Genome and Transcriptome Analyses Facilitate Genetic Control of <i>Wohlfahrtia magnifica</i>, a Myiasis-Causing Flesh Fly
Myiasis caused by <i>Wohlfahrtia magnifica</i> is a widespread parasitic infestation in mammals. The infested host suffers from damage as the developing larvae feed on its tissues. For the control of myiasis infestation, genetic methods have been shown to be effective and promising as an...
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MDPI AG
2023-07-01
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| Series: | Insects |
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| Online Access: | https://www.mdpi.com/2075-4450/14/7/620 |
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| author | Zhipeng Jia Surong Hasi Deng Zhan Bin Hou Claus Vogl Pamela A. Burger |
| author_facet | Zhipeng Jia Surong Hasi Deng Zhan Bin Hou Claus Vogl Pamela A. Burger |
| author_sort | Zhipeng Jia |
| collection | DOAJ |
| description | Myiasis caused by <i>Wohlfahrtia magnifica</i> is a widespread parasitic infestation in mammals. The infested host suffers from damage as the developing larvae feed on its tissues. For the control of myiasis infestation, genetic methods have been shown to be effective and promising as an alternative to insecticides. Combining genome, isoform sequencing (Iso-Seq), and RNA sequencing (RNA-seq) data, we isolated and characterized two sex-determination genes, <i>W. magnifica transformer (Wmtra)</i> and <i>W. magnifica transformer2</i> (<i>Wmtra2</i>), whose orthologs in a number of insect pests have been utilized to develop genetic control approaches. <i>Wmtra</i> transcripts are sex-specifically spliced; only the female transcript encodes a full-length functional protein, while the male transcript encodes a truncated and non-functional polypeptide due to the presence of the male-specific exon containing multiple in-frame stop codons. The existence of five predicted TRA/TRA2 binding sites in the male-specific exon and the surrounding intron of <i>Wmtra</i>, as well as the presence of an RNA-recognition motif in WmTRA2 may suggest the auto-regulation of <i>Wmtra</i> by its own protein interacting with WmTRA2. This results in the skipping of the male-specific exon and translation of the full-length functional protein only in females. Our comparative study in dipteran species showed that both the WmTRA and WmTRA2 proteins exhibit a high degree of similarity to their orthologs in the myiasis-causing blow flies. Additionally, transcriptome profiling performed between adult females and adult males reported 657 upregulated and 365 downregulated genes. Functional analysis showed that among upregulated genes those related to meiosis and mitosis Gene Ontology (GO) terms were enriched, while, among downregulated genes, those related to muscle cell development and aerobic metabolic processes were enriched. Among the female-biased gene set, we detected five candidate genes, <i>vasa</i> (<i>vas</i>), <i>nanos</i> (<i>nanos</i>), <i>bicoid</i> (<i>bcd</i>), <i>Bicaudal C</i> (<i>BicC</i>), and <i>innexin5</i> (<i>inx5</i>). The promoters of these genes may be able to upregulate Cas9 expression in the germline in Cas9-based homing gene drive systems as established in some flies and mosquitoes. The isolation and characterization of these genes is an important step toward the development of genetic control programs against <i>W. magnifica</i> infestation. |
| first_indexed | 2024-03-11T00:58:26Z |
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| institution | Directory Open Access Journal |
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| publishDate | 2023-07-01 |
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| spelling | doaj.art-26b585ad83884f6f8e458a7cd8db31902023-11-18T19:49:05ZengMDPI AGInsects2075-44502023-07-0114762010.3390/insects14070620Genome and Transcriptome Analyses Facilitate Genetic Control of <i>Wohlfahrtia magnifica</i>, a Myiasis-Causing Flesh FlyZhipeng Jia0Surong Hasi1Deng Zhan2Bin Hou3Claus Vogl4Pamela A. Burger5Research Institute of Wildlife Ecology, Department of Interdisciplinary Life Sciences, University of Veterinary Medicine Vienna, Savoyenstrasse 1, 1160 Vienna, AustriaKey Laboratory of Clinical Diagnosis and Treatment Technology in Animal Disease, Ministry of Agriculture and Rural Affairs, Inner Mongolia Agricultural University, Hohhot 010018, ChinaKey Laboratory of Clinical Diagnosis and Treatment Technology in Animal Disease, Ministry of Agriculture and