Secretome analysis of the rice bacterium Xanthomonas oryzae (Xoo) using in vitro and in planta systems

Proteomics

Volumn 13, Issue 12-13, 2013, Pages 1901-1912

  Wang, Yiming ^a   Kim, Sang Gon ^a   Wu, Jingni ^a   Huh, Hyun Hye ^b   Lee, Su Ji ^b   Rakwal, Randeep ^c,d,e   Kumar Agrawal, Ganesh ^e   Park, Zee Yong ^f   Young Kang, Kyu ^a   Kim, Sun Tae ^b  

^a Gyeongsang National University   (South Korea)

^b Pusan National University   (South Korea)

^c UNIVERSITY OF TSUKUBA   (Japan)

^d SHOWA UNIVERSITY   (Japan)

^e Research Laboratory for Biotechnology and Biochemistry RLABB   (Nepal)

^f Gwangju Institute of Science and Technology (GIST)   (South Korea)

Author keywords

2DE; MS; Plant proteomics; Rice; Secretome; Xanthomonas oryzae

Indexed keywords

OUTER MEMBRANE PROTEIN A; SECRETORY PROTEIN; SUPEROXIDE DISMUTASE;

AEROBIC METABOLISM; ARTICLE; BACTERIAL BLIGHT; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CARBON METABOLISM; HOST RESISTANCE; IN VITRO STUDY; ION TRANSPORT; LEAF SHEATH; NONHUMAN; NUTRIENT UPTAKE; OUTER MEMBRANE; OXIDATION REDUCTION REACTION; OXYGEN TENSION; PATHOGENICITY; PLANT DISEASE; PLANT LEAF; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; RICE; SECRETORY PATHWAY; SEED YIELD; TRANSIENT EXPRESSION; XANTHOMONAS ORYZAE;

2DE; MS; PLANT PROTEOMICS; RICE; SECRETOME; XANTHOMONAS ORYZAE;

BACTERIAL PROTEINS; COMPUTATIONAL BIOLOGY; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HOST-PATHOGEN INTERACTIONS; MASS SPECTROMETRY; ORYZA SATIVA; PLANT DISEASES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; XANTHOMONAS;

EID: 84880083951     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201200454     Document Type: Article

References (58)

