A Eucalyptus bacterial wilt isolate from South Africa is pathogenic on Arabidopsis and manipulates host defences

Forest Pathology

Volumn 41, Issue 2, 2011, Pages 101-113

  Naidoo, S ^a   Fouche Weich J ^a   Law, P ^a   Denby, K J ^b   Marco, Y ^c   Berger, D K ^a  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DISEASE; DICOTYLEDON; GENE EXPRESSION; GENETIC ANALYSIS; GENOMICS; HYPOTHESIS TESTING; PATHOGENICITY; WILT;

SOUTH AFRICA;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); BOTRYOTINIA FUCKELIANA; EUCALYPTUS; LYCOPERSICON ESCULENTUM; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. TOMATO; RALSTONIA SOLANACEARUM;

EID: 79953320417     PISSN: 14374781     EISSN: 14390329     Source Type: Journal    
DOI: 10.1111/j.1439-0329.2010.00642.x     Document Type: Article

References (63)

1. Adie, B. A.; Perez-Perez, J.; Perez-Perez, M. M.; Godoy, M.; Sanchez-Serrano, J. J.; Schmelz, E. A.; Solano, R., 2007: ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19, 1665-1681.
2. Aldon, D.; Brito, B.; Boucher, C.; Genin, S., 2000: A bacterial sensor of plant cell contact controls the transcriptional induction of Ralstonia solanacearum pathogenicity genes. EMBO J. 19, 2304-2314.
3. Angot, A.; Peeters, N.; Lechner, E.; Vailleau, F.; Baud, C.; Gentzbittel, L.; Sartorel, E.; Genschik, P.; Boucher, C.; 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. U.S.A. 103, 14620-14625.
4. Arlat, M.; Gough, C. L.; Zischek, C.; Barberis, P. A.; Trigalet, A.; Boucher, C. A., 1992: Transcriptional organization and expression of the large hrp gene cluster of Pseudomonas solanacearum. Mol. Plant Microbe Interact. 5, 187-193.
5. Beißbarth, T.; Speed, T. P., 2004: GOstat: find statistically overrepresented gene ontologies within a group of genes. Bioinformatics 20, 1464-1465.
6. Boucher, C. A.; Barberis, P.; Trigalet, A. P.; Demery, D. A., 1985: Transposon mutagenesis of Pseudomonas solanacearum: isolation of Tn5-induced avirulent mutants. J. Gen. Microbiol. 131, 2449-2457.
7. Cao, P. J.; Bartley, L. E.; Jung, K. H.; Ronald, P. C., 2008: Construction of a rice glycosyltransferase phylogenomic database and identification of rice-diverged glycosyltransferases. Mol. Plant 1, 858.
8. Coutinho, T. A.; Roux, J.; Riedel, K. H.; Terblanche, J.; Wingfield, M. J., 2000: First report of bacterial wilt caused by Ralstonia solanacearum on eucalypts in South Africa. For. Pathol. 30, 205-210.
9. Cunnac, S.; Boucher, C.; 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.
10. Cunnac, S.; Occhialini, A.; Barberis, P.; Boucher, C.; 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.
11. Dardick, C.; Ronald, P., 2006: Plant and animal pathogen recognition receptors signal through non-RD kinases. PLoS Pathog. 2, e2.
12. Debroy, S.; Thilmony, R.; Kwack, Y. B.; Nomura, K.; He, S. Y., 2004: A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proc. Natl Acad. Sci. U.S.A. 101, 9927-9932.
13. Deslandes, L.; Pileur, F.; Liaubet, L.; Camut, S.; Can, C.; Williams, K.; Holub, E.; Beynon, J.; Arlat, M.; 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.
14. Deslandes, L.; Olivier, J.; Theulieres, F.; Hirsch, J.; Feng, D. X.; Bittner-Eddy, P.; Beynon, J.; 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. U.S.A. 99, 2404-2409.
15. Felix, G.; Duran, J. D.; Volko, S.; Boller, T., 1999: Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265-276.
16. Fouché-Weich, J.; Poussier, S.; Trigalet Demery, D.; Berger, D.; Coutinho, T., 2006: Molecular identification of some African strains of Ralstonia solanacearum from eucalypt and potato. J. Gen. Plant Pathol. 72, 369-373.
17. Freebain, H. T.; Buddenhagen, I. W., 1964: Ethylene production by Pseudomonas solanacearum. Nature 202, 313-314.
18. 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.; Gonzalez, 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.; 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.
19. Genin, S.; Boucher, C., 2002b: Ralstonia solanacearum: secrets of a major pathogen unveiled by analysis of its genome. Mol. Plant Pathol. 3, 111-118.
20. Glazebrook, J., 2005: Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Ann. Rev. Phytopathol. 43, 205-227.
