Skip to main content

Advertisement

SpringerLink
Log in

Effect of xylem fluid from susceptible and resistant grapevines on developmental biology of Xylella fastidiosa

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Xylella fastidiosa causes Pierce’s disease (PD), a serious disease in grapevines, and grapevine cultivars vary in susceptibility to X. fastidiosa in the field. The mechanism(s) by which this occurs has not been clearly elucidated. To explore possible mechanisms, X. fastidiosa cells from a PD strain were grown in pure xylem fluid of PD-susceptible grapevines, Vitis vinifera and V. labrusca, versus PD-resistant grapevines, V. champinii and V. smalliana. When grown in xylem fluid from the susceptible species, X. fastidiosa cells formed a heavier biofilm compared to those in xylem fluid from the resistant species. Differential expression of selected genes of X. fastidiosa cultured in the xylem fluids of V. vinifera and V. smalliana was analyzed using a DNA macroarray. Compared with xylem fluid of V. smalliana, xylem fluid of V. vinifera stimulated the expression of X. fastidiosa genes involved in virulence regulation, such as rpfC, gacA, xrvA, gcvR, and cysB, and genes involved in biogenesis of pili and twitching motility, such as pilI, pilU, pilE and pilG. Increased expression of virulence genes likely contributes to the expression of PD symptom in the susceptible grapevines, whereas reduced expression of these genes may lead to limitation of symptoms in resistant grapevines.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

PD:

Pierce’s disease

RT-PCR:

Reverse transcription polymerase chain reaction

References

  • Alves, E., Marucci, C. R., Lopes, J. R. S., & Leite, B. (2004). Leaf symptoms on plum, coffee and citrus and the relationship with the extent of xylem vessels colonized by Xylella fastidiosa. Journal of Phytopathology, 152, 291–297.

    Article  Google Scholar 

  • Andersen, P. C. (2002) Biological, cultural, genetic, and chemical control of Pierce’s Disease: xylem fluid chemistry mediation of resistance to Pierce’s Disease. p. 43–44. In: Proceedings of the Pierce’s Disease Research Symposium. California Department of Food and Agriculture, San Diego, CA.

  • Andersen, P. C., Brodbeck, B. V., Oden, S., Shriner, A., & Leite, B. (2007). Influence of xylem fluid chemistry on planktonic growth, biofilm formation and aggregation of Xylella fastidiosa. FEMS Microbiology Letters, 274, 210–217.

    Article  PubMed  CAS  Google Scholar 

  • Basha, S. M., Mazhar, H., & Vasanthaiah, H. K. N. (2010). Proteomics approach to identify unique xylem fluid proteins in Pierce’s disease-tolerant Vitis Species. Applied Biochemistry and Biotechnology, 160, 932–944.

    Article  PubMed  CAS  Google Scholar 

  • Bi, J. L., Dumenyo, C. K., Hernandez-Martinez, R., Cooksey, D. A., & Toscano, N. C. (2007). Effect of host plant xylem fluid on growth, aggregation, and attachment of Xylella fastidiosa. Journal of Chemical Ecology, 33, 493–500.

    Article  PubMed  CAS  Google Scholar 

  • Biles, C. L., & Abeles, F. B. (1991). Xylem sap proteins. Plant Physiology, 96, 597–601.

    Article  PubMed  CAS  Google Scholar 

  • Chatterjee, S., Wistrom, C., & Lindow, S. E. (2008). A cell-cell signaling sensor is required for virulence and insect transmission of Xylella fastidiosa. Proceedings of the National Academy of Sciences of the United States of America, 105, 2670–2675.

    Article  PubMed  CAS  Google Scholar 

  • Clayton, C. N. (1975). Diseases of muscadine and bunch grapes in North Carolina and their control. North Carolina Agricultural Experiment Station Technical Bulletin, 451, 37.

    Google Scholar 

  • Costa, H. S., Raetz, E., Pinlard, T. R., Gispert, C., Hernandez-Martinez, R., Dumenyo, C. K., & Cooksey, D. A. (2004). Plant hosts of Xylella fastidiosa in and near southern California vineyards. Plant Disease, 88, 1255–1261.

    Article  Google Scholar 

  • de Souza, A. A., Takita, M. A., Pereira, E. O., Coletta-Filho, H. D., & Machado, M. A. (2005). Expression of pathogenicity-related genes of Xylella fastidiosa in vitro and in planta. Current Microbiology, 50, 223–228.

