Phytohormone-mediated interkingdom signaling shapes the outcome of rice-Xanthomonas oryzae pv. oryzae interactions

BMC Plant Biology

Volumn 15, Issue 1, 2015, Pages

  Xu, Jing ^a   Zhou, Lian ^b   Venturi, Vittorio ^c   He, Ya Wen ^b   Kojima, Mikiko ^d   Sakakibari, Hitoshi ^d   Höfte, Monica ^a   De Vleesschauwer, David ^a  

^a GHENT UNIVERSITY   (Belgium)

^b Shanghai Jiao Tong University   (China)

^c INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^d RIKEN Center for Sustainable Resource Science   (Japan)

Author keywords

Defense; Hormone signaling; Oryza sativa; Pathogenicity; Plant immunity; Quorum sensing

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); ORYZA SATIVA; XANTHOMONAS ORYZAE PV. ORYZAE;

3-HYDROXYBENZOIC ACID; 4 HYDROXYBENZOIC ACID ESTER; 4-HYDROXYBENZOIC ACID; BACTERIAL PROTEIN; BIOPOLYMER; HYDROXYBENZOIC ACID DERIVATIVE; PHYTOHORMONE; SALICYLIC ACID;

BIOLOGICAL MODEL; BIOSYNTHESIS; DRUG EFFECTS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; ORYZA; PHYSIOLOGY; QUORUM SENSING; SIGNAL TRANSDUCTION; XANTHOMONAS;

BACTERIAL PROTEINS; BIOPOLYMERS; HOST-PATHOGEN INTERACTIONS; HYDROXYBENZOATES; MODELS, BIOLOGICAL; ORYZA; PARABENS; PLANT GROWTH REGULATORS; QUORUM SENSING; SALICYLIC ACID; SIGNAL TRANSDUCTION; XANTHOMONAS;

EID: 84938802634     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-014-0411-3     Document Type: Article

References (69)