21. Grant, M. R.; Jones, J. D., 2009: Hormone (dis)harmony moulds plant health and disease. Science 324, 750-752.
22. He, P.; Shan, L.; Lin, N. C.; Martin, G. B.; Kemmerling, B.; Nurnberger, T.; Sheen, J., 2006: Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125, 563-575.
23. He, K.; Gou, X.; Yuan, T.; Lin, H.; Asami, T.; Yoshida, S.; Russell, S. D.; Li, J., 2007: BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Curr. Biol. 17, 1109-1115.
24. Hernandez-Blanco, C.; Feng, D. X.; Hu, J.; Sanchez-Vallet, A.; Deslandes, L.; Llorente, F.; Berrocal-Lobo, M.; Keller, H.; Barlet, X.; Sanchez-Rodriguez, C.; Anderson, L. K.; Somerville, S.; Marco, Y.; Molina, A., 2007: Impairment of cellulose synthases required for Arabidopsis secondary cell wall formation enhances disease resistance. Plant Cell 19, 890-903.
25. Hikichi, Y.; Yoshimochi, T.; Tsujimoto, S.; Shinohara, R.; Nakaho, K.; Kanda, A.; Kiba, A.; Ohnishi, K., 2007: Global regulation of pathogenicity mechanism of Ralstonia solanacearum. Plant Biotech. 24, 149-154.
26. Hirsch, J.; Deslandes, L.; Feng, D. X.; Balague, C.; 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.
27. Hu, J.; Barlet, X.; Deslandes, L.; Hirsch, J.; Feng, D. X.; Somssich, I.; Marco, Y., 2008: Transcriptional responses of Arabidopsis thaliana during wilt disease caused by the soil-borne phytopathogenic bacterium, Ralstonia solanacearum. PLoS ONE 3, e2589.
28. Jones, J. D.; Dangl, J. L., 2006: The plant immune system. Nature 444, 323-329.
29. Law, P. J.; Claudel-Renard, C.; Joubert, F.; Louw, A. I.; Berger, D. K., 2008: MADIBA: a web server toolkit for biological interpretation of plasmodium and plant gene clusters. BMC Genomics 9, 105-116.
30. Maniatis, T.; Fritsch, E. F.; Sambrook, J., 1982: Molecular Cloning. New York: Cold Spring Harbor Laboratory, Cold Spring Harbor.
31. Meyer, A.; Puhler, A.; Niehaus, K., 2001: The lipopolysaccharides of the phytopathogen Xanthomonas campestris pv. campestris induce an oxidative burst reaction in cell cultures of Nicotiana tabacum. Planta 213, 214-222.
32. Meyer, D.; Cunnac, S.; Gueneron, M.; Declercq, C.; Van Gijsegem, F.; Lauber, E.; Boucher, C.; Arlat, M., 2006: PopF1 and PopF2, two proteins secreted by the type III protein secretion system of Ralstonia solanacearum, are translocators belonging to the HrpF/NopX family. J. Bacteriol. 188, 4903-4917.
33. Minic, Z., 2008: Physiological roles of plant glycoside hydrolases. Planta 227, 723-740.
34. Morita, M. T.; Sakaguchi, K.; Kiyose, S.; Taira, K.; Kato, T.; Nakamura, M.; Tasaka, M., 2006: A C2H2-type zinc finger protein, SGR5, is involved in early events of gravitropism in Arabidopsis inflorescence stems. Plant J. 47, 619-628.
35. Mukaihara, T.; Tamura, N.; Murata, Y.; Iwabuchi, M., 2004: Genetic screening of Hrp type III-related pathogenicity genes controlled by the HrpB transcriptional activator in Ralstonia solanacearum. Mol. Microbiol. 54, 863-875.
36. Murashige, T.; Skoog, F., 1962: A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
37. Myburg, A. A.; Grattapaglia, D.; Tuskan, G. A.; Schmutz, J.; Barry, K.; Bristow, J., 2008: The Eucalyptus Genome Network. Sequencing the Eucalyptus Genome: Genomic Resources for Renewable Energy and Fiber Production. Plant & Animal Genome XVI Conference. Abstract W195, San Diego, CA.
38. Naidoo, S.; Murray, S.; Denby, K.; Berger, D., 2007: Microarray analysis of the Arabidopsis thaliana cir 1(constitutively induced resistance 1) mutant reveals candidate defence response genes against Pseudomonas syringae pv tomato DC 3000. S. Afr. J. Bot. 73, 412-421.
39. Newman, M.; Roepenack, E. V.; Daniels, M.; Dow, M., 2000: Lipopolysaccharides and plant responses to phytopathogenic bacteria. Mol. Plant Pathol. 1, 25-31.
40. Occhialini, A.; Cunnac, S.; Reymond, N.; Genin, S.; 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.
41. Pfund, C.; Tans-Kersten, J.; Dunning, F. M.; Alonso, J. M.; Ecker, J. R.; Allen, C.; Bent, A. F., 2004: Flagellin is not a major defense elicitor in Ralstonia solanacearum cells or extracts applied to Arabidopsis thaliana. Mol. Plant Microbe Interact. 17, 696-706.
42. Potter, S.; Uknes, S.; Lawton, K.; Winter, A. M.; Chandler, D.; Dimaio, J.; Novitzky, R.; Ward, E.; Ryals, J., 1993: Regulation of a hevein-like gene in Arabidopsis. Mol. Plant Microbe Interact. 6, 680-685.
