Neofunctionalization driven by positive selection led to the retention of the loqs2 gene encoding an Aedes specific dsRNA binding protein
Abstract Background Mosquito borne viruses, such as dengue, Zika, yellow fever and Chikungunya, cause millions of infections every year. These viruses are mostly transmitted by two urban-adapted mosquito species, Aedes aegypti and Aedes albopictus. Although mechanistic understanding remains largely...
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| Format: | Article |
| Language: | English |
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BMC
2024-01-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-024-01821-4 |
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| author | Carlos F. Estevez-Castro Murillo F. Rodrigues Antinéa Babarit Flávia V. Ferreira Elisa G. de Andrade Eric Marois Rodrigo Cogni Eric R. G. R. Aguiar João T. Marques Roenick P. Olmo |
| author_facet | Carlos F. Estevez-Castro Murillo F. Rodrigues Antinéa Babarit Flávia V. Ferreira Elisa G. de Andrade Eric Marois Rodrigo Cogni Eric R. G. R. Aguiar João T. Marques Roenick P. Olmo |
| author_sort | Carlos F. Estevez-Castro |
| collection | DOAJ |
| description | Abstract Background Mosquito borne viruses, such as dengue, Zika, yellow fever and Chikungunya, cause millions of infections every year. These viruses are mostly transmitted by two urban-adapted mosquito species, Aedes aegypti and Aedes albopictus. Although mechanistic understanding remains largely unknown, Aedes mosquitoes may have unique adaptations that lower the impact of viral infection. Recently, we reported the identification of an Aedes specific double-stranded RNA binding protein (dsRBP), named Loqs2, that is involved in the control of infection by dengue and Zika viruses in mosquitoes. Preliminary analyses suggested that the loqs2 gene is a paralog of loquacious (loqs) and r2d2, two co-factors of the RNA interference (RNAi) pathway, a major antiviral mechanism in insects. Results Here we analyzed the origin and evolution of loqs2. Our data suggest that loqs2 originated from two independent duplications of the first double-stranded RNA binding domain of loqs that occurred before the origin of the Aedes Stegomyia subgenus, around 31 million years ago. We show that the loqs2 gene is evolving under relaxed purifying selection at a faster pace than loqs, with evidence of neofunctionalization driven by positive selection. Accordingly, we observed that Loqs2 is localized mainly in the nucleus, different from R2D2 and both isoforms of Loqs that are cytoplasmic. In contrast to r2d2 and loqs, loqs2 expression is stage- and tissue-specific, restricted mostly to reproductive tissues in adult Ae. aegypti and Ae. albopictus. Transgenic mosquitoes engineered to express loqs2 ubiquitously undergo developmental arrest at larval stages that correlates with massive dysregulation of gene expression without major effects on microRNAs or other endogenous small RNAs, classically associated with RNA interference. Conclusions Our results uncover the peculiar origin and neofunctionalization of loqs2 driven by positive selection. This study shows an example of unique adaptations in Aedes mosquitoes that could ultimately help explain their effectiveness as virus vectors. |
| first_indexed | 2024-03-07T15:26:16Z |
| format | Article |
| id | doaj.art-ee5a87bf4bc848d481097ff4e59ad9ab |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-03-07T15:26:16Z |
| publishDate | 2024-01-01 |
| publisher | BMC |
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| series | BMC Biology |
| spelling | doaj.art-ee5a87bf4bc848d481097ff4e59ad9ab2024-03-05T16:43:18ZengBMCBMC Biology1741-70072024-01-0122112010.1186/s12915-024-01821-4Neofunctionalization driven by positive selection led to the retention of the loqs2 gene encoding an Aedes specific dsRNA binding proteinCarlos F. Estevez-Castro0Murillo F. Rodrigues1Antinéa Babarit2Flávia V. Ferreira3Elisa G. de Andrade4Eric Marois5Rodrigo Cogni6Eric R. G. R. Aguiar7João T. Marques8Roenick P. Olmo9Department of Biochemistry and Immunology, Instituto de Ciências Biológicas, Universidade Federal de Minas GeraisInstitute of Ecology and Evolution, University of OregonCNRS UPR9022, Inserm U1257, Université de StrasbourgDepartment of Biochemistry and Immunology, Instituto de Ciências Biológicas, Universidade Federal de Minas GeraisDepartment