Current knowledge on the Ralstonia solanacearum type III secretion system

Microbial Biotechnology

Volumn 6, Issue 6, 2013, Pages 614-620

  Coll, Núria S ^a   Valls, Marc ^a,b  

^a CENTRE FOR RESEARCH IN AGRICULTURAL GENOMICS CRAG   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AGRICULTURE; ARTICLE; BACTERIAL PLANT DISEASE; BACTERIAL VIRULENCE; BACTERIAL WILT; CROP IMPROVEMENT; FOOD SAFETY; GENOMICS; NONHUMAN; PLANT CELL; RALSTONIA SOLANACEARUM; TYPE III SECRETION SYSTEM;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; PLANT DISEASES; RALSTONIA SOLANACEARUM;

EID: 84881225292     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/1751-7915.12056     Document Type: Article

References (54)

1. Aldon, D., Brito, B., Boucher, C., and Genin, S. (2000) A bacterial sensor of plant cell contact controls the transcriptional induction of Ralstonia solanacearum pathogenicity genes. EMBO J 19: 2304-2314.
2. Angot, A., Peeters, N., Lechner, E., Vailleau, F., Baud, C., Gentzbittel, L., etal. (2006) 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.
3. Arlat, M., Gough, C.L., Zischek, C., Barberis, P.A., Trigalet, A., and Boucher, C.A. (1992) Transcriptional organization and expression of the large hrp gene cluster of Pseudomonas solanacearum. Mol Plant Microbe Interact 5: 187-193.
4. Baltrus, D.A., Nishimura, M.T., Romanchuk, A., Chang, J.H., Mukhtar, M.S., Cherkis, K., etal. (2011) Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLoS Pathog 7: e1002132.
5. Bernoux, M., Timmers, T., Jauneau, A., Briere, C., de Wit, P.J., Marco, Y., and Deslandes, L. (2008) RD19, an Arabidopsis cysteine protease required for RRS1-R-mediated resistance, is relocalized to the nucleus by the Ralstonia solanacearum PopP2 effector. Plant Cell 20: 2252-2264.
6. Boucher, C., Genin, S., and Van Gijsegem, F. (1994) Conservation of secretion pathways for pathogenicity determinants for plant and animal bacteria. Trends Microbiol 1: 175-180.
7. Boucher, C.A., Barberis, P.A., Trigalet, A.P., and Demery, D.A. (1985) Transposon mutagenesis of Pseudomonas solanacearum: isolation of Tn5-induced avirulent mutants. J Gen Microbiol 131: 2449-2457.
8. Brito, B., Marenda, M., Barberis, P., Boucher, C., and Genin, S. (1999) prhJ and hrpG, two new components of the plant signal-dependent regulatory cascade controlled by PrhA in Ralstonia solanacearum. Mol Microbiol 31: 237-251.
9. Brito, B., Aldon, D., Barberis, P., Boucher, C., and Genin, S. (2002) A signal transfer system through three compartments transduces the plant cell contact-dependent signal controlling Ralstonia solanacearum hrp genes. Mol Plant Microbe Interact 15: 109-119.
10. Carney, B.F., and Denny, T.P. (1990) A cloned avirulence gene from Pseudomonas solanacearum determines incompatibility on Nicotiana tabacum at the host species level. J Bacteriol 172: 4836-4843.
11. Chen, X.L., Tang, D.J., Jiang, R.P., He, Y.Q., Jiang, B.L., Lu, G.T., and Tang, J.L. (2011) sRNA-Xcc1, an integron-encoded transposon- and plasmid-transferred trans-acting sRNA, is under the positive control of the key virulence regulators HrpG and HrpX of Xanthomonas campestris pathovar campestris. RNA Biol 8: 947-953.
12. Cunnac, S., Boucher, C., and Genin, S. (2004a) Characterization of the cis-acting regulatory element controlling HrpB-mediated activation of the type III secretion system and effector genes in Ralstonia solanacearum. J Bacteriol 186: 2309-2318.
13. Cunnac, S., Occhialini, A., Barberis, P., Boucher, C., and Genin, S. (2004b) Inventory and functional analysis of the large Hrp regulon in Ralstonia solanacearum: identification of novel effector proteins translocated to plant host cells through the Type III secretion system. Mol Microbiol 53: 115-128.
14. Cunnac, S., Chakravarthy, S., Kvitko, B.H., Russell, A.B., Martin, G.B., and Collmer, A. (2011) Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae. Proc Natl Acad Sci U S A 108: 2975-2980.
15. Deslandes, L., and Rivas, S. (2012) Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci 17: 644-655.
16. Deslandes, L., Olivier, J., Theulieres, F., Hirsch, J., Feng, D.X., Bittner-Eddy, P., etal. (2002) Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc Natl Acad Sci U S A 99: 2404-2409.
