MPMI PhytoFrontiers Phytobiomes all journals
RESEARCH

Candidatus Liberibacter solanacearum’ Infection of Physalis ixocarpa Brot. (Solanales: Solanaceae) in Saltillo, Mexico

    Affiliations
    Authors and Affiliations
    • Cesar A. Reyes-Corral1 2
    • W. Rodney Cooper2
    • Alexander V. Karasev1
    • Carolina Delgado-Luna3
    • Sergio R. Sanchez-Peña3
    1. 1Department of Entomology, Plant Pathology and Nematology, University of Idaho, Moscow, ID 83844, U.S.A.
    2. 2United States Department of Agriculture–Agricultural Research Service, Temperate Tree Fruit and Vegetable Research Unit, Wapato, WA 98951, U.S.A.
    3. 3Departamento de Parasitología, Universidad Autónoma Agraria Antonio Narro, Saltillo, Coahuila, 25315 Mexico

    Published Online:https://doi.org/10.1094/PDIS-10-20-2240-RE

    The potato psyllid Bactericera cockerelli (Šulc) (Hemiptera: Triozidae) is a pest of solanaceous crops (order Solanales), including potato (Solanum tuberosum L.) and tomato (S. lycopersicum L.). Feeding by high populations of nymphs causes psyllid yellows while adults and nymphs are vectors of the plant pathogen ‘Candidatus Liberibacter solanacearum’. Foliar symptoms that were consistent with either ‘Ca. L. solanacearum’ infection or psyllid yellows were observed in 2019 on tomatillo (Physalis ixocarpa Brot.; family Solanaceae) grown within an experimental plot located near Saltillo, Mexico. This study had three primary objectives: 9i) determine whether the foliar symptoms observed on tomatillo were associated with ‘Ca. L. solanacearum’ infection, (ii) identify the haplotypes of ‘Ca. L. solanacearum’ and potato psyllids present in the symptomatic plot, and (iii) use gut content analysis to infer the plant sources of ‘Ca. L. solanacearum’-infected psyllids. Results confirmed that 71% of symptomatic plants and 71% of psyllids collected from the plants were infected with ‘Ca. L. solanacearum’. The detection of ‘Ca. L. solanacearum’ in plants and psyllids and the lack of nymphal populations associated with psyllid yellows strongly suggests that the observed foliar symptoms were caused by ‘Ca. L. solanacearum’ infection. All infected plants and insects harbored the more virulent ‘Ca. L. solanacearum’ haplotype B but one psyllid was also coinfected with haplotype A. The potato psyllids were predominantly of the central haplotype but one psyllid was identified as the western haplotype. Molecular gut content analysis of psyllids confirmed the movement of psyllids between noncrop habitats and tomatillo and indicated that ‘Ca. L. solanacearum’ infection of psyllids was associated with increased plant diversity in their diet.

    Literature Cited

    • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410. https://doi.org/10.1016/S0022-2836(05)80360-2 Crossref, ISIGoogle Scholar
    • Buchman, J. L., Heilman, B. E., and Munyaneza, J. E. 2011. Effects of Liberibacter-infective Bactericera cockerelli (Hemiptera: Triozidae) density on zebra chip potato disease incidence, potato yield, and tuber processing quality. J. Econ. Entomol. 104:1783-1792. https://doi.org/10.1603/EC11146 Crossref, ISIGoogle Scholar
    • Burckhardt, D., Ouvrard, D., Queiroz, D., and Percy, D. 2014. Psyllid host-plants (Hemiptera: Psylloidea): Resolving a semantic problem. Fla. Entomol. 97:242-246. https://doi.org/10.1653/024.097.0132 Crossref, ISIGoogle Scholar
    • Castillo-Carrillo, C., Fu, Z., and Burckhardt, D. 2019. First record of the tomato potato psyllid Bactericera cockerelli from South America. Bull. Insectol. 72:85-91. ISIGoogle Scholar
