the guanyl nucleotide-binding protein of the adenylate cyclase system. Proc. Natl. Acad. Sci. U.S.A. 75, 2669-2673.
5. Chardin, P., Boquet, P., Madaule, P., Popoff, M. R., Rubin, E. J., and Gill, D. M. (1989). The mammalian G protein rhoC is ADP-ribosylated by Clostridium botulinum exoenzyme C3 and affects actin microfilaments in Vero cells. EMBO J. 8, 1087-1092.
6. Collier, R. J. (1967). Effect of diphtheria toxin on protein synthesis: inactivation of one of the transfer factors. J. Mol. Biol. 25, 83-98.
7. Collier, R. J. (2001). Understanding the mode of action of diphtheria toxin: a perspective on progress during the 20th century. Toxicon 39, 1793-1803.
8. Day, B., Dahlbeck, D., Huang, J., Chisholm, S. T., Li, D., and Staskawicz, B. J. (2005). Molecular basis for the RIN4 negative regulation of RPS2 disease resistance. Plant Cell 17, 1295-1305.
9. Deng, Q., and Barbieri, J. T. (2008). Molecular mechanisms of the cytotoxicity of ADP-ribosylating toxins. Annu. Rev. Microbiol. 62, 271-288.
10. Di Girolamo, M., Dani, N., Stilla, A., and Corda, D. (2005). Physiological relevance of the endogenous mono-(ADP-ribosyl)ation of cellular proteins. FEBS J. 272, 4565-4575.
11. Fu, Z. Q., Guo, M., Jeong, B. R., Tian, F., Elthon, T. E., Cerny, R. L., Staiger, D., and Alfano, J. R. (2007). A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447, 284-288.
12. Heintzen, C., Nater, M., Apel, K., and Staiger, D. (1997). AtGRP7, a nuclear RNA-binding protein as a component of a circadian-regulated negative feedback loop in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 94, 8515-8520.
13. Holbourn, K. P., Shone, C. C., and Acharya, K. R. (2006). A family of killer toxins. Exploring the mechanism of ADP-ribosylating toxins. FEBS J. 273, 4579-4593.
14. Honjo, T., Nishizuka, Y., and Hayaishi, O. (1968). Diphtheria toxin-dependent adenosine diphosphate ribosylation of aminoacyl transferase II and inhibition of protein synthesis. J. Biol. Chem. 243, 3553-3555.
15. Hooykaas, P. J., Dulk-Ras, H., and Schilperoort, R. A. (1988). The Agrobacterium tumefaciens T-DNA gene 6b is anonc gene. Plant Mol. Biol. 11, 791-794.
16. Iglewski, B. H., Liu, P. V., and Kabat, D. (1977). Mechanism of action of Pseudomonas aeruginosa exotoxin: adenosine diphosphate-ribosylation of mammalian elongation factor 2 in vitro and in vivo. Infect. Immun. 15, 138-144.
17. Jeong, B. R., Lin, Y., Joe, A., Guo, M., Korneli, C., Yang, H., Wang, P., Yu, M., Cerny, R. L., Staiger, D., Alfano, J. R., and Xu, Y. (2011). Structure function analysis of an ADP-ribosyltransferase type III effector and its RNA-binding target in plant immunity. J. Biol. Chem. 286, 43272-43281.
18. Kidner, C. A., and Martienssen, R. A. (2004). Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428, 81-84.
19. Kim, H. S., Desveaux, D., Singer, A. U., Patel, P., Sondek, J., and Dangl, J. L. (2005). The Pseudomonas syringaeeffector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proc. Natl. Acad. Sci. U.S.A. 102, 6496-6501.
20. Kleine, H., Poreba, E., Lesniewicz, K., Hassa, P. O., Hottiger, M. O., Litchfield, D. W., Shilton, B. H., and Lüscher, B. (2008). Substrate-assisted catalysis by PARP10 limits its activity to mono-ADP-ribosylation. Mol. Cell 32, 57-69.
