Proteomic analysis reveals novel extracellular virulence-associated proteins and functions regulated by the diffusible signal factor (DSF) in Xanthomonas oryzae pv. oryzicola

Journal of Proteome Research

Volumn 12, Issue 7, 2013, Pages 3327-3341

  Qian, Guoliang ^a   Zhou, Yijing ^a   Zhao, Yancun ^a   Song, Zhiwei ^a   Wang, Suyan ^a   Fan, Jiaqin ^a   Hu, Baishi ^a   Venturi, Vittorio ^b   Liu, Fengquan ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

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

Author keywords

DSF; extracellular protein; proteomics; quorum sensing; Xanthomonas oryzae pv. oryzicola

Indexed keywords

BACTERIAL PROTEIN; DIFFUSIBLE SIGNAL FACTOR; POLYSACCHARIDE; PROTEIN AX21; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL LOAD; BACTERIAL VIRULENCE; BIOFILM; CATABOLISM; CELL MOTILITY; CELL STRUCTURE; GENE DELETION; GENE EXPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; OPEN READING FRAME; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; QUORUM SENSING; SEQUENCE ANALYSIS; TYPE II SECRETION SYSTEM; XANTHOMONAS ORYZAE;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; ORYZA SATIVA; PLANT DISEASES; PROTEOMICS; QUORUM SENSING; SIGNAL TRANSDUCTION; VIRULENCE; XANTHOMONAS;

BACTERIA (MICROORGANISMS); XANTHOMONAS; XANTHOMONAS ORYZAE PV. ORYZICOLA;

EID: 84879922853     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr4001543     Document Type: Article

References (70)