1. Nino-Liu, D. O., Ronald, P. C., Bongdanove, A. J., A pathovars: model pathogens of a model crop. Mol. Plant. Pathol. 2006, 7, 303-324.
2. Ezuka, A., Kaku, H., A historical review of bacterial blight of rice. Bull. Natl. Inst. Agrobiol. Resour. 2000, 15, 53-54.
3. Goff, S. A., Ricke, D., Lan, T. H., Presting, G. et al., A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 2002, 296, 92-100.
4. Yu, J., Hu, S., Wang, J., Wong, G. K. et al., A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 2002, 296, 79-92.
5. Kikuchi, S., Satoh, K., Nagata, T., Kawagashira, N. et al., Collection, mapping, and annotation of over 28, 000 cDNA clones from japonica rice. Science 2003, 301, 376-379.
6. Salzberg, S. L., Sommer, D. D., Schatz, M. C., Phillippy, A. M. et al., Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC Genomics 2008, 9, 204-220.
7. Agrawal, G. K., Rakwal, R., Rice proteomics: a cornerstone for cereal food crop proteomes. Mass Spectrom. Rev. 2006, 25, 1-53.
8. Khush, G. S., What it will take to feed 5.0 billion rice consumers in 2030. Plant Mol. Biol. 2005, 59, 1-6.
9. Thiellement, H., Zivy, M., Damerval, C., Mechin, V., In: Thiellement, H., Zivy, M., Damerval, C., Mechin, V. (Eds.), Plant Proteomics: Methods and Protocols, Humana Press, Totowa, NJ 2007, 27-36.
10. Agrawal, G. K., Rakwal, R., Plant Proteomics: Technologies, Strategies, and Applications. In: Agrawal, G. K., Rakwal, R. (Eds.), Wiley, Hoboken, NJ 2008, 83-89.
11. Agrawal, G. K., Jwa, N.-S., Lebrun, M. H., Job, D., Rakwal, R., Plant secretome: unlocking secrets of the secreted proteins. Proteomics 2010, 10, 799-827.
12. Knief, C., Delmotte, N., Vorholt, J. A., Bacterial adaptation to life in association with plants-a proteomic perspective from culture to in situ conditions. Proteomics 2011, 11, 3086-3105.
13. Chen, F., Yuan, Y., Li, Q., He, Z. Proteomic analysis of rice plasma membrane reveals proteins involved in early defense response to bacterial blight. Proteomics 2007, 7, 1529-1539.
14. Wang, Y., Wu, J., Park, Z. Y., Kim, S. G. et al., Comparative secretome investigation of Magnaporthe oryzae proteins responsive to nitrogen starvation. J. Proteome Res. 2011, 10, 3136-3148.
15. Chivasa, S., Ndimba, B. K., Simon, W. J., Robertson, D., Yu, X. L. et al., Proteomic analysis of the Arabidopsis thaliana cell wall. Electrophoresis 2002, 23, 1754-1765.
16. Kim, S. T., Kang, Y. H., Wang, Y., Wu, J. et al., Secretome analysis of differentially induced proteins in rice suspension-cultured cells triggered by rice blast fungus and elicitor. Proteomics 2009, 9, 1302-1313.
17. Chen, X. Y., Kim, S. T., Cho, W. K., Rim, Y. et al., Proteomics of weakly bound cell wall proteins in rice calli. J. Plant Physiol. 2009, 166, 675-685.
18. Hiller, K., Grote, A., Scheer, M., Munch, R., Jahn, D., PrediSi: Prediction of signal peptides and their cleavage positions. Nucleic Acids Res. 2004, 32, 375-379.
19. Klee, E. W., Sosa, C. P., Computationalclassification of classically secreted proteins. Drug Discov. Today 2007, 12, 234-240.
20. von Heijne, G., A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986, 14, 4683-4690.
21. Thanassi, D. G., Hultgren, S. J., Multiple pathways allow protein secretion across the bacterial outer membrane. Curr. Opin. Cell Biol. 2000, 12, 420-430.
22. Himmelbach, A., Zierold, U., Hensel, G., Riechen, J. et al., A set of modular binary vectors for the transformation of cereals. Plant Physiol. 2007, 145, 1192-1200.
23. Braaksma, M., Martens-Uzunova, E. S., Punt, P. J., Schaap, P. J., An inventory of the Aspergillus niger secretome by combining in silico predictions with shotgun proteomics data. BMC Genomics 2010, 11, 584-596.
24. Nikaido, H., Saier, M. H., Transport proteins in bacteria-common themes in their design. Science 1992, 258, 936-942.
25. Nikaido, H., Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 2003, 67, 593-656.
26. Watt, S. A., Wilke, A., Patschkowski, T., Niehaus, K., Comprehensive analysis of the extracellular proteins from Xanthomonas campestrispv. campestris B100. Proteomics 2005, 5, 153-167.
27. Khan, N. A., Shin, S., Chung, J. W., Kim, K. J. et al., Outer membrane protein A and cytotoxic necrotizing factor-1 use diverse signaling mechanisms for Escherichia coli K1 invasion of human brain microvascular endothelial cells. Microb. Pathog. 2003, 35, 35-42.
28. Teng, C. H., Xie, Y., Shin, S., Di Cello, F. et al., Effects of ompA deletion on expression of type 1 fimbriae in Escherichia coli K1 strain RS218 and on the association of E. coli with human brain microvascular endothelial cells. Infect. Immun. 2006, 74, 5609-5616.
29. Rott, P., Fleites, L., Marlow, G. C., Royer, M., Gabriel, D. W., An OmpA family outer membrane protein is required for both disease symptom development and sugarcane stalk colonization by Xanthomonas albilineans. Phytopathology 2009, 99, S110-S111.
30. Martinez-Canamero, M., Munoz-Dorado, J., Farez-Vidal, E., Inouye, M., Inouye, S., Oar, a 115-kilodalton membrane protein required for development of Myxococcus xanthus. J. Bacteriol. 1993, 175, 4756-4763.
31. Braun, V., Hancock, R. E. W., Hantke, K., Hartman, A., Functional organization of the outer membrane in Escherichia coli: phage and colicin receptors as components of iron uptake systems. J. Supramol. Struct. 1976, 5, 37-58.
