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Evolutionary driving forces of A‐to‐I editing in metazoans

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Abstract Adenosine‐to‐inosine (A‐to‐I) RNA editing is an evolutionarily conserved mechanism that converts adenosines to inosines in metazoans' transcriptomes. However, the landscapes of editomes have considerably changed during evolution. Here, we review some of our current knowledge of A‐to‐I editing in the metazoan transcriptomes, focusing on the possible evolutionary driving forces underlying the editing events. First, we review the evolution of ADAR gene family in animals. Then, we summarize the recent advances in characterizing the editomes of various metazoan species. Next, we highlight several factors contributing to the interspecies differences in editomes, including variations in copy number and expression patterns of ADAR genes, the differences in genomic architectures and contents, and the differences in the efficacy of natural selection. After that, we review the possible diversifying and restorative effects of the editing (recoding) events that change the protein sequences. Finally, we discuss the possible convergent evolution of RNA editing in distantly related clades. This article is categorized under: RNA Evolution and Genomics > RNA and Ribonucleoprotein Evolution RNA Processing > RNA Editing and Modification
The preference of ADAR proteins and the functional impact of A‐to‐I editing. (a) Inosine (I) is structurally similar to guanosine (G). (b) ADAR preferentially binds dsRNA structures. (c) The 3‐mer motif recognized by ADAR in Drosophila (Duan et al., 2017). (d) A‐to‐I editing could lead to synonymous (not changing the amino acid) or recoding (nonsynonymous, changing the amino acid) events
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Convergent adaptation of recoding in honeybees and fruitflies (Duan et al., 2021). (a) The numbers of orthologous genes edited in the coding regions were significantly higher than random sampling the same numbers of genes, suggesting convergent evolution. (b) The auto‐recoding sites in Adar transcript were gained in fruitflies and bees independently (Duan et al., 2021). D. mel, Drosophila melanogaster; D. sim, Drosophila simulans; D. sec, Drosophila sechellia; D. ere, Drosophila erecta; A. mel, Apis mellifera; B. ter, Bombus terrestris. G, Gly; I, Ile; S, Ser; V, Val. The branch lengths in the phylogenetic tree are unscaled
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Two complementary theories explaining the observed high frequency and editing levels of recoding sites. (a) The diversifying theory assumes that editing increases the proteomic diversity, and the organisms that have both the edited and unedited molecules will have a higher fitness (Gommans et al., 2009). (b) The restorative theory posits that the A‐to‐I editing reverses the deleterious effect of a G‐to‐A DNA mutation, and that allows the G‐to‐A DNA mutation to accumulate at a high frequency or even become fixed in the population (Jiang & Zhang, 2019)
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A summary of the editing sites in 16 representative species. The divergence between species was retrieved from the TimeTree website (http://www.timetree.org/). The numbers of total editing sites and recoding sites were shown next to each species. The studies used for each species are: human (Picardi et al., 2017; Ramaswami & Li, 2014), macaque (An et al., 2019; Chen et al., 2014; Yang et al., 2015), mouse (Licht et al., 2019; Ramaswami & Li, 2014), pig (Wang et al., 2019), bumblebee (Porath et al., 2019), honeybee (Duan et al., 2021), ant (Li et al., 2014), and four cephalopods (Liscovitch‐Brauer et al., 2017). For the three Drosophila species, the numbers outside the parentheses refer to the sites identified by our own study (brain) (Duan et al., 2017). The numbers in the parentheses refer to the union of all sites reported to date: Drosophila melanogaster (Duan et al., 2017; Graveley et al., 2011; Ramaswami & Li, 2014; Rodriguez et al., 2012; St Laurent et al., 2013; Yu et al., 2016; Zhang et al., 2017), D. simulans (Duan et al., 2017; Yu et al., 2016; Zhang et al., 2017), and D. pseudoobscura (Duan et al., 2017; Yu et al., 2016; Zhang et al., 2017). In corals, the numbers of sites in eggs were reported by Porath et al. (2017). Eggs possessed the greatest number of sites. For cephalopod species, only editing sites in coding regions were reported
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Evolution of ADAR gene family. (a) Phylogenetic tree based on the protein sequences of ADAR, ADAD, and ADAT genes in 16 metazoan species (see Supplementary File 1 for the detailed methods). The Escherichia coli TadA was chosen as outgroup. (b) Domain architecture of ADAR, ADAD, and ADAT proteins of three representative metazoans: Homo sapiens, Drosophila melanogaster, and Caenorhabditis elegans. The E. coli TadA protein was presented as the ancestral state. Deaminase, the deaminase domain; DRBM, double‐stranded RNA binding domain; Z‐binding, Z‐DNA binding domain
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RNA Processing > RNA Editing and Modification
RNA Evolution and Genomics > RNA and Ribonucleoprotein Evolution

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