1887

Abstract

The genome of , the causal agent of sugar cane leaf scald, carries a gene cluster encoding a predicted quorum sensing system that is highly related to the diffusible signalling factor (DSF) systems of the plant pathogens and . In these latter pathogens, a cluster of regulation of pathogenicity factors () genes encodes the DSF system and is involved in control of various cellular processes. Mutation of , encoding a predicted DSF synthase, in Florida strain XaFL07-1 resulted in a small reduction of disease severity (DS). Single-knockout mutations of and (encoding a predicted DSF sensor and regulator, respectively) had no effect on DS or swimming motility of the pathogen. However, capacity of the pathogen to cause disease was slightly reduced and swimming motility was severely affected when and were both deleted. Similar results were obtained when the entire region was deleted. Surprisingly, when the pathogen was mutated in or (single or double mutations) it was able to colonize sugar cane spatially more efficiently than the wild-type. Mutation in alone did not affect the degree of spatial invasion. We conclude that the DSF signal contributes to symptom expression but not to invasion of sugar cane stalks by strain XaFL07-1, which is mainly controlled by the RpfCG two-component system.

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2013-06-01
2021-10-24
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References

  1. Barber C. E., Tang J. L., Feng J. X., Pan M. Q., Wilson T. J. G., Slater H., Dow J. M., Williams P., Daniels M. J.( 1997). A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol Microbiol 24:555–566 [View Article][PubMed]
    [Google Scholar]
  2. Birch R. G.( 2001). Xanthomonas albilineans and the antipathogenesis approach to disease control. Mol Plant Pathol 2:1–11 [View Article][PubMed]
    [Google Scholar]
  3. Castañeda A., Reddy J. D., El-Yacoubi B., Gabriel D. W.( 2005). Mutagenesis of all eight avr genes in Xanthomonas campestris pv. campestris had no detected effect on pathogenicity, but one avr gene affected race specificity. Mol Plant Microbe Interact 18:1306–1317 [View Article][PubMed]
    [Google Scholar]
  4. Champoiseau P., Daugrois J.-H., Girard J.-C., Royer M., Rott P. C.( 2006). Variation in albicidin biosynthesis genes and in pathogenicity of Xanthomonas albilineans, the sugarcane leaf scald pathogen. Phytopathology 96:33–45 [View Article][PubMed]
    [Google Scholar]
  5. Chatterjee S., Almeida R. P. P., Lindow S. E.( 2008a). Living in two worlds: the plant and insect lifestyles of Xylella fastidiosa.. Annu Rev Phytopathol 46:243–271 [View Article][PubMed]
    [Google Scholar]
  6. Chatterjee S., Newman K. L., 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 [View Article][PubMed]
    [Google Scholar]
  7. Chatterjee S., Wistrom C., Lindow S. E.( 2008c). 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 [View Article][PubMed]
    [Google Scholar]
  8. Chatterjee S., Killiny N., Almeida R. P. P., Lindow S. E.( 2010). Role of cyclic di-GMP in Xylella fastidiosa biofilm formation, plant virulence, and insect transmission. Mol Plant Microbe Interact 23:1356–1363 [View Article][PubMed]
    [Google Scholar]
  9. Danhorn T., Fuqua C.( 2007). Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61:401–422 [View Article][PubMed]
    [Google Scholar]
  10. Daugrois J.-H., Dumont V., Champoiseau P., Costet L., Boisne-Noc R., Rott P.( 2003). Aerial contamination of sugarcane in Guadeloupe by two strains of Xanthomonas albilineans.. Eur J Plant Pathol 109:445–458 [View Article]
    [Google Scholar]
  11. Daugrois J.-H., Boisne-Noc R., Champoiseau P., Rott P.( 2012). The revisited infection cycle of Xanthomonas albilineans, the causal agent of leaf scald of sugarcane. Func Plant Sci Biotech 6:()91–97
    [Google Scholar]
  12. Davis M. J., Rott P., Baudin P., Dean J. L.( 1994). Evaluation of selective media and immunoassays for detection of Xanthomonas albilineans, causal agent of sugarcane leaf scald disease. Plant Dis 78:78–82 [View Article]