1. Leyns, F.; DeCleene, M.; Swings, J. G.; Deley, J. The host range of the genus Xanthomonas Bot. Rev. 1984, 50, 308-356
2. Watt, S. A.; Wilke, A.; Patschkowski, T.; Niehaus, K. Comprehensive analysis of the extracellular proteins from Xanthomonas campestris pv. campestris B100 Proteomics 2005, 5, 153-167
3. BÜttner, D.; Bonas, U. Regulation and secretion of Xanthomonas virulence factors FEMS Microbiol Rev. 2010, 34, 107-133
4. Ray, S. K.; Rajeshwari, R.; Sonti, R. V. Mutants of Xanthomonas oryzae pv. oryzae deficient in general secretory pathway are virulence deficient and unable to secrete xylanase Mol. Plant-Microbe Interact. 2000, 13, 394-401
5. Ray, S. K.; Rajeshwari, R.; Sharma, Y.; Sonti, R. V. A high molecular-weight outer membrane protein of Xanthomonas oryzae pv. oryzae exhibits similarity to non-fimbrial adhesins of animal pathogenic bacteria and is required for optimum virulence Mol. Microbiol. 2002, 46, 637-47
6. Dharmapuri, S.; Sonti, R. V. A transposon insertion in the gumG homologue of Xanthomonas oryzae pv. oryzae causes loss of extracellular polysaccharide production and virulence FEMS Microbiol. Lett. 1999, 179, 53-59
7. Zhu, W.; MaGbanua, M. M.; White, F. F. Identification of two novel hrp -associated genes in the hrp gene cluster of Xanthomonas oryzae pv. oryzae J. Bacteriol. 2000, 182, 1844-1853
8. He, Y. W.; Wu, J. E.; Cha, J. S.; Zhang, L. H. Rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae produces multiple DSF-family signals in regulation of virulence factor production BMC Microbiol. 2010, 10, 187
9. Lee, S. W.; Jeong, K. S.; Han, S. W.; Lee, S. E.; Phee, B. K.; Hahn, T. R. Ronald, P. The Xanthomonas oryzae pv. oryzae PhoPQ two-component system is required for AvrXA21 activity, hrpG expression, and virulence J. Bacteriol. 2008, 190 (6) 283-2197
10. Zou, L. F.; Wang, X. P.; Xiang, Y.; Zhang, B.; Li, Y. R.; Xiao, Y. L.; Wang, J. S.; Walmsley, A. R.; Chen, G. Y. 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. 2006, 72, 6216-6224
11. Zhao, Y. C.; Qian, G. L.; Yin, F. Q.; Fan, J. Q.; Zhai, Z. W.; Liu, C. H.; Hu, B. S.; Liu, F. Q. Proteomic analysis of the regulatory function of DSF-dependent quorum sensing in Xanthomonas oryzae pv. oryzicola Microb. Pathog. 2011, 50, 48-55
12. Zhao, Y. C.; Qian, G. L.; Fan, J. Q.; Liu, C. H.; Yin, F. Q.; Zhou, Y. J.; Shen, Q.; Hu, B. S; Liu, F. Q. Identification and characterization of a novel gene hshB in Xanthomonas oryzae pv. oryzicola co-regulated by quorum sensing and clp Phytopathology 2012, 102 (3) 252-259
13. Wang, L.; Makino, S.; Subedee, A.; Bogdanove, A. J. Novel candidate virulence factors in rice pathogen Xanthomonas oryzae pv. oryzicola as revealed by mutational analysis Appl. Environ. Microbiol. 2007, 73, 8023-8027
14. Uzureau, S.; Lemaire, J.; Delaive, E.; Dieu, M.; Gaigneaux, A.; Raes, M.; Bolle, X. D.; Letesson, J. J. Global analysis of quorum sensing targets in the intracellular pathogen Brucella melitensis 16M J. Proteome Res. 2010, 9, 3200-3217
15. Miller, M. B.; Bassler, B. L. Quorum sensing in bacteria Annu. Rev. Microbiol. 2001, 55, 165-199
16. Whitehead, N. A.; Barnard, A. M. L.; Slater, H.; Simpson, N. J. L.; Salmond, G. P. C. Quorum-sensing in gram-negative bacteria FEMS Microbiol. Rev. 2001, 25, 365-404
17. Sun, J.; Daniel, R.; Wagner-Döbler, I.; Zeng, A. P. (2004) Is autoinducer-2 a universal signal for interspecies communication: a comparative genomic and phylogenetic analysis of the synthesis and signal transduction pathways BMC Evol. Biol. 2004, 4, 36
18. Wang, L. H.; He, Y. W.; Gao, Y. F.; Wu, J. E.; Dong, Y. H.; He, C. Z.; Wang, S. X.; Weng, L. X.; Xu, J. L.; Tay, L.; Fang, R. X.; Zhang, L. H. A bacterial cell-cell communication signal with cross-kingdom structural analogues Mol. Microbiol. 2004, 51, 903-912
