Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic era

Molecular Plant Pathology

Volumn 14, Issue 7, 2013, Pages 651-662

  Peeters, Nemo ^a   Guidot, Alice ^a   Vailleau, Fabienne ^a,b   Valls, Marc ^c  

^a LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

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

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; GENETICS; GENOMICS; HOST RANGE; MICROBIOLOGY; PATHOGENICITY; PHYLOGENY; PHYSIOLOGY; PLANT; PLANT DISEASE; RALSTONIA SOLANACEARUM;

GENOMICS; HOST SPECIFICITY; PHYLOGENY; PLANT DISEASES; PLANTS; RALSTONIA SOLANACEARUM;

EID: 84881264308     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/mpp.12038     Document Type: Article

References (124)

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., Sartorel, E., Genschik, P., Boucher, C. and Genin, S. (2006) Ralstonia solanacearum requires F-box-like domain-containing type III effectors to promote disease on several host plants. Proc. Natl. Acad. Sci. USA, 103, 14 620-14 625.
3. Angot, A., Vergunst, A., Genin, S. and Peeters, N. (2007) Exploitation of eukaryotic ubiquitin signaling pathways by effectors translocated by bacterial type III and type IV secretion systems. PLoS Pathog. 3, e3.
4. Araud-Razou, I., Vasse, J., Montrozier, H., Etchebar, C. and Trigalet, A. (1998) Detection and visualization of the major acidic exopolysaccharide of Ralstonia solanacearum and its role in tomato root infection and vascular colonization. Eur. J. Plant Pathol. 104, 795-809.
5. 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.
6. Arlat, M., Van Gijsegem, F., Huet, J.C., Pernollet, J.C. and Boucher, C.A. (1994) PopA1, a protein which induces a hypersensitivity-like response on specific Petunia genotypes, is secreted via the Hrp pathway of Pseudomonas solanacearum. EMBO J. 13, 543-553.
7. Ben, C., Debelle, F., Berges, H., Bellec, A., Jardinaud, M.F., Anson, P., Huguet, T., Gentzbittel, L. and Vailleau, F. (2013) MtQRRS1, a R-locus required for Medicago truncatula quantitative resistance to Ralstonia solanacearum. New Phytol. doi: 10.111/nph.12299.
8. 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.
9. Boucher, C., 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.
10. 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.
11. 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.
12. Brown, D.G. and Allen, C. (2004) Ralstonia solanacearum genes induced during growth in tomato: an inside view of bacterial wilt. Mol. Microbiol. 53, 1641-1660.
13. Carmeille, A., Caranta, C., Dintinger, J., Prior, P., Luisetti, J. and Besse, P. (2006) Identification of QTLs for Ralstonia solanacearum race 3-phylotype II resistance in tomato. Theor. Appl. Genet. 113, 110-121.
14. Cases, I. and de Lorenzo, V. (2001) The black cat/white cat principle of signal integration in bacterial promoters. EMBO J. 20, 1-11.
15. Castillo, J.A. and Greenberg, J.T. (2007) Evolutionary dynamics of Ralstonia solanacearum. Appl. Environ. Microbiol. 73, 1225-1238.
16. Cellier, G., Remenant, B., Chiroleu, F., Lefeuvre, P. and Prior, P. (2012) Phylogeny and population structure of brown rot- and Moko disease-causing strains of Ralstonia solanacearum phylotype II. Appl. Environ. Microbiol. 78, 2367-2375.
17. Clough, S.J., Lee, K.E., Schell, M.A. and Denny, T.P. (1997) A two-component system in Ralstonia (Pseudomonas) solanacearum modulates production of PhcA-regulated virulence factors in response to 3-hydroxypalmitic acid methyl ester. J. Bacteriol. 179, 3639-3648.
18. Coll, N.S. and Valls, M. (2013) Current knowledge on the Ralstonia solanacearum type III secretion system. Microb. Biotechnol. doi: 10.1111/1751-7915.12056.
19. Coupat, B., Chaumeille-Dole, F., Fall, S., Prior, P., Simonet, P., Nesme, X. and Bertolla, F. (2008) Natural transformation in the Ralstonia solanacearum species complex: number and size of DNA that can be transferred. FEMS Microbiol. Ecol. 66, 14-24.