    Article  PubMed  Google Scholar 

  • Fritschi, F. B., Lin, H., & Walker, M. A. (2007). Xylella fastidiosa population dynamics in grapevine genotypes differing in susceptibility to Pierce’s disease. American Journal of Enology and Viticulture, 3, 326–332.

    Google Scholar 

  • Fry, S. M., & Milholland, R. D. (1990). Response of resistant, resistance and susceptible grapevine tissue to invasion by the Pierce’s disease bacterium, Xylella fastidiosa. Phytopathology, 80, 66–69.

    Article  Google Scholar 

  • Gray, D. (2003). New plants for Florida: Grape. Circular 1440. In R. L. Jones, M. L. Duryea, & B. J. Treat (Eds.), Florida agricultural experiment station. Gainesville: Institute of Food and Agricultural Sciences, University of Florida.

    Google Scholar 

  • Gusnanto, A., Ploner, A., & Pawitan, Y. (2005). Fold-change estimation of differentially expressed genes using mixture mixed-model. Statistical Applications in Genetics and Molecular Biology, 4, 1145–1149.

    Article  Google Scholar 

  • Hopkins, D. L. (1984). Variability of virulence in grapevine among isolates of Pierce’s disease bacterium. Phytopathology, 74, 1395–1398.

    Article  Google Scholar 

  • Hopkins, D. L., & Purcell, A. H. (2002). Xylella fastidiosa: cause of Pierce’s disease of grapevine and other emerging diseases. Plant Disease, 86, 1056–1066.

    Article  Google Scholar 

  • Leite, B., Andersen, P. C., & Ishida, M. L. (2004). Colony aggregation and biofilm formation in xylem chemistry-based media for Xylella fastidiosa. FEMS Microbiology Letters, 230, 283–290.

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Millan, A. F., Morales, F., Abadia, A., & Abadia, J. (2000). Effects of iron deficiency on the composition of the leaf apoplastic fluid and xylem sap in sugar beet. Implications for iron and carbon transport. Plant Physiololgy, 124, 873–884.

    Article  CAS  Google Scholar 

  • Lu, J., Ren, Z. B., & Cousins, P. (2008). Evaluation of grape rootstocks for resistance to Pierce’s disease and adaptation to north Florida environment. Acta Horticulture, 772, 257–262.

    Google Scholar 

  • Marques, L. L. R., Manfio, G. P., Reid, D. M., Ceri, H., & Olson, M. E. (2001). Xylella fastidiosa are biofilm-forming phytopathogenic bacteria. Phytopathology, 91, S58.

    Google Scholar 

  • Meng, Y., Li, Y., Galvani, C. D., Hao, G., Turner, J. N., Burr, T. J., & Hoch, H. C. (2005). Upstream migration of Xylella fastidiosa via pilusdriven twitching motility. Journal of Bacteriology, 187, 5560–5567.

    Article  PubMed  CAS  Google Scholar 

  • Osiro, D., Colnago, L. A., Otoboni, A. M., Lemos, E. G., de Souza, A. A., Coletta Filho, H. D., & Machado, M. A. (2004). A kinetic model for Xylella fastidiosa adhesion, biofilm formation, and virulence. FEMS Microbiology Letters, 236, 313–318.

    Article  PubMed  CAS  Google Scholar 

  • Redak, R. A., Purcell, A. H., Lopes, J. R. S., Blua, M. J., Mizell, R. F., III, & Andersen, P. C. (2004). The biology of xylem fluid-feeding insect vectors of Xylella fastidiosa and their relation to disease epidemiology. Annual Review of Entomology, 49, 243–270.

    Article  PubMed  CAS  Google Scholar 

  • Shi, X. Y., Dumenyo, C. K., Hernandez-Martinez, R., Azad, H., & Cooksey, D. A. (2007). Characterization of regulatory pathways in Xylella fastidiosa: genes and phenotypes controlled by algU. Applied and Environmental Microbiology, 73, 6748–6756.

    Article  PubMed  CAS  Google Scholar 

  • Shi, X. Y., Dumenyo, C. K., Hernandez-Martinez, R., Azad, H., & Cooksey, D. A. (2009). Characterization of regulatory pathways in Xylella fastidiosa: genes and phenotypes controlled by gacA. Applied and Environmental Microbiology, 75, 2275–2283.

