On the origin and evolution of RNA editing in metazoans

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  • Pei Zhang
  • Yuanzhen Zhu
  • Qunfei Guo
  • Ji Li
  • Xiaoyu Zhan
  • Hao Yu
  • Nianxia Xie
  • Huishuang Tan
  • Lundholm, Nina
  • Lydia Garcia-Cuetos
  • Michael D. Martin
  • Meritxell Antó Subirats
  • Yi-Hsien Su
  • Iñaki Ruiz-Trillo
  • Mark Q. Martindale
  • Jr-Kai Yu
  • Gilbert, Tom
  • KU, thw266
  • Qiye Li

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.

TidsskriftCell Reports
Udgave nummer2
Antal sider22
StatusUdgivet - 2023

Bibliografisk note

Funding Information:
We thank Nicole King for providing the frozen stocks of S. rosetta and M. brevicollis and the protocols for starting and maintaining the cultures; Bernard Degnan and Kathrein E. Roper for providing the biopsies of A. queenslandica; Leo W. Buss for providing the starter culture of T. adhaerens and the protocol for maintaining the culture; Robert E. Steele for providing the H. vulgaris samples; Ulrich Technau for providing the N. vectensis samples; Xiaotong Wang for providing the C. gigas samples; Qi Zhou for providing the D. melanogaster and D. simulans samples; Bo Dong for providing the C. savignyi samples; and Changwei Shao for providing the D. rerio samples. This work was supported by the National Natural Science Foundation of China (nos. 31501057 to Q.L. and 31970573 to G.Z.); a Villum Investigator grant (no. 25900 ) from The Villum Foundation to G.Z.; a European Research Council Consolidator Grant (no. ERC-2012-Co-616960 ) to I.R.-T.; the Academia Sinica intramural funds to J.-K.Y.; and grants from the National Science and Technology Council , Taiwan (nos. 110-2311-B-001-031-MY3 to Y.H.S. and 105-2628-B-001-003-MY3 and 108-2311-B-001-035-MY3 to J.-K.Y.).

Publisher Copyright:
© 2023 The Author(s)

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