Deep transcriptome profiling reveals limited conservation of A-to-I RNA editing in Xenopus

Background: Xenopus has served as a valuable model system for biomedical research over the past decades. Notably, ADAR was first detected in frog oocytes and embryos as an activity that unwinds RNA duplexes. However, the scope of A-to-I RNA editing by the ADAR enzymes in Xenopus remains underexplore...

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Main Authors: Nguyen, Tram Anh, Heng, Joel Jia Wei, Ng, Yan Ting, Sun, Rui, Fisher, Shira, Oguz, Gokce, Kaewsapsak, Pornchai, Xue, Shifeng, Reversade, Bruno, Ramasamy, Adaikalavan, Eisenberg, Eli, Tan, Meng How
Other Authors: School of Chemistry, Chemical Engineering and Biotechnology
Format: Article
Language:English
Published: 2024
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Online Access:https://hdl.handle.net/10356/173050
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Institution: Nanyang Technological University
Language: English
id sg-ntu-dr.10356-173050
record_format dspace
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Science::Biological sciences
RNA Editing
Xenopus
spellingShingle Science::Biological sciences
RNA Editing
Xenopus
Nguyen, Tram Anh
Heng, Joel Jia Wei
Ng, Yan Ting
Sun, Rui
Fisher, Shira
Oguz, Gokce
Kaewsapsak, Pornchai
Xue, Shifeng
Reversade, Bruno
Ramasamy, Adaikalavan
Eisenberg, Eli
Tan, Meng How
Deep transcriptome profiling reveals limited conservation of A-to-I RNA editing in Xenopus
description Background: Xenopus has served as a valuable model system for biomedical research over the past decades. Notably, ADAR was first detected in frog oocytes and embryos as an activity that unwinds RNA duplexes. However, the scope of A-to-I RNA editing by the ADAR enzymes in Xenopus remains underexplored. Results: Here, we identify millions of editing events in Xenopus with high accuracy and systematically map the editome across developmental stages, adult organs, and species. We report diverse spatiotemporal patterns of editing with deamination activity highest in early embryogenesis before zygotic genome activation and in the ovary. Strikingly, editing events are poorly conserved across different Xenopus species. Even sites that are detected in both X. laevis and X. tropicalis show largely divergent editing levels or developmental profiles. In protein-coding regions, only a small subset of sites that are found mostly in the brain are well conserved between frogs and mammals. Conclusions: Collectively, our work provides fresh insights into ADAR activity in vertebrates and suggest that species-specific editing may play a role in each animal’s unique physiology or environmental adaptation.
author2 School of Chemistry, Chemical Engineering and Biotechnology
author_facet School of Chemistry, Chemical Engineering and Biotechnology
Nguyen, Tram Anh
Heng, Joel Jia Wei
Ng, Yan Ting
Sun, Rui
Fisher, Shira
Oguz, Gokce
Kaewsapsak, Pornchai
Xue, Shifeng
Reversade, Bruno
Ramasamy, Adaikalavan
Eisenberg, Eli
Tan, Meng How
format Article
author Nguyen, Tram Anh
Heng, Joel Jia Wei
Ng, Yan Ting
Sun, Rui
Fisher, Shira
Oguz, Gokce
Kaewsapsak, Pornchai
Xue, Shifeng
Reversade, Bruno
Ramasamy, Adaikalavan
Eisenberg, Eli
Tan, Meng How
author_sort Nguyen, Tram Anh
title Deep transcriptome profiling reveals limited conservation of A-to-I RNA editing in Xenopus
title_short Deep transcriptome profiling reveals limited conservation of A-to-I RNA editing in Xenopus
title_full Deep transcriptome profiling reveals limited conservation of A-to-I RNA editing in Xenopus
title_fullStr Deep transcriptome profiling reveals limited conservation of A-to-I RNA editing in Xenopus
title_full_unstemmed Deep transcriptome profiling reveals limited conservation of A-to-I RNA editing in Xenopus
title_sort deep transcriptome profiling reveals limited conservation of a-to-i rna editing in xenopus
publishDate 2024
url https://hdl.handle.net/10356/173050
_version_ 1789483183178252288
spelling sg-ntu-dr.10356-1730502024-01-12T15:32:10Z Deep transcriptome profiling reveals limited conservation of A-to-I RNA editing in Xenopus Nguyen, Tram Anh Heng, Joel Jia Wei Ng, Yan Ting Sun, Rui Fisher, Shira Oguz, Gokce Kaewsapsak, Pornchai Xue, Shifeng Reversade, Bruno Ramasamy, Adaikalavan Eisenberg, Eli Tan, Meng How School of Chemistry, Chemical Engineering and Biotechnology School of Biological Sciences Genome Institute of Singapore, A*STAR HP-NTU Digital Manufacturing Corporate Lab Science::Biological sciences RNA Editing Xenopus Background: Xenopus has served as a valuable model system for biomedical research over the past decades. Notably, ADAR was first detected in frog oocytes and embryos as an activity that unwinds RNA duplexes. However, the scope of A-to-I RNA editing by the ADAR enzymes in Xenopus remains underexplored. Results: Here, we identify millions of editing events in Xenopus with high accuracy and systematically map the editome across developmental stages, adult organs, and species. We report diverse spatiotemporal patterns of editing with deamination activity highest in early embryogenesis before zygotic genome activation and in the ovary. Strikingly, editing events are poorly conserved across different Xenopus species. Even sites that are detected in both X. laevis and X. tropicalis show largely divergent editing levels or developmental profiles. In protein-coding regions, only a small subset of sites that are found mostly in the brain are well conserved between frogs and mammals. Conclusions: Collectively, our work provides fresh insights into ADAR activity in vertebrates and suggest that species-specific editing may play a role in each animal’s unique physiology or environmental adaptation. Economic Development Board (EDB) Ministry of Education (MOE) Nanyang Technological University National Research Foundation (NRF) Published version M.H.T. is supported by a National Research Foundation Singapore grant (NRF2017-NRF-ISF002-2673), a Ministry of Education Singapore grant (T2EP30222-0012), an EMBO Global Investigatorship, an ASPIRE League seed grant from Nanyang Technological University, core funds from the Genome Institute of Singapore, and funds for Final Year Project (FYP) from the School of Chemistry, Chemical Engineering and Biotechnology. E.E. is supported by Israel Science Foundation grants (2673/17 and 1945/18). J.W.J.H. is supported by a Ph.D. research scholarship from the School of Chemistry, Chemical Engineering and Biotechnology. Y.T.N. is supported under the Economic Development Board Industrial Postgraduate Programme (EDB-IPP). We also wish to acknowledge the funding support for this project from Nanyang Technological University under the URECA Undergraduate Research Programme. 2024-01-10T05:33:33Z 2024-01-10T05:33:33Z 2023 Journal Article Nguyen, T. A., Heng, J. J. W., Ng, Y. T., Sun, R., Fisher, S., Oguz, G., Kaewsapsak, P., Xue, S., Reversade, B., Ramasamy, A., Eisenberg, E. & Tan, M. H. (2023). Deep transcriptome profiling reveals limited conservation of A-to-I RNA editing in Xenopus. BMC Biology, 21(1), 251-. https://dx.doi.org/10.1186/s12915-023-01756-2 1741-7007 https://hdl.handle.net/10356/173050 10.1186/s12915-023-01756-2 37946231 2-s2.0-85176257394 1 21 251 en NRF2017-NRF-ISF002-2673 T2EP30222-0012 BMC Biology © The Author(s) 2023. Open Access. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. application/pdf