1. Adaptation of A-to-I RNA editing in Drosophila
- Author
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Duan, Yuange, Dou, Shengqian, Luo, Shiqi, Zhang, Hong, and Lu, Jian
- Subjects
Evolutionary Genetics ,Male ,RNA editing ,Protein Folding ,Adenosine ,Arthropoda ,Genome, Insect ,Glycobiology ,Gene Expression ,Research and Analysis Methods ,Biochemistry ,Synaptic Transmission ,Epigenesis, Genetic ,Model Organisms ,Species Specificity ,Invertebrate Genomics ,Genetics ,Animals ,Conserved Sequence ,Evolutionary Biology ,Nucleotides ,Drosophila Melanogaster ,Gene Expression Profiling ,Organisms ,Temperature ,Biology and Life Sciences ,Computational Biology ,Nucleosides ,Animal Models ,Genomics ,Genome Analysis ,Genomic Libraries ,Invertebrates ,Glycosylamines ,Inosine ,Insects ,Nucleic acids ,Experimental Organism Systems ,Animal Genomics ,Mutation ,RNA ,Drosophila ,Female ,Research Article - Abstract
Adenosine-to-inosine (A-to-I) editing is hypothesized to facilitate adaptive evolution by expanding proteomic diversity through an epigenetic approach. However, it is challenging to provide evidences to support this hypothesis at the whole editome level. In this study, we systematically characterized 2,114 A-to-I RNA editing sites in female and male brains of D. melanogaster, and nearly half of these sites had events evolutionarily conserved across Drosophila species. We detected strong signatures of positive selection on the nonsynonymous editing sites in Drosophila brains, and the beneficial editing sites were significantly enriched in genes related to chemical and electrical neurotransmission. The signal of adaptation was even more pronounced for the editing sites located in X chromosome or for those commonly observed across Drosophila species. We identified a set of gene candidates (termed “PSEB” genes) that had nonsynonymous editing events favored by natural selection. We presented evidence that editing preferentially increased mutation sequence space of evolutionarily conserved genes, which supported the adaptive evolution hypothesis of editing. We found prevalent nonsynonymous editing sites that were favored by natural selection in female and male adults from five strains of D. melanogaster. We showed that temperature played a more important role than gender effect in shaping the editing levels, although the effect of temperature is relatively weaker compared to that of species effect. We also explored the relevant factors that shape the selective patterns of the global editomes. Altogether we demonstrated that abundant nonsynonymous editing sites in Drosophila brains were adaptive and maintained by natural selection during evolution. Our results shed new light on the evolutionary principles and functional consequences of RNA editing., Author summary Adenosine-to-inosine (A-to-I