Skip to main content
Log in

Settling and feeding behavior of sharpshooter vectors of Xylella fastidiosa on plum genotypes resistant to leaf scald disease

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

Abstract

Plum leaf scald (PLS) is a serious disease caused by Xylella fastidiosa subsp. multiplex, a pathogenic bacterium transmitted by xylem-sap feeding leafhoppers, commonly named sharpshooters (Hemiptera: Cicadellidae: Cicadellinae). In Brazil, the development of plum genotypes that apparently are not infected under field conditions has opened new perspectives for disease control based on host plant resistance. For example, PLS incidence on ‘SC13’ and ‘SC7’ genotypes is almost null under field conditions, although ‘SC13’ is infected by graft inoculation. Thus, we hypothesized that the performance of these genotypes in the field may be related to vector behavior. To verify this hypothesis, we investigated the settling preference and probing and feeding behavior of the sharpshooters Bucephalogonia xanthophis (Berg) and Sibovia sagata (Signoret) on the PLS-resistant plum genotypes, ‘SC7’ and ‘SC13’, and on the naturally infected cultivar, ‘Laetitia’. In the settling experiments, ‘SC7’ was less preferred by both vector species. For S. sagata held on ‘SC13’, reduced sap ingestion rates were observed. For B. xanthophis, probing and feeding activities differed between individuals held on ‘SC13’ and ‘Laetitia’. Specifically, duration of the stylet pathway phase, duration of xylem sap ingestion events, and number of interruptions of the xylem phase differed for B. xanthophis held on ‘SC13’ and ‘Laetitia’. The results show that the resistant genotypes affected host plant selection by the sharpshooters and highlight the importance of incorporating vector behavior into studies aimed at identifying or developing X. fastidiosa-resistant genotypes.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Almeida, R. P. P., & Nunney, L. (2015). How do plant diseases caused by Xylella fastidiosa emerge? Plant Disease, 99, 1457–1467. https://doi.org/10.1094/PDIS-02-15-0159-FE.

    Article  PubMed  Google Scholar 

  • Almeida, R. P. P., & Purcell, A. H. (2003). Transmission of Xylella fastidiosa to grapevines by Homalodisca coagulata (Hemiptera: Cicadellidae). Journal of Economic Entomology, 2, 264–271.

    Article  Google Scholar 

  • Andersen, P. C., Brodbeck, B. V., & Mizell III, R. F. (1992). Feeding by the leafhopper, Homalodisca coagulata, in relation to xylem fluid chemistry and tension. Journal of Insect Physiology, 38, 611–622. https://doi.org/10.1016/0022-1910(92)90113-R.

    Article  CAS  Google Scholar 

  • Azevedo Filho, W. S., de Tolotti, A., Carvalho, G. S., Muller, C., Botton, M., & Lopes, J. R. S. (2016). Guia ilustrado: Cigarrinhas na cultura da ameixeira. Pelotas: União Sul-América de Estudos da Biodiversidade.

    Google Scholar 

  • Backus, E. A., & Bennett, W. H. (2009). The AC–DC correlation monitor: New EPG design with flexible input resistors to detect both R and emf components for any piercing–sucking hemipteran. Journal of Insect Physiology, 55(10), 869–884.

    Article  CAS  Google Scholar 

  • Backus, E. A., & McLean, D. L. (1985). Behavioral evidence that the precibarial sensilla of leafhoppers are chemosensory and function in host discrimination. Entomologia Experimentalis et Applicata, 37(3), 219–228.

    Article  Google Scholar 

  • Backus, E. A., Cline, A. R., Ellerseick, M. R., & Serrano, M. S. (2007). Lygus Hesperus (Hemiptera: Miridae) feeding on cotton: New methods and parameters for analysis of non-sequential electrical penetration graph data. Annals of the Entomological Society of America, 100, 296–310. https://doi.org/10.1603/0013-8746(2007)100[296:LHHMFO]2.0.CO;2.

    Article  Google Scholar 

  • Brodbeck, B. V., Mizell III, R. F., & Andersen, P. C. (1993). Physiological and behavioral adaptations of three species of leafhoppers in response to the dilute nutrient content of xylem fluid. Journal of Insect Physiology, 39(1), 73–81.

    Article  CAS  Google Scholar 

  • Bullas-Appleton, E. S., Otis, G., Gillard, C., & Schaafsma, A. W. (2004). Varietal preferences in edible beans in relation to visual and olfactory cues. Environmental Entomology, 33, 1381–1388. https://doi.org/10.1603/0046-225X-33.5.1381.