of Biochemistry and Immunology, Instituto de Ciências Biológicas, Universidade Federal de Minas GeraisCNRS UPR9022, Inserm U1257, Université de StrasbourgDepartment of Ecology, Institute of Biosciences, University of São PauloDepartment of Biological Science, Center of Biotechnology and Genetics, State University of Santa CruzDepartment of Biochemistry and Immunology, Instituto de Ciências Biológicas, Universidade Federal de Minas GeraisDepartment of Biochemistry and Immunology, Instituto de Ciências Biológicas, Universidade Federal de Minas GeraisAbstract Background Mosquito borne viruses, such as dengue, Zika, yellow fever and Chikungunya, cause millions of infections every year. These viruses are mostly transmitted by two urban-adapted mosquito species, Aedes aegypti and Aedes albopictus. Although mechanistic understanding remains largely unknown, Aedes mosquitoes may have unique adaptations that lower the impact of viral infection. Recently, we reported the identification of an Aedes specific double-stranded RNA binding protein (dsRBP), named Loqs2, that is involved in the control of infection by dengue and Zika viruses in mosquitoes. Preliminary analyses suggested that the loqs2 gene is a paralog of loquacious (loqs) and r2d2, two co-factors of the RNA interference (RNAi) pathway, a major antiviral mechanism in insects. Results Here we analyzed the origin and evolution of loqs2. Our data suggest that loqs2 originated from two independent duplications of the first double-stranded RNA binding domain of loqs that occurred before the origin of the Aedes Stegomyia subgenus, around 31 million years ago. We show that the loqs2 gene is evolving under relaxed purifying selection at a faster pace than loqs, with evidence of neofunctionalization driven by positive selection. Accordingly, we observed that Loqs2 is localized mainly in the nucleus, different from R2D2 and both isoforms of Loqs that are cytoplasmic. In contrast to r2d2 and loqs, loqs2 expression is stage- and tissue-specific, restricted mostly to reproductive tissues in adult Ae. aegypti and Ae. albopictus. Transgenic mosquitoes engineered to express loqs2 ubiquitously undergo developmental arrest at larval stages that correlates with massive dysregulation of gene expression without major effects on microRNAs or other endogenous small RNAs, classically associated with RNA interference. Conclusions Our results uncover the peculiar origin and neofunctionalization of loqs2 driven by positive selection. This study shows an example of unique adaptations in Aedes mosquitoes that could ultimately help explain their effectiveness as virus vectors.https://doi.org/10.1186/s12915-024-01821-4loqs2RNA interference (RNAi)Aedes mosquitoesDouble-stranded RNA (dsRNA)dsRNA binding protein (dsRBP) |
| spellingShingle | Carlos F. Estevez-Castro Murillo F. Rodrigues Antinéa Babarit Flávia V. Ferreira Elisa G. de Andrade Eric Marois Rodrigo Cogni Eric R. G. R. Aguiar João T. Marques Roenick P. Olmo Neofunctionalization driven by positive selection led to the retention of the loqs2 gene encoding an Aedes specific dsRNA binding protein BMC Biology loqs2 RNA interference (RNAi) Aedes mosquitoes Double-stranded RNA (dsRNA) dsRNA binding protein (dsRBP) |
| title | Neofunctionalization driven by positive selection led to the retention of the loqs2 gene encoding an Aedes specific dsRNA binding protein |
| title_full | Neofunctionalization driven by positive selection led to the retention of the loqs2 gene encoding an Aedes specific dsRNA binding protein |
| title_fullStr | Neofunctionalization driven by positive selection led to the retention of the loqs2 gene encoding an Aedes specific dsRNA binding protein |
| title_full_unstemmed | Neofunctionalization driven by positive selection led to the retention of the loqs2 gene encoding an Aedes specific dsRNA binding protein |
| title_short | Neofunctionalization driven by positive selection led to the retention of the loqs2 gene encoding an Aedes specific dsRNA binding protein |
| title_sort | neofunctionalization driven by positive selection led to the retention of the loqs2 gene encoding an aedes specific dsrna binding protein |
| topic | loqs2 RNA interference (RNAi) Aedes mosquitoes Double-stranded RNA (dsRNA) dsRNA binding protein (dsRBP) |
| url | https://doi.org/10.1186/s12915-024-01821-4 |
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