Developmental mRNA m5C landscape and regulatory innovations of massive m5C modification of maternal mRNAs in animals

Jianheng Liu, Tao Huang, Wanying Chen, Chenhui Ding, Tianxuan Zhao, Xueni Zhao, Bing Cai, Yusen Zhang, Song Li, Ling Zhang, Maoguang Xue, Xiuju He, Wanzhong Ge (), Canquan Zhou (), Yanwen Xu () and Rui Zhang ()
Additional contact information
Jianheng Liu: Sun Yat-Sen University
Tao Huang: Sun Yat-Sen University
Wanying Chen: Sun Yat-Sen University
Chenhui Ding: Sun Yat-Sen University
Tianxuan Zhao: Sun Yat-Sen University
Xueni Zhao: Sun Yat-Sen University
Bing Cai: Sun Yat-Sen University
Yusen Zhang: Sun Yat-Sen University
Song Li: Sun Yat-Sen University
Ling Zhang: Sun Yat-Sen University
Maoguang Xue: Zhejiang University School of Medicine
Xiuju He: Sun Yat-Sen University
Wanzhong Ge: Zhejiang University School of Medicine
Canquan Zhou: Sun Yat-Sen University
Yanwen Xu: Sun Yat-Sen University
Rui Zhang: Sun Yat-Sen University

Nature Communications, 2022, vol. 13, issue 1, 1-13

Abstract: Abstract m5C is one of the longest-known RNA modifications, however, its developmental dynamics, functions, and evolution in mRNAs remain largely unknown. Here, we generate quantitative mRNA m5C maps at different stages of development in 6 vertebrate and invertebrate species and find convergent and unexpected massive methylation of maternal mRNAs mediated by NSUN2 and NSUN6. Using Drosophila as a model, we reveal that embryos lacking maternal mRNA m5C undergo cell cycle delays and fail to timely initiate maternal-to-zygotic transition, implying the functional importance of maternal mRNA m5C. From invertebrates to the lineage leading to humans, two waves of m5C regulatory innovations are observed: higher animals gain cis-directed NSUN2-mediated m5C sites at the 5' end of the mRNAs, accompanied by the emergence of more structured 5'UTR regions; humans gain thousands of trans-directed NSUN6-mediated m5C sites enriched in genes regulating the mitotic cell cycle. Collectively, our studies highlight the existence and regulatory innovations of a mechanism of early embryonic development and provide key resources for elucidating the role of mRNA m5C in biology and disease.

Date: 2022
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Persistent link: https://EconPapers.repec.org/RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30210-0

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DOI: 10.1038/s41467-022-30210-0

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