Pest status, molecular evolution, and epigenetic factors derived from the genome assembly of Frankliniella fusca, a thysanopteran phytovirus vector
Abstract Background The tobacco thrips (Frankliniella fusca Hinds; family Thripidae; order Thysanoptera) is an important pest that can transmit viruses such as the tomato spotted wilt orthotospovirus to numerous economically important agricultural row crops and vegetables. The structural and functio...
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| Format: | Article |
| Language: | English |
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BMC
2023-06-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-023-09375-5 |
| _version_ | 1827917123304816640 |
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| author | Michael A. Catto Paul E. Labadie Alana L. Jacobson George G. Kennedy Rajagopalbabu Srinivasan Brendan G. Hunt |
| author_facet | Michael A. Catto Paul E. Labadie Alana L. Jacobson George G. Kennedy Rajagopalbabu Srinivasan Brendan G. Hunt |
| author_sort | Michael A. Catto |
| collection | DOAJ |
| description | Abstract Background The tobacco thrips (Frankliniella fusca Hinds; family Thripidae; order Thysanoptera) is an important pest that can transmit viruses such as the tomato spotted wilt orthotospovirus to numerous economically important agricultural row crops and vegetables. The structural and functional genomics within the order Thysanoptera has only begun to be explored. Within the > 7000 known thysanopteran species, the melon thrips (Thrips palmi Karny) and the western flower thrips (Frankliniella occidentalis Pergrande) are the only two thysanopteran species with assembled genomes. Results A genome of F. fusca was assembled by long-read sequencing of DNA from an inbred line. The final assembly size was 370 Mb with a single copy ortholog completeness of ~ 99% with respect to Insecta. The annotated genome of F. fusca was compared with the genome of its congener, F. occidentalis. Results revealed many instances of lineage-specific differences in gene content. Analyses of sequence divergence between the two Frankliniella species’ genomes revealed substitution patterns consistent with positive selection in ~ 5% of the protein-coding genes with 1:1 orthologs. Further, gene content related to its pest status, such as xenobiotic detoxification and response to an ambisense-tripartite RNA virus (orthotospovirus) infection was compared with F. occidentalis. Several F. fusca genes related to virus infection possessed signatures of positive selection. Estimation of CpG depletion, a mutational consequence of DNA methylation, revealed that F. fusca genes that were downregulated and alternatively spliced in response to virus infection were preferentially targeted by DNA methylation. As in many other insects, DNA methylation was enriched in exons in Frankliniella, but gene copies with homology to DNA methyltransferase 3 were numerous and fragmented. This phenomenon seems to be relatively unique to thrips among other insect groups. Conclusions The F. fusca genome assembly provides an important resource for comparative genomic analyses of thysanopterans. This genomic foundation allows for insights into molecular evolution, gene regulation, and loci important to agricultural pest status. |
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| format | Article |
| id | doaj.art-8ab9fa07352d4abf9c07acce797cafc1 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-03-13T03:24:21Z |
| publishDate | 2023-06-01 |
| publisher | BMC |
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| spelling | doaj.art-8ab9fa07352d4abf9c07acce797cafc12023-06-25T11:09:56ZengBMCBMC Genomics1471-21642023-06-0124111710.1186/s12864-023-09375-5Pest status, molecular evolution, and epigenetic factors derived from the genome assembly of Frankliniella fusca, a thysanopteran phytovirus vectorMichael A. Catto0Paul E. Labadie1Alana L. Jacobson2George G. Kennedy3Rajagopalbabu Srinivasan4Brendan G. Hunt5Department of Entomology, University of GeorgiaDepartment of Entomology and Plant Pathology, North Carolina State UniversityDepartment of Entomology and Plant Pathology, Auburn University College of AgricultureDepartment of Entomology and Plant Pathology, North Carolina State UniversityDepartment of Entomology, University of GeorgiaDepartment of Entomology, University of GeorgiaAbstract Background The tobacco thrips (Frankliniella fusca Hinds; family Thripidae; order Thysanoptera) is an important pest that can transmit viruses such as the tomato spotted wilt orthotospovirus to numerous economically important agricultural row crops and vegetables. The structural and functional genomics within the order Thysanoptera has only begun to be explored. Within the > 7000 known thysanopteran species, the melon thrips (Thrips palmi Karny) and the western flower thrips (Frankliniella occidentalis Pergrande) are the only two thysanopteran species with assembled genomes. Results A genome of F. fusca was assembled by long-read sequencing of DNA from an inbred line. The final assembly size was 370 Mb with a single copy ortholog completeness of ~ 99% with respect to Insecta. The annotated genome of F. fusca was compared with the genome of its congener, F. occidentalis. Results revealed many instances of lineage-specific differences in gene content. Analyses of sequence divergence between the two Frankliniella species’ genomes revealed substitution patterns consistent with positive selection in ~ 5% of the protein-coding genes with 1:1 orthologs. Further, gene content related to its pest status, such as xenobiotic detoxification and response to an ambisense-tripartite RNA virus (orthotospovirus) infection was compared with F. occidentalis. Several F. fusca genes related to virus infection possessed signatures of positive selection. Estimation of CpG depletion, a mutational consequence of DNA methylation, revealed that F. fusca genes that were downregulated and alternatively spliced in response to virus infection were preferentially targeted by DNA methylation. As in many other insects, DNA methylation was enriched in exons in Frankliniella, but gene copies with homology to DNA methyltransferase 3 were numerous and fragmented. This phenomenon seems to be relatively unique to thrips among other insect groups. Conclusions The F. fusca genome assembly provides an important resource for comparative genomic analyses of thysanopterans. This genomic foundation allows for insights into molecular evolution, gene regulation, and loci important to agricultural pest status.https://doi.org/10.1186/s12864-023-09375-5Crop pestThripsOrthotospovirusSelection pressuresCpGo/ei5K |
| spellingShingle | Michael A. Catto Paul E. Labadie Alana L. Jacobson George G. Kennedy Rajagopalbabu Srinivasan Brendan G. Hunt Pest status, molecular evolution, and epigenetic factors derived from the genome assembly of Frankliniella fusca, a thysanopteran phytovirus vector BMC Genomics Crop pest Thrips Orthotospovirus Selection pressures CpGo/e i5K |
| title | Pest status, molecular evolution, and epigenetic factors derived from the genome assembly of Frankliniella fusca, a thysanopteran phytovirus vector |
| title_full | Pest status, molecular evolution, and epigenetic factors derived from the genome assembly of Frankliniella fusca, a thysanopteran phytovirus vector |
| title_fullStr | Pest status, molecular evolution, and epigenetic factors derived from the genome assembly of Frankliniella fusca, a thysanopteran phytovirus vector |
| title_full_unstemmed | Pest status, molecular evolution, and epigenetic factors derived from the genome assembly of Frankliniella fusca, a thysanopteran phytovirus vector |
| title_short | Pest status, molecular evolution, and epigenetic factors derived from the genome assembly of Frankliniella fusca, a thysanopteran phytovirus vector |
| title_sort | pest status molecular evolution and epigenetic factors derived from the genome assembly of frankliniella fusca a thysanopteran phytovirus vector |
| topic | Crop pest Thrips Orthotospovirus Selection pressures CpGo/e i5K |
| url | https://doi.org/10.1186/s12864-023-09375-5 |
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