1. Niño-Liu DO, Ronald PC, Bogdanove AJ. Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol Plant Pathol. 2006;7:303-24.
2. Shen Y, Ronald P. Molecular determinants of disease and resistance in interactions of Xanthomonas oryzae pv. oryzae and rice. Microbes Infect. 2002;4:1361-7.
3. Büttner D, Bonas U. Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiol Rev. 2010;34:107-33.
4. Von Bodman SB, Bauer WD, Coplin DL. Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol. 2003;41:455-82.
5. Atkinson S, Williams P. Quorum sensing and social networking in the microbial world. J R Soc Interface. 2009;6:959-78.
6. Von Bodman SB, Willey JA, Diggle SP. Cell-cell communication in bacteria: united we stand. J Bacteriol. 2008;190:4377-91.
7. Barber CE, Tang JL, Feng JX, Pan MQ, Wilson TJ, Slater H, et al. A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol Microbiol. 1997;24:555-66.
8. Deng YY, Wu JE, Tao F, Zhang LH. Listening to a new language: DSF-based quorum sensing in Gram-negative bacteria. Chem Rev. 2005;111:160-73.
9. Jeong KS, Lee SE, Han JW, Yang SU, Lee BM, Noh TH, et al. Virulence reduction and differing regulation of virulence genes in rpf mutants of Xanthomonas oryzae pv. oryzae. Plant Pathol J. 2008;24:143-51.
10. Wang LH, He YW, Gao YY, Wu JE, Dong YH, He C, et al. A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol Microbiol. 2004;51:903-12.
11. Zhao YC, Qian GL, Yin FQ, Fan JQ, Zhai ZW, Liu CH, et al. Proteomic analysis of the regulatory function of DSF-dependent quorum sensing in Xanthomonas oryzae pv. oryzicola. Microb Pathog. 2011;50:48-55.
12. Boon C, Deng Y, Wang L-H, He Y, Xu J-L, Fan Y, et al. A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME J. 2008;2:27-36.
13. Val A, Simionato C, Santos D, Lambais MR, Carrilho E. Characterization of a putative Xylella fastidiosa diffusible signal factor by HRGC-EI-MS. J Mass Spectrom. 2007;42:490-6.
14. Huang TP, Lee Wong AC. Extracellular fatty acids facilitate flagella-independent translocation by Stenotrophomonas maltophilia. Res Microbiol. 2007;158:702-11.
15. Bi H, Yu Y, Dong H, Wang H, Cronan JE. Xanthomonas campestris RpfB is a fatty Acyl-CoA ligase required to counteract the thioesterase activity of the RpfF diffusible signal factor (DSF) synthase. Mol Microbiol. 2014;93:262-75.
16. Ryan RP, Fouhy Y, Lucey JF, Crossman LC, Spiro S, He YW, et al. Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci U S A. 2006;103:6712-7.
17. He YW, Wang C, Zhou L, Song HW, Dow JM, Zhang LH. Dual signaling functions of the hybrid sensor kinase RpfC of Xanthomonas campestris involve either phosphorelay or receiver domain-protein interaction. J Biol Chem. 2006;281:33414-21.
18. Slater H, Alvarez-Morales A, Barber CE, Daniels MJ, Dow JM. A two-component system involving an HD-GYP domain protein links cell-cell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol Microbiol. 2000;38:986-1003.
19. Cheng Z, He YW, Lim SC, Qamra R, Walsh M, Zhang LH, et al. Structural basis of the sensor-synthase interaction in autoinduction of the quorum sensing signal DSF biosynthesis. Structure. 2010;18:1199-209.
20. Zhou L, Wang JY, Wang JH, Poplawsky A, Lin SJ, Zhu BS, et al. The diffusible factor synthase XanB2 is a bifunctional chorismatase that links the shikimate pathway to ubiquinone and xanthomonadins biosynthetic pathways. Mol Microbiol. 2013;87:80-93.
21. Kennedy A, En K. Chemotaxonomic significance of the xanthomonadins, novel brominated aryl-polyene pigments produced by bacteria of the genus Xanthomonas. Arch Microbiol. 1977;9:1-9.
22. Jenkins CL, Starr MP. The brominated aryl-polyene (Xanthomonadin) pigments of Xanthomonas juglandis protect against photobiological damage. Curr Microbiol. 1982;7:323-6.
23. Poplawsky AR, Urban SC, Chun W. Biological role of xanthomonadin pigments in Xanthomonas campestris pv. campestris. Appl Environ Microbiol. 2000;66:5123-7.
24. Rajagopal L, Sundari CS, Balasubramanian D, Sonti RV. The bacterial pigment xanthomonadin offers protection against photodamage. FEBS Lett. 1997;415:125-8.