    Article  Google Scholar 

  • Chatterjee, S., Almeida, R. P. P., & Lindow, S. E. (2008). Living in two worlds: The plant and insect lifestyles of Xylella fastidiosa. Annual Review of Phytopathology, 46, 243–271. https://doi.org/10.1146/annurev.phyto.45.062806.094342.

    Article  CAS  PubMed  Google Scholar 

  • Cornara, D., Sicard, A., Zeilinger, A. R., Porcelli, F., Purcell, A. H., & Almeida, R. P. P. (2016). Transmission of Xylella fastidiosa to grapevine by the meadow spittlebug. Phytopathology, 106, 1285–1290.

    Article  CAS  Google Scholar 

  • Cornara, D., Garzo, E., Morente, M., Moreno, A., Alba-Tercedor, J., & Fereres, A. (2018). EPG combined with micro-CT and video recording reveals new insights on the feeding behavior of Philaenus spumarius. PlosOne, 13, e0199154. https://doi.org/10.1371/journal.pone.0199154.

    Article  Google Scholar 

  • Dalbó, M. A., Klabunde, G. H. F., Nodari, R. O., Fernandes, D., & Basso, M. F. (2010). Evolution of the response of segregating populations of plums and the association with microsatellite markers of leaf scald. Crop Breeding and Applied Biotechnology, 10, 337–344. https://doi.org/10.1590/S1984-70332010000400008.

    Article  Google Scholar 

  • Dalbó, M. A., Bruna, E. D., Nodari, R. O., & Saifert, L. (2016). Plum selections with total resistance to leaf scald (Xylella fastidiosa). Acta Horticulturae. https://doi.org/10.17660/ActaHortic.2016.1127.11.

  • Dalbó, M. A., Dela Bruna, E., & Souza, A. L. K. (2018). SCS 438 – Zafira – a new plum cultivar resistant to leaf scald (Xylella fastidiosa). Crop Breeding and Applied Biotechnology, 18, 229–233. https://doi.org/10.1590/1984-70332018v18n2c33.

    Article  Google Scholar 

  • Daugherty, M. P., Bosco, D., & Almeida, R. P. P. (2009). Temperature mediates vector transmission efficiency: Inoculum supply and plant infection dynamics. Annals of Applied Biology, 155(3), 361–369.

    Article  Google Scholar 

  • Daugherty, M. P., Rashed, A., Almeida, R. P. P., & Perring, T. M. (2011). Vector preference for hosts differing in infection status: Sharpshooter movement and Xylella fastidiosa transmission. Ecological Entomology, 36, 654–662. https://doi.org/10.1111/j.1365-2311.2011.01309.x.

    Article  Google Scholar 

  • Eidam, T., Pavanello, A. P., & Ayub, R. A. (2012). Ameixeira no Brasil. Revista Brasileira de Fruticultura, 34. https://doi.org/10.1590/S0100-29452012000100001.

  • Esteves, M. B., Kleina, H. T., Sales, T. M., Oliveira, T. P., De Lara, I. A. R., Almeida, R. P. P., Coletta-Filho, H. D., & Lopes, J. R. S. (2019). Transmission efficiency of Xylella fastidiosa subsp. pauca sequence types by sharpshooter vectors after in vitro acquisition. Phytopathology. https://doi.org/10.1094/PHYTO-07-18-0254-FI.

  • Faostat – Food and Agriculture Organization of the United Nations. (2020) Countries by commodities - imports. http://www.fao.org/faostat/en/#rankings/countries_by_commodity_imports Accessed 03 July 2020.

  • Fereres, A., & Moreno, A. (2009). Behavioral aspects influencing plant virus transmission by homopteran insects. Virus Research, 141, 158–168. https://doi.org/10.1016/j.virusres.2008.10.020.

    Article  CAS  PubMed  Google Scholar 

  • Fereres, A., Kampmeier, G. E., & Irwin, M. E. (1999). Aphid attraction and preference for soybean and pepper plants infected with Potyviridae. Annals of the Entomological Society of America, 92, 542–548. https://doi.org/10.1093/aesa/92.4.542.

    Article  Google Scholar 

  • He, C. X., Li, W. B., Ayres, A. J., Hartung, J. S., Miranda, V. S., & Teixeira, D. C. (2000). Distribution of Xylella fastidiosa in citrus rootstocks and transmission of citrus variegated chlorosis between sweet orange plants through natural root grafts. Plant Disease, 84, 622–626. https://doi.org/10.1094/PDIS.2000.84.6.622.