21. Lamb, R. S., Citarelli, M., and Teotia, S. (2012). Functions of the poly-ADP-ribose-polymerase superfamily in plants. Cell. Mol. Life Sci. 69, 175-189.
22. Mackey, D., Belkhadir, Y., Alonso, J. M., Ecker, J. R., and Dangl J. L. (2003). Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379-389.
23. Navarro, L., Dunoyer, P., Jay, F., Arnold, B., Dharmasiri, N., Estelle, M., Voinnet, O., and Jones, J. D. (2006). A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436-439.
24. O'Neal, C. J., Jobling, M. G., Holmes, R. K., and Hol, W. G. (2005). Structural basis for the activation of cholera toxin by human ARF6-GTP. Science 309, 1093-1096.
25. Robert-Seilaniantz, A., Shan, L., Zhou, J. M., and Tang, X. (2006). The Pseudomonas syringae pv. tomato DC3000 type III effector HopF2 has a putative myristoylation site required for its avirulence and virulence functions. Mol. Plant Microbe Interact. 19, 130-138.
26. Schöning, J. C., Streitner, C., Page, D. R., Hennig, S., Uchida, K., Wolf, E., Furuya, M., and Staiger, D. (2007). Auto-regulation of the circadian slave oscillator component AtGRP7 and regulation of its targets is impaired by a single RNA recognition motif point mutation. Plant J. 52, 1119-1130.
27. Schreiber, V., Dantzer, F., Ame, J. C., and de Murcia, G. (2006). Poly-(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol. 7, 517-28.
28. Sun, J., Maresso, A. W., Kim, J. J. P., and Barbieri, J. T. (2004). How bacterial ADP-ribosylating toxins recognize substrates. Nat. Struct. Mol. Biol. 11, 868-876.
29. Singer, A. U., Desveaux, D., Betts, L., Chang, J. H., Nimchuk, Z., Grant, S. R., Dangl, J. L., and Sondek, J. (2004). Crystal structures of the type III effector protein AvrPphF and its chaperone reveal residues required for plant pathogenesis. Structure 12, 1669-1681.
30. Tinland, B., Huss, B., Paulus, F., Bonnard, G., and Otten, L. (1989). Agrobacterium tumefaciens 6b genes are strain-specific and affect the activity of auxin as well as cytokinin genes. Mol. Gen. Genet. 219, 217-224.
31. Tsiamis, G., Mansfield, J. W., Hockenhull, R., Jackson, R. W., Sesma, A., Athanassopoulos, E., Bennett, M. A., Stevens, C., Vivian, A., Taylor, J. D., and Murillo, J. (2000). Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseolicola, the cause of bean halo-blight disease. EMBO J. 19, 3204-3214.
32. Vanden Broeck, D., Horvath, C., and De Wolf, M. J. (2007). Vibrio cholerae: cholera toxin. Int. J. Biochem. Cell Biol. 39, 1771-1775.
33. van der Hoorn, R. A., and Kamoun, S. (2008). From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20, 2009-2017.
34. Wang, H., Liang, Q., Cao, K., and Ge, X. (2011a). Endogenous protein mono-ADP-ribosylation in Arabidopsis thaliana. Planta 233, 1287-1292.
35. Wang, M., Soyano, T., Machida, S., Yang, J. Y., Jung, C., Chua, N. H., and Yuan, Y. A. (2011b). Molecular insights into plant cell proliferation disturbance by Agrobacterium protein 6b. Genes Dev. 64-76.
36. Wang, Y., Li, J., Hou, S., Wang, X., Li, Y., Ren, D., Chen, S., Tang, X., and Zhou, J. M. (2010). A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell 22, 2033-2044.
37. Wilton, M., Rajagopal, S., Elmore, J., Felsensteiner, C., Coaker, G., and Desvaux, D. (2010). The type III effector HopF2 Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence, Proc. Natl. Acad. Sci. U.S.A. 107, 2349-2354
38. Yang, L., Liu, Z., Lu, F., Dong, A., and Huang, H. (2006). SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. Plant J. 47, 841-850.