Reading and writing of mRNA m6A modification orchestrate maternal-to-zygotic transition in mice

Abstract N6-methyladenosine (m6A) modification has been shown to regulate RNA metabolism. Here, we investigate m6A dynamics during maternal-to-zygotic transition (MZT) in mice through multi-omic analysis. Our results show that m6A can be maternally inherited or de novo gained after fertilization. In...

Full description

Bibliographic Details
Main Authors: Wencheng Zhu, Yufeng Ding, Juan Meng, Lei Gu, Wenjun Liu, Li Li, Hongyu Chen, Yining Wang, Ziyi Li, Chen Li, Yidi Sun, Zhen Liu
Format: Article
Language:English
Published: BMC 2023-04-01
Series:Genome Biology
Subjects:
Online Access:https://doi.org/10.1186/s13059-023-02918-9
_version_ 1797850017687404544
author Wencheng Zhu
Yufeng Ding
Juan Meng
Lei Gu
Wenjun Liu
Li Li
Hongyu Chen
Yining Wang
Ziyi Li
Chen Li
Yidi Sun
Zhen Liu
author_facet Wencheng Zhu
Yufeng Ding
Juan Meng
Lei Gu
Wenjun Liu
Li Li
Hongyu Chen
Yining Wang
Ziyi Li
Chen Li
Yidi Sun
Zhen Liu
author_sort Wencheng Zhu
collection DOAJ
description Abstract N6-methyladenosine (m6A) modification has been shown to regulate RNA metabolism. Here, we investigate m6A dynamics during maternal-to-zygotic transition (MZT) in mice through multi-omic analysis. Our results show that m6A can be maternally inherited or de novo gained after fertilization. Interestingly, m6A modification on maternal mRNAs not only correlates with mRNA degradation, but also maintains the stability of a small group of mRNAs thereby promoting their translation after fertilization. We identify Ythdc1 and Ythdf2 as key m6A readers for mouse preimplantation development. Our study reveals a key role of m6A mediated RNA metabolism during MZT in mammals.
first_indexed 2024-04-09T18:53:34Z
format Article
id doaj.art-2815cc0862a749eebd1438a1ac5ce677
institution Directory Open Access Journal
issn 1474-760X
language English
last_indexed 2024-04-09T18:53:34Z
publishDate 2023-04-01
publisher BMC
record_format Article
series Genome Biology
spelling doaj.art-2815cc0862a749eebd1438a1ac5ce6772023-04-09T11:17:45ZengBMCGenome Biology1474-760X2023-04-0124111610.1186/s13059-023-02918-9Reading and writing of mRNA m6A modification orchestrate maternal-to-zygotic transition in miceWencheng Zhu0Yufeng Ding1Juan Meng2Lei Gu3Wenjun Liu4Li Li5Hongyu Chen6Yining Wang7Ziyi Li8Chen Li9Yidi Sun10Zhen Liu11Institute of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, CAS Key Laboratory of Primate Neurobiology, State Key Laboratory of Neuroscience, Chinese Academy of SciencesInstitute of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, CAS Key Laboratory of Primate Neurobiology, State Key Laboratory of Neuroscience, Chinese Academy of SciencesInstitute of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, CAS Key Laboratory of Primate Neurobiology, State Key Laboratory of Neuroscience, Chinese Academy of SciencesCenter for Single-Cell Omics, School of Public Health, Shanghai Jiao Tong University School of MedicineInstitute of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, CAS Key Laboratory of Primate Neurobiology, State Key Laboratory of Neuroscience, Chinese Academy of SciencesInstitute of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, CAS Key Laboratory of Primate Neurobiology, State Key Laboratory of Neuroscience, Chinese Academy of SciencesInstitute of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, CAS Key Laboratory of Primate Neurobiology, State Key Laboratory of Neuroscience, Chinese Academy of SciencesInstitute of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, CAS Key Laboratory of Primate Neurobiology, State Key Laboratory of Neuroscience, Chinese Academy of SciencesShanghai Applied Protein Technology Co., Ltd.Center for Single-Cell Omics, School of Public Health, Shanghai Jiao Tong University School of MedicineInstitute of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, CAS Key Laboratory of Primate Neurobiology, State Key Laboratory of Neuroscience, Chinese Academy of SciencesInstitute of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, CAS Key Laboratory of Primate Neurobiology, State Key Laboratory of Neuroscience, Chinese Academy of SciencesAbstract N6-methyladenosine (m6A) modification has been shown to regulate RNA metabolism. Here, we investigate m6A dynamics during maternal-to-zygotic transition (MZT) in mice through multi-omic analysis. Our results show that m6A can be maternally inherited or de novo gained after fertilization. Interestingly, m6A modification on maternal mRNAs not only correlates with mRNA degradation, but also maintains the stability of a small group of mRNAs thereby promoting their translation after fertilization. We identify Ythdc1 and Ythdf2 as key m6A readers for mouse preimplantation development. Our study reveals a key role of m6A mediated RNA metabolism during MZT in mammals.https://doi.org/10.1186/s13059-023-02918-9m6A landscapeMulti-omicsMaternal-to-zygotic transitionYthdc1Ythdf2
spellingShingle Wencheng Zhu
Yufeng Ding
Juan Meng
Lei Gu
Wenjun Liu
Li Li
Hongyu Chen
Yining Wang
Ziyi Li
Chen Li
Yidi Sun
Zhen Liu
Reading and writing of mRNA m6A modification orchestrate maternal-to-zygotic transition in mice
Genome Biology
m6A landscape
Multi-omics
Maternal-to-zygotic transition
Ythdc1
Ythdf2
title Reading and writing of mRNA m6A modification orchestrate maternal-to-zygotic transition in mice
title_full Reading and writing of mRNA m6A modification orchestrate maternal-to-zygotic transition in mice
title_fullStr Reading and writing of mRNA m6A modification orchestrate maternal-to-zygotic transition in mice
title_full_unstemmed Reading and writing of mRNA m6A modification orchestrate maternal-to-zygotic transition in mice
title_short Reading and writing of mRNA m6A modification orchestrate maternal-to-zygotic transition in mice
title_sort reading and writing of mrna m6a modification orchestrate maternal to zygotic transition in mice
topic m6A landscape
Multi-omics
Maternal-to-zygotic transition
Ythdc1
Ythdf2
url https://doi.org/10.1186/s13059-023-02918-9
work_keys_str_mv AT wenchengzhu readingandwritingofmrnam6amodificationorchestratematernaltozygotictransitioninmice
AT yufengding readingandwritingofmrnam6amodificationorchestratematernaltozygotictransitioninmice
AT juanmeng readingandwritingofmrnam6amodificationorchestratematernaltozygotictransitioninmice
AT leigu readingandwritingofmrnam6amodificationorchestratematernaltozygotictransitioninmice
AT wenjunliu readingandwritingofmrnam6amodificationorchestratematernaltozygotictransitioninmice
AT lili readingandwritingofmrnam6amodificationorchestratematernaltozygotictransitioninmice
AT hongyuchen readingandwritingofmrnam6amodificationorchestratematernaltozygotictransitioninmice
AT yiningwang readingandwritingofmrnam6amodificationorchestratematernaltozygotictransitioninmice
AT ziyili readingandwritingofmrnam6amodificationorchestratematernaltozygotictransitioninmice
AT chenli readingandwritingofmrnam6amodificationorchestratematernaltozygotictransitioninmice
AT yidisun readingandwritingofmrnam6amodificationorchestratematernaltozygotictransitioninmice
AT zhenliu readingandwritingofmrnam6amodificationorchestratematernaltozygotictransitioninmice