17. Deslandes, L., Olivier, J., Peeters, N., Feng, D.X., Khounlotham, M., Boucher, C., etal. (2003) Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc Natl Acad Sci U S A 100: 8024-8029.
18. Genin, S., and Denny, T.P. (2012) Pathogenomics of the Ralstonia solanacearum species complex. Annu Rev Phytopathol 50: 67-89.
19. Genin, S., Gough, C.L., Zischek, C., and Boucher, C.A. (1992) Evidence that the hrpB gene encodes a positive regulator of pathogenicity genes from Pseudomonas solanacearum. Mol Microbiol 6: 3065-3076.
20. Genin, S., Brito, B., Denny, T.P., and Boucher, C. (2005) Control of the Ralstonia solanacearum Type III secretion system (Hrp) genes by the global virulence regulator PhcA. FEBS Lett 579: 2077-2081.
21. Jacobs, J.M., Babujee, L., Meng, F., Milling, A., and Allen, C. (2012) The in planta transcriptome of Ralstonia solanacearum: conserved physiological and virulence strategies during bacterial wilt of tomato. mBio 3: e00114-12.
22. Kamoun, S., and Kado, C.I. (1990) A plant-inducible gene of Xanthomonas campestris pv. campestris encodes an exocellular component required for growth in the host and hypersensitivity on nonhosts. J Bacteriol 172: 5165-5172.
23. Koebnik, R., Kruger, A., Thieme, F., Urban, A., and Bonas, U. (2006) Specific binding of the Xanthomonas campestris pv. vesicatoria AraC-type transcriptional activator HrpX to plant-inducible promoter boxes. J Bacteriol 188: 7652-7660.
24. Lavie, M., Shillington, E., Eguiluz, C., Grimsley, N., and Boucher, C. (2002) PopP1, a new member of the YopJ/AvrRxv family of type III effector proteins, acts as a host-specificity factor and modulates aggressiveness of Ralstonia solanacearum. Mol Plant Microbe Interact 15: 1058-1068.
25. Li, Y.R., Zou, H.S., Che, Y.Z., Cui, Y.P., Guo, W., Zou, L.F., etal. (2011) A novel regulatory role of HrpD6 in regulating hrp-hrc-hpa genes in Xanthomonas oryzae pv. oryzicola. Mol Plant Microbe Interact 24: 1086-1101.
26. Lindeberg, M., Cunnac, S., and Collmer, A. (2012) Pseudomonas syringae type III effector repertoires: last words in endless arguments. Trends Microbiol 20: 199-208.
27. Lipscomb, L., and Schell, M.A. (2011) Elucidation of the regulon and cis-acting regulatory element of HrpB, the AraC-type regulator of a plant pathogen-like type III secretion system in Burkholderia pseudomallei. J Bacteriol 193: 1991-2001.
28. Macho, A.P., Guidot, A., Barberis, P., Beuzon, C.R., and Genin, S. (2010) A Competitive index assay identifies several Ralstonia solanacearum type iii effector mutant strains with reduced fitness in host plants. Mol Plant Microbe Interact 23: 1197-1205.
29. Mansfield, J., Genin, S., Magori, S., Citovsky, V., Sriariyanum, M., Ronald, P., etal. (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 13: 614-629.
30. Martin, C., and French, E.R. (1985) Bacterial Wilt of Potato: Pseudomonas solanacearum, Vol. 13. Lima, Peru: International Potato Center.
31. Monteiro, F., Van Dijk, I., Solé, M., Genin, S., and Valls, M. (2009) Visualising the transcription of Ralstonia solanacearum key pathogenicity genes in planta (Poster). In XIV International Congress on Molecular Plant-Microbe Interactions. Quebec, Canada.
32. Monteiro, F., Genin, S., van Dijk, I., and Valls, M. (2012a) A luminescent reporter evidences active expression of Ralstonia solanacearum type III secretion system genes throughout plant infection. Microbiology 158: 2107-2116.
33. Monteiro, F., Sole, M., van Dijk, I., and Valls, M. (2012b) A chromosomal insertion toolbox for promoter probing, mutant complementation, and pathogenicity studies in Ralstonia solanacearum. Mol Plant Microbe Interact 25: 557-568.
34. Mukaihara, T., Tamura, N., and Iwabuchi, M. (2010) Genome-wide identification of a large repertoire of Ralstonia solanacearum type III effector proteins by a new functional screen. Mol Plant Microbe Interact 23: 251-262.
35. O'Connor, T.J., Boyd, D., Dorer, M.S., and Isberg, R.R. (2012) Aggravating genetic interactions allow a solution to redundancy in a bacterial pathogen. Science 338: 1440-1444.
36. Occhialini, A., Cunnac, S., Reymond, N., Genin, S., and Boucher, C. (2005) Genome-wide analysis of gene expression in Ralstonia solanacearum reveals that the hrpB gene acts as a regulatory switch controlling multiple virulence pathways. Mol Plant Microbe Interact 18: 938-949.
