Diffusible signal factor (DSF) synthase RpfF of Xylella fastidiosa is a multifunction protein also required for response to DSF

Journal of Bacteriology

Volumn 195, Issue 23, 2013, Pages 5273-5284

  Ionescu, Michael ^a   Baccari, Clelia ^a   Da Silva, Aline Maria ^b   Garcia, Angelica ^a   Yokota, Kenji ^c   Lindow, Steven E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL PROTEIN RPFC; BACTERIAL PROTEIN RPFF; DIFFUSIBLE SIGNAL FACTOR SYNTHETASE; SYNTHETASE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; GENE EXPRESSION; HXFA BACTERIAL GENE; HXFB BACTERIAL GENE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; XANTHOMONAS CAMPESTRIS; XYLELLA FASTIDIOSA;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MUTATION; PLANT DISEASES; VITIS; XYLELLA;

EID: 84887516255     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00713-13     Document Type: Article

References (43)

1. Purcell AH, Hopkins DL. 1996. Fastidious xylem-limited bacterial plant pathogens. Annu. Rev. Phytopathol. 34:131-151.
2. Hopkins DL, Purcell AH. 2002. Xylella fastidiosa: cause of Pierce's disease of grapevine and other emergent diseases. Plant Dis. 86:1056-1066.
3. Chatterjee S, Newman KL, Lindow SE. 2008. Cell-cell signaling in Xylella fastidiosa suppresses movement and xylem vessel colonization in grape. Mol. Plant Microbe Interact. 21:1309-1315.
4. Chatterjee S, Almeida RPP, Lindow SE. 2008. Living in two worlds: the plant and insect lifestyles of Xylella fastidiosa. Annu. Rev. Phytopathol. 46:243-271.
5. Barber CE, Tang JL, Feng JX, Pan MQ, Wilson TJG, Slater H, Dow JM, Williams P, Daniels MJ. 1997. A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol. Microbiol. 24:555-566.
6. Newman KL, Almeida RPP, Purcell A, Lindow SE. 2004. Cell-cell signaling controls Xylella fastidiosa interactions with both insects and plants. Proc. Natl. Acad. Sci. U.S.A. 101:1737-1742.
7. Deng Y, Wu J, Tao F, Zhang LH. 2011. Listening to a new language: DSF-based quorum sensing in Gram-negative bacteria. Chem. Rev. 111:160-173.
8. Wang LH, He Y, Gao Y, Wu JE, Dong YH, He C, Wang SX, Weng LX, Xu JL, Tay L, Fang RX, Zhang LH. 2004. A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol. Microbiol. 51:903-912.
9. He YW, Wu J, Cha JS, Zhang LH. 2010. Rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae produces multiple DSF-family signals in regulation of virulence factor production. BMC Microbiol. 10:187. doi:10.1186/1471-2180-10-187.
10. Boon C, Deng Y, Wang LH, He Y, Xu JL, Fan Y, Pan SQ, Zhang LH. 2008. A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME J. 2:27-36.
11. Beaulieu ED, Ionescu M, Chatterjee S, Yokota K, Trauner D, Lindow S. 2013. Characterization of a diffusible signaling factor (DSF) from Xylella fastidiosa. mBio 4(1):e00539-12. doi:10.1128/mBio.00539-12.
12. Colnaghi Simionato AV, da Silva DD, Lambais MR, Carrilho E. 2007. Characterization of a putative Xylella fastidiosa diffusible signal factor by HRGC-EI-MS. J. Mass Spectrom. 42:1375-1381.
13. Bi H, Christensen QH, Feng Y, Wang H, Cronan JE. 2012. The Burkholderia cenocepacia BDSF quorum sensing fatty acid is synthesized by a bifunctional crotonase homologue having both dehydratase and thioesterase activities. Mol. Microbiol. 83:840-855.
14. Ryan RP, Fouhy Y, Lucey JF, Crossman LC, Spiro S, He YW, Zhang LH, Heeb S, Camara M, Williams P, Dow JM. 2006. 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. 103:6712-6717.
15. He YW, Wang C, Zhou L, Song H, Dow JM, Zhang LH. 2006. 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. 59:610-622.
16. He YW, Wang C, Zhou L, Song H, Dow JM, Zhang LH. 2006. Dual signaling functions of the hybrid sensor kinase RpfC of Xanthomonas campestris involve either phosphorelay or receiver domain-protein interaction. J. Biol. Chem. 281:33414-33421.
17. Guo Y, Zhang Y, Li JL, Wang N. 2012. Diffusible signal factor-mediated quorum sensing plays a central role in coordinating gene expression of Xanthomonas citri subsp. citri. Mol. Plant Microbe Interact. 25:165-179.
18. Rai R, Ranjan M, Pradhan B, Chatterjee S. 2012. Atypical regulation of virulence-associated functions by a diffusible signal factor in Xanthomonas oryzae pv. oryzae. Mol. Plant Microbe Interact. 25:789-801.
19. Chatterjee S, Wistrom C, Lindow SE. 2008. A cell-cell signaling sensor is required for virulence and insect transmission of Xylella fastidiosa. Proc. Natl. Acad. Sci. U.S.A. 105:2670-2675.
20. Wang N, Li JL, Lindow SE. 2012. RpfF-dependent regulon of Xylella fastidiosa. Phytopathology 102:1045-1053.
