1887

Abstract

colonizes the xylem network of host plant species as well as the foregut of its required insect vectors to ensure efficient propagation. Disease management strategies remain inefficient due to a limited comprehension of the mechanisms governing both insect and plant colonization. It was previously shown that has a functional chitinase (ChiA), and that chitin likely serves as a carbon source for this bacterium. We expand on that research, showing that a mutant strain is unable to grow on chitin as the sole carbon source. Quantitative PCR assays allowed us to detect bacterial cells in the foregut of vectors after pathogen acquisition; populations of the wild-type and complemented mutant strain were both significantly larger than the mutant strain 10 days, but not 3 days, post acquisition. These results indicate that adhesion of the mutant strain to vectors may not be impaired, but that cell multiplication is limited. The mutant was also affected in its transmission by vectors to plants. In addition, the mutant strain was unable to colonize host plants, suggesting that the enzyme has other substrates associated with plant colonization. Lastly, ChiA requires other protein(s) for its chitinolytic activity. The observation that the mutant strain is not able to colonize plants warrants future attention to be paid to the substrates for this enzyme.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000438
2017-04-01
2019-12-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/163/4/502.html?itemId=/content/journal/micro/10.1099/mic.0.000438&mimeType=html&fmt=ahah

References

  1. Chatterjee S, Almeida RP, Lindow S. Living in two worlds: the plant and insect lifestyles of Xylella fastidiosa. Annu Rev Phytopathol 2008;46:243–271 [CrossRef][PubMed]
    [Google Scholar]
  2. Hopkins DL, Purcell AH. Xylella fastidiosa: cause of Pierce's disease of grapevine and other emergent diseases. Plant Dis 2002;86:1056–1066 [CrossRef]
    [Google Scholar]
  3. Almeida RPP, Blua MJ, Lopes JRS, Purcell AH. Vector transmission of Xylella fastidiosa: applying fundamental knowledge to generate disease management strategies. Ann Entomol Soc Am 2005;98:775–786 [CrossRef]
    [Google Scholar]
  4. Daugherty MP, Lopes J, Almeida RPP. Vector within-host feeding preference mediates transmission of a heterogeneously distributed pathogen. Ecol Entomol 2010;35:360–366 [CrossRef]
    [Google Scholar]
  5. Daugherty MP, Rashed A, Almeida RPP, Perring TM. Vector preference for hosts differing in infection status: sharpshooter movement and Xylella fastidiosa transmission. Ecol Entomol 2011;36:654–662 [CrossRef]
    [Google Scholar]
  6. Lopes JRS, Daugherty MP, Almeida RPP. Context-dependent transmission of a generalist plant pathogen: host species and pathogen strain mediate insect vector competence. Entomol Exp Appl 2009;131:216–224 [CrossRef]
    [Google Scholar]
  7. Almeida RPP, Purcell AH. Patterns of Xylella fastidiosa colonization on the precibarium of sharpshooter vectors relative to transmission to plants. Ann Entomol Soc Am 2006;99:884–890 [CrossRef]
    [Google Scholar]
  8. Killiny N, Almeida RP. Xylella fastidiosa afimbrial adhesins mediate cell transmission to plants by leafhopper vectors. Appl Environ Microbiol 2009;75:521–528 [CrossRef][PubMed]
    [Google Scholar]
  9. Purcell AH, Finlay AH, Mclean DL. Pierce's disease bacterium: mechanism of transmission by leafhopper vectors. Science 1979;206:839–841 [CrossRef][PubMed]
    [Google Scholar]
