Embryonic piRNAs target horizontally transferred vertebrate transposons in assassin bugs
IntroductionPiwi proteins and the associated Piwi-interacting RNAs (piRNAs) coordinate a surveillance system that protects the animal genome from DNA damage induced by transposable element (TE) mobilization. While the pathway has been described in detail in the fruit fly Drosophila melanogaster, muc...
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Frontiers Media S.A.
2024-11-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2024.1481881/full |
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| author | Tarcísio Fontenele de Brito Maira Arruda Cardoso Nazerke Atinbayeva Nazerke Atinbayeva Ingrid Alexandre de Abreu Brito Lucas Amaro da Costa Nicola Iovino Attilio Pane Attilio Pane |
| author_facet | Tarcísio Fontenele de Brito Maira Arruda Cardoso Nazerke Atinbayeva Nazerke Atinbayeva Ingrid Alexandre de Abreu Brito Lucas Amaro da Costa Nicola Iovino Attilio Pane Attilio Pane |
| author_sort | Tarcísio Fontenele de Brito |
| collection | DOAJ |
| description | IntroductionPiwi proteins and the associated Piwi-interacting RNAs (piRNAs) coordinate a surveillance system that protects the animal genome from DNA damage induced by transposable element (TE) mobilization. While the pathway has been described in detail in the fruit fly Drosophila melanogaster, much less is known in more basal insects. Rhodnius prolixus is an hemipteran insect and one of the major vectors of Chagas disease. Rhodnius acquired specific classes of horizontally transferred transposons (HTTs) by feeding on bats, opossums and squirrel monkeys, thus providing the opportunity to investigate the piRNA-base response against HTTs in this species.MethodsSmallRNA-Seq reads mapping to HTTs and resident transposable elements were quantified and checked for piRNA features like 1U a 10A biases, ping-pong and phasing signatures. Uniquely mapped piRNAs were used to identify piRNA clusters in Rhodnius’ genome. RNA-Seq data was used to quantify transposon and Rp-PIWI genes expression levels and were validated by qRT-PCR.ResultsBy analyzing the temporal dynamics of piRNA cluster expression and piRNA production during critical stages of Rhodnius development, we show that peak levels of ∼28 nt long piRNAs correlate with reduced HTT and resident TE expression primarily during embryogenesis. Strikingly, while resident TEs piRNAs seem to engage in a typical ping-pong amplification mechanism, sense and antisense HTT piRNAs instead overlap by ∼20 nt or do not display ping-pong signatures.DiscussionOur data shed light on the biogenesis and functions of the piRNAs in Rhodnius prolixus and reveal that piRNAs, but not the siRNA pathway, responded to HTTs that were recently transferred from vertebrate tetrapods to a hematophagous insect of medical relevance. |
| format | Article |
| id | doaj-art-dda472065e044e07ad3f5eb3a1b54128 |
| institution | Kabale University |
| issn | 2296-634X |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj-art-dda472065e044e07ad3f5eb3a1b541282024-11-20T06:26:45ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2024-11-011210.3389/fcell.2024.14818811481881Embryonic piRNAs target horizontally transferred vertebrate transposons in assassin bugsTarcísio Fontenele de Brito0Maira Arruda Cardoso1Nazerke Atinbayeva2Nazerke Atinbayeva3Ingrid Alexandre de Abreu Brito4Lucas Amaro da Costa5Nicola Iovino6Attilio Pane7Attilio Pane8Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilInstituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilDepartment of Chromatin Regulation, Max Planck Institute of Immunobiology and Epigenetics, Freiburg im Breisgau, GermanyAlbert-Ludwigs-Universität Freiburg, Freiburg im Breisgau, GermanyInstituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilInstituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilDepartment of Chromatin Regulation, Max Planck Institute of Immunobiology and Epigenetics, Freiburg im Breisgau, GermanyInstituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilInstituto Nacional de Ciência e Tecnologia em Entomologia Molecular, Rio de Janeiro, BrazilIntroductionPiwi proteins and the associated Piwi-interacting RNAs (piRNAs) coordinate a surveillance system that protects the animal genome from DNA damage induced by transposable element (TE) mobilization. While the pathway has been described in detail in the fruit fly Drosophila melanogaster, much less is known in more basal insects. Rhodnius prolixus is an hemipteran insect and one of the major vectors of Chagas disease. Rhodnius acquired specific classes of horizontally transferred transposons (HTTs) by feeding on bats, opossums and squirrel monkeys, thus providing the opportunity to investigate the piRNA-base response against HTTs in this species.MethodsSmallRNA-Seq reads mapping to HTTs and resident transposable elements were quantified and checked for piRNA features like 1U a 10A biases, ping-pong and phasing signatures. Uniquely mapped piRNAs were used to identify piRNA clusters in Rhodnius’ genome. RNA-Seq data was used to quantify transposon and Rp-PIWI genes expression levels and were validated by qRT-PCR.ResultsBy analyzing the temporal dynamics of piRNA cluster expression and piRNA production during critical stages of Rhodnius development, we show that peak levels of ∼28 nt long piRNAs correlate with reduced HTT and resident TE expression primarily during embryogenesis. Strikingly, while resident TEs piRNAs seem to engage in a typical ping-pong amplification mechanism, sense and antisense HTT piRNAs instead overlap by ∼20 nt or do not display ping-pong signatures.DiscussionOur data shed light on the biogenesis and functions of the piRNAs in Rhodnius prolixus and reveal that piRNAs, but not the siRNA pathway, responded to HTTs that were recently transferred from vertebrate tetrapods to a hematophagous insect of medical relevance.https://www.frontiersin.org/articles/10.3389/fcell.2024.1481881/fullrhodniusHTTpiRNA pathwaytransposonsiRNA |
| spellingShingle | Tarcísio Fontenele de Brito Maira Arruda Cardoso Nazerke Atinbayeva Nazerke Atinbayeva Ingrid Alexandre de Abreu Brito Lucas Amaro da Costa Nicola Iovino Attilio Pane Attilio Pane Embryonic piRNAs target horizontally transferred vertebrate transposons in assassin bugs Frontiers in Cell and Developmental Biology rhodnius HTT piRNA pathway transposon siRNA |
| title | Embryonic piRNAs target horizontally transferred vertebrate transposons in assassin bugs |
| title_full | Embryonic piRNAs target horizontally transferred vertebrate transposons in assassin bugs |
| title_fullStr | Embryonic piRNAs target horizontally transferred vertebrate transposons in assassin bugs |
| title_full_unstemmed | Embryonic piRNAs target horizontally transferred vertebrate transposons in assassin bugs |
| title_short | Embryonic piRNAs target horizontally transferred vertebrate transposons in assassin bugs |
| title_sort | embryonic pirnas target horizontally transferred vertebrate transposons in assassin bugs |
| topic | rhodnius HTT piRNA pathway transposon siRNA |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2024.1481881/full |
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