21. Cheng Z, He YW, Lim SC, Qamra R, Walsh MA, Zhang LH, Song H. 2010. Structural basis of the sensor-synthase interaction in autoinduction of the quorum sensing signal DSF biosynthesis. Structure 18:1199-1209.
22. King E, Ward M, Raney D. 1954. Two simple media for the demonstration of pyocyanin and fluorescin. J. Lab. Clin. Med. 44:301-307.
23. Davis MJ, Whitcomb RF, Gillaspie AG, Jr. 1981. Fastidious bacteria of plant vascular tissue and invertebrates (including so called Rickettsia-like bacteria), p 2172-2188. In Starr MP, Stolp H, Truper HG, Balows A, Schlegel HG (ed), The prokaryotes: a handbook on habitats, isolation, and identification of bacteria. Springer-Verlag, Heidelberg, Germany.
24. Marco ML, Legac J, Lindow SE. 2005. Pseudomonas syringae genes induced during colonization of leaf surfaces. Environ. Microbiol. 7:1379-1391.
25. Ionescu M, Belkin S. 2009. Overproduction of exopolysaccharides by an Escherichia coli K-12 rpoS mutant in response to osmotic stress. Appl. Environ. Microbiol. 75:483-492.
26. Almeida RP, Killiny N, Newman KL, Chatterjee S, Ionescu M, Lindow SE. 2012. Contribution of rpfB to cell-to-cell signal synthesis, virulence, and vector transmission of Xylella fastidiosa. Mol. Plant Microbe Interact. 25:453-462.
27. Kudla G, Murray AW, Tollervey D, Plotkin JB. 2009. Coding-sequence determinants of gene expression in Escherichia coli. Science 324:255-258.
28. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM, II, Peterson KM. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
29. Kung SH, Almeida RP. 2011. Natural competence and recombination in the plant pathogen Xylella fastidiosa. Appl. Environ. Microbiol. 77:5278-5284.
30. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-Delta Delta C(T) method. Methods 25:402-408.
31. Matsumoto A, Young GM, Igo MM. 2009. Chromosome-based genetic complementation system for Xylella fastidiosa. Appl. Environ. Microbiol. 75:1679-1687.
32. Matsumoto A, Igo MM. 2010. Species-specific type II restrictionmodification system of Xylella fastidiosa temecula1. Appl. Environ. Microbiol. 76:4092-4095.
33. Torriani A. 1968. Alkaline phosphatase of Escherichia coli, p 212-218. In Grossman L, Moldave K (ed), Methods in enzymology, vol 12B. Academic Press, New York, NY.
34. Hill BL, Purcell AH. 1995. Multiplication and movement of Xylella fastidiosa within grapevine and four other plants. Phytopathology 85:1368-1372.
35. Baccari C, Lindow SE. 2011. Assessment of the process of movement of Xylella fastidiosa within susceptible and resistant grape cultivars. Phytopathology 101:77-84.
36. Guilhabert MR, Kirkpatrick BC. 2005. Identification of Xylella fastidiosa antivirulence genes: hemagglutinin adhesins contribute to biofilm maturation to X. fastidiosa and colonization and attenuate virulence. Mol. Plant Microbe Interact. 18:856-868.
37. Hsiao YM, Liao HY, Lee MC, Yang TC, Tseng YH. 2005. Clp upregulates transcription of engA gene encoding a virulence factor in Xanthomonas campestris by direct binding to the upstream tandem Clp sites. FEBS Lett. 579:3525-3533.
38. He YW, Ng AY, Xu M, Lin K, Wang LH, Dong YH, Zhang LH. 2007. Xanthomonas campestris cell-cell communication involves a putative nucleotide receptor protein Clp and a hierarchical signaling network. Mol. Microbiol. 64:281-292.
39. Slater H, Alvarez-Morales A, Barber CE, Daniels MJ, Dow JM. 2000. A two-component system involving an HD-GYP domain protein links cellcell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol. Microbiol. 38:986-1003.
40. Deng Y, Schmid N, Wang C, Wang J, Pessi G, Wu D, Lee J, Aguilar C, Ahrens CH, Chang C, Song H, Eberl L, Zhang LH. 2012. Cis-2-dodecenoic acid receptor RpfR links quorum-sensing signal perception with regulation of virulence through cyclic dimeric guanosine monophosphate turnover. Proc. Natl. Acad. Sci. U.S.A. 109:15479-15484.
41. An SQ, Febrer M, McCarthy Y, Tang DJ, Clissold L, Kaithakottil G, Swarbreck D, Tang JL, Rogers J, Dow JM, Ryan RP. 2013. Highresolution transcriptional analysis of the regulatory influence of cell-tocell signalling reveals novel genes that contribute to Xanthomonas phytopathogenesis. Mol. Microbiol. 88:1058-1069.
42. Shepherd RW, Lindow SE. 2009. Two dissimilar N-acyl-homoserine lactone acylases of Pseudomonas syringae influence colony and biofilm morphology. Appl. Environ. Microbiol. 75:45-53.
43. Loper JE, Lindow SE. 1994. A biological sensor for iron available to bacteria in their habitats on plant surfaces. Appl. Environ. Microbiol. 60:1934-1941.