  10. Simpson AJ, Reinach FC, Arruda P, Abreu FA, Acencio M et al. The genome sequence of the plant pathogen Xylella fastidiosa. The Xylella fastidiosa consortium of the organization for nucleotide sequencing and analysis. Nature 2000;406:151–159 [CrossRef][PubMed]
    [Google Scholar]
  11. Killiny N, Almeida RP. Host structural carbohydrate induces vector transmission of a bacterial plant pathogen. Proc Natl Acad Sci USA 2009;106:22416–22420 [CrossRef][PubMed]
    [Google Scholar]
  12. Killiny N, Almeida RPP. Factors affecting the initial adhesion and retention of the plant pathogen Xylella fastidiosa in the foregut of an insect vector. Appl Environ Microbiol 2014;80:420–426 [CrossRef]
    [Google Scholar]
  13. Killiny N, Rashed A, Almeida RP. Disrupting the transmission of a vector-borne plant pathogen. Appl Environ Microbiol 2012;78:638–643 [CrossRef][PubMed]
    [Google Scholar]
  14. Labroussaa F, Zeilinger AR, Almeida RP. Blocking the transmission of a noncirculative vector-borne plant pathogenic bacterium. Mol Plant Microbe Interact 2016;29:535–544 [CrossRef][PubMed]
    [Google Scholar]
  15. Killiny N, Prado SS, Almeida RP. Chitin utilization by the insect-transmitted bacterium Xylella fastidiosa. Appl Environ Microbiol 2010;76:6134–6140 [CrossRef][PubMed]
    [Google Scholar]
  16. Hill BL, Purcell AH. Acquisition and retention of Xylella fastidiosa by an efficient vector, Graphocephala atropunctata. Phytopathology 1995;85:209–212[CrossRef]
    [Google Scholar]
  17. Almeida RP, Purcell AH. Transmission of Xylella fastidiosa to grapevines by Homalodisca coagulata (Hemiptera: Cicadellidae). J Econ Entomol 2003;96:264–271 [CrossRef][PubMed]
    [Google Scholar]
  18. Severin HHP. Transmission of the virus of Pierce's disease of grapevines by leafhoppers. Hilgardia 1949;19:190–206 [CrossRef]
    [Google Scholar]
  19. Van Sluys MA, De Oliveira MC, Monteiro-Vitorello CB, Miyaki CY, Furlan LR et al. Comparative analyses of the complete genome sequences of Pierce's disease and citrus variegated chlorosis strains of Xylella fastidiosa. J Bacteriol 2003;185:1018–1026 [CrossRef][PubMed]
    [Google Scholar]
  20. Freitag JH. Host range of Pierce’s disease virus of grapes as determined by insect transmission. Phytopathology 1951;41:920–934
    [Google Scholar]
  21. Purcell AH. Evidence for noncirculative transmission of Pierce's disease bacterium by sharpshooter leafhoppers. Phytopathology 1979;69:393–395 [CrossRef]
    [Google Scholar]
  22. Kung SH, Almeida RP. Natural competence and recombination in the plant pathogen Xylella fastidiosa. Appl Environ Microbiol 2011;77:5278–5284 [CrossRef][PubMed]
    [Google Scholar]
  23. De Souza AA, Ionescu M, Baccari C, Da Silva AM, Lindow SE. Phenotype overlap in Xylella fastidiosa is controlled by the cyclic di-GMP phosphodiesterase Eal in response to antibiotic exposure and diffusible signal factor-mediated cell-cell signaling. Appl Environ Microbiol 2013;79:3444–3454 [CrossRef][PubMed]
    [Google Scholar]
  24. Kung SH, Almeida RP. Biological and genetic factors regulating natural competence in a bacterial plant pathogen. Microbiology 2014;160:37–46 [CrossRef][PubMed]
    [Google Scholar]
  25. Matsumoto A, Young GM, Igo MM. Chromosome-based genetic complementation system for Xylella fastidiosa. Appl Environ Microbiol 2009;75:1679–1687 [CrossRef][PubMed]
    [Google Scholar]
  26. Haran S, Schickler H, Oppenheim A, Chet I. New components of the chitinolytic system of Trichoderma harzianum. Mycol Res 1995;99:441–446 [CrossRef]
    [Google Scholar]