20. Coupat-Goutaland, B., Bernillon, D., Guidot, A., Prior, P., Nesme, X. and Bertolla, F. (2011) Ralstonia solanacearum virulence increased following large interstrain gene transfers by natural transformation. Mol. Plant-Microbe Interact. 24, 497-505.
21. 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.
22. 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.
23. Danesh, D., Aarons, S., McGill, G.E. and Young, N.D. (1994) Genetic dissection of oligogenic resistance to bacterial wilt in tomato. Mol. Plant-Microbe Interact. 7, 464-471.
24. Dang, F.F., Wang, Y.N., Yu, L., Eulgem, T., Lai, Y., Liu, Z.Q., Wang, X., Qiu, A.L., Zhang, T.X. and Lin, J. (2012) CaWRKY40, a WRKY protein of pepper, plays an important role in the regulation of tolerance to heat stress and resistance to Ralstonia solanacearum infection. Plant Cell Environ. 36, 757-774.
25. Delannoy, E., Stanley, W.A., Bond, C.S. and Small, I.D. (2007) Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem. Soc. Trans. 35, 1643-1647.
26. Delaspre, F., Nieto Penalver, C.G., Saurel, O., Kiefer, P., Gras, E., Milon, A., Boucher, C., Genin, S. and Vorholt, J.A. (2007) The Ralstonia solanacearum pathogenicity regulator HrpB induces 3-hydroxy-oxindole synthesis. Proc. Natl. Acad. Sci. USA, 104, 15 870-15 875.
27. Denance, N., Ranocha, P., Oria, N., Barlet, X., Riviere, M.P., Yadeta, K.A., Hoffmann, L., Perreau, F., Clément, G., Maia-Grondard, A., van den Berg, G.C., Savelli, B., Fournier, S., Aubert, Y., Pelletier, S., Thomma, B.P., Molina, A., Jouanin, L., Marco, Y. and Goffner, D. (2012) Arabidopsis wat1 (walls are thin1)-mediated resistance to the bacterial vascular pathogen, Ralstonia solanacearum, is accompanied by cross-regulation of salicylic acid and tryptophan metabolism. Plant J. 73, 225-239.
28. Denny, T.P. and Baek, S.R. (1991) Genetic evidence that extracellular polysaccharide is a virulence factor of Pseudomonas solanacearum. Mol. Plant-Microbe Interact. 4, 198-206.
29. Deslandes, L., Pileur, F., Liaubet, L., Camut, S., Can, C., Williams, K., Holub, E., Beynon, J., Arlat, M. and Marco, Y. (1998) Genetic characterization of RRS1, a recessive locus in Arabidopsis thaliana that confers resistance to the bacterial soilborne pathogen Ralstonia solanacearum. Mol. Plant-Microbe Interact. 11, 659-667.
30. Deslandes, L., Olivier, J., Theulieres, F., Hirsch, J., Feng, D.X., Bittner-Eddy, P., Holub, E., Beynon, J., Arlat, M. and Marco, Y. (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. USA, 99, 2404-2409.
31. Deslandes, L., Olivier, J., Peeters, N., Feng, D.X., Khounlotham, M., Boucher, C., Somssich, I., Genin, S. and Marco, Y. (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. USA, 100, 8024-8029.
32. Digonnet, C., Martinez, Y., Denance, N., Chasseray, M., Dabos, P., Ranocha, P., Marco, Y., Jauneau, A. and Goffner, D. (2012) Deciphering the route of Ralstonia solanacearum colonization in Arabidopsis thaliana roots during a compatible interaction: focus at the plant cell wall. Planta, 236, 1419-1431.
33. Elphinstone, J.G. (2005) The current Bacterial Wilt situation: a global overview. In: Bacterial Wilt Disease and the Ralstonia Solanaceaum Species Complex (Allen, C., Prior, P. and Hayward, A.C., eds), pp. 9-28. St. Paul, MN: The American Phytopathological Society.
34. Erhardt, M., Namba, K. and Hughes, K.T. (2010) Bacterial nanomachines: the flagellum and type III injectisome. Cold Spring Harb. Perspect. Biol. 2, a000299.
35. Fall, S., Mercier, A., Bertolla, F., Calteau, A., Gueguen, L., Perriere, G., Vogel, T.M. and Simonet, P. (2007) Horizontal gene transfer regulation in bacteria as a 'spandrel' of DNA repair mechanisms. PLoS ONE, 2, e1055.