    [Google Scholar]
  13. De Feyter R., Gabriel D. W.( 1991). Use of cloned DNA methylase genes to increase the frequency of transfer of foreign genes into Xanthomonas campestris pv. malvacearum.. J Bacteriol 173:6421–6427[PubMed]
    [Google Scholar]
  14. De Feyter R., Yang Y., Gabriel D. W.( 1993). Gene-for-gene interactions between cotton R genes and Xanthomonas campestris pv. malvacearum avr genes. Mol Plant Microbe Interact 6:225–237 [View Article][PubMed]
    [Google Scholar]
  15. Dow M.( 2008). Diversification of the function of cell-to-cell signaling in regulation of virulence within plant pathogenic xanthomonads. Sci Signal 1:pe23 [View Article][PubMed]
    [Google Scholar]
  16. Dow J. M., Crossman L., Findlay K., He Y.-Q., Feng J.-X., Tang J.-L.( 2003). 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 100:10995–11000 [View Article][PubMed]
    [Google Scholar]
  17. Fouhy Y., Scanlon K., Schouest K., Spillane C., Crossman L., Avison M. B., Ryan R. P., Dow J. M.( 2007). Diffusible signal factor-dependent cell–cell signaling and virulence in the nosocomial pathogen Stenotrophomonas maltophilia.. J Bacteriol 189:4964–4968 [View Article][PubMed]
    [Google Scholar]
  18. Geier G. E., Modrich P.( 1979). Recognition sequence of the dam methylase of Escherichia coli K12 and mode of cleavage of DpnI endonuclease. J Biol Chem 254:1408–1413[PubMed]
    [Google Scholar]
  19. Guo Y., Zhang Y., Li J.-L., 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 [View Article][PubMed]
    [Google Scholar]
  20. He Y.-W., Zhang L.-H.( 2008). Quorum sensing and virulence regulation in Xanthomonas campestris.. FEMS Microbiol Rev 32:842–857 [View Article][PubMed]
    [Google Scholar]
  21. 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.& other authors ( 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 [View Article][PubMed]
    [Google Scholar]
  22. He Y.-W., Wu J., Cha J. S., Zhang L.-H.( 2010). Rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae produces multiple DSF-family signals in regulation of virulence factor production. BMC Microbiol 10:187 [View Article][PubMed]
    [Google Scholar]
  23. Klett P., Rott P.( 1994). Inoculum sources for the spread of leaf scald disease of sugarcane caused by Xanthomonas albilineans in Guadeloupe. J Phytopathol 142:283–291 [View Article]
    [Google Scholar]
  24. Li Y., Hao G., Galvani C. D., Meng Y., De La Fuente L., Hoch H. C., 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 [View Article][PubMed]
    [Google Scholar]
  25. Marguerettaz M., Pieretti I., Gayral P., Puig J., Brin C., Cociancich S., Poussier S., Rott P., Royer M.( 2011). Genomic and evolutionary features of the SPI-1 type III secretion system that is present in Xanthomonas albilineans but is not essential for xylem colonization and symptom development of sugarcane leaf scald. Mol Plant Microbe Interact 24:246–259 [View Article][PubMed]
    [Google Scholar]
  26. Newman K. L., Almeida R. P. P., Purcell A. H., 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 [View Article][PubMed]
    [Google Scholar]
  27. Pieretti I., Royer M., Barbe V., Carrere S., Koebnik R., Cociancich S., Couloux A., Darrasse A., Gouzy J.& other authors ( 2009). The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae. BMC Genomics 10:616 [View Article][PubMed]
    [Google Scholar]
  28. Pieretti I., Royer M., Barbe V., Carrere S., Koebnik R., Couloux A., Darrasse A., Gouzy J., Jacques M.-A.& other authors ( 2012). Genomic insights into strategies used by Xanthomonas albilineans with its reduced artillery to spread within sugarcane xylem vessels. BMC Genomics 13:658 [View Article][PubMed]
    [Google Scholar]
  29. Ricaud C., Ryan C. C.( 1989). Leaf scald. Diseases of Sugarcane. Major Diseases39–58 Ricaud C., Egan B. T., Gillaspie A. G. Jr, Hughes C. G. Amsterdam, The Netherlands: Elsevier Science Publishers; [View Article]
    [Google Scholar]
  30. Rott P., Davis M. J.( 2000). Leaf scald. A Guide to Sugarcane Diseases38–44 Rott P., Bailey R. A., Comstock J. C., Croft B. J., Saumtally A. S. Montpellier, France: La Librairie du Cirad;