19. Chatterjee, S.; Newman, K. L.; Lindow, S. E. Cell-to-cell signaling in Xylella fastidiosa suppresses movement and xylem vessel colonization in grape Mol. Plant-Microbe Interact. 2008, 21 (10) 1309-1315
20. Boon, C.; Deng, Y.; Wang, L. H.; He, Y. W.; Xu, J. L.; Fan, Y.; Pan, S. Q.; Zhang, L. H. A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition ISME J. 2008, 2, 27-36
21. Parker, C. T.; Sperandio, V. Cell-to-cell signalling during pathogenesis Cell Microbiol. 2009, 11, 363-369
22. He, Y. W.; Xu, M.; Lin, K.; Ng, Y. J.; Wen, C. M.; Wang, L. H.; Liu, Z. D.; Zhang, H. B.; Dong, Y. H.; Dow, J. M.; Zhang, L. H. Genome scale analysis of diffusible signal factor regulon in Xanthomonas campestris pv. campestris: identification of novel cell-cell communication-dependent genes and functions Mol. Microbiol. 2006, 59 (2) 610-622
23. Guo, Y. P.; Zhang, Y. P.; Li, J. L.; Wang, N. Diffusible Signal Factor-Mediated Quorum Sensing Plays a Central Role in Coordinating Gene Expression of Xanthomonas citri subsp. citri Mol. Plant-Microbe Interact. 2012, 25 (2) 165-179
24. Barber, C. E.; Tang, J. L.; Feng, J. X.; Pan, M. Q.; Wilson, T. J.; Slater, H.; Dow, J. M.; Williams, P.; Daniels, M. J. A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule Mol. Microbiol. 1997, 24, 555-566
25. Mole, B. M.; Baltrus, D. A.; Dangl, J. L.; Grant, S. R. Global virulence regulation networks in phytopathogenic bacteria Trends Microbiol. 2007, 15 (8) 363-371
26. He, Y. W.; Zhang, L. H. Quorum sensing and virulence regulation in Xanthomonas campestris FEMS Microbiol. Rev. 2008, 32, 842-857
27. He, Y. W.; Ng, A. Y.; Xu, M.; Lin, K.; Wang, L. H.; Dong, Y. H.; Zhang, L. H. (2007) Xanthomonas campestris cell-cell communication involves a putative nucleotide receptor protein Clp and a hierarchical signalling network Mol. Microbiol. 2007, 64, 281-292
28. Schuster, M.; Lostroh, P.; Ogi, T.; Greenberg, E. P. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis J. Bacteriol. 2003, 85 (7) 2066 e79
29. Gygi, S. P.; Rochon, Y.; Franza, B. R.; Aebersold, R. Correlation between protein and mRNA abundance in yeast Mol. Cell. Biol. 1999, 19, 1720-1730
30. Goo, E.; Kang, Y. S.; kim, H. S.; Hwang, I. Y. Proteomic analysis of quorum sensing-dependent proteins in Burkholderia glumae J. Proteome Res. 2010, 9, 3184-3199
31. Arevalo-Ferro, C.; Hentzer, M.; Reil, G.; Gorg, A.; Kjelleberg, S.; Givskov, M.; Riedel, K.; Eberl, L. Identification of quorum-sensing regulated proteins in the opportunistic pathogen Pseudomonas aeruginosa by proteomics Environ. Microbiol. 2003, 5, 1350-1369
32. González, J. F.; Degrassi, G.; Devescovi, G.; VIeesschauwer, D. D.; Höfte, M.; Myers, M. P.; Venturi, V. A proteomic study of Xanthomonas oryzae pv. oryzae in rice xylem sap J. Proteomics 2012, 75 (18) 5911-5919
33. Liu, H.; Coulthurst, S. J.; Pritchard, L.; Hedley, P. E.; Ravensdale, M.; Humphris, S.; Burr, T.; Takle, G.; Brurberg, M. B.; Birch, P. R.; Salmond, G. P.; Toth, I. K. Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum PLoS Pathog. 2008, 4, e1000093
34. Chung, W. J.; Shu, H. Y.; Lu, C. Y.; Wu, C. Y.; Tseng, Y. H.; Tsai, S. F.; Lin, C. H. Qualitative and comparative proteomic analysis of Xanthomonas campestris pv campestris Proteomics 2007, 7, 2047-2058
35. Joo, W. A.; Kang, M. J.; Son, W. K.; Lee, H. J.; Lee, E.; Kim, C. W. Monitoring protein expression by proteomics: Human plama exposed to benzene Proteomics 2003, 3, 2402-2411