36. Fegan, M. and Prior, P. (2005) How complex is the 'Ralstonia solanacearum Species Complex'. In: Bacterial Wilt Disease and the Ralstonia Solanaceaum Species Complex (Allen, C., Prior, P. and Hayward, A.C., eds), pp. 449-461. St. Paul, MN: The American Phytopathological Society.
37. Feng, D.X., Deslandes, L., Keller, H., Revers, F., Favery, B., Lecomte, P., Hirsch, J., Olivier, J. and Marco, Y. (2004) Isolation and characterization of a novel Arabidopsis thaliana mutant unable to develop wilt symptoms after inoculation with a virulent strain of Ralstonia solanacearum. Phytopathology, 94, 289-295.
38. Feng, D.X., Tasset, C., Hanemian, M., Barlet, X., Hu, J., Trémousaygue, D., Deslandes, L. and Marco, Y. (2012) Biological control of bacterial wilt in Arabidopsis thaliana involves abscisic acid signalling. New Phytol. 194, 1035-1045.
39. Flavier, A.B., Clough, S.J., Schell, M.A. and Denny, T.P. (1997) Identification of 3-hydroxypalmitic acid methyl ester as a novel autoregulator controlling virulence in Ralstonia solanacearum. Mol. Microbiol. 26, 251-259.
40. Gabriel, D.W., Allen, C., Schell, M., Denny, T.P., Greenberg, J.T., Duan, Y.P., Flores-Cruz, Z., Huang, Q., Clifford, J.M., Presting, G., González, E.T., Reddy, J., Elphinstone, J., Swanson, J., Yao, J., Mulholland, V., Liu, L., Farmerie, W., Patnaikuni, M., Balogh, B., Norman, D., Alvarez, A., Castillo, J.A., Jones, J., Saddler, G., Walunas, T., Zhukov, A. and Mikhailova, N. (2006) Identification of open reading frames unique to a select agent: Ralstonia solanacearum race 3 biovar 2. Mol. Plant-Microbe Interact. 19, 69-79.
41. Garg, R.P., Huang, J.Z., Yindeeyoungyeon, W., Denny, T.P. and Schell, M.A. (2000) Multicomponent transcriptional regulation at the complex promoter of the exopolysaccharide I biosynthetic operon of Ralstonia solanacearum. J. Bacteriol. 182, 6659-6666.
42. Genin, S. (2010) Molecular traits controlling host range and adaptation to plants in Ralstonia solanacearum. New Phytol. 187, 920-928.
43. Genin, S. and Denny, T.P. (2012) Pathogenomics of the Ralstonia solanacearum species complex. Annu. Rev. Phytopathol. 50, 67-89.
44. 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.
45. 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.
46. Gillings, M., Fahy, P. and Davies, C. (1993) Restriction analysis of an amplified polygalacturonase gene fragment differentiates strains of the phytopathogenic bacterium Pseudomonas solanacearum. Lett. Appl. Microbiol. 1, 44-48.
47. Godiard, L., Sauviac, L., Torii, K.U., Grenon, O., Mangin, B., Grimsley, N.H. and Marco, Y. (2003) ERECTA, an LRR receptor-like kinase protein controlling development pleiotropically affects resistance to bacterial wilt. Plant J. 36, 353-365.
48. Guidot, A., Prior, P., Schoenfeld, J., Carrere, S., Genin, S. and Boucher, C. (2007) Genomic structure and phylogeny of the plant pathogen Ralstonia solanacearum inferred from gene distribution analysis. J. Bacteriol. 189, 377-387.
49. Guidot, A., Coupat, B., Fall, S., Prior, P. and Bertolla, F. (2009) Horizontal gene transfer between Ralstonia solanacearum strains detected by comparative genomic hybridization on microarrays. ISME J. 3, 549-562.
50. Hernandez-Blanco, C., Feng, D.X., Hu, J., Sanchez-Vallet, A., Deslandes, L., Llorente, F., Berrocal-Lobo, M., Keller, H., Barlet, X., Sánchez-Rodríguez, C., Anderson, L.K., Somerville, S., Marco, Y. and Molina, A. (2007) Impairment of cellulose synthases required for Arabidopsis secondary cell wall formation enhances disease resistance. Plant Cell, 19, 890-903.
51. Hirsch, J., Deslandes, L., Feng, D.X., Balague, C. and Marco, Y. (2002) Delayed symptom development in ein2-1, an Arabidopsis ethylene-insensitive mutant, in response to bacterial wilt caused by Ralstonia solanacearum. Phytopathology, 92, 1142-1148.