    [Google Scholar]
  31. Rott P., Abel M., Soupa D., Feldmann P., Letourmy P.( 1994). Population dynamics of Xanthomonas albilineans in sugarcane plants as determined with an antibiotic-resistant mutant. Plant Dis 78:241–247 [View Article]
    [Google Scholar]
  32. Rott P., Mohamed I. S., Klett P., Soupa D., de Saint-Albin A., Feldmann P., Letourmy P.( 1997). Resistance to leaf scald disease is associated with limited colonization of sugarcane and wild relatives by Xanthomonas albilineans.. Phytopathology 87:1202–1213 [View Article][PubMed]
    [Google Scholar]
  33. Rott P., Fleites L., Marlow G., Royer M., Gabriel D. W.( 2011). Identification of new candidate pathogenicity factors in the xylem-invading pathogen Xanthomonas albilineans by transposon mutagenesis. Mol Plant Microbe Interact 24:594–605 [View Article][PubMed]
    [Google Scholar]
  34. Ryan R. P., Dow J. M.( 2011). Communication with a growing family: diffusible signal factor (DSF) signaling in bacteria. Trends Microbiol 19:145–152 [View Article][PubMed]
    [Google Scholar]
  35. Ryan R. P., McCarthy Y., Andrade M., Farah C. S., Armitage J. P., Dow J. M.( 2010). Cell–cell signal-dependent dynamic interactions between HD-GYP and GGDEF domain proteins mediate virulence in Xanthomonas campestris.. Proc Natl Acad Sci U S A 107:5989–5994 [View Article][PubMed]
    [Google Scholar]
  36. Ryan R. P., McCarthy Y., Kiely P. A., O’Connor R., Farah C. S., Armitage J. P., Dow J. M.( 2012). Dynamic complex formation between HD-GYP, GGDEF and PilZ domain proteins regulates motility in Xanthomonas campestris.. Mol Microbiol 86:557–567 [View Article][PubMed]
    [Google Scholar]
  37. Sambrook J., Fritsch E. F., Maniatis T.( 1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  38. Siciliano F., Torres P., Sendin L., Bermejo C., Filippone P., Vellice G., Ramallo J., Castagnaro A., Vojnov A., Marano M. R.( 2006). Analysis of the molecular basis of Xanthomonas axonopodis pv. citri pathogenesis in Citrus limon.. Electron J Biotechnol 9:199–204 [View Article]
    [Google Scholar]
  39. Slater H., Alvarez-Morales A., Barber C. E., Daniels M. J., Dow J. M.( 2000). A two-component system involving an HD-GYP domain protein links cell–cell signalling to pathogenicity gene expression in Xanthomonas campestris.. Mol Microbiol 38:986–1003 [View Article][PubMed]
    [Google Scholar]
  40. Sun L., Wu M., Chen H., He C.( 2010). Diffusible signal factor production and virulence expression in ΔrpfFxoo, ΔrpfCxoo and ΔrpfGxoo, the gene deletion mutants of DSF/Rpf signaling proteins of Xanthomonas oryzae pv. oryzae.. Acta Microbiol Sin 50:717–723
    [Google Scholar]
  41. Tang J. L., Liu Y. N., Barber C. E., Dow J. M., Wootton J. C., Daniels M. J.( 1991). 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 226:409–417 [View Article][PubMed]
    [Google Scholar]
  42. Thowthampitak J., Shaffer B. T., Prathuangwong S., Loper J. E.( 2008). Role of rpfF in virulence and exoenzyme production of Xanthomonas axonopodis pv. glycines, the causal agent of bacterial pustule of soybean. Phytopathology 98:1252–1260 [View Article][PubMed]
    [Google Scholar]
  43. Torres P. S., Malamud F., Rigano L. A., Russo D. M., Marano M. R., Castagnaro A. P., Zorreguieta A., Bouarab K., Dow J. M., Vojnov A. A.( 2007). Controlled synthesis of the DSF cell–cell signal is required for biofilm formation and virulence in Xanthomonas campestris.. Environ Microbiol 9:2101–2109 [View Article][PubMed]
    [Google Scholar]
  44. Wang L.-H., He Y., Gao Y., Wu J. E., Dong Y.-H., He C., Wang S. X., Weng L.-X., Xu J.-L.& other authors ( 2004). A bacterial cell–cell communication signal with cross-kingdom structural analogues. Mol Microbiol 51:903–912 [View Article][PubMed]
    [Google Scholar]
  45. Wang N., Li J.-L., Lindow S. E.( 2012). RpfF-dependent regulon of Xylella fastidiosa.. Phytopathology 102:1045–1053 [View Article][PubMed]
    [Google Scholar]
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