36. Zou, L. F.; Li, Y. R.; Chen, G. Y. A non-marker mutagenesis strategy to generate poly- hrp gene mutants in the rice pathogen Xanthomonas oryzae pv oryzicola Agric. Sci. China 2011, 10, 1139-1150
37. Feng, J. X.; Song, Z. Z.; Duan, C. J.; Zhao, S.; Wu, Y. Q.; Wang, C.; Dow, J. M.; Tang, J. L. The xrvA gene of Xanthomonas oryzae pv. oryzae, encoding an H-NS-like protein, regulates virulence in rice Microbiology. 2009, 155, 3033-3044
38. Lan, L. F.; Murray, T. S.; Kazmierczak, B. I.; He, C. Pseudomonas aeruginosa OspR is an oxidative sensing regulator that affects pigment production, antibiotic resistance and dissemination during infection Mol. Microbiol. 2010, 75 (1) 76-91
39. Tang, J. L.; Liu, Y. N.; Barber, C. E; Dow, J. M.; Wootton, J. C.; Daniels, M. J. Genetic and molecular analysis of a cluster of rpf genes involved in positive regulation of synthesis of extracellular enzymes and polysaccharide in Xanthomonas campestris pathovar campestris Mol. Gen. Genet. 1991, 226, 409-417
40. Ryan, R. P.; Fouhy, Y.; Lucey, J. F.; Crossman, L. C.; Spiro, S.; He, Y. W.; Zhang, L. H.; Heeb, S.; Cámara, M.; Williams, P.; Dow, J. M. 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, 6712-6717
41. Wang, P.; Zhong, Z. T.; Zhou, J.; Cai, T.; Zhu, J. Exopolysaccharide biosynthesis is important for Mesorhizobium tianshanense: plant host interaction Arch. Microbiol. 2008, 189, 525-530
42. Lee, S. W.; Han, S. W.; Sririyanum, M.; Park, C. J.; Seo, Y. S.; Ronald, P. C. A type I-secreted, sulfated peptide triggers XA21-mediated innate 168 immunity Science 2009, 326, 850-853
43. Park, C. J.; Han, S. W.; Chen, X.; Ronald, P. C. Elucidation of XA21-mediated innate immunity Cell Microbiol. 2010, 12, 1017-1025
44. da Silva, F. G.; Shen, Y.; Dardick, C.; Burdman, S.; Yadav, R. C.; De Leon, A. L.; Ronald, P. C. Bacterial genes involved in type I secretion and sulfation are required to elicit the rice Xa21 -mediated innate immune response Mol. Plant-Microbe Interact. 2004, 17, 593-601
45. Han, S. W.; Lee, S. W.; Ronald, P. C. Secretion, modification, and regulation of Ax21 Curr. Opin. Microbiol. 2011, 14 (1) 62-67
46. Han, S. W.; Sriariyanun, M.; Lee, S. W.; Sharma, M.; Bahar, O.; Bower, Z.; Ronald, P. C. Small protein-mediated quorum sensing in a Gram-negative bacterium PLoS One 2011, 6 (12) e29192
47. Nouwens, A. S.; Beatson, S. A.; Whitchurch, C. B.; Walsh, B. J.; Schweizer, H. P.; Mattick, J. S.; Cordwell, S. J. Proteome analysis of extracellular proteins regulated by the las and rhl quorum sensing systems in Pseudomonas aeruginosa PAO1 Microbiology 2003, 149, 1311-1322
48. Riedel, K.; Arevalo-Ferro, C.; Reil, G.; Görg, A.; Lottspeich, F.; Eberl, L. Analysis of the quorum-sensing regulon of the opportunistic pathogen Burkholderia cepacia H111 by proteomics Electrophoresis 2003, 24, 740-750
49. Soares, M. R.; Facincani, A. P.; Ferreira, R. M.; Moreira, L. M.; de Oliveira, J. C.; Ferro, J. A.; Ferro, M. I.; Meneghini, R.; Gozzo, F. C. Proteome of the phytopathogen Xanthomonas citri subsp. citri: a global expression profile Proteome Sci. 2010, 8, 55
50. Yin, F. Q.; Zhao, Y. C.; Liu, C. H.; Qian, G. L.; Fan, J. Q.; Hu, B. S.; Liu, F. Q. Analysis of the flgD and flgE genes regulated by diffusible signal factor in Xanthomonas oryzae pv. oryzicola Acta Microbiol. Sin. 2011, 51 (7) 891-897
51. Baker, C. J.; Orlandi, E. W. Active oxygen in plant pathogenesis Annu. Rev. Phytopathol. 1995, 33, 299-321
52. Charoenlap, N.; Buranajitpakorn, S.; Duang-Nkern, J.; Namchaiw, P.; Vattanaviboon, P.; Mongkolsuk, S. Evaluation of the virulence of Xanthomonas campestris pv. campestris mutant strains lacking functional genes in the OxyR regulon Curr. Microbiol. 2011, 63, 232-237