52. Ho, M.S., Ou, C., Chan, Y.R., Chien, C.T. and Pi, H. (2008) The utility F-box for protein destruction. Cell. Mol. Life Sci. 65, 1977-2000.
53. Huang, J., Carney, B.F., Denny, T.P., Weissinger, A.K. and Schell, M.A. (1995) A complex network regulates expression of eps and other virulence genes of Pseudomonas solanacearum. J. Bacteriol. 177, 1259-1267.
54. Huang, J., Yindeeyoungyeon, W., Garg, R.P., Denny, T.P. and Schell, M.A. (1998) Joint transcriptional control of xpsR, the unusual signal integrator of the Ralstonia solanacearum virulence gene regulatory network, by a response regulator and a LysR-type transcriptional activator. J. Bacteriol. 180, 2736-2743.
55. Husain, A. and Kelman, A. (1958) Relation of slime production to mechanism of wilting and pathogenicity of Pseudomonas solanacearum. Phytopathology, 48, 155-164.
56. Jacobs, J.M., Babujee, L., Meng, F., Milling, A. and Allen, C. (2012) The inplanta transcriptome of Ralstonia solanacearum: conserved physiological and virulence strategies during bacterial wilt of tomato. Mbio, 3, e00114-12.
57. Jones, J.D. and Dangl, J.L. (2006) The plant immune system. Nature, 444, 323-329.
58. Kajava, A.V., Anisimova, M. and Peeters, N. (2008) Origin and evolution of GALA-LRR, a new member of the CC-LRR subfamily: from plants to bacteria? PLoS ONE, 3, e1694.
59. Kanda, A., Yasukohchi, M., Ohnishi, K., Kiba, A., Okuno, T. and Hikichi, Y. (2003) Ectopic expression of Ralstonia solanacearum effector protein PopA early in invasion results in loss of virulence. Mol. Plant-Microbe Interact. 16, 447-455.
60. Kang, Y.W., Liu, H.L., Genin, S., Schell, M.A. and Denny, T.P. (2002) Ralstonia solanacearum requires type 4 pili to adhere to multiple surfaces and for natural transformation and virulence. Mol. Microbiol. 46, 427-437.
61. Kao, C.C., Barlow, E. and Sequeira, L. (1992) Extracellular polysaccharide is required for wild-type virulence of Pseudomonas solanacearum. J. Bacteriol. 174, 1068-1071.
62. Konstantinidis, K.T. and Tiedje, J.M. (2005) Genomic insights that advance the species definition for prokaryotes. Proc. Natl. Acad. Sci. USA, 102, 2567-2572.
63. Konstantinidis, K.T., Ramette, A. and Tiedje, J.M. (2006) The bacterial species definition in the genomic era. Philos. Trans. R. Soc. London, Ser. B: Biol. Sci. 361, 1929-1940.
64. 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.
65. Lebeau, A., Daunay, M.C., Frary, A., Palloix, A., Wang, J.F., Dintinger, J., Chiroleu, F., Wicker, E. and Prior, P. (2011) Bacterial wilt resistance in tomato, pepper, and eggplant: genetic resources respond to diverse strains in the Ralstonia solanacearum species complex. Phytopathology, 101, 154-165.
66. Lebeau, A., Gouy, M., Daunay, M.C., Wicker, E., Chiroleu, F., Prior, P., Frary, A. and Dintinger, J. (2013) Genetic mapping of a major dominant gene for resistance to Ralstonia solanacearum in eggplant. Theor. Appl. Genet. 126, 143-158.
67. Li, L., Atef, A., Piatek, A., Ali, Z., Piatek, M., Aouida, M., Sharakuu, A., Mahjoub, A., Wang, G., Khan, S., Fedoroff, N.V., Zhu, J.K. and Mahfouz, M.M. (2013) Characterization and DNA-binding specificities of Ralstonia TAL-like effectors. Mol. Plant doi: 10.1093/mp/sst006.
68. Li, Y.R., Zou, H.S., Che, Y.Z., Cui, Y.P., Guo, W., Zou, L.F., Chatterjee, S., Biddle, E.M., Yang, C.H. and Chen, G.Y. (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.
69. 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.
70. Mangin, B., Thoquet, P., Olivier, J. and Grimsley, N.H. (1999) Temporal and multiple quantitative trait loci analyses of resistance to bacterial wilt in tomato permit the resolution of linked loci. Genetics, 151, 1165-1172.
