Identification of phytoplasmas representing multiple new genetic lineages from phloem-feeding leafhoppers highlights the diversity of phytoplasmas and their potential vectors

Authors: Wei, Wei; TRIVELLONE, VALERIA - Illinois Natural History Survey; DIETRICH, CHRISTOPHER - Illinois Natural History Survey; Zhao, Yan; Bottner, Kristi; IVANAUSKAS, ALGIRDAS - Nature Research Centre

Submitted to: Pathogens
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/15/2021
Publication Date: 3/15/2021
Citation: Wei, W., Trivellone, V., Dietrich, C.H., Zhao, Y., Bottner-Parker, K.D., Ivanauskas, A. 2021 Identification of phytoplasmas representing multiple new genetic lineages from phloem-feeding leafhoppers highlights the diversity of phytoplasmas and their potential vectors Pathogens. 10(3):352. https://doi.org/10.3390/pathogens10030352.
DOI: https://doi.org/10.3390/pathogens10030352

Interpretive Summary: Phytoplasmas are small obligate intracellular phytopathogenic bacteria. Besides inhibiting in the plant phloem tissues and infecting various plant species, phytoplasmas also replicate and colonize in insect vectors primarily leafhoppers, which play an essential role in the transmission and epidemiology of phytoplasmas. Phytoplasmas have been discovered mostly in symptomatic plants (mainly crops and ornamentals) in managed agroecosystems and plantations, while phytoplasma detection in natural habitats has been largely overlooked. In this study, ARS scientists detected ten phytoplasmas strains in 76 leafhopper samples (provided by the collaborators in Illinois Natural History Survey) collected from largely unexplored non-economically natural habitats worldwide. ARS scientists further identified and classified these phytoplasma strains, which not only represented five new subgroup genetic lineages from four distinct phytoplasma classification groups, but also extended previously unknown geographical distributions. In addition, phytoplasma-harboring leafhoppers belonged to seven known species, none of which were previously reported phytoplasma vectors. The results from this study broaden our understanding of the genetic diversity, geographical distribution, and potential insect host range of phytoplasmas. This article will benefit scientists and students who are interested in phytoplasma detection, identification, and classification. The work reported in this article will help researchers understand genetic diversity and insect host range of phytoplasmas, and vector-borne phytoplasma transmission and epidemiology.

Technical Abstract: Phytoplasmas are obligate transkingdom bacterial parasites that infect a variety of plant species and replicate in phloem-feeding insects in the order Hemiptera, mainly leafhoppers (Cicadellidae). The insect capacity in acquisition, transmission, survival, and host range directly determines the epidemiology of phytoplasmas. However, due to the difficulty of insect sampling and the lack of follow-up transmission trials, the known phytoplasma insect hosts are still limited compared with the identified plant hosts. In this study, 76 leafhoppers collected from previously overlooked natural and semi-natural habitats were examined for the presence of phytoplasmas by nested polymerase chain reaction (PCR) using DNA extracted from each single insect specimen. A total of ten phytoplasma strains were identified in leafhoppers from four countries including South Africa, Kyrgyzstan, Australia, and China. Based on virtual restriction fragment length polymorphism (RFLP) analysis, these ten phytoplasma strains were classified into four distinct 16Sr taxonomic groups (16SrI, 16SrIII, 16SrXIV and 16SrXV), representing five new subgroups (16SrI-AO, 16SrXIV-D, 16SrXIV-E, 16SrXIV-F, and 16SrXV-C). The results strongly suggest that the newly identified phytoplasma strains not only represent new genetic subgroup lineages, but also extend previously undiscovered geographical distributions. In addition, ten phytoplasma-harboring leafhoppers belonged to seven known leafhopper species, none of them were previously reported insect vectors or “carriers” of phytoplasmas. The findings from this study provide fresh insight into genetic diversity, geographical distribution, and insect host range of phytoplasmas. Further transmission trials and screening of new potential host plants and weed reservoirs in areas adjacent to collection sites of phytoplasma harboring leafhoppers will contribute to a better understanding of insect-borne phytoplasma transmission and epidemiology.