    Article  CAS  PubMed  Google Scholar 

  • Hopkins, D. L., & Purcell, A. H. (2002). Xylella fastidiosa: Cause of Pierce’s disease of grapevine and other emergent diseases. Plant Disease, 86, 1056–1066. https://doi.org/10.1094/PDIS.2002.86.10.1056.

    Article  CAS  PubMed  Google Scholar 

  • Lara, F. M. (1991). Princípios de resistência de plantas a Insetos. São Paulo: Ícone.

    Google Scholar 

  • Leite, R. M., Leite Junior, R. P., & Ceresini, P. C. (1997). Hospedeiros alternativos de Xylella fastidiosa entre plantas invasoras de pomares de ameixeira com escaldadura da folha. Fitopatologia Brasileira, 22, 54–57.

    Google Scholar 

  • Markheiser, A., Cornara, D., Fereres, A., & Maixner, M. (2019). Analysis of vector behavior as a tool to predict Xylella fastidiosa patterns of spread. Entomologia Generalis, 40, 1–13.

  • Marucci, R. C., Giustolin, T. A., Miranda, M. P., Miquelote, H., Almeida, R. P. P., & Lopes, J. R. S. (2003). Identification of a non-host plant of Xylella fastidiosa to rear healthy sharpshooter vectors. Scientia Agricola, 60, 669–675. https://doi.org/10.1590/S0103-90162003000400010.

    Article  Google Scholar 

  • Marucci, R. C., Lopes, J. R. S., Vendramim, J. D., & Corrente, J. E. (2005). Influence of Xylella fastidiosa infection of citrus on host selection by leafhopper vectors. Entomologia Experimentalis et Applicata, 117, 95–103. https://doi.org/10.1111/j.1570-7458.2005.00336.x.

    Article  Google Scholar 

  • McCullagh, P., John, A., & Nelder, J. A. (1989) Generalized linear models. Chapman & Hall/CRC, 2 ed., 532p.

  • McLean, D. L., & Kinsey, M. G. (1964). A technique for electronically recording of aphid feeding and salivation. Nature, 202, 1358–1359. https://doi.org/10.1038/2021358a0.

    Article  Google Scholar 

  • Miranda, M. P., Fereres, A., Appezzato-da-Glória, B., & Lopes, J. R. S. (2009). Characterization of electrical penetration graphs of Bucephalogonia xanthophis, a vector of Xylella fastidiosa in citrus. Entomologia Experimentalis et Applicata, 130, 35–46. https://doi.org/10.1111/j.1570-7458.2008.00794.x.

    Article  Google Scholar 

  • Mizell, R. F., III, Tipping, C., Andersen, P. C., Brodbeck, B., Hunter, W. B., & Northfield T. (2008). Behavior model for Homalodisca vitripennis (Hemiptera: Cicadellidea): optimization of host plant utilization and management implication. Environmental Entomology 37, 1049–1062.

  • Moral, R. A., Hinde, J., & Demétrio, C. G. B. (2017). Half-normal plots and overdispersed models in R: The hnp package. Journal of Statistical Software. https://doi.org/10.18637/jss.v081.i10.

  • Ojima, M., Rigitano, O., Dall’orto, F. A. C., Scaranari, H. J., Martins, F. P., & Tombolato, A. F. C. (1983). ‘Rosa Mineira’ – Novo cultivar IAC de ameixa pouco exigente de frio. Bragantia, 42(1), 233–238.

    Article  Google Scholar 

  • Purcell, A. H., & Finlay, A. (1979). Evidence for noncirculative transmission of Pierce’s disease bacterium by sharpshooter leafhoppers. Phytopathology, 69, 393. https://doi.org/10.1094/Phyto-69-393.

    Article  Google Scholar 

  • R Core Team (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org. Accessed 25 February 2020.

  • Raju, B. C., Wells, J. M., Nyland, G., Brlansky, R. H., & Lowe, S. K. (1982). Plum leaf scald isolation culture and pathogenicity of the causal agent. Phytopathology, 72, 1460. https://doi.org/10.1094/Phyto-72-1460.

    Article  Google Scholar 

  • Redak, R. A., Purcell, A. H., Lopes, J. R. S., Blua, M. J., Mizell, R. F., & 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. https://doi.org/10.1146/annurev.ento.49.061802.123403.