71. Meng, F., Yao, J. and Allen, C. (2011) A MotN mutant of Ralstonia solanacearum is hypermotile and has reduced virulence. J. Bacteriol. 193, 2477-2486.
72. Mole, B.M., Baltrus, D.A., Dangl, J.L. and Grant, S.R. (2007) Global virulence regulation networks in phytopathogenic bacteria. Trends Microbiol. 15, 363-371.
73. 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.
74. 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.
75. 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.
76. Mukhtar, M.S., Deslandes, L., Auriac, M.C., Marco, Y. and Somssich, I.E. (2008) The Arabidopsis transcription factor WRKY27 influences wilt disease symptom development caused by Ralstonia solanacearum. Plant J. 56, 935-947.
77. Murata, Y., Tamura, N., Nakaho, K. and Mukaihara, T. (2006) Mutations in the IrpE gene of Ralstonia solanacearum affects Hrp Pili production and virulence. Mol. Plant-Microbe Interact. 19, 884-895.
78. 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.
79. Orgambide, G., Montrozier, H., Servin, P., Roussel, J., Trigalet-Demery, D. and Trigalet, A. (1991) High heterogeneity of the exopolysaccharides of Pseudomonas solanacearum strain GMI 1000 and the complete structure of the major polysaccharide. J. Biol. Chem. 266, 8312-8321.
80. 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.
81. Plener, L., Boistard, P., Gonzalez, A., Boucher, C. and Genin, S. (2012) Metabolic adaptation of Ralstonia solanacearum during plant infection: a methionine biosynthesis case study. PLoS ONE, 7, e36877.
82. Poueymiro, M. and Genin, S. (2009) Secreted proteins from Ralstonia solanacearum: a hundred tricks to kill a plant. Curr. Opin. Microbiol. 12, 44-52.
83. Poueymiro, M., Cunnac, S., Barberis, P., Deslandes, L., Peeters, N., Cazale-Noel, A.C., Boucher, C. and Genin, S. (2009) Two type III secretion system effectors from Ralstonia solanacearum GMI1000 determine host-range specificity on tobacco. Mol. Plant-Microbe Interact. 22, 538-550.
84. Qian, Y.L., Wang, X.S., Wang, D.Z., Zhang, L.N., Zu, C.L., Gao, Z.L., Zhang, H.J., Wang, Z.Y., Sun, X.Y. and Yao, D.N. (2012) The detection of QTLs controlling bacterial wilt resistance in tobacco (N.tabacum L.). Euphitica, doi: 10.1007/s10681-012-0846-2.
85. Remenant, B., Coupat-Goutaland, B., Guidot, A., Cellier, G., Wicker, E., Allen, C., Fegan, M., Pruvost, O., Elbaz, M., Calteau, A., Salvignol, G., Mornico, D., Mangenot, S., Barbe, V., Médigue, C. and Prior, P. (2010) Genomes of three tomato pathogens within the Ralstonia solanacearum species complex reveal significant evolutionary divergence. BMC Genomics, 11, 379.
86. Remenant, B., de Cambiaire, J.C., Cellier, G., Jacobs, J.M., Mangenot, S., Barbe, V. etal. (2011) Ralstonia syzygii, the blood disease bacterium and some Asian R.solanacearum strains form a single genomic species despite divergent lifestyles. PLoS ONE, 6, e24356.
87. Remenant, B., Babujee, L., Lajus, A., Medigue, C., Prior, P. and Allen, C. (2012) Sequencing of K60, type strain of the major plant pathogen Ralstonia solanacearum. J. Bacteriol. 194, 2742-2743.
88. Remigi, P., Anisimova, M., Guidot, A., Genin, S. and Peeters, N. (2011) Functional diversification of the GALA type III effector family contributes to Ralstonia solanacearum adaptation on different plant hosts. New Phytol. 192, 976-987.
89. Roberts, S.J., Edengreen, S.J., Jones, P. and Ambler, D.J. (1990) Pseudomonas syzygii, sp-nov, the cause of Sumatra disease of cloves. Syst. Appl. Microbiol. 13, 34-43.
90. 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.