    Article  PubMed  CAS  Google Scholar 

  • Shi, X. Y., Bi, J. L., Morse, J. G., Toscano, N. C., & Cooksey, D. C. (2010). Differential expression of genes of Xylella fastidiosa in xylem fluid of citrus and grapevine. FEMS Microbiology Letters, 304, 82–88.

    Article  PubMed  CAS  Google Scholar 

  • Simpson, A. J., Reinach, F. C., Arruda, P., Abreu, F. A., Acencio, M., Alvarenga, R., Alves, L. M., Araya, J. E., Baia, G. S., Baptista, C. S., Barros, M. H., et al. (2000). The genome sequence of the plant pathogen Xylella fastidiosa. Nature, 406, 151–157.

    Article  PubMed  CAS  Google Scholar 

  • St. Geme, J. W., III, & Cutter, D. (1995). Evidence that surface fibrils expressed by Haemophilus influenzae type b promote attachment to human epithelial cells. Molecular Microbiology, 15, 77–85.

    Article  Google Scholar 

  • Sun, Q., Greve, C. L., & Labavitch, J. M. (2011). Polysaccharide Compositions of Intervessel Pit Membranes Contribute to Pierce’s Disease Resistance of Grapevines. Plant Physiololgy, 155, 1976–1987.

    Article  CAS  Google Scholar 

  • Takiya, D. M., McKamey, S. H., & Cavichioli, R. R. (2006). Validity of Homalodisca and of H. vitripennis as the name for glassy-winged sharpshooter (Hemiptera: Cicadellidae Cicadellinae). Annals of the Entomological Society of America, 99, 648–655.

    Article  Google Scholar 

  • Van Sluys, M. A., de Oliveira, M. C., Monteiro-Vitorello, C. B., Miyaki, C. Y., Furlan, L. R., Camargo, L. E., da Silva, A. C., Moon, D. H., Takita, M. A., Lemos, E. G., Machado, M. A., et al. (2003). Comparative analyses of the complete genome sequences of Pierce’s disease and citrus variegated chlorosis strains of Xylella fastidiosa. Journal of Bacteriology, 185, 1018–1026.

    Article  PubMed  Google Scholar 

  • Wells, J. M., Raju, B. C., Huang, H. Y., Weiburh, W. G., Mandelcopaul, L., & Brennder, D. J. (1987). Xylella fastidiosa gen. nov.: Gram negative, xylem limited fastidious plant bacteria related to Xanthomonas spp. International Journal of Systematic Bacteriology, 36, 136–143.

    Article  Google Scholar 

  • Zaini, P. A., De La Fuente, H. L., Hoch, C., & Burr, T. J. (2009). Grapevine xylem sap enhances biofilm development by Xylella fastidiosa. FEMS Microbiology Letters, 259, 129–134.

    Article  Google Scholar 

Download references

Acknowledgments

We thank Jiue-in Yang for collecting the xylem fluids. This work was supported in part by the University of California’s Pierce’s Disease Research Grants Program via a grant from USDA CSREES, the California Department of Food and Agriculture Pierce’s Disease/Glassy-winged Sharpshooter Board, and the University of California Agricultural Experiment Station.

Author information

Authors and Affiliations

  1. Department of Plant Pathology and Microbiology, University of California Riverside, Riverside, CA, 92521, USA

    Xiangyang Shi & Donald A. Cooksey

  2. University of California Cooperative Extension, Salinas, CA, 93901, USA

    Jianlong Bi

  3. Department of Entomology, University of California Riverside, Riverside, CA, 92521, USA

    Joseph G. Morse & Nick C. Toscano

  4. United States Department of Agriculture-Agricultural Research Service, Crop Disease, Pests and Genetics Research Unit, San Joaquin Valley Agricultural Sciences Center, 9611 South Riverbend Avenue, Parlier, CA, 93648, USA

    Xiangyang Shi

Authors
  1. Xiangyang Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jianlong Bi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joseph G. Morse
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nick C. Toscano
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Donald A. Cooksey
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiangyang Shi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shi, X., Bi, J., Morse, J.G. et al. Effect of xylem fluid from susceptible and resistant grapevines on developmental biology of Xylella fastidiosa . Eur J Plant Pathol 135, 127–135 (2013). https://doi.org/10.1007/s10658-012-0071-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-012-0071-9

Keywords

Search

Navigation