Identification of an operon, Pil-Chp, that controls twitching motility and virulence in Xylella fastidiosa

Molecular Plant-Microbe Interactions

Volumn 24, Issue 10, 2011, Pages 1198-1206

  Cursino, Luciana ^a,b   Galvani, Cheryl D ^a,b   Athinuwat, Dusit ^a   Zaini, Paulo A ^a,c   Li, Yaxin ^a   De La Fuente, Leonardo ^a,d   Hoch, Harvey C ^a   Burr, Thomas J ^a   Mowery, Patricia ^b  

^a School of Integrative Plant Science College of Agriculture and Life Sciences   (United States)

^b HOBART AND WILLIAM SMITH COLLEGES   (United States)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d AUBURN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BIOFILM; FIMBRIA; GENETICS; GRAPE; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; MICROBIOLOGY; MOLECULAR GENETICS; MOVEMENT (PHYSIOLOGY); MUTATION; NUCLEOTIDE SEQUENCE; OPERON; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; SEQUENCE HOMOLOGY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; VIRULENCE; XYLELLA;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; BIOFILMS; DNA, BACTERIAL; FIMBRIAE, BACTERIAL; GENES, BACTERIAL; HOST-PATHOGEN INTERACTIONS; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; MOVEMENT; MUTATION; OPERON; PLANT DISEASES; SEQUENCE HOMOLOGY, AMINO ACID; VIRULENCE; VITIS; XYLELLA;

BACTERIA (MICROORGANISMS); XYLELLA FASTIDIOSA;

EID: 80052645279     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-10-10-0252     Document Type: Article

References (44)

