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Sex-specific probing behaviour of the carrot psyllid Bactericera trigonica and its implication in the transmission of ‘Candidatus Liberibacter solanacearum’

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Abstract

‘Candidatus Liberibacter solanacearum (Lso)’ is a pathogen of Solanaceae but also causes serious physiological disorders in carrots and celery (Apiaceae). In carrots, this pathogen is transmitted by the psyllids Bactericera trigonica and Trioza apicalis. How vector sex influences Lso transmission has not been yet elucidated. Here we report the probing behaviours of male and female B. trigonica and their impact on Lso titre transmitted, percentage of transmission, and symptoms produced on carrots when Lso is transmitted by males or females of B. trigonica. Vector sex affected the inoculation of Lso; our results suggest that females might inoculate higher Lso titres than males. However, the percentage of transmission was not affected by vector sex at a density of one or eight psyllids per plant. The number of yellow leaves and root weight were not different when Lso was transmitted by males or females at either of the psyllid densities tested, except for groups of females whose Lso transmission resulted in a higher number of yellow leaves than did Lso transmitted by groups of males. Electrical penetration graphs (EPG) showed that the proportion of individuals who reached phloem tissues was similar for males and females. However, EPGs also showed that females probed more times, ingested longer from phloem sieve elements and reached phloem tissues more frequently than did males during an 8-h inoculation access period (IAP). Our study shows that differences in probing behaviours between males and females of B. trigonica could modulate how Lso is inoculated by psyllids. These results highlight the importance of taking sex into consideration in psyllid studies of probing behaviour and bacterial transmission.

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References

  • Abad, J. A., Bandla, M., French-Monar, R. D., Liefting, L. W., & Clover, G. R. G. (2009). First report of the detection of ‘Candidatus Liberibacter’ species in zebra chip disease-infected potato plants in the United States. Plant Disease, 93, 108.

    Article  Google Scholar 

  • Alfaro-Fernandez, A., Silveiro, F., Cebrian, M. C., Villaescua, M. J., & Font, M. I. (2012). ‘Candidatus Liberibacter solanacearum’ associated with Bactericera trigonica-affected carrots in the Canary Islands. Plant Disease, 96, 581.

    Article  Google Scholar 

  • Alvarado, V. Y., Odokonyero, D., Duncan, O., Mirkov, T. E., & Scholthof, H. B. (2012). Molecular and physiological properties associated with zebra complex disease in potatoes and its relation with Candidatus Liberibacter contents in psyllid vectors. PloS One, 7, e37345.

    Article  CAS  PubMed  PubMed Central  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 nonsequential electrical penetration graph data. Annals of the Entomological Society of America, 100, 296–310.

    Article  Google Scholar 

  • Bertolini, E., Felipe, R. T. A., Sauer, A. V., Lopes, S. A., Arilla, A., Vidal, E., Mourão Filho, F. A. A., Nunes, W. M. C., Bové, J. M., López, M. M., & Cambra, M. (2014). Tissue-print and squash real-time polymerase chain reaction for direct detection of 'Candidatus Liberibacter' species in citrus plants and psyllid vectors. Plant Pathology, 63, 1149–1158.

    Article  CAS  Google Scholar 

  • Bertolini, E., Teresani, G. R., Loiseau, M., Tanaka, F. A. O., Barbé, S., Martínez, C., Gentit, P., Lopez, M. M., & Cambra, M. (2015). Transmission of ‘Candidatus Liberibacter solanacearum’ in carrot seeds. Plant Pathology, 64, 276–285.

    Article  CAS  Google Scholar 

  • Bonani, J. P., Fereres, A., Garzo, E., Miranda, M. P., Appezzato-Da-Gloria, B., & Lopes, J. R. S. (2010). Characterization of electrical penetration graphs of the Asian citrus psyllid, Diaphorina citri, in sweet orange seedlings. Entomologia Experimentalis et Applicata, 134, 35–49.

    Article  Google Scholar 

  • Cicero, J. M., Fisher, T. W., & Brown, J. K. (2016). Localization of Candidatus Liberibacter solanacearum and evidence of surface appendages in the potato psyllid vector. Phytopathology. doi:10.1094/PHYTO-04-15-0088-R.