37. Ortiz-Martin, I., Thwaites, R., Macho, A.P., Mansfield, J.W., and Beuzon, C.R. (2010) Positive regulation of the Hrp type III secretion system in Pseudomonas syringae pv. phaseolicola. Mol Plant Microbe Interact 23: 665-681.
38. Plener, L., Manfredi, P., Valls, M., and Genin, S. (2010) PrhG, a transcriptional regulator responding to growth conditions, is involved in the control of the type III secretion system regulon in Ralstonia solanacearum. J Bacteriol 192: 1011-1019.
39. Poueymiro, M., and Genin, S. (2009) Secreted proteins from Ralstonia solanacearum: a hundred tricks to kill a plant. Curr Opin Microbiol 12: 44-52.
40. Poueymiro, M., Cunnac, S., Barberis, P., Deslandes, L., Peeters, N., Cazale-Noel, A.C., etal. (2009) Two type III secretion system effectors from Ralstonia solanacearum GMI1000 determine host-range specificity on tobacco. Mol Plant Microbe Interact 22: 538-550.
41. Racapé, J., Belbahri, L., Engelhardt, S., Lacombe, B., Lee, J., Lochman, J., etal. (2005) Ca2+-dependent lipid binding and membrane integration of PopA, a harpin-like elicitor of the hypersensitive response in tobacco. Mol Microbiol 58: 1406-1420.
42. Robertson, A.E., Wechter, W.P., Denny, T.P., Fortnum, B.A., and Kluepfel, D.A. (2004) Relationship between avirulence gene (avrA) diversity in Ralstonia solanacearum and bacterial wilt incidence. Mol Plant Microbe Interact 17: 1376-1384.
43. Salanoubat, M., Genin, S., Artiguenave, F., Gouzy, J., Mangenot, S., Arlat, M., etal. (2002) Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415: 497-502.
44. Schmidtke, C., Findeiss, S., Sharma, C.M., Kuhfuss, J., Hoffmann, S., Vogel, J., etal. (2012) Genome-wide transcriptome analysis of the plant pathogen Xanthomonas identifies sRNAs with putative virulence functions. Nucleic Acids Res 40: 2020-2031.
45. Solé, M., Popa, C., Mith, O., Sohn, K.H., Jones, J.D., Deslandes, L., and Valls, M. (2012) The awr gene family encodes a novel class of Ralstonia solanacearum type III effectors displaying virulence and avirulence activities. Mol Plant Microbe Interact 25: 941-953.
46. Tamura, N., Murata, Y., and Mukaihara, T. (2005) Isolation of Ralstonia solanacearum hrpB constitutive mutants and secretion analysis of hrpB-regulated gene products that share homology with known type III effectors and enzymes. Microbiology 151: 2873-2884.
47. Tasset, C., Bernoux, M., Jauneau, A., Pouzet, C., Briere, C., Kieffer-Jacquinod, S., etal. (2010) Autoacetylation of the Ralstonia solanacearum effector PopP2 targets a lysine residue essential for RRS1-R-mediated immunity in Arabidopsis. PLoS Pathog 6: e1001202.
48. Thwaites, R., Spanu, P.D., Panopoulos, N.J., Stevens, C., and Mansfield, J.W. (2004) Transcriptional regulation of components of the type III secretion system and effectors in Pseudomonas syringae pv. phaseolicola. Mol Plant Microbe Interact 17: 1250-1258.
49. Turner, M., Jauneau, A., Genin, S., Tavella, M.J., Vailleau, F., Gentzbittel, L., and Jardinaud, M.F. (2009) Dissection of bacterial wilt on Medicago truncatula revealed two type III secretion system effectors acting on root infection process and disease development. Plant Physiol 150: 1713-1722.
50. Valls, M., Genin, S., and Boucher, C. (2006) Integrated regulation of the type III secretion system and other virulence determinants in Ralstonia solanacearum. PLoS Pathog 2: e82.
51. Wengelnik, K., and Bonas, U. (1996) HrpXv, an AraC-type regulator, activates expression of five of the six loci in the hrp cluster of Xanthomonas campestris pv. vesicatoria. J Bacteriol 178: 3462-3469.
52. Yoshimochi, T., Hikichi, Y., Kiba, A., and Ohnishi, K. (2008) The global virulence regulator PhcA negatively controls the Ralstonia solanacearum hrp regulatory cascade by repressing expression of the PrhIR signalling proteins. J Bacteriol 191: 3424-3428.
53. Zhang, Y., Kiba, A., Hikichi, Y., and Ohnishi, K. (2011) prhKLM genes of Ralstonia solanacearum encode novel activators of hrp regulon and are required for pathogenesis in tomato. FEMS Microbiol Lett 317: 75-82.
54. Zou, L.F., Wang, X.P., Xiang, Y., Zhang, B., Li, Y.R., Xiao, Y.L., etal. (2006) Elucidation of the hrp clusters of Xanthomonas oryzae pv. oryzicola that control the hypersensitive response in nonhost tobacco and pathogenicity in susceptible host rice. Appl Environ Microbiol 72: 6212-6224.