1. Alexander, R. P., and Zhulin, I. B. 2007. Evolutionary genomics reveals conserved structural determinants of signaling and adaptation in microbial chemoreceptors. Proc. Natl. Acad. Sci. U.S.A. 104:2885-2890. (Pubitemid 46327974)
2. Almeida, R. P. P., Blua, M. J., Lopes, J. R. S., and Purcell, A. H. 2005. Transmission of Xylella fastidiosa: Applying fundamental knowledge to generate disease management strategies. Annu. Entomol. Soc. Am. 98:775-786. (Pubitemid 41701329)
3. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhag, Z., Miller, W., and Lipman, D. J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402. (Pubitemid 27359211)
4. Bateman, A., Birney, E., Cerruti, L., Durbin, R., Etwiller, L., Eddy, S. R., Griffiths-Jones, S., Howe, K. L., Marshall, M., and Sonnhammer, E. L. 2002. The Pfam protein families database. Nucleic Acids Res. 30:276-280. (Pubitemid 34679563)
5. Bhaya, D., Takahashi, A., and Grossman, A. R. 2001. Light regulation of type IV pilus-dependent motility by chemosensor-like elements in Synechocystis PCC6803. Proc. Natl. Acad. Sci. U.S.A. 98:7540-7545. (Pubitemid 32567984)
6. Chatterjee, S., Almeida, R. P. P., and Lindow, S. 2008a. Living in two worlds: The plant and insect lifestyles of Xylella fastidiosa. Annu. Rev. Phytopathol. 46:243-271.
7. Chatterjee, S., Newman, K. L., and Lindow, S. E. 2008b. Cell-to-cell signaling in Xylella fastidiosa suppresses movement and xylem vessel colonization in grape. Mol. Plant-Microbe Interact. 21:1309-1315.
8. Cursino, L., Li, Y., Zaini, P. A., De La Fuente, L., Hoch, H. C., and Burr, T. J. 2009. Twitching motility and biofilm formation are associated with tonB1 in Xylella fastidiosa. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 299:193-199.
9. Darzins, A. 1993. The pilG gene product, required for Pseudomonas aeruginosa pilus production and twitching motility, is homologous to the enteric, single-domain response regulator CheY. J. Bacteriol. 175:5934-5944. (Pubitemid 23277442)
10. Darzins, A. 1994. Characterization of a Pseudomonas aeruginosa gene cluster involved in pilus biosynthesis and twitching motility: Sequence similarity to the chemotaxis proteins of enterics and the gliding bacterium Myxococccus xanthus. Mol. Microbiol. 11:137-153.
11. da Silva Neto, J. F., Koide, T., Abe, C. M., Gomes, S. L., and Marques, M. V. 2008. Role of sigma54 in the regulation of genes involved in type I and type IV pili biogenesis in Xylella fastidiosa. Arch Microbiol. 189:249-261.
12. Davis, M. J., French, W. J., and Schaad, N. W. 1981. Axenic culture of the bacteria associated with phony disease of peach and plum leaf scald. Curr. Microbiol. 6:309-314.
13. De La Fuente, L., Burr, T. J., and Hoch, H. C. 2007a. Mutations in type I and type IV pilus biosynthetic genes affect twitching motility rates in Xylella fastidiosa. J. Bacteriol. 189:7507-7510. (Pubitemid 47557368)
14. De La Fuente, L., Montanes, E., Meng, Y., Li, Y., Burr, T. J., Hoch, H. C., and Wu, M. 2007b. Assessing adhesion forces of type I and type IV pili of Xylella fastidiosa using a microfluidic flow chamber. Appl. Environ. Microbiol. 73:2690-2696. (Pubitemid 46668763)
15. DeLange, P. A., Collins, T. L., Pierce, G. E., and Robinson, J. B. 2007. PilJ localizes to cell poles and is required for type IV pilus extension in Pseudomonas aeruginosa. Curr. Microbiol. 55:389-395. (Pubitemid 47536826)
16. Falke, J. J., and Hazelbauer, G. L. 2001. Transmembrane signaling in bacterial chemoreceptors. Trends Biochem. Sci. 26:257-265. (Pubitemid 32289244)
17. Ferandez, A., Hawkins, A. C., Summerfield, D. T., and Harwood, C. S. 2002. Cluster II che genes from Pseudomonas aeruginosa are required for an optimal chemotactic response. J. Bacteriol. 184:4374-4383. (Pubitemid 34832565)
18. Fulcher, N. B., Holliday, P. M., Klem, E., Cann, M. J., and Wolfgang, M. C. 2010. The Pseudomonas aeruginosa Chp chemosensory system regulates intracellular cAMP levels by modulatine adenylate cyclase activity. Mol. Microbiol. 76:889-904.
19. Galvani, C. D., Li, Y., Burr, T. J., and Hoch, H. C. 2007. Twitching motility among pathogenic Xylella fastidiosa isolates and the influence of bovine serum albumin on twitching-dependent colony fringe morphology. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 268:202-208.
20. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M. R., Appel, R. D., and Bairoch, A. 2005. Protein identification and analysis tools on the ExPASy server. Pages 571-607 in: The Proteomics Protocols Handbook. J. M. Walker, ed. Humana Press, Totowa, NJ, U.S.A.
21. Guilhabert, M. R., and Kirkpatrick, B. C. 2005. Identification of Xylella fastidiosa avirulence genes: Hemagglutinin adhesins contribute to X. fastidiosa biofilm maturation and colonization and attenuate virulence. Mol. Plant-Microbe Interact. 18:856-868. (Pubitemid 41061484)
22. Hamer, R., Chen, P. Y., Armitage, J. P., Reinert, G., and Deane, C. M. 2010. Deciphering chemotaxis pathways using cross species comparisons. BMC Syst. Biol. 4:3.