91. Salanoubat, M., Genin, S., Artiguenave, F., Gouzy, J., Mangenot, S., Arlat, M., Billault, A., Brottier, P., Camus, J.C., Cattolico, L., Chandler, M., Choisne, N., Claudel-Renard, C., Cunnac, S., Demange, N., Gaspin, C., Lavie, M., Moisan, A., Robert, C., Saurin, W., Schiex, T., Siguier, P., Thébault, P., Whalen, M., Wincker, P., Levy, M., Weissenbach, J. and Boucher, C.A. (2002) Genome sequence of the plant pathogen Ralstonia solanacearum. Nature, 415, 497-502.
92. Schell, M.A. (2000) Control of virulence and pathogenicity genes of Ralstonia solanacearum by an elaborate sensory network. Annu. Rev. Phytopathol. 38, 263-292.
93. Schell, M.A., Denny, T.P. and Huang, J. (1994) VsrA, a second two-component sensor regulating virulence genes of Pseudomonas solanacearum. Mol. Microbiol. 11, 489-500.
94. Singer, A.U., Rohde, J.R., Lam, R., Skarina, T., Kagan, O., Dileo, R., Chirgadze, N.Y., Cuff, M.E., Joachimiak, A., Tyers, M., Sansonetti, P.J., Parsot, C. and Savchenko, A. (2008) Structure of the Shigella T3SS effector IpaH defines a new class of E3 ubiquitin ligases. Nat. Struct. Mol. Biol. 15, 1293-1301.
95. Sole, 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.
96. Taghavi, M., Hayward, C., Sly, I. and Fegan, M. (1996) Analysis of the phylogenetic relationships of straons of Burkholderia solanacearum, Pseudomonas syzygii, and the blood disease bacterium of banana based on 16S rRNA gene sequences. Int. J. Syst. Bacteriol. 46, 10-15.
97. Tampakaki, A.P., Skandalis, N., Gazi, A.D., Bastaki, M.N., Sarris, P.F., Charova, S.N., Kokkinidis, M. and Panopoulos, N.J. (2010) Playing the 'Harp': evolution of our understanding of hrp/hrc genes. Annu. Rev. Phytopathol. 48, 347-370.
98. Tang, X., Xiao, Y. and Zhou, J.M. (2006) Regulation of the type III secretion system in phytopathogenic bacteria. Mol. Plant-Microbe Interact. 19, 1159-1166.
99. Tans-Kersten, J., Huang, H.Y. and Allen, C. (2001) Ralstonia solanacearum needs motility for invasive virulence on tomato. J. Bacteriol. 183, 3597-3605.
100. Tasset, C., Bernoux, M., Jauneau, A., Pouzet, C., Briere, C., Kieffer-Jacquinod, S., Rivas, S., Marco, Y. and Deslandes, L. (2010) Autoacetylation of the Ralstonia solanacearum effector PopP2 targets a lysine residue essential for RRS1-R-mediated immunity in Arabidopsis. PLoS Pathog. 6, e1001202.
101. Thoquet, P., Olivier, J., Sperisen, C., Rogowsky, P., Laterrot, H. and Grimsley, N. (1996a) Quantitative trait loci determining resistance to bacterial wilt in tomato cultivar Hawaii7996. Mol. Plant-Microbe Interact. 9, 826-836.
102. Thoquet, P., Olivier, J., Sperisen, C., Rogowsky, P., Prior, P., Anaïs, G., Mangin, B., Bazin, B., Nazer, R. and Grimsley, N. (1996b) Polygenic resistance of tomato plants to bacterial wilt in the French West Indies. Mol. Plant-Microbe Interact. 9, 837-842.
103. Torii, K.U., Mitsukawa, N., Oosumi, T., Matsuura, Y., Yokoyama, R., Whittier, R.F. and Komeda, Y. (1996) The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell, 8, 735-746.
104. 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.
105. Vailleau, F., Sartorel, E., Jardinaud, M.F., Chardon, F., Genin, S., Huguet, T., Gentzbittel, L. and Petitprez, M. (2007) Characterization of the interaction between the bacterial wilt pathogen Ralstonia solanacearum and the model legume plant Medicago truncatula. Mol. Plant-Microbe Interact. 20, 159-167.
106. 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, 798-807.
107. Van der Linden, L., Bredenkamp, J., Naidoo, S., Fouché-Weich, J., Denby, K.J., Genin, S., Marco, Y. and Berger, D.K. (2013) Gene-for-gene tolerance to bacterial wilt in Arabidopsis. Mol. Plant-Microbe Interact. 26, 398-406.