    Google Scholar 

  • Civolani, S., Leis, M., Grandi, G., Garzo, E., Pasqualini, E., Musacchi, S., Chicca, M., Castaldelli, G., Rossi, R., & Tjallingii, F. W. (2011). Stylet penetration of Cacopsylla pyri; an electrical penetration graph (EPG) study. Journal of Insect Physiology, 57, 1407–1419.

    Article  CAS  PubMed  Google Scholar 

  • Cooper, W. R., Sengoda, V. G., & Munyaneza, J. E. (2014). Localization of ‘Candidatus Liberibacter solanacearum' (Rhizobiales: Rhizobiaceae) in Bactericera cockerelli (Hemiptera: Triozidae). Annals of the Entomological Society of America, 107, 204–210.

    Article  Google Scholar 

  • Gharaei, A. M., Ziaaddini, M., Jalali, M. A., & Michaud, J. P. (2014). Sex-specific responses of the Asian citrus psyllid to volatiles of conspecific and host-plant origin. Journal of Applied Entomology, 138, 500–509.

    Article  Google Scholar 

  • IBM Corp (2012). IBM SPSS Statistics for Windows, Version 21.0. Armonk, NY: IBM Corp.

    Google Scholar 

  • Jiang, Y. X., de Blas, C., Barrios, L., & Fereres, A. (2000). Correlation between whitefly (Homoptera: Aleyrodidae) feeding behavior and transmission of Tomato yellow leafcurl virus. Annals of the Entomological Society of America, 93, 573–579.

    Article  Google Scholar 

  • Liefting, L. W., Perez-Egusquiza, Z. C., Clover, G. R. G., & Anderson, J. A. D. (2008a). A new ‘Candidatus Liberibacter’ species in Solanum tuberosum in New Zealand. Plant Disease, 92, 1474.

    Article  Google Scholar 

  • Liefting, L. W., Ward, L. I., Shiller, J. B., & Clover, G. R. G. (2008b). A new ‘Candidatus Liberibacter’ species in Solanum betaceum (tamarillo) and Physalis peruviana (cape gooseberry) in New Zealand. Plant Disease, 92, 1588.

    Article  Google Scholar 

  • Liefting, L. W., Sutherland, P. W., Ward, L. I., Paice, K. L., Weir, B. S., & Clover, G. R. G. (2009). A new “Candidatus Liberibacter” species associated with diseases of solanaceous crops. Plant Disease, 93, 208–214.

    Article  CAS  Google Scholar 

  • Loiseau, M., Garnier, S., Boirin, V., Merieau, M., Leguay, A., Renaudin, I., Renvoisé, J. P., & Gentit, P. (2014). First Report of ‘Candidatus Liberibacter solanacearum’ in carrot in France. Plant Disease, 98, 839.

    Article  Google Scholar 

  • Martini, X., Hoffmann, M., Coy, M. R., Stelinski, L. L., & Pelz-Stelinski, K. S. (2015). Infection of an insect vector with a bacterial plant pathogen increases its propensity for dispersal. PloS One, 10, e0129373.

    Article  PubMed  PubMed Central  Google Scholar 

  • Moreno-Delafuente, A., Garzo, E., Moreno, A., & Fereres, A. (2013). A plant virus manipulates the behavior of its whitefly vector to enhance its transmission efficiency and spread. PloS One, 8, e61543.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munyaneza, JE., Crosslin, J. M., Upton, J. E. (2007). Association of Bactericera cockerelli (Homoptera: Psyllidae) with “zebra chip”, a new potato disease in southwestern United States and Mexico. Journal of Economic Entomology, 100, 656–663.

  • Munyaneza, J. E. (2012). Zebra chip disease of potato: biology, epidemiology, and management. American Journal of Potato Research, 89, 329–350.

    Article  Google Scholar 

  • Munyaneza, J. E. (2015). A. zebra Chip disease, Candidatus Liberibacter, and potato psyllid: a global threat to the potato industry. American Journal of Potato Research, 92, 230–235.

    Article  Google Scholar 

  • Munyaneza, J. E., Fisher, T. W., Sengoda, V. G., & Garczynski, S. F. (2010a). First report of “Candidatus Liberibacter solanacearum” associated with psyllid-affected carrots in Europe. Plant Disease, 94, 639.

    Article  Google Scholar 

  • Munyaneza, J. E., Fisher, T. W., Venkatesan, G., Sengoda, S. F., Garczynski, S. F., Nissinen, A., & Lemmetty, A. (2010b). Association of “Candidatus Liberibacter solanacearum” with the psyllid, Trioza apicalis (Hemiptera: Triozidae) in Europe. Journal of Economic Entomology, 103, 1060–1070.

    Article  CAS  PubMed  Google Scholar 

  • Munyaneza, J. E., Swisher, K. D., Buck, H., & Meadow, R. (2015b). First report of Candidatus Liberibacter solanacearum associated with psyllid infested carrots in Germany. Plant Disease, 99, 1269.

    Article  Google Scholar 

  • Murray, M. G., & Thompson, W. F. (1980). Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research, 8, 4321–4325.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mustafa, T., Horton, D. R., Cooper, W. R., Swisher, K. D., Zack, R. S., & Pappu, H. R. (2015). Use of electrical penetration graph technology to examine transmission of ‘Candidatus Liberibacter solanacearum’ to potato by three haplotypes of potato psyllid (Bactericera cockerelli; Hemiptera: Triozidae). PloS One, 10, e0138946.

    Article  PubMed  PubMed Central  Google Scholar 

  • Narayana, Y. D., & Muniyappa, V. (1996). Virus-vector relationships of a planthopper (Peregrinus maidis)-borne sorghum stripe tenuivirus. Internatianal Journal Pest Management, 42, 165–170.

    Article  Google Scholar 

  • Ning, W., Shi, X., Liu, B., Pan, H., Wei, W., Zeng, Y., Sun, X., Xie, W., Wang, S., Wu, Q., Cheng, J., Peng, Z., Zhang, Y (2015). Transmission of Tomato Yellow Leaf Curl Virus by Bemisia tabaci as affected by whitefly sex and biotype. Scientific Reports, 5, doi:10.1038/srep10744.

  • Nissinen, A., Vanhala, P., Holopainen, J. K., & Tiilikkala, K. (2007). Short feeding period of carrot psyllid (Trioza Apicalis) females at early growth stages of carrot reduces yield and causes leaf discolouration. Entomologia Experimentalis et Applicata, 125, 277–283.

    Article  Google Scholar 

  • Nissinen, A., Lemmetty, A., Pihlava, J. M., Jauhiainen, L., Munyaneza, J. E., & Vanhala, P. (2012). Effects of carrot psyllid (Trioza apicalis) feeding on carrot yield and content of sugars and phenolic compounds. Annals of Applied Biology, 161, 68–80.

    Article  Google Scholar 

  • Nissinen, A., Haapalainen, M., Jauhiainen, L., Lindman, M., & Pirhonen, M. (2014). Different symptoms in carrots caused by male and female carrot psyllid feeding and infection by ‘Candidatus Liberibacter solanacearum’. Plant Pathology, 63, 812–820.

    Article  Google Scholar 

  • Olmos, A., Dasi, M. A., Candresse, T., & Cambra, M. (1996). Print-capture PCR: a simple and highly sensitive method for the detection of plum pox virus (PPV) in plant tissues. Nucleic Acids Research, 24, 2192–2193.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pearson, C. C., Backus, E. A., Shugart, H. J., & Munyaneza, J. E. (2014). Characterization and correlation of EPG waveforms of Bactericera cockerelli (Hemiptera: Triozidae): variability in waveform appearance in relation to applied signal. Annals of the Entomological Society of America, 107, 650–666.

    Article  Google Scholar 

  • Rashed, A., Nash, T. D., Paetzold, L., Workneh, F., & Rush, C. M. (2012). Transmission efficiency of 'Candidatus Liberibacter solanacearum' and potato zebra chip disease progress in relation to pathogen titer, vector numbers, and feeding sites. Phytopathology, 102, 1079–1085.

    Article  CAS  PubMed  Google Scholar 

  • Sandanayaka, W. R., Moreno, A., Tooman, N. K., Page-Weir, N. E., & Fereres, A. (2014). Stylet penetration activities linked to the acquisition and inoculation of Candidatus Liberibacter solanacearum by its vector tomato potato psyllid. Entomologia Experimentalis et Applicata, 151, 170–181.

    Article  CAS  Google Scholar 

  • Sarria, E., Cid, M., Garzo, E., & Fereres, A. (2009). Excel workbook for automatic parameter calculation of EPG data. Computers and Electronics in Agriculture, 67, 35–42.

    Article  Google Scholar 

  • Secor, G. A., Rivera-Varas, V., Abad, J. A., Lee, I. M., Clover, G. R. G, Liefting, L. W., Li, X., De Boer, S. H. (2009). Association of ‘Candidatus Liberibacter solanacearum’ with zebra chip disease of potato established by graft and psyllid transmission, electron microscopy, and PCR. Plant Disease, 93, 574–583.

  • Sengoda, V. G., Cooper, W. R., Swisher, K. D., Henne, D. C., & Munyaneza, J. E. (2014). Latent period and transmission of "Candidatus Liberibacter solanacearum" by the potato psyllid Bactericera cockerelli (Hemiptera: Triozidae). PloS One, 9, e93475.

    Article  PubMed  PubMed Central  Google Scholar 

  • Serikawa, R. H (2011). Electrical penetration graphs investigations of Asian citrus psyllid (Diaphorina citri Kuwayama) feeding behaviour: Effects of insecticides on the potential transmission of Candidatus Liberibacter solanacearum. Florida, United States of America: University of Florida, PhD Thesis.

  • Swenson, K. G. (1971). Relation of age, sex, and mating of Macrosteles faaeifrona to transmission of aster yellows. Phytopathology, 61, 657–659.

    Article  Google Scholar 

  • Tahzima, R., Maes, M., Achbanni, E. H., Swicher, K. D., Munyaneza, J. E., & De Jonghe, K. (2014). First report of ‘Candidatus Liberibacter solanacearum’ on carrot in Africa. Plant Disease, 981, 1426.

    Article  Google Scholar 

  • Teresani, G. R., Bertolini, E., Alfaro-Fernandez, A., Martinez, C., Tanaka, F. A., Kitajima, E. W., Roselló, M., Sanjuán, S., Ferrándiz, J. C., Lopez, M. M., Cambra, M., & Font, M. I. (2014). Association of 'Candidatus Liberibacter solanacearum' with a vegetative disorder of celery in Spain and development of a real-time PCR method for its detection. Phytopathology, 104, 804–811.

    CAS  PubMed  Google Scholar 

  • Tjallingii, W. F. (1985). Electrical nature of recorded signals during stylet penetration by aphids. Entomologia Experimentalis et Applicata, 38, 177–186.

    Article  Google Scholar 

  • Van de Wetering, F., Van der Hoek, M., Goldbach, R., & Peters, D. (1999). Differences in tomato spotted wilt virus vector competency between males and females of Frankliniella occidentalis. Entomologia Experimentalis et Applicata, 93, 105–112.

    Article  Google Scholar 

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Acknowledgments

We thank Dr. Estrella Hernandez from the Instituto Canario de Investigaciones Agrarias (ICIA) for providing the infected B. trigonica colony used and Laura Barrios (Consejo Superior de Investigaciones Científicas) for her advices in data analysis. We also thank Dr. Edson Bertolini and Dr. Mariano Cambra from the Instituto Valenciano de Investigaciones Agrarias (IVIA), who kindly provided the Lso cDNA to establish the standard curve for the QRT-PCR assay. This work has received funding from the European Union’s Horizon 2020 research and innovation programme under the grant agreement No 635646, POnTE (Pest Organisms Threatening Europe), from the National Institute for Agronomic Research (INIA) (E-RTA2014-00008-C04-04) and from the Secretary of State of Research of the Spanish Ministry of Science and Innovation AGL2013-47603-C2-2-R. The first author is a recipient of a PhD scholarship from the Departamento Administrativo de Ciencia, Tecnología e Inovación (Colciencias) from Colombia.

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  1. Instituto de Ciencias Agrarias (ICA), Consejo Superior de Investigaciones Científicas (CSIC), Calle Serrano 115 dpdo, 28006, Madrid, Spain

    C.A. Antolínez, A. Fereres & A. Moreno

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  1. C.A. Antolínez
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Antolínez, C., Fereres, A. & Moreno, A. Sex-specific probing behaviour of the carrot psyllid Bactericera trigonica and its implication in the transmission of ‘Candidatus Liberibacter solanacearum’. Eur J Plant Pathol 147, 627–637 (2017). https://doi.org/10.1007/s10658-016-1031-6

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