23. Hazelbauer, G. L., Falke, J. J., and Parkinson, J. S. 2008. Bacterial chemoreceptors: High-performance signaling in networked arrays. Trends Biochem. Sci. 33:9-19.
24. Hopkins D. L. 1984. Variability of virulence in grapevine among isolates of the Pierce's disease bacterium. Phytopathology 74:1395-1398.
25. Kirby, J. R. 2009. Chemotaxis-like regulatory systems: Unique roles in diverse bacteria. Annu. Rev. Microbiol. 63:45-59.
26. Krueger, J. K., Stock, J., and Schutt, C. E. 1992. Evidence that the methylesterase of bacterial chemotaxis may be a serine hydrolase. Biochim. Biophys. Acta 1119:332-326.
27. Letunic, I., Goodstadt, L., Dickens, N. J., Doerks, T., Schultz, J., Mott, R., Ciccarelli, F., Copley, R. R., Ponting, C. P., and Bork, P. 2002. Recent improvements to the SMART domain-based sequence annotation resource. Nucleic Acids Res. 30:242-244. (Pubitemid 34679554)
28. Li, Y., Hao, G., Galvani, C. D., Meng, Y., De La Fuente, L., Hoch, H. C., and Burr, T. J. 2007. Type I and type IV pili of Xylella fastidiosa affect twitching motility, biofilm formation and cell-cell aggregation. Microbiology 153:719-726. (Pubitemid 46444370)
29. Marchler-Bauer, A., Anderson, J. B., Derbyshire, M. K., DeWeese-Scott, C., Gonzales, N. R., Gwadz, M., Hao, L., He, S., Hurwitz, D. I., Jackson, J. D., Ke, Z., Krylov, D., Lanczycki, C. J., Liebert, C. A., Liu, C., Lu, F., Lu, S., Marchler, G. H., Mullokandov, M., Song, J. S., Thanki, N., Yamashita, R. A., Yin, J. J., Zhang, D., and Bryant, S.H. 2007. CDD: A conserved domain database for interactive domain family analysis. Nucleic Acids Res. 35:237-240.
30. Matsumoto, A., Young, G. M., and Igo, M. M. 2009. Chromosome-based genetic complementation system for Xylella fastidiosa. Appl. Environ. Microbiol. 75:1679-1687.
31. Mattick, J. S. 2002. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56:289-314. (Pubitemid 35217457)
32. Meng, Y., Galvani, C. D., Hao, G., Turner, J. N., Burr, T. J., and Hoch, H. C. 2005. Upstream migration of Xylella fastidiosa via pilus-driven twitching motility. J. Bacteriol. 187:5560-5567. (Pubitemid 41134290)
33. Newman, K. L., Almeida, R. P. P., Purcell, A. H., and Lindow, S. E. 2004. Cell-cell signaling controls Xylella fastidiosa interactions with both insects and plants. Proc. Natl. Acad. Sci. U.S.A. 101:1737-1742. (Pubitemid 38234223)
34. Purcell, A. H., and Hopkins, D. L. 1996. Fastidious xylem-limited bacterial plant pathogens. Annu. Rev. Phytopathol. 34:131-151. (Pubitemid 26399507)
35. Roper, M. C., Greve, L. C., Warren, J. G., Labavitch, J. M., and Kirkpatrick, B. C. 2007. Xylella fastidiosa requires polygalacturonase for colonization and pathogenicity in Vitis vinifera grapevines. Mol. Plant-Microbe Interact. 50:411-419. (Pubitemid 46449399)
36. Sanders, D. A., Gillece-Castro, B. L., Stock, A. M., Burlingame, A. L., and Koshland, D.E., Jr. 1989. Identification of the site of phosphorylation of the chemotaxis response regulator protein, CheY. J. Biol. Chem. 264:21770-21778. (Pubitemid 20028746)
37. Shi, X. Y., Dumenyo, C. K., Hernandez-Martinez, R., Azad, H., and Cooksey, D. A. 2007. Characterization of regulatory pathways in Xylella fastidiosa: Genes and phenotypes controlled by algU. Appl. Environ. Microbiol. 73:6748-6756. (Pubitemid 350076793)
38. Shi, X. Y., Dumenyo, C. K., Hernandez-Martinez, R., Azad, H., and Cooksey, D. A. 2009. Characterization of regulatory pathways in Xylella fastidiosa: Genes and phenotypes controlled by gacA. Appl. Environ. Microbiol. 75:2275-2283.
39. West, A. H., Martinez-Hackert, E., and Stock, A. M. 1995. Crystal structure of the catalytic domain of the chemotaxis receptor methylesterase, CheB. J. Mol. Biol. 250:276-290.
40. Whitchurch, C. B., Leech, A. J., Young, M. D., Kennedy, D., Sargent, J. L., Bertrand, J. J., Semmler, A. B., Mellick, A. S., Martin, P. R., Alm, R. A., Hobbs, M., Beatson, S. A., Huang, B., Nguyen, L., Commolli, J. C., Engel, J. N., Darzins, A., and Mattick, J. S. 2004. Characterization of a complex chemosensory signal transduction system which controls twitching motility in Pseudomonas aeruginosa. Mol. Microbiol. 52:873-893. (Pubitemid 38621755)
41. Winther-Larsen, H. C., and Koomey, M. 2002. Transcriptional, chemosensory and cell-contact-dependent regulation of type IV pilus expression. Curr. Opin. Microbiol. 5:173-178. (Pubitemid 34289925)
42. Wuichet, K., Alexander, R. P., and Zhulin, I. B. 2007. Comparative genomic and protein sequence analyses of a complex system controlling bacterial chemotaxis. Methods Enzymol. 422:1-31.
43. Zaini, P. A., De La Fuente, L., Hoch, H. C., and Burr, T. J. 2009. Grapevine xylem sap enhances biofilm development by Xylella fastidiosa. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 295:129-134.
44. Zusman, D. R., Scott, A. E., Yang, Z., and Kirby, J. R. 2007. Chemosensory motility and development in Myxococcus xanthus. Nat. Rev. Microbiol. 5:862-872. (Pubitemid 47578387)