Rural Affairs, Inner Mongolia Agricultural University, Hohhot 010018, ChinaKey Laboratory of Clinical Diagnosis and Treatment Technology in Animal Disease, Ministry of Agriculture and Rural Affairs, Inner Mongolia Agricultural University, Hohhot 010018, ChinaInstitute of Animal Breeding and Genetics, Department of Biomedical Sciences, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, AustriaResearch Institute of Wildlife Ecology, Department of Interdisciplinary Life Sciences, University of Veterinary Medicine Vienna, Savoyenstrasse 1, 1160 Vienna, AustriaMyiasis caused by <i>Wohlfahrtia magnifica</i> is a widespread parasitic infestation in mammals. The infested host suffers from damage as the developing larvae feed on its tissues. For the control of myiasis infestation, genetic methods have been shown to be effective and promising as an alternative to insecticides. Combining genome, isoform sequencing (Iso-Seq), and RNA sequencing (RNA-seq) data, we isolated and characterized two sex-determination genes, <i>W. magnifica transformer (Wmtra)</i> and <i>W. magnifica transformer2</i> (<i>Wmtra2</i>), whose orthologs in a number of insect pests have been utilized to develop genetic control approaches. <i>Wmtra</i> transcripts are sex-specifically spliced; only the female transcript encodes a full-length functional protein, while the male transcript encodes a truncated and non-functional polypeptide due to the presence of the male-specific exon containing multiple in-frame stop codons. The existence of five predicted TRA/TRA2 binding sites in the male-specific exon and the surrounding intron of <i>Wmtra</i>, as well as the presence of an RNA-recognition motif in WmTRA2 may suggest the auto-regulation of <i>Wmtra</i> by its own protein interacting with WmTRA2. This results in the skipping of the male-specific exon and translation of the full-length functional protein only in females. Our comparative study in dipteran species showed that both the WmTRA and WmTRA2 proteins exhibit a high degree of similarity to their orthologs in the myiasis-causing blow flies. Additionally, transcriptome profiling performed between adult females and adult males reported 657 upregulated and 365 downregulated genes. Functional analysis showed that among upregulated genes those related to meiosis and mitosis Gene Ontology (GO) terms were enriched, while, among downregulated genes, those related to muscle cell development and aerobic metabolic processes were enriched. Among the female-biased gene set, we detected five candidate genes, <i>vasa</i> (<i>vas</i>), <i>nanos</i> (<i>nanos</i>), <i>bicoid</i> (<i>bcd</i>), <i>Bicaudal C</i> (<i>BicC</i>), and <i>innexin5</i> (<i>inx5</i>). The promoters of these genes may be able to upregulate Cas9 expression in the germline in Cas9-based homing gene drive systems as established in some flies and mosquitoes. The isolation and characterization of these genes is an important step toward the development of genetic control programs against <i>W. magnifica</i> infestation.https://www.mdpi.com/2075-4450/14/7/620<i>Wohlfahrtia magnifica</i>myiasis<i>tra</i> gene<i>tra2</i> geneIso-SeqRNA-seq |
| spellingShingle | Zhipeng Jia Surong Hasi Deng Zhan Bin Hou Claus Vogl Pamela A. Burger Genome and Transcriptome Analyses Facilitate Genetic Control of <i>Wohlfahrtia magnifica</i>, a Myiasis-Causing Flesh Fly Insects <i>Wohlfahrtia magnifica</i> myiasis <i>tra</i> gene <i>tra2</i> gene Iso-Seq RNA-seq |
| title | Genome and Transcriptome Analyses Facilitate Genetic Control of <i>Wohlfahrtia magnifica</i>, a Myiasis-Causing Flesh Fly |
| title_full | Genome and Transcriptome Analyses Facilitate Genetic Control of <i>Wohlfahrtia magnifica</i>, a Myiasis-Causing Flesh Fly |
| title_fullStr | Genome and Transcriptome Analyses Facilitate Genetic Control of <i>Wohlfahrtia magnifica</i>, a Myiasis-Causing Flesh Fly |
| title_full_unstemmed | Genome and Transcriptome Analyses Facilitate Genetic Control of <i>Wohlfahrtia magnifica</i>, a Myiasis-Causing Flesh Fly |
| title_short | Genome and Transcriptome Analyses Facilitate Genetic Control of <i>Wohlfahrtia magnifica</i>, a Myiasis-Causing Flesh Fly |
| title_sort | genome and transcriptome analyses facilitate genetic control of i wohlfahrtia magnifica i a myiasis causing flesh fly |
| topic | <i>Wohlfahrtia magnifica</i> myiasis <i>tra</i> gene <i>tra2</i> gene Iso-Seq RNA-seq |
| url | https://www.mdpi.com/2075-4450/14/7/620 |
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