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

m 5 C 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 m 5 C maps at different stages of development in 6 vertebrate and invertebrate species and find convergent and unexp...

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Published inNature communications Vol. 13; no. 1; pp. 2484 - 13
Main Authors Liu, Jianheng, Huang, Tao, Chen, Wanying, Ding, Chenhui, Zhao, Tianxuan, Zhao, Xueni, Cai, Bing, Zhang, Yusen, Li, Song, Zhang, Ling, Xue, Maoguang, He, Xiuju, Ge, Wanzhong, Zhou, Canquan, Xu, Yanwen, Zhang, Rui
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 05.05.2022
Nature Publishing Group
Nature Portfolio
Subjects
38/70
45/91
5' Untranslated Regions
631/208/212/748
631/337/1645/2570
Animals
Cell cycle
Convergence
Developmental stages
Embryogenesis
Embryonic growth stage
Gene mapping
Humanities and Social Sciences
Innovations
Invertebrates
Methylation
mRNA
multidisciplinary
Science
Science (multidisciplinary)
Vertebrates
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Abstract m 5 C 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 m 5 C 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 m 5 C undergo cell cycle delays and fail to timely initiate maternal-to-zygotic transition, implying the functional importance of maternal mRNA m 5 C. From invertebrates to the lineage leading to humans, two waves of m 5 C regulatory innovations are observed: higher animals gain cis-directed NSUN2-mediated m 5 C 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 m 5 C 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 m 5 C in biology and disease. mRNAs are known to be decorated with m5C at a low-to-medium level. Here, the authors generate atlases of mRNA m5C during animal development in 6 species and identify convergent and unexpected massive methylation of maternal mRNAs by NSUN2 and NSUN6.
AbstractList 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.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.
m 5 C 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 m 5 C 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 m 5 C undergo cell cycle delays and fail to timely initiate maternal-to-zygotic transition, implying the functional importance of maternal mRNA m 5 C. From invertebrates to the lineage leading to humans, two waves of m 5 C regulatory innovations are observed: higher animals gain cis-directed NSUN2-mediated m 5 C 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 m 5 C 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 m 5 C in biology and disease. mRNAs are known to be decorated with m5C at a low-to-medium level. Here, the authors generate atlases of mRNA m5C during animal development in 6 species and identify convergent and unexpected massive methylation of maternal mRNAs by NSUN2 and NSUN6.
mRNAs are known to be decorated with m5C at a low-to-medium level. Here, the authors generate atlases of mRNA m5C during animal development in 6 species and identify convergent and unexpected massive methylation of maternal mRNAs by NSUN2 and NSUN6.
m 5 C 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 m 5 C 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 m 5 C undergo cell cycle delays and fail to timely initiate maternal-to-zygotic transition, implying the functional importance of maternal mRNA m 5 C. From invertebrates to the lineage leading to humans, two waves of m 5 C regulatory innovations are observed: higher animals gain cis-directed NSUN2-mediated m 5 C 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 m 5 C 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 m 5 C in biology and disease.
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.mRNAs are known to be decorated with m5C at a low-to-medium level. Here, the authors generate atlases of mRNA m5C during animal development in 6 species and identify convergent and unexpected massive methylation of maternal mRNAs by NSUN2 and NSUN6.
ArticleNumber 2484
Author Li, Song
Xu, Yanwen
Ge, Wanzhong
Xue, Maoguang
Zhao, Tianxuan
Huang, Tao
Liu, Jianheng
Zhou, Canquan
He, Xiuju
Chen, Wanying
Zhao, Xueni
Zhang, Yusen
Zhang, Rui
Ding, Chenhui
Zhang, Ling
Cai, Bing
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Snippet m 5 C is one of the longest-known RNA modifications, however, its developmental dynamics, functions, and evolution in mRNAs remain largely unknown. Here, we...
m5C is one of the longest-known RNA modifications, however, its developmental dynamics, functions, and evolution in mRNAs remain largely unknown. Here, we...
mRNAs are known to be decorated with m5C at a low-to-medium level. Here, the authors generate atlases of mRNA m5C during animal development in 6 species and...
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SubjectTerms 38/70
45/91
5' Untranslated Regions
631/208/212/748
631/337/1645/2570
Animals
Cell cycle
Convergence
Developmental stages
Embryogenesis
Embryonic growth stage
Gene mapping
Humanities and Social Sciences
Innovations
Invertebrates
Methylation
mRNA
multidisciplinary
Science
Science (multidisciplinary)
Vertebrates
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Title Developmental mRNA m5C landscape and regulatory innovations of massive m5C modification of maternal mRNAs in animals
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