43. Poueymiro, M.; Genin, S., 2009: Secreted proteins from Ralstonia solanacearum: a hundred tricks to kill a plant. Curr. Opin. Microbiol. 12, 44-52.
44. Ran, L. X.; Li, Z. N.; Wu, G. J.; Van Loon, L. C.; Bakker, P., 2005a: Induction of systemic resistance against bacterial wilt in Eucalyptus urophylla by fluorescent Pseudomonas spp. Eur. J. Plant Pathol. 113, 59-70.
45. Ran, L.; Liu, C.; Wu, G.; Van Loon, L.; Bakker, P., 2005b: Suppression of bacterial wilt in Eucalyptus urophylla by fluorescent Pseudomonas spp. in China. Biol. Control 32, 111-120.
46. Roux, J.; Coutinho, T. A.; Wingfield, M. J.; Byabashaija, D. M., 2001: Diseases of plantation Eucalyptus in Uganda. S. Afr. J. Sci. 97, 16-18.
47. Saeed, A. I.; Sharov, V.; White, J.; Li, J.; Liang, W.; Bhagabati, N.; Braisted, J.; Klapa, M.; Currier, T.; Thiagarajan, M.; Sturn, A.; Snuffin, M.; Rezantsev, A.; Popov, D.; Ryltsov, A.; Kostukovich, E.; Borisovsky, I.; Liu, Z.; Vinsavich, A.; Trush, V.; Quackenbush, J., 2003: TM4: a free, open-source system for microarray data management and analysis. BioTechniques 34, 374-378.
48. 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.; Thebault, P.; Whalen, M.; Wincker, P.; Levy, M.; Weissenbach, J.; Boucher, C. A., 2002: Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415, 497-502.
49. Samac, D. A.; Hironaka, C. M.; Yallaly, P. E.; Shah, D. M., 1990: Isolation and characterization of the genes encoding basic and acidic chitinase in Arabidopsis thaliana. Plant Physiol. 93, 907-914.
50. Shan, L.; He, P.; Li, J.; Heese, A.; Peck, S. C.; Nurnberger, T.; Martin, G. B.; Sheen, J., 2008: Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4, 17-27.
51. Tao, Y.; Xie, Z.; Chen, W.; Glazebrook, J.; Chang, H. S.; Han, B.; Zhu, T.; Zou, G.; Katagiri, F., 2003: Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15, 317-330.
52. Thatcher, L. F.; Anderson, J. P.; Singh, K. B., 2005: Plant defense responses: what have we learnt from Arabidopsis? Functional Plant Biol. 32, 1-19.
53. Thilmony, R.; Underwood, W.; He, S. Y., 2006: Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. Plant J. 46, 34-53.
54. Thomma, B. P.; Eggermont, K.; Tierens, K. F.; Broekaert, W. F., 1999: Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiol. 121, 1093-1102.
55. Truman, W.; De Zabala, M. T.; Grant, M., 2006: Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance. Plant J. 46, 14-33.
56. Valls, M.; Genin, S.; Boucher, C., 2006: Integrated regulation of the type III secretion system and other virulence determinants in Ralstonia solanacearum. PLoS Pathog. 2, e82.
57. Vasse, J.; Genin, S.; Frey, P.; Boucher, C.; Brito, B., 2000: The hrpB and hrpG regulatory genes of Ralstonia solanacearum are required for different stages of the tomato root infection process. Mol. Plant Microbe Interact. 13, 259-267.
58. Winstead, N. N.; Kelman, A., 1952: Inoculation techniques for evaluating resistance to Pseudomonas solanacearum. Phytopathology 42, 628-634.
59. Wolfinger, R. D.; Gibson, G.; Wolfinger, E. D.; Bennett, L.; Hamadeh, H.; Bushel, P.; Afshari, C.; Paules, R. S., 2001: Assessing gene significance from cDNA microarray expression data via mixed models. J. Comput. Biol. 8, 625-637.
60. Wroblewski, T.; Caldwell, K. S.; Piskurewicz, U.; Cavanaugh, K. A.; Xu, H.; Kozik, A.; Ochoa, O.; Mchale, L. K.; Lahre, K.; Jelenska, J., 2009: Comparative large-scale analysis of interactions between several crop species and the effector repertoires from multiple pathovars of Pseudomonas and Ralstonia. Plant Physiol. 150, 1733.
61. Xu, J.; Pan, Z. C.; Prior, P.; Xu, J. S.; Zhang, Z.; Zhang, H.; Zhang, L. Q.; He, L. Y.; Feng, J., 2009: Genetic diversity of Ralstonia solanacearum strains from China. Eur. J. Plant Pathol. 125, 1-13.
62. Zeidler, D.; Zahringer, U.; Gerber, I.; Dubery, I.; Hartung, T.; Bors, W.; Hutzler, P.; Durner, J., 2004: Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proc. Natl Acad. Sci. U.S.A. 101, 15811-15816.
63. Zimmermann, P.; Hennig, L.; Gruissem, W., 2005: Gene-expression analysis and network discovery using Genevestigator. Trends Plant Sci. 10, 407-409.