108. Vasse, J., Frey, P. and Trigalet, A. (1995) Microscopic studies of intercellular infection and protoxylem invasion of tomato roots by Pseudomonas solanacearum. Mol. Plant-Microbe Interact. 8, 241-251.
109. Wairuri, C.K., van der Waals, J.E., van Schalkwyk, A. and Theron, J. (2012) Ralstonia solanacearum needs Flp pili for virulence on potato. Mol. Plant-Microbe Interact. 25, 546-556.
110. Wang, J.F., Olivier, J., Thoquet, P., Mangin, B., Sauviac, L. and Grimsley, N.H. (2000) Resistance of tomato line Hawaii7996 to Ralstonia solanacearum Pss4 in Taiwan is controlled mainly by a major strain-specific locus. Mol. Plant-Microbe Interact. 13, 6-13.
111. Wang, J.F., Ho, F.I., Truong, H.T.H., Huang, S.M., Balatero, C.H., Dittapongpitch, V. and Hidayati, N. (2013a) Identification of major QTLs associated with stable resistance of tomato cultivar 'Hawaii 7996' to Ralstonia solanacearum. Euphytica, 190, 241-252.
112. Wang, K., Dang, F., Liu, Z., Wang, X., Eulgem, T., Lai, Y., Yu, L., She, J., Shi, Y., Lin, J., Chen, C., Guan, D., Qiu, A. and He, S. (2013b) CaWRKY58, encoding a group I WRKY transcription factor of Capsicum annuum, negatively regulates resistance to Ralstonia solanacearum infection. Mol. Plant Pathol. 14, 131-144.
113. 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.
114. Wicker, E., Grassart, L., Coranson-Beaudu, R., Mian, D., Guilbaud, C., Fegan, M. and Prior, P. (2007) Ralstonia solanacearum strains from Martinique (French West Indies) exhibiting a new pathogenic potential. Appl. Environ. Microbiol. 73, 6790-6801.
115. Wicker, E., Grassart, L., Coranson-Beaudu, R., Mian, D. and Prior, P. (2009) Epidemiological evidence for the emergence of a new pathogenic variant of Ralstonia solanacearum in Martinique (French West Indies). Plant Pathol. 58, 853-861.
116. Wicker, E., Lefeuvre, P., de Cambiaire, J.C., Lemaire, C., Poussier, S. and Prior, P. (2012) Contrasting recombination patterns and demographic histories of the plant pathogen Ralstonia solanacearum inferred from MLSA. ISME J. 6, 961-974.
117. Xu, J., Zheng, H.J., Liu, L., Pan, Z.C., Prior, P., Tang, B., Xu, J.S., Zhang, H., Tian, Q., Zhang, L.Q. and Feng, J. (2011) Complete genome sequence of the plant pathogen Ralstonia solanacearum Strain Po82. J. Bacteriol. 193, 4261-4262.
118. Yao, J. and Allen, C. (2006) Chemotaxis is required for virulence and competitive fitness of the bacterial wilt pathogen Ralstonia solanacearum. J. Bacteriol. 188, 3697-3708.
119. Yao, J. and Allen, C. (2007) The plant pathogen Ralstonia solanacearum needs aerotaxis for normal biofilm formation and interactions with its tomato host. J. Bacteriol. 189, 6415-6424.
120. Yoshimochi, T., Hikichi, Y., Kiba, A. and Ohnishi, K. (2009a) The global virulence regulator PhcA negatively controls the Ralstonia solanacearum hrp regulatory cascade by repressing expression of the PrhIR signalling proteins. J. Bacteriol. 1, 3424-3428.
121. Yoshimochi, T., Zhang, Y., Kiba, A., Hikichi, Y. and Ohnishi, K. (2009b) Expression of hrpG and activation of response regulator HrpG are controlled by distinct signal cascades in Ralstonia solanacearum. J. Gen. Plant Pathol. 75, 196-204.
122. 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.
123. Zolobowska, L. and Van Gijsegem, F. (2006) Induction of lateral root structure formation on petunia roots: a novel effect of GMI1000 Ralstonia solanacearum infection impaired in Hrp mutants. Mol. Plant-Microbe Interact. 19, 597-606.
124. Zou, L.F., Wang, X.P., Xiang, Y., Zhang, B., Li, Y.R., Xiao, Y.L., Wang, J.S., Walmsley, A.R. and Chen, G.Y. (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.