32. Devanathan, S., Postle, K., Studies on colicin B translocation: FepA is gated by TonB. Mol. Microbiol. 2007, 65, 441-453.
33. Guterman, S. K., Dann, L., Excretion of enterochelin by exbA and exbB mutants of Escherichia coli. J. Bacteriol. 1973, 114, 1225-1230.
34. Winkelmann, G., van der Helm, D., Neilands, J. B. (Eds.), Iron Transport in Microbes, Plants, and Animals. VCH Verlagsgesellschaft, Weinheim, Germany, 1987.
35. Apel, K., Hirt, H., Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 2004, 55, 373-399.
36. 2 from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 4800-4805.
37. Chamnongpol, S., Mongkolsuk, S., Vattanaviboon, P., Fuangthong, M., Unusual growth phase and oxygen tension regulation of oxidative stress protection enzymes, catalase and superoxide dismutase, in the phytopathogen Xanthomonas oryzae pv. oryzae. Appl. Environ. Microbiol. 1995, 61, 393-396.
38. Li, X., Pang, X., Zhi, D., Wang, J., Li, M. et al., Extracellular superoxide anion production contributes to the virulence of Xanthomonas oryzae pv. oryzae. Can. J. Microbiol. 2009, 55, 110-116.
39. Fuangthong, M., Atichartpongkul, S., Mongkolsuk, S., Helmann, J. D., OhrR is a repressor of ohrA, a key organic hydroperoxide resistance determinant in Bacillus subtilis. J. Bacteriol. 2001, 183, 4134-4141.
40. Mongkolsuk, S., Praituan, W., Loprasert, S., Fuangthong, M., Chamnongpol, S., Identification and characterization of a new organic hydroperoxide resistance (ohr) gene with a novel pattern of oxidative stress regulation from Xanthomonas campestris pv. phaseoli. J. Bacteriol. 1998, 180, 2636-2643.
41. Ochsner, U. A., Hassett, D. J., Vasil, M. L., Genetic and physiological characterization of ohr, encoding a protein involved in organic hydroperoxide resistance in Pseudomonas aeruginosa. J. Bacteriol. 2001, 183, 773-778.
42. Sukchawalit, R., Loprasert, S., Atichartpongkul, S., Mongkolsuk, S., Complex regulation of the organic hydroperoxide resistance gene (ohr) from Xanthomonas involves OhrR, a novel organic peroxide-inducible negative regulator, and posttranscriptional modifications. J. Bacteriol. 2001, 183, 4405-4412.
43. Klomsiri, C., Panmanee, W., Dharmsthiti, S., Vattanaviboon, P., Mongkolsuk, S., Novel roles of ohrR-ohr in Xanthomonas sensing, metabolism, and physiological adaptive response to lipid hydroperoxide. J. Bacteriol. 2005, 187, 3277-3281.
44. Feldman, A. R., Lee, J., Delmas, B., Paetzel, M., Crystal structure of a novel viral protease with a serine/lysine catalytic dyad mechanism. J. Mol. Biol. 2006, 358, 1378-1389.
45. Hara, H., Yamamoto, Y., Higashitani, A., Suzuki, H., Nishimura, Y., Cloning, mapping, and characterization of the Escherichia coli prc gene, which is involved in C-terminal processing of penicillin-binding protein 3. J. Bacteriol. 1991, 173, 4799-4813.
46. Ostberg, Y., Carroll, J. A., Pinne, M., Krum et al., Pleiotropic effects of inactivating a carboxyl-terminal protease, CtpA, in Borrelia burgdorferi. J. Bacteriol. 2004, 186, 2074-2084.
47. Izoré, T., Job, V., Dessen, A., Biogenesis, regulation, and targeting of the type III secretion system. Structure 2011, 19, 603-612.
48. White, F. F., Potnis, N., Jones, J. B., Koebnik, R., The type III effectors of Xanthomonas. Mol. Plant Pathol. 2009, 10, 749-766.
49. Novik, V., Hofreuter, D., Galán, J. E., Characterization of a Campylobacter jejuni VirK protein homolog as a novel virulence determinant. Infect. Immun. 2009, 77, 5428-5436.
50. Rossier, O., Van den Ackerveken, G., Bonas, U., HrpB2 and HrpF from Xanthomonas are type III-secreted proteins and essential for pathogenicity and recognition by the host plant. Mol. Microbiol. 2000, 38, 828-838.
51. Abramovitch, R. B., Martin, G. B., Strategies used by bacterial pathogens to suppress plant defenses. Curr. Opin. Plant Biol. 2004, 7, 356-364.
52. Abramovitch, R. B., Anderson, J. C., Martin, G. B., Bacterial elicitation and evasion of plant innate immunity. Nat. Rev. Mol. Cell Biol. 2006, 7, 601-611.
53. 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 adhesions of animal pathogenic bacteria and is required for optimum virulence. Mol. Microbiol. 2002, 46, 637-647.
54. Das, A., Rangaraj, N., Sonti, R. V., Multiple adhesin-like functions of Xanthomonas oryzaepv. oryzae are involved in promoting leaf attachment, entry, and virulence on rice. Mol. Plant Microbe Interact. 2009, 22, 73-85.
55. Kim, S. T., Yu, S., Kim, S. G., Kim, H. J. et al., Proteome analysis of rice blast fungus (Magnaporthe grisea) proteome during appressorium formation. Proteomics 2004, 4, 3579-3587.
56. Hwang, D. H., Kim, S. T., Kim, S. G., Kang, K. Y., Comprehensive analysis of the expression of twenty-seven β-1, 3-glucanase genes in rice (Oryza sativa L.). Mol. Cells 2007, 23, 207-214.
57. Kuwabara, C., Arakawa, K., Yoshida, S., Abscisic acid-induced secretory proteins in suspension-cultured cells of winter wheat. Plant Cell Physiol. 1999, 40, 184-191.
58. Kim, S. T., Kim, S. G., Kang, Y. H., Wang, Y. et al., Proteomics analysis of rice lesion mimic mutant (spl1) reveals tightly localized probenazole-induced protein (PBZ1) in cells undergoing programmed cell death. J. Proteome Res. 2008, 7, 1750-1760.