25. Goel AK, Rajagopal L, Nagesh N, Sonti RV. Genetic locus encoding functions involved in biosynthesis and outer membrane localization of xanthomonadin in Xanthomonas oryzae pv. oryzae. J Bacteriol. 2002;184:3539-48.
26. Poplawsky AR, Chun W. pigB determines a diffusible factor needed for extracellular polysaccharide slime and xanthomonadin production in Xanthomonas. J Bacteriol. 1997;179:439-44.
27. He YW, Wu J, Zhou L, Yang F, He YQ, Le JB, et al. Xanthomonas campestris diffusible factor is 3-hydroxybenzoic acid and is associated with xanthomonadin biosynthesis, cell viability, antioxidant activity, and systemic invasion. Mol Plant Microbe Interact. 2011;24:948-57.
28. Ferluga S, Venturi V. OryR is a LuxR-Family protein involved in interkingdom signaling between pathogenic Xanthomonas oryzae pv. oryzae and rice. J Bacteriol. 2009;191:890-7.
29. Gonzalez JF, Venturi V. A novel widespread interkingdom signaling circuit. Trends Plant Sci. 2013;18:167-74.
30. De Vos M, Van Oosten VR, Van Poecke RMP, Van Pelt JA, Pozo MJ, Mueller MJ, et al. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact. 2005;18:923-37.
31. Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM. Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol. 2012;28:489-521.
32. Yuan ZC, Edlind MP, Liu P, Saenkham P, Banta LM, Wise AA, et al. The plant signal salicylic acid shuts down expression of the vir regulon and activates quormone-quenching genes in Agrobacterium. Proc Natl Acad Sci U S A. 2007;104:11790-5.
33. Prithiviraj B, Bais HP, Weir T, Suresh B, Najarro EH, Dayakar BV, et al. Down regulation of virulence factors of Pseudomonas aeruginosa by salicylic acid attenuates its virulence on Arabidopsis thaliana and Caenorhabditis elegans. Infect Immun. 2005;73:5319-28.
34. Chow S, Gu K, Jiang L, Nassour A. Salicylic acid affects swimming, twitching and swarming sotility in Pseudomonas aeruginosa, resulting in decreased biofilm formation. J Exp Microbiol Immunol. 2011;15:22-9.
35. Bandara MBK, Zhu H, Sankaridurg PR, Willcox MDP. Salicylic acid reduces the production of several potential virulence factors of Pseudomonas aeruginosa associated with microbial keratitis. Invest Ophthalmol Vis Sci. 2006;47:4453-60.
36. De Vleesschauwer D, Gheysen G, Höfte M. Hormone defense networking in rice: tales from a different world. Trends Plant Sci. 2013;18:555-65.
37. Xu J, Audenaert K, Höfte M, De Vleesschauwer D. Abscisic acid promotes susceptibility to the rice leaf blight pathogen Xanthomonas oryzae pv. oryzae by suppressing salicylic acid-mediated defenses. PLoS One. 2013;8:e67413.
38. Yuan YX, Zhong SH, Li Q, Zhu ZR, Lou YG, Wang LY, et al. Functional analysis of rice NPR1-like genes reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotechnol J. 2007;5:313-24.
39. Liu H, Li X, Xiao J, Wang S. A convenient method for simultaneous quantification of multiple phytohormones and metabolites: application in study of rice-bacterium interaction. Plant Methods. 2012;8:2-13.
40. Kojima M, Kamada-Nobusada T, Komatsu H, Takei K, Kuroha T, Mizutani M, et al. Highly sensitive and high-throughput analysis of plant hormones using MS-probe modification and liquid chromatography-tandem mass spectrometry: an application for hormone profiling in Oryza sativa. Plant Cell Physiol. 2009;50:1201-14.
41. Rai R, Ranjan M, Pradhan BB, Chatterjee S. Atypical regulation of virulence-associated functions by a diffusible signal factor in Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact. 2012;25:789-801.
42. He YW, Wu JE, Cha JS, Zhang LH. Rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae produces multiple DSF-family signals in regulation of virulence factor production. BMC Microbiol. 2010;10:187-95.
43. Gonzalez JF, Myers MP, Venturi V. The inter-kingdom solo OryR regulator of Xanthomonas oryzae is important for motility. Mol Plant Pathol. 2013;14:211-21.
44. Dow JM, Crossman L, Findlay K, He YQ, Feng JX, Tang JL. Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc Natl Acad Sci U S A. 2003;100:10995-1000.
45. Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F. Microbial Exopolysaccharides. In: Prokaryotes-Applied Bacteriol Biotechnol. Berlin, Heidelberg: Springer; 2013. p. 179-92.
46. Chatterjee S, Sonti RV. rpfF mutants of Xanthomonas oryzae pv. oryzae are deficient for virulence and growth under low iron conditions. Mol Plant Microbe Interact. 2002;15:463-71.
47. Guo J, Li H, Chang JW, Lei Y, Li S, Chen LL. Prediction and characterization of protein-protein interaction network in Xanthomonas oryzae pv. oryzae PXO99A. Res Microbiol. 2013;164:1035-44.
48. Zhou L, Huang TW, Sun S, Wang JY, Chen G, Poplawsky AR, et al. The rice bacterial pathogen Xanthomonas oryzae pv. oryzae produces 3-hydroxybenzoic acid and 4-hydroxybenzoic acid via XanB2 for use in xanthomonadin, ubiquinone and exopolysaccharide biosynthesis. Mol Plant-Microbe Interact. 2013;26:1239-48.
49. Schikora A, Schenk ST, Stein E, Molitor A, Zuccaro A, Kogel KH. N-acyl-homoserine lactone confers resistance toward biotrophic and hemibiotrophic pathogens via altered activation of AtMPK6. Plant Physiol. 2011;157:1407-18.
50. Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anolles G, Rolfe BG, et al. Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci. 2003;100:1444-9.
51. Sperandio V, Torres AG, Jarvis B, Nataro JP, Kaper JB. Bacteria-host communication: the language of hormones. Proc Natl Acad Sci U S A. 2003;100:8951-6.
52. Williams P. Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology. 2007;153:3923-38.
53. Kunin CM, Hua TH, Bakaletz LO. Effect of salicylate on expression of flagella by Escherichia coli and Proteus, Providencia, and Pseudomonas spp. Infect Immun. 1995;63:1796-9.
54. Lee BM, Park YJ, Park DS, Kang HW, Kim JG, Song ES, et al. The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Res. 2005;33:577-86.
55. Aldridge P, Hughes KT. Regulation of flagellar assembly. Curr Opin Microbiol. 2002;5:160-5.
56. Silverman P, Seskar M, Kanter D, Schweizer P, Metraux JP, Raskin I. Salicylic acid in rice: biosynthesis, conjugation, and possible role. Plant Physiol. 1995;108:633-9.
57. Shah J. The salicylic acid loop in plant defense. Curr Opin Plant Biol. 2003;6:365-71.
58. Cluis CP, Burja AM, Martin VJJ. Current prospects for the production of coenzyme Q10 in microbes. Trends Biotechnol. 2007;25:514-21.
59. Denny T. Involvement of bacterial polysaccharides in plant pathogenesis. Phytopathology. 1995;33:173-97.
60. Blocker A, Komoriya K, Aizawa SI. Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc Natl Acad Sci U S A. 2003;100:3027-30.
61. Ferluga S, Bigirimana J, Höfte M, Venturi V. A LuxR homologue of Xanthomonas oryzae pv. oryzae is required for optimal rice virulence. Mol Plant Pathol. 2007;8:529-38.
62. Ahmer BMM. Cell-to-cell signalling in Escherichia coli and Salmonella enterica. Mol Microbiol. 2004;52:933-45.
63. Patel HK, Suárez-Moreno ZR, Degrassi G, Subramoni S, González JF, Venturi V. Bacterial LuxR solos have evolved to respond to different molecules including signals from plants. Front Plant Sci. 2013;4:447-51.
64. Bauer WD, Mathesius U. Plant responses to bacterial quorum sensing signals. Curr Opin Plant Biol. 2004;7:429-33.
65. Hartmann A, Rothballer M, Hense BA, Schröder P. Bacterial quorum sensing compounds are important modulators of microbe-plant interactions. Front Plant Sci. 2014;5:1-4.
66. Von Rad U, Klein I, Dobrev PI, Kottova J, Zazimalova E, Fekete A, et al. Response of Arabidopsis thaliana to N-hexanoyl-DL-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta. 2008;229:73-85.
67. Gudesblat GE, Torres PS, Vojnov AA. Xanthomonas campestris overcomes Arabidopsis stomatal innate immunity through a DSF cell-to-cell signal-regulated virulence factor. Plant Physiol. 2009;149:1017-27.
68. Pradhan BB, Ranjan M, Chatterjee S. XadM, a novel adhesin of Xanthomonas oryzae pv. oryzae, exhibits similarity to Rhs family proteins and is required for optimum attachment, biofilm formation and virulence. Mol Plant-Microbe Interact. 2012;25:1157-70.
69. Jain M, Nijhawa A, Tyagi AK, Khurana JP. Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun. 2006;345:646-51.