    Article  CAS  PubMed  Google Scholar 

  • Sandanayaka, W. R. M., & Backus, E. A. (2008). Quantitative comparison of stylet penetration behaviors of glassy winged sharpshooter, Homalodisca vitripennis on selected hosts. Journal of Economic Entomology, 101, 1183–1197.

    Article  CAS  Google Scholar 

  • Sandanayaka, W. R. M., Chhagan, A., & Ramankutty, P. (2007). Host plant testing of the spittle bug Carystoterpa fingens by stylet penetration behaviour. New Zealand Plant Protection, 60, 78–84.

    Article  Google Scholar 

  • Sandanayaka, W. R. M., Jia, Y., & Charles, J. G. (2013). EPG technique as a tool to reveal host plant acceptance by xylem sap-feeding insects. Journal of Applied Entomology, 137(7), 519–529.

    Article  Google Scholar 

  • Sandanayaka, M., Nielsen, M., Davis, V., & Butler, R. (2017). Do spittlebugs feed on grape? Assessing transmission potential for Xylella fastidiosa. New Zealand Plant Protection. https://doi.org/10.30843/nzpp.2017.70.23.

  • Sellers, K., & Shmueli, G. (2010). A flexible regression model for count data. The Annals of Applied Statistics, 4, 943–961. https://doi.org/10.1214/09-AOAS306.

    Article  Google Scholar 

  • Smith, T. R., & Capinera, J. L. (2005). Host preferences and habitat associations of some Florida grasshoppers Orthoptera : Acrididae. Environmental Entomology, 34, 210–224.

    Article  Google Scholar 

  • Tertuliano, M., Srinivasan, R., & Scherm, H. (2012). Settling behavior of the glassy-winged sharpshooter, Homalodisca vitripennis, vector of Xylella fastidiosa, on southern highbush blueberry cultivars. Entomologia Experimentalis et Applicata, 143, 67–73. https://doi.org/10.1111/j.1570-7458.2012.01228.x.

    Article  Google Scholar 

  • Tjallingii, W. F. (1978). Electronic recording of penetration behaviour by aphids. Entomologia Experimentalis et Applicata, 24, 721–730. https://doi.org/10.1111/j.1570-7458.1978.tb02836.x.

    Article  Google Scholar 

  • Tjallingii, W. F. (1993). Host plant acceptance by aphids: An EPG analysis. Bulletin OILB/SROP., 16, 173–177.

    Google Scholar 

  • van Helden, M., & Tjallingii, W. F. (2000). Experimental design and analysis in EPG experiments with emphasis on plant resistance research. In G. P. Walker & E. A. Backus (Eds.), Principles and applications of electronic monitoring and other techniques in the study of homopteran feeding electrical penetration graphs of Diaphorina citri behavior (pp. 144–171). Lanham: Entomological Society of America.

    Google Scholar 

  • Ver Hoef, J. M., & Boveng, P. L. (2007). Quasi-Poisson vs. negative binomial regression: How should we model overdispersed count data? Ecology. https://doi.org/10.1890/07-0043.1.

  • Wells, J. M., Raju, B. C., Hung, H. Y., Weisburg, W. G., Mandelco-Paul, L., & Brenner, D. J. (1987). Xylella fastidiosa gev. nov. sp. nov: Gram-negative, xylem-limited fastidious plant bacteria related to Xanthomonas spp. International Journal of Systematic Bacteriology, 37(2), 136–143.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was financed in part by the ‘Coordenação de Aperfeiçoamento de Pessoal de Nível Superior’ - Brasil (CAPES) - Finance Code 001. The last two authors received research fellowships from National Council for Scientific and Technological Development (CNPq)/Brazil. We extend our thanks for the Science Foundation Ireland (SFI) under grant number SFI/12/RC/2289, co-funded by the European Regional Development Fund.

Funding

This research was funded in part by the ‘Coordenação de Aperfeiçoamento de Pessoal de Nível Superior’ (CAPES) - Finance Code 001. The last author received research fellowships from ‘National Council for Scientific and Technological Development’ (CNPq).

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. The first draft of the manuscript was written by the first author and all coauthors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Heloisa Thomazi Kleina.

Ethics declarations

Disclosure of potential conflicts of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Not applicable

Electronic supplementary material

ESM 1

(DOCX 787 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kleina, H.T., Kudlawiec, K., Esteves, M.B. et al. Settling and feeding behavior of sharpshooter vectors of Xylella fastidiosa on plum genotypes resistant to leaf scald disease. Eur J Plant Pathol 158, 633–644 (2020). https://doi.org/10.1007/s10658-020-02104-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-020-02104-8

Keywords

Navigation