53. Johnson, T. L.; Abendroth, J.; Hol, W. G. J.; Sandkvist, M. Type II secretion: from structure to function FEMS Microbiol. Lett. 2006, 255, 175-186
54. Jha, G.; Rajeshwari, R.; Sonti, R. V. Bacterial type two secretion system secreted proteins: double-edged swords for plant pathogens Mol. Plant-Microbe Interact. 2005, 18, 891-898
55. Zou, H. S.; Song, X.; Zou, L. F.; Yuan, L.; Li, Y. R.; Guo, W.; Che, Y. Z.; Zhao, W. X.; Duan, Y. P.; Chen, G. Y. EcpA, an extracellular protease, is a specific virulence factor required by Xanthomonas oryzae pv. oryzicola but not by X. oryzae pv. oryzae in rice Microbiology 2012, 158, 2372-2383
56. Dow, J. M.; Daniels, M. J.; Dums, F.; Turner, P. C.; Gough, C. Genetic and biochemical analysis of protein export from Xanthomonas campestris J. Cell Sci., Suppl. 1989, 11, 59-72
57. Cianciotto, N. P. Type II secretion: a protein secretion system for all seasons Trends Microbiol. 2005, 13, 581-588
58. DebRoy, S.; Dao, J.; Söderberg, M.; Rossier, O.; Cianciotto, N. P. Legionella pneumophila type II secretome reveals unique exoproteins and a Chitinase that promotes bacterial persistence in the lung Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 19146-19151
59. Voulhoux, R.; Ball, G.; Ize, B.; Vasil, M. L.; Lazdunski, A.; Wu, L. F.; Filloux, A. Involvement of the twin-arginine translocation system in protein secretion via the type II pathway EMBO J. 2001, 20, 6735-6741
60. Rajeshwari, R.; Jha, G.; Sonti, R. V. Role of an in planta expressed xylanase of Xanthomonas oryzae pv. oryzae in promoting virulence on rice Mol. Plant-Microbe Interact. 2005, 18, 830-837
61. Furutani, A.; Tsuge, S.; Ohnishi, K.; Hikichi, Y.; Oku, T.; Tsuno, K.; Inoue, Y.; Ochiai, H.; Kaku, H.; Kubo, Y. Evidence for HrpXo-dependent expression of type II secretory proteins in Xanthomonas oryzae pv. oryzae J. Bacteriol. 2004, 186, 1374-1380
62. Sun, Q. H.; Hu, J.; Huang, G. X.; Ge, C.; Fang, R. X.; He, C. Z. Type II secretion pathway structural gene xpsE, xylanase- and cellulase secretion and virulence in Xanthomonas oryzae pv. oryzae Plant Pathol. 2005, 54, 15-21
63. Hu, J.; Qian, W.; He, C. Z. The Xanthomonas oryzae pv. oryzae eglXoB endoglucanase gene is required for virulence to rice FEMS Microbiol Lett. 2007, 269, 273-279
64. Hsiao, Y. M.; Zheng, M. H.; Hu, R. M.; Yang, T. C.; Tseng, Y. H. Regulation of the pehA gene encoding the major polygalacturonase of Xanthomonas campestris by Clp and RpfF Microbiology 2008, 154, 705-713
65. Gauthier, Y. P.; Thibault, F. M.; Paucod, J. C.; Vidal, D. R. Protease production by Burkholderia pseudomallei and virulence in mice Acta Trop. 2000, 74, 215-220
66. Valade, E.; Thibault, F. M.; Gauthier, Y. P.; Palencia, M.; Popoff, M. Y.; Vidal, D. R. The Pml I- Pml R quorum-sensing system in Burkholderia pseudomallei plays a key role in virulence and modulates production of the MprA protease J. Bacteriol. 2004, 186, 2288-2294
67. Sokol, P. A.; Sajjan, U.; Visser, M. B.; Gingues, S.; Forstner, J.; Kooi, C. The CepIR quorum-sensing system contributes to the virulence of Burkholderia cenocepacia respiratory infections Microbiology 2003, 149, 3649-3658
68. McCarthy, Y.; Dow, J. M.; Ryan, R. P. The Ax21 protein is a cell-cell signal 1 al regulating virulence in the nosocomial 2 pathogen Stenotrophomonas maltophilia J. Bacteriol. 2011, 193 (22) 6375-6378
69. 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.; Chen, G. Y. A novel regulatory role of HrpD6 in regulating hrp-hrc-hpa genes in Xanthomonas oryzae pv. oryzicola Mol. Plant-Microbe Interact. 2011, 24 (9) 1086-1101
70. De, F. R.; Kado, C. I.; Gabriel, D. W. Small, stable shuttle vectors for use in Xanthomonas Gene 1990, 88, 65-72