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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Lara, F. M. (1991). Princípios de resistência de plantas a Insetos. São Paulo: Ícone.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Smith, T. R., & Capinera, J. L. (2005). Host preferences and habitat associations of some Florida grasshoppers Orthoptera : Acrididae. Environmental Entomology, 34, 210–224.
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.
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.
Tjallingii, W. F. (1993). Host plant acceptance by aphids: An EPG analysis. Bulletin OILB/SROP., 16, 173–177.
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.
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.
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
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
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
About this article
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
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-020-02104-8