On the origin and evolution of RNA editing in metazoans
© 2023 The Author(s). This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
| Autores: | , , , , , , , , , , , , , , , , , |
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| Tipo de documento: | artigo |
| Estado: | Versão publicada |
| Data de publicação: | 2023 |
| País: | España |
| Recursos: | Consejo Superior de Investigaciones Científicas (CSIC) |
| Repositório: | DIGITAL.CSIC. Repositorio Institucional del CSIC |
| OAI Identifier: | oai:digital.csic.es:10261/348440 |
| Acesso em linha: | http://hdl.handle.net/10261/348440 |
| Access Level: | Acceso aberto |
| Palavra-chave: | Holozoa Animal RNA editing Adar A-to-I editing Evolution Sense-antisense Recoding editing Neural system Cytoskeleton |
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On the origin and evolution of RNA editing in metazoansZhang, PeiZhu, YuanzhenGuo, QunfeiLi, JiZhan, XiaoyuYu, HaoXie, NianxiaTan, HuishuangLundholm, NinaGarcia-Cuetos, LydiaMartin, Michael D.Antó, MeritxellSu, Yi-HsienRuiz-Trillo, IñakiMartindale, Mark Q.Yu, Jr-KaiGilbert, M. Thomas P.Zhang, GuojieHolozoaAnimalRNA editingAdarA-to-I editingEvolutionSense-antisenseRecoding editingNeural systemCytoskeleton© 2023 The Author(s). This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).[Summary] Extensive adenosine-to-inosine (A-to-I) editing of nuclear-transcribed mRNAs is the hallmark of metazoan transcriptional regulation. Here, by profiling the RNA editomes of 22 species that cover major groups of Holozoa, we provide substantial evidence supporting A-to-I mRNA editing as a regulatory innovation originating in the last common ancestor of extant metazoans. This ancient biochemistry process is preserved in most extant metazoan phyla and primarily targets endogenous double-stranded RNA (dsRNA) formed by evolutionarily young repeats. We also find intermolecular pairing of sense-antisense transcripts as an important mechanism for forming dsRNA substrates for A-to-I editing in some but not all lineages. Likewise, recoding editing is rarely shared across lineages but preferentially targets genes involved in neural and cytoskeleton systems in bilaterians. We conclude that metazoan A-to-I editing might first emerge as a safeguard mechanism against repeat-derived dsRNA and was later co-opted into diverse biological processes due to its mutagenic nature.This work was supported by the National Natural Science Foundation of China (nos. 31501057 to Q.L. and 31970573 to G.Z.); a Villum Investigator grant (no. 25900) from The Villum Foundation to G.Z.; a European Research Council Consolidator Grant (no. ERC-2012-Co-616960) to I.R.-T.; the Academia Sinica intramural funds to J.-K.Y.; and grants from the National Science and Technology Council, Taiwan (nos. 110-2311-B-001-031-MY3 to Y.H.S. and 105-2628-B-001-003-MY3 and 108-2311-B-001-035-MY3 to J.-K.Y.).Peer reviewedCell PressNational Natural Science Foundation of ChinaVillum FondenEuropean Research CouncilAcademia Sinica (Taiwan)National Science and Technology Council (Taiwan)Ruiz-Trillo, Iñaki [0000-0001-6547-5304]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/348440reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Ingléshttps://doi.org/10.1016/j.celrep.2023.112112Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3484402026-05-22T06:33:51Z |
| dc.title.none.fl_str_mv |
On the origin and evolution of RNA editing in metazoans |
| title |
On the origin and evolution of RNA editing in metazoans |
| spellingShingle |
On the origin and evolution of RNA editing in metazoans Zhang, Pei Holozoa Animal RNA editing Adar A-to-I editing Evolution Sense-antisense Recoding editing Neural system Cytoskeleton |
| title_short |
On the origin and evolution of RNA editing in metazoans |
| title_full |
On the origin and evolution of RNA editing in metazoans |
| title_fullStr |
On the origin and evolution of RNA editing in metazoans |
| title_full_unstemmed |
On the origin and evolution of RNA editing in metazoans |
| title_sort |
On the origin and evolution of RNA editing in metazoans |
| dc.creator.none.fl_str_mv |
Zhang, Pei Zhu, Yuanzhen Guo, Qunfei Li, Ji Zhan, Xiaoyu Yu, Hao Xie, Nianxia Tan, Huishuang Lundholm, Nina Garcia-Cuetos, Lydia Martin, Michael D. Antó, Meritxell Su, Yi-Hsien Ruiz-Trillo, Iñaki Martindale, Mark Q. Yu, Jr-Kai Gilbert, M. Thomas P. Zhang, Guojie |
| author |
Zhang, Pei |
| author_facet |
Zhang, Pei Zhu, Yuanzhen Guo, Qunfei Li, Ji Zhan, Xiaoyu Yu, Hao Xie, Nianxia Tan, Huishuang Lundholm, Nina Garcia-Cuetos, Lydia Martin, Michael D. Antó, Meritxell Su, Yi-Hsien Ruiz-Trillo, Iñaki Martindale, Mark Q. Yu, Jr-Kai Gilbert, M. Thomas P. Zhang, Guojie |
| author_role |
author |
| author2 |
Zhu, Yuanzhen Guo, Qunfei Li, Ji Zhan, Xiaoyu Yu, Hao Xie, Nianxia Tan, Huishuang Lundholm, Nina Garcia-Cuetos, Lydia Martin, Michael D. Antó, Meritxell Su, Yi-Hsien Ruiz-Trillo, Iñaki Martindale, Mark Q. Yu, Jr-Kai Gilbert, M. Thomas P. Zhang, Guojie |
| author2_role |
author author author author author author author author author author author author author author author author author |
| dc.contributor.none.fl_str_mv |
National Natural Science Foundation of China Villum Fonden European Research Council Academia Sinica (Taiwan) National Science and Technology Council (Taiwan) Ruiz-Trillo, Iñaki [0000-0001-6547-5304] Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72] |
| dc.subject.none.fl_str_mv |
Holozoa Animal RNA editing Adar A-to-I editing Evolution Sense-antisense Recoding editing Neural system Cytoskeleton |
| topic |
Holozoa Animal RNA editing Adar A-to-I editing Evolution Sense-antisense Recoding editing Neural system Cytoskeleton |
| description |
© 2023 The Author(s). This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). |
| publishDate |
2023 |
| dc.date.none.fl_str_mv |
2023 2024 2024 |
| dc.type.none.fl_str_mv |
info:eu-repo/semantics/article http://purl.org/coar/resource_type/c_6501 Publisher's version info:eu-repo/semantics/publishedVersion |
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article |
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publishedVersion |
| dc.identifier.none.fl_str_mv |
http://hdl.handle.net/10261/348440 |
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http://hdl.handle.net/10261/348440 |
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Inglés |
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Inglés |
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https://doi.org/10.1016/j.celrep.2023.112112 Sí |
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info:eu-repo/semantics/openAccess |
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openAccess |
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application/pdf |
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Cell Press |
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Cell Press |
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reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC instname:Consejo Superior de Investigaciones Científicas (CSIC) |
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Consejo Superior de Investigaciones Científicas (CSIC) |
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DIGITAL.CSIC. Repositorio Institucional del CSIC |
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DIGITAL.CSIC. Repositorio Institucional del CSIC |
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