Screening potential insect vectors in a museum biorepository reveals undiscovered diversity of plant pathogens in natural areas

Authors: TRIVELLONE, VALERIA - Illinois Natural History Survey; Wei, Wei; DIETRICH, CHRISTOPHER - Illinois Natural History Survey; FILIPPIN, LUISA - Council For Research And Experimentation In Agriculture – Research Centre For Industrial Crops

Submitted to: Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/15/2021
Publication Date: 5/1/2021
Citation: Trivellone, V., Wei, W., Dietrich, C.H., Filippin, L. 2021 Screening potential insect vectors in a museum biorepository reveals undiscovered diversity of plant pathogens in natural areas Ecology and Evolution 10.1002/ece3.7502. https://doi.org/10.1002/ece3.7502
DOI: https://doi.org/10.1002/ece3.7502

Interpretive Summary: Phytoplasmas are small and cell wall-less bacteria. They not only infect nearly a thousand plant species, but also reside in insects mainly leafhoppers, which play a key role in the transmission and epidemiology of phytoplasmas. Most known phytoplasmas have been discovered in symptomatic plants in managed agroecosystems and plantation forests with low biodiversity and high inputs. Subsequent insect vector surveys have always been conducted in the same agroecosystems and plantations where the phytoplasmas were found. Therefore, compared with the number of known plant hosts, far less phytoplasma insect vectors have been identified because of the difficulty of insect sampling and the lack of follow-up transmission trials. In this study, employing PCR approach, ARS scientists and the collaborators in Illinois Natural History Survey performed a preliminary phytoplasma screening on 227 leafhoppers (a small portion of an entire leafhopper collection) from natural habitats. A total of six phytoplasma strains from leafhopper samples were identified, which represented different genetic lineages. Phytoplasma harboring leafhoppers were identified as belonging to six known leafhopper species, all recorded for the first time as potential phytoplasma vectors. These results strongly suggested that phytoplasma diversity and potential insect host range were indeed underestimated, and further large-scale investigations will contribute to a better understanding of phytoplasma genetic diversity, insect host range, and insect-borne phytoplasma transmission. The findings will be instructive for the screening of new plant hosts and weed reservoirs of phytoplasmas and provide an early warning for the emergence of new phytoplasma diseases that may occur in agroecosystems. The work from this study will help scientists and students who are interested in phytoplasma diversity, insect host, and epidemiology of phytoplasmas.

Technical Abstract: hytoplasmas (Mollicutes, Acholeplasmataceae), vector-borne obligate bacterial plant-parasites, infect nearly 1,000 plant species and unknown numbers of insects, mainly leafhoppers (Hemiptera, Deltocephalinae), which play a key role in transmission and epidemiology. Although the plant-phytoplasma-insect association has been evolving for >300 million years, nearly all known phytoplasmas have been discovered as a result of the damage inflicted by phytoplasma diseases on crops. Few efforts have been made to study phytoplasmas occurring in non-economically important plants in natural habitats. In this study, a sub-sample of leafhopper specimens preserved in a large museum biorepository was analyzed to unveil potential new associations. PCR screening for phytoplasmas performed on 227 phloem-feeding leafhoppers collected worldwide from natural habitats revealed the presence of 6 different phytoplasma strains, which belong to four different classification groups. This indicates that museum collections of herbivorous insects represent a rich and largely untapped resource for discovery of new plant pathogens, that natural areas worldwide harbor a diverse but largely undiscovered diversity of phytoplasmas and potential insect vectors, and that independent epidemiological cycles occur in such habitats, posing a potential threat of disease spillover into agricultural systems. Larger-scale future investigations will contribute to a better understanding of phytoplasma genetic diversity, insect host range, and insect-borne phytoplasma transmission and provide an early warning for the emergence of new phytoplasma diseases that may occur in agroecosystems.