    • Chapman, R. I., Macias-Velasco, J. F., Arp, A. P., and Bextine, B. R. 2012. Using quantitative real time PCR melt curve analysis of partial co1 sequence for rapid biotype differentiation of Bactericera cockerelli (Hemiptera: Triozidae). Southwest. Entomol. 37:475-484. https://doi.org/10.3958/059.037.0405 Crossref, ISIGoogle Scholar
    • Chen, S. L., Yao, H., Han, J. P., Liu, C., Song, J. Y., Shi, L. C., Zhu, Y. J., Ma, X. Y., Gao, T., Pang, X. H., Luo, K., Li, Y., Li, X. W., Jia, X. C., Lin, Y. L., and Leon, C. 2010. Validation of the ITS2 region as a novel DNA barcode for identifying medicinal plant species. PLoS One 5:e8613. https://doi.org/10.1371/journal.pone.0008613 Crossref, ISIGoogle Scholar
    • Contreras-Rendón, A., Sánchez-Pale, J. R., Fuentes-Aragón, D., Alanís-Martínez, I., and Silva-Rojas, H. V. 2020. Conventional and qPCR reveals the presence of ‘Candidatus Liberibacter solanacearum’ haplotypes A, and B in Physalis philadelphica plant, seed, and Bactericera cockerelli psyllids, with the assignment of a new haplotype H in Convolvulaceae. Antonie Leeuwenhoek 113:533-551. https://doi.org/10.1007/s10482-019-01362-9 Crossref, ISIGoogle Scholar
    • Cooper, W. R., Horton, D. R., Miliczky, E., Wohleb, C. H., and Waters, T. D. 2019a. The weed link in zebra chip epidemiology: Suitability of non-crop Solanaceae and Convolvulaceae to potato psyllid and “Candidatus Liberibacter solanacearum”. Am. J. Potato Res. 96:262-271. https://doi.org/10.1007/s12230-019-09712-z Crossref, ISIGoogle Scholar
    • Cooper, W. R., Horton, D. R., Miliczky, E., Wohleb, C. H., and Waters, T. D. 2019b. The weed link in zebra chip epidemiology. Potato Prog. XIX:1-7. Google Scholar
    • Cooper, W. R., Horton, D. R., Unruh, T. R., and Garczynski, S. F. 2016. Gut content analysis of a phloem-feeding insect, Bactericera cockerelli (Hemiptera: Triozidae). Environ. Entomol. 45:938-944. https://doi.org/10.1093/ee/nvw060 Crossref, ISIGoogle Scholar
    • Cooper, W. R., Horton, D. R., Wildung, M. R., Jensen, A. S., Thinakaran, J., Rendon, D., Nottingham, L. B., Beers, E. H., Wohleb, C. H., Hall, D. G., and Stelinski, L. L. 2019c. Host and non-host ‘whistle stops’ for psyllids: Molecular gut content analysis by high-throughput sequencing reveals landscape-level movements of Psylloidea (Hemiptera). Environ. Entomol. 48:554-566. https://doi.org/10.1093/ee/nvz038 Crossref, ISIGoogle Scholar
    • Cooper, W. R., Swisher, K. D., Garczynski, S. F., Mustafa, T., Munyaneza, J. E., and Horton, D. R. 2015. Wolbachia infection differs among divergent mitochondrial haplotypes of Bactericera cockerelli (Hemiptera: Triozidae). Ann. Entomol. Soc. Am. 108:137-145. https://doi.org/10.1093/aesa/sau048 Crossref, ISIGoogle Scholar
    • Crosslin, J. M., Lin, H., and Munyaneza, J. E. 2011. Detection of ‘Candidatus Liberibacter solanacearum’ in the potato psyllid, Bactericera cockerelli (Sulc), by conventional and real-time PCR. Southwest. Entomol. 36:125-135. https://doi.org/10.3958/059.036.0202 Crossref, ISIGoogle Scholar
    • Crosslin, J. M., and Munyaneza, J. E. 2009. Evidence that the zebra chip disease and the putative causal agent can be maintained in potatoes by grafting and in vitro. Am. J. Potato Res. 86:183-187. https://doi.org/10.1007/s12230-009-9070-6 Crossref, ISIGoogle Scholar
    • Dahan, J., Wenninger, E. J., Thompson, B. D., Eid, S., Olsen, N., and Karasev, A. V. 2019. Prevalence of ‘Candidatus Liberibacter solanacearum’ Haplotypes in potato tubers and psyllid vectors in Idaho From 2012 to 2018. Plant Dis. 103:2587-2591. https://doi.org/10.1094/PDIS-11-18-2113-RE Link, ISIGoogle Scholar
