On the origin and evolution of RNA editing in metazoans

Research output: Contribution to journal › Journal article › Research › peer-review

Standard

On the origin and evolution of RNA editing in metazoans. / Zhang, Pei; Zhu, Yuanzhen; Guo, Qunfei; Li, Ji; Zhan, Xiaoyu; Yu, Hao; Xie, Nianxia; Tan, Huishuang; Lundholm, Nina; Garcia-Cuetos, Lydia; Martin, Michael D.; Subirats, Meritxell Antó; Su, Yi-Hsien; Ruiz-Trillo, Iñaki; Martindale, Mark Q.; Yu, Jr-Kai; Gilbert, M. Thomas P.; Zhang, Guojie; Li, Qiye.

In: Cell Reports, Vol. 42, No. 2, 112112, 2023.

Research output: Contribution to journal › Journal article › Research › peer-review

Harvard

Zhang, P, Zhu, Y, Guo, Q, Li, J, Zhan, X, Yu, H, Xie, N, Tan, H, Lundholm, N, Garcia-Cuetos, L, Martin, MD, Subirats, MA, Su, Y-H, Ruiz-Trillo, I, Martindale, MQ, Yu, J-K, Gilbert, MTP, Zhang, G & Li, Q 2023, 'On the origin and evolution of RNA editing in metazoans', Cell Reports, vol. 42, no. 2, 112112. https://doi.org/10.1016/j.celrep.2023.112112

APA

Zhang, P., Zhu, Y., Guo, Q., Li, J., Zhan, X., Yu, H., Xie, N., Tan, H., Lundholm, N., Garcia-Cuetos, L., Martin, M. D., Subirats, M. A., Su, Y-H., Ruiz-Trillo, I., Martindale, M. Q., Yu, J-K., Gilbert, M. T. P., Zhang, G., & Li, Q. (2023). On the origin and evolution of RNA editing in metazoans. Cell Reports, 42(2), [112112]. https://doi.org/10.1016/j.celrep.2023.112112

Vancouver

Zhang P, Zhu Y, Guo Q, Li J, Zhan X, Yu H et al. On the origin and evolution of RNA editing in metazoans. Cell Reports. 2023;42(2). 112112. https://doi.org/10.1016/j.celrep.2023.112112

Author

Zhang, Pei ; Zhu, Yuanzhen ; Guo, Qunfei ; Li, Ji ; Zhan, Xiaoyu ; Yu, Hao ; Xie, Nianxia ; Tan, Huishuang ; Lundholm, Nina ; Garcia-Cuetos, Lydia ; Martin, Michael D. ; Subirats, Meritxell Antó ; Su, Yi-Hsien ; Ruiz-Trillo, Iñaki ; Martindale, Mark Q. ; Yu, Jr-Kai ; Gilbert, M. Thomas P. ; Zhang, Guojie ; Li, Qiye. / On the origin and evolution of RNA editing in metazoans. In: Cell Reports. 2023 ; Vol. 42, No. 2.

Bibtex

@article{3c0f420bf62d48c3b6aa64c76767c252,

title = "On the origin and evolution of RNA editing in metazoans",

abstract = "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.",

keywords = "A-to-I editing, Adar, animal, CP: Molecular biology, cytoskeleton, evolution, Holozoa, neural system, recoding editing, RNA editing, sense-antisense",

author = "Pei Zhang and Yuanzhen Zhu and Qunfei Guo and Ji Li and Xiaoyu Zhan and Hao Yu and Nianxia Xie and Huishuang Tan and Nina Lundholm and Lydia Garcia-Cuetos and Martin, {Michael D.} and Subirats, {Meritxell Ant{\'o}} and Yi-Hsien Su and I{\~n}aki Ruiz-Trillo and Martindale, {Mark Q.} and Jr-Kai Yu and Gilbert, {M. Thomas P.} and Guojie Zhang and Qiye Li",

note = "Publisher Copyright: {\textcopyright} 2023 The Author(s)",

year = "2023",

doi = "10.1016/j.celrep.2023.112112",

language = "English",

volume = "42",

journal = "Cell Reports",

issn = "2211-1247",

publisher = "Cell Press",

number = "2",

}

RIS

TY - JOUR

T1 - On the origin and evolution of RNA editing in metazoans

AU - Zhang, Pei

AU - Zhu, Yuanzhen

AU - Guo, Qunfei

AU - Li, Ji

AU - Zhan, Xiaoyu

AU - Yu, Hao

AU - Xie, Nianxia

AU - Tan, Huishuang

AU - Lundholm, Nina

AU - Garcia-Cuetos, Lydia

AU - Martin, Michael D.

AU - Subirats, Meritxell Antó

AU - Su, Yi-Hsien

AU - Ruiz-Trillo, Iñaki

AU - Martindale, Mark Q.

AU - Yu, Jr-Kai

AU - Gilbert, M. Thomas P.

AU - Zhang, Guojie

AU - Li, Qiye

PY - 2023

Y1 - 2023

N2 - 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.

AB - 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.

KW - A-to-I editing

KW - Adar

KW - animal

KW - CP: Molecular biology

KW - cytoskeleton

KW - evolution

KW - Holozoa

KW - neural system

KW - recoding editing

KW - RNA editing

KW - sense-antisense

U2 - 10.1016/j.celrep.2023.112112

DO - 10.1016/j.celrep.2023.112112

M3 - Journal article

C2 - 36795564

AN - SCOPUS:85148018309

VL - 42

JO - Cell Reports

JF - Cell Reports

SN - 2211-1247

IS - 2

M1 - 112112

ER -

ID: 337577047

Natural History Museum of Denmark