  27. Francis M, Lin H, Rosa JC-L, Doddapaneni H, Civerolo EL. Genome-based PCR primers for specific and sensitive detection and quantification of Xylella fastidiosa. Eur J Plant Pathol 2006;115:203–213 [CrossRef]
    [Google Scholar]
  28. Rashed A, Kwan J, Baraff B, Ling D, Daugherty MP et al. Relative susceptibility of Vitis vinifera cultivars to vector-borne Xylella fastidiosa through time. PLoS One 2013;8:e55326 [CrossRef][PubMed]
    [Google Scholar]
  29. R Core Team R: A Language and Environment for Statistical Computing Vienna, Austria: R Foundation for Statistical Computing; 2016;www.R-project.org/
    [Google Scholar]
  30. Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J Stat Softw 2015;67:1–48 [CrossRef]
    [Google Scholar]
  31. Kosmidis I. 2013; Brglm: bias reduction in binomial-response generalized linear models. www.ucl.ac.uk/~ucakiko/software.html accessed June 2016
  32. Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biom J 2008;50:346–363 [CrossRef][PubMed]
    [Google Scholar]
  33. Frederiksen RF, Paspaliari DK, Larsen T, Storgaard BG, Larsen MH et al. Bacterial chitinases and chitin-binding proteins as virulence factors. Microbiology 2013;159:833–847 [CrossRef][PubMed]
    [Google Scholar]
  34. Frederiksen RF, Yoshimura Y, Storgaard BG, Paspaliari DK, Petersen BO et al. A diverse range of bacterial and eukaryotic chitinases hydrolyzes the LacNAc (Galβ1-4GlcNAc) and LacdiNAc (GalNAcβ1-4GlcNAc) motifs found on vertebrate and insect cells. J Biol Chem 2015;290:5354–5366 [CrossRef][PubMed]
    [Google Scholar]
  35. Newman KL, Almeida RP, Purcell AH, Lindow SE. Use of a green fluorescent strain for analysis of Xylella fastidiosa colonization of Vitis vinifera. Appl Environ Microbiol 2003;69:7319–7327 [CrossRef][PubMed]
    [Google Scholar]
  36. Roper MC, Greve LC, Warren JG, Labavitch JM, Kirkpatrick BC. Xylella fastidiosa requires polygalacturonase for colonization and pathogenicity in Vitis vinifera grapevines. Mol Plant Microbe Interact 2007;20:411–419 [CrossRef][PubMed]
    [Google Scholar]
  37. Fukamizo T. Chitinolytic enzymes: catalysis, substrate binding, and their application. Curr Protein Pept Sci 2000;1:105–124 [CrossRef][PubMed]
    [Google Scholar]
  38. Watanabe T, Ito Y, Yamada T, Hashimoto M, Sekine S et al. The roles of the C-terminal domain and type III domains of chitinase A1 from Bacillus circulans WL-12 in chitin degradation. J Bacteriol 1994;176:4465–4472 [CrossRef][PubMed]
    [Google Scholar]
  39. Chaudhuri S, Bruno JC, Alonzo F, Xayarath B, Cianciotto NP et al. Contribution of chitinases to Listeria monocytogenes pathogenesis. Appl Environ Microbiol 2010;76:7302–7305 [CrossRef][PubMed]
    [Google Scholar]
  40. Kirn TJ, Jude BA, Taylor RK. A colonization factor links Vibrio cholerae environmental survival and human infection. Nature 2005;438:863–866 [CrossRef][PubMed]
    [Google Scholar]
  41. Francetic O, Badaut C, Rimsky S, Pugsley AP. The ChiA (YheB) protein of Escherichia coli K-12 is an endochitinase whose gene is negatively controlled by the nucleoid-structuring protein H-NS. Mol Microbiol 2000;35:1506–1517 [CrossRef][PubMed]
    [Google Scholar]
  42. Hervé C, Rogowski A, Blake AW, Marcus SE, Gilbert HJ et al. Carbohydrate-binding modules promote the enzymatic deconstruction of intact plant cell walls by targeting and proximity effects. Proc Natl Acad Sci USA 2010;107:15293–15298 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000438
Loading
/content/journal/micro/10.1099/mic.0.000438
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error