    • Hansen, A. K., Trumble, J. T., Stouthamer, R., and Paine, T. D. 2008. A new huanglongbing species, ‘Candidatus Liberibacter psyllaurous’, found to infect tomato and potato, is vectored by the psyllid Bactericera cockerelli (Sulc). Appl. Environ. Microbiol. 74:5862-5865. https://doi.org/10.1128/AEM.01268-08 Crossref, ISIGoogle Scholar
    • Harrison, K., Tamborindeguy, C., Scheuring, D. C., Mendoza-Herrera, A., Silva, A., Badillo-Vargas, I. E., Miller, J. C., and Levy, J. G. 2019. Differences in zebra chip severity between ‘Candidatus Liberibacter solanacearum’ haplotypes in Texas. Am. J. Potato Res. 96:86-93. https://doi.org/10.1007/s12230-018-9692-7 Crossref, ISIGoogle Scholar
    • Horton, D. R., Cooper, W. R., Munyaneza, J., and Swisher, K. D. 2015a. Non-potato host plants of potato psyllid in the Pacific Northwest: A year-round complication. Potato Prog. XV:1-5. Google Scholar
    • Horton, D. R., Cooper, W. R., Munyaneza, J. E., Swisher, K. D., Echegaray, E. R., Murphy, A. F., Rondon, S. I., Wohleb, C. H., Waters, T. D., and Jensen, A. S. 2015b. A new problem and old questions: Potato psyllid in the Pacific Northwest. Am. Entomol. (Lanham Md.) 61:234-244. https://doi.org/10.1093/ae/tmv047 CrossrefGoogle Scholar
    • Horton, D. R., Miliczky, E., Munyaneza, J. E., Swisher, K. D., and Jensen, A. S. 2014. Absence of photoperiod effects on mating and ovarian maturation by three haplotypes of potato psyllid, Bactericera cockerelli (Hemiptera: Triozidae). J. Entomol. Soc. B.C. 111:1-12. Google Scholar
    • Jagoueix, S., Bove, J. M., and Garnier, M. 1996. PCR detection of the two ‘Candidatus’ liberobacter species associated with greening disease of citrus. Mol. Cell. Probes 10:43-50. https://doi.org/10.1006/mcpr.1996.0006 Crossref, ISIGoogle Scholar
    • Kaur, N., Cooper, W. R., Duringer, J. M., Badillo-Vargas, I. E., Esparza-Díaz, G., Rashed, A., and Horton, D. R. 2018. Survival and development of potato psyllid (Hemiptera: Triozidae) on Convolvulaceae: Effects of a plant-fungus symbiosis (Periglandula). PLoS One 13:e0201506. https://doi.org/10.1371/journal.pone.0201506 Crossref, ISIGoogle Scholar
    • Knapp, S. 2013. A revision of the Dulcamaroid clade of Solanum L. (Solanaceae). PhytoKeys 22:1-428. https://doi.org/10.3897/phytokeys.22.4041 Crossref, ISIGoogle Scholar
    • Knowlton, G. F., and Thomas, W. L. 1934. Host plants of potato psyllid. J. Econ. Entomol. 27:547. CrossrefGoogle Scholar
    • Levy, J., Ravindran, A., Gross, D., Tamborindeguy, C., and Pierson, E. 2011. Translocation of ‘Candidatus Liberibacter solanacearum’, the zebra chip pathogen, in potato and tomato. Phytopathology 101:1285-1291. https://doi.org/10.1094/PHYTO-04-11-0121 Link, ISIGoogle Scholar
    • Li, W. B., Abad, J. A., French-Monar, R. D., Rascoe, J., Wen, A. M., Gudmestad, N. C., Secor, G. A., Lee, I. M., Duan, Y. P., and Levy, L. 2009. Multiplex real-time PCR for detection, identification and quantification of ‘Candidatus Liberibacter solanacearum’ in potato plants with zebra chip. J. Microbiol. Methods 78:59-65. https://doi.org/10.1016/j.mimet.2009.04.009 Crossref, ISIGoogle Scholar
    • Liefting, L. W., Sutherland, P. W., Ward, L. I., Paice, K. L., Weir, B. S., and Clover, G. R. G. 2009. A new ‘Candidatus Liberibacter’ species associated with diseases of solanaceous crops. Plant Dis. 93:208-214. https://doi.org/10.1094/PDIS-93-3-0208 Link, ISIGoogle Scholar
    • Lin, H., Islam, M. S., Bai, Y., Wen, A., Lan, S., Gudmestad, N. C., and Civerolo, E. L. 2012. Genetic diversity of “Candidatus Liberibacter solanacearum” strains in the United States and Mexico revealed by simple sequence repeat markers. Eur. J. Plant Pathol. 132:297-308. https://doi.org/10.1007/s10658-011-9874-3 Crossref, ISIGoogle Scholar
    • Liu, D., Trumble, J. T., and Stouthamer, R. 2006. Genetic differentiation between eastern populations and recent introductions of potato psyllid (Bactericera cockerelli) into western North America. Entomol. Exp. Appl. 118:177-183. https://doi.org/10.1111/j.1570-7458.2006.00383.x Crossref, ISIGoogle Scholar
    • Mauck, K. E., Sun, P., Meduri, V., and Hansen, A. K. 2019. New Ca. Liberibacter psyllaurous haplotype resurrected from a 49-year-old specimen of Solanum umbelliferum: A native host of the psyllid vector. Sci. Rep. 9:9530. https://doi.org/10.1038/s41598-019-45975-6 Crossref, ISIGoogle Scholar
    • Mendoza-Herrera, A., Levy, J., Harrison, K., Yao, J., Ibanez, F., and Tamborindeguy, C. 2018. Infection by ‘Candidatus Liberibacter solanacearum’ haplotypes A and B in Solanum lycopersicum ‘Moneymaker’. Plant Dis. 102:2009-2015. https://doi.org/10.1094/PDIS-12-17-1982-RE Link, ISIGoogle Scholar
    • Munyaneza, J. E. 2012. Zebra chip disease of potato: Biology, epidemiology, and management. Am. J. Potato Res. 89:329-350. https://doi.org/10.1007/s12230-012-9262-3 Crossref, ISIGoogle Scholar
    • Munyaneza, J. E., Crosslin, J. M., and Upton, J. E. 2007. Association of Bactericera cockerelli (Homoptera: Psyllidae) with “zebra chip,” a new potato disease in southwestern United States and Mexico. J. Econ. Entomol. 100:656-663. Crossref, ISIGoogle Scholar
    • Munyaneza, J. E., Fisher, T. W., Sengoda, V. G., Garczynski, S. F., Nissinen, A., and Lemmetty, A. 2010. Association of ‘Candidatus Liberibacter solanacearum’ with the psyllid, Trioza apicalis (Hemiptera: Triozidae) in Europe. J. Econ. Entomol. 103:1060-1070. https://doi.org/10.1603/EC10027 Crossref, ISIGoogle Scholar
    • Mustafa, T., Horton, D. R., Cooper, W. R., Swisher, K. D., Zack, R. S., and Munyaneza, J. E. 2015a. Interhaplotype fertility and effects of host plant on reproductive traits of three haplotypes of Bactericera cockerelli (Hemiptera: Triozidae). Environ. Entomol. 44:300-308. https://doi.org/10.1093/ee/nvu029 Crossref, ISIGoogle Scholar
    • Mustafa, T., Horton, D. R., Cooper, W. R., Swisher, K. D., Zack, R. S., Pappu, H. R., and Munyaneza, J. E. 2015b. 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. https://doi.org/10.1371/journal.pone.0138946 Crossref, ISIGoogle Scholar
    • Mustafa, T., Horton, D. R., Swisher, K. D., Zack, R. S., and Munyaneza, J. E. 2015c. Effects of host plant on development and body size of three haplotypes of Bactericera cockerelli (Hemiptera: Triozidae). Environ. Entomol. 44:593-600. https://doi.org/10.1093/ee/nvv018 Crossref, ISIGoogle Scholar
    • Nelson, W. R., Fisher, T. W., and Munyaneza, J. E. 2011. Haplotypes of “Candidatus Liberibacter solanacearum” suggest long-standing separation. Eur. J. Plant Pathol. 130:5-12. https://doi.org/10.1007/s10658-010-9737-3 Crossref, ISIGoogle Scholar
    • Reyes Corral, C. A., Cooper, W. R., Horton, D. R., and Karasev, A. V. 2020. Susceptibility of Physalis longifolia (Solanales: Solanaceae) to Bactericera cockerelli (Hemiptera: Triozidae) and ‘Candidatus Liberibacter solanacearum’. J. Econ. Entomol. 113:2595-2603. https://doi.org/10.1093/jee/toaa210 Crossref, ISIGoogle Scholar
    • Rojas-Martinez, R. I., Camacho-Tapia, M., Zavaleta-Mejia, E., and Levy, J. 2016. First report of the presence of haplotypes A and B of Candidatus Liberibacter solanacearum in chili (Capsicum annuum L.) in the central region of Mexico. J. Plant Pathol. 98:111-115. ISIGoogle Scholar
    • Sengoda, V. G., Cooper, W. R., Swisher, K. D., Henne, D. C., and Munyaneza, J. E. 2014. Latent period and transmission of ‘Candidatus Liberibacter solanacearum’ by the potato psyllid Bactericera cockerelli (Hemiptera: Triozidae). PLoS One 9:e93475. https://doi.org/10.1371/journal.pone.0093475 Crossref, ISIGoogle Scholar
    • Silva-Rojas, H., Contreras-Rendón, A., and Sanchez-Pale, J. 2016. Candidatus Liberibacter solanacearum associated to Physalis philadelphica, a new solanaceous host. (Abstr.) Phytopathology 106:100. ISIGoogle Scholar
    • Swisher, K. D., Arp, A. P., Bextine, B. R., Alvarez, E. Y. A., Crosslin, J. M., and Munyaneza, J. E. 2013a. Haplotyping the potato psyllid, Bactericera cockerelli, in Mexico and Central America. Southwest. Entomol. 38:201-208. https://doi.org/10.3958/059.038.0205 Crossref, ISIGoogle Scholar
    • Swisher, K. D., Henne, D. C., and Crosslin, J. M. 2014. Identification of a fourth haplotype of Bactericera cockerelli (Hemiptera: Triozidae) in the United States. J. Insect Sci. 14:161. https://doi.org/10.1093/jisesa/ieu023 CrossrefGoogle Scholar
    • Swisher, K. D., Munyaneza, J. E., and Crosslin, J. M. 2012. High resolution melting analysis of the cytochrome oxidase I gene identifies three haplotypes of the potato psyllid in the United States. Environ. Entomol. 41:1019-1028. https://doi.org/10.1603/EN12066 Crossref, ISIGoogle Scholar
    • Swisher, K. D., Munyaneza, J. E., Velasquez-Valle, R., and Mena-Covarrubias, J. 2018. Detection of pathogens associated with psyllids and leafhoppers in Capsicum annuum L. in the Mexican States of Durango, Zacatecas, and Michoacan. Plant Dis. 102:146-153. https://doi.org/10.1094/PDIS-05-17-0758-RE Link, ISIGoogle Scholar
    • Swisher, K. D., Sengoda, V. G., Dixon, J., Echegaray, E., Murphy, A. F., Rondon, S. I., Munyaneza, J. E., and Crosslin, J. M. 2013b. Haplotypes of the potato psyllid, Bactericera cockerelli, on the wild host plant, Solanum dulcamara, in the Pacific Northwestern United States. Am. J. Potato Res. 90:570-577. https://doi.org/10.1007/s12230-013-9330-3 Crossref, ISIGoogle Scholar
    • Swisher Grimm, K. D., and Garczynski, S. F. 2019. Identification of a new haplotype of ‘Candidatus Liberibacter solanacearum’ in Solanum tuberosum. Plant Dis. 103:468-474. https://doi.org/10.1094/PDIS-06-18-0937-RE Link, ISIGoogle Scholar
    • Swisher Grimm, K. D., Mustafa, T., Cooper, W. R., and Munyaneza, J. E. 2018. Role of ‘Candidatus Liberibacter solanacearum’ and Bactericera cockerelli haplotypes in zebra chip incidence and symptom severity. Am. J. Potato Res. 95:709-719. https://doi.org/10.1007/s12230-018-9678-5 Crossref, ISIGoogle Scholar
    • Taberlet, P., Gielly, L., Pautou, G., and Bouvet, J. 1991. Universal primers for amplification of three noncoding regions of chloroplast DNA. Plant Mol. Biol. 17:1105-1109. https://doi.org/10.1007/BF00037152 Crossref, ISIGoogle Scholar
    • Wallis, R. L. 1955. Ecological studies on the potato psyllid as a pest of potatoes. USDA Tech. Bull. 1107:1-24. Google Scholar
    • Wen, A. M., Johnson, C., and Gudmestad, N. C. 2013. Development of a PCR assay for the rapid detection and differentiation of ‘‘Candidatus Liberibacter solanacearum’ haplotypes and their spatiotemporal distribution in the United States. Am. J. Potato Res. 90:229-236. https://doi.org/10.1007/s12230-012-9293-9 Crossref, ISIGoogle Scholar
    • Wenninger, E. J., Dahan, J., Thornton, M., and Karasev, A. V. 2019. Associations of the potato psyllid and ‘Candidatus Liberibacter solanacearum’ in Idaho with the noncrop host plants bittersweet nightshade and field bindweed. Environ. Entomol. 48:747-754. https://doi.org/10.1093/ee/nvz033 Crossref, ISIGoogle Scholar