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Phytoplasmas are a group of plant-pathogenic, cell-wall-less bacteria vectored primarily by leafhoppers (Hemiptera Cicadellidae), one of the most diverse families of insects. Despite the importance of documenting associations between phytoplasmas, their insect vectors, and plant hosts to prevent disease outbreaks, such knowledge is currently highly incomplete and largely neglects the diversity of the system in natural areas. Here, we used anchored hybrid enrichment (AHE) to recover the DNA of five plant genes (rbcL, matK, ITS1, ITS2, and trnH-psbA) in 58 phloem-feeding leafhoppers from around the world that had previously tested positive for phytoplasma infection. Using BLASTn and a strict filtering approach, we assigned taxonomic classifications to the plant sequences and tested for cophylogenetic signals between potential Deltocephalinae leafhopper vectors and their associated plants. We observed incongruence between plant and insect phylogenies. Many leafhopper species, including presumed grass specialists, fed on distantly related plant lineages; 66% of sampled leafhoppers fed on plants from at least two different orders. By disentangling phytoplasma–leafhopper–plant interactions, we identify locations at risk of phytoplasma disease outbreaks. Furthermore, the observed wide diet breadth raises questions about how phytoplasma infection may manipulate the feeding preference of their insect host and helps fill the gaps in understanding the ecology and diversification of the tripartite association.
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Identification of Potential Host Plants of Sap-Sucking Insects (Hemiptera: Cicadellidae) Using Anchored Hybrid By-Catch Data
Reliable host plant records are available for only a small fraction of herbivorous insect species, despite their potential agricultural importance. Most available data on insect–plant associations have been obtained through field observations of occurrences of insects on particular plants. Molecular methods have more recently been used to identify potential host plants using DNA extracted from insects, but most prior studies using these methods have focused on chewing insects that ingest tissues expected to contain large quantities of plant DNA. Screening of Illumina data obtained from sap feeders of the hemipteran family Cicadellidae (leafhoppers) using anchored hybrid enrichment indicates that, despite feeding on plant fluids, these insects often contain detectable quantities of plant DNA. Although inclusion of probes for bacterial 16S in the original anchored hybrid probe kit yielded relatively high detection rates for chloroplast 16S, the Illumina short reads also, in some cases, included DNA for various plant barcode genes as “by-catch”. Detection rates were generally only slightly higher for Typhlocybinae, which feed preferentially on parenchyma cell contents, compared to other groups of leafhoppers that feed preferentially on phloem or xylem. These results indicate that next-generation sequencing provides a powerful tool to investigate the specific association between individual insect and plant species.
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- Award ID(s):
- 1639601
- PAR ID:
- 10312175
- Date Published:
- Journal Name:
- Insects
- Volume:
- 12
- Issue:
- 11
- ISSN:
- 2075-4450
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Phytoplasmas (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 noneconomically important plants in natural habitats. In this study, a subsample 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 previously unknown phytoplasma strains. 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 across global agroecosystems.more » « less
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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 confirmed phytoplasma insect hosts are still limited compared with the identified plant hosts. Recently, quantitative polymerase chain reaction (qPCR)-based quick screening of 227 leafhoppers collected in natural habitats unveiled the presence of previously unknown phytoplasmas in six samples. In the present study, 76 leafhoppers, including the six prescreened positive samples, were further examined to identify and characterize the phytoplasma strains by semi-nested PCR. 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 ribosomal (16Sr) 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 which were previously reported insect vectors 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 phytoplasma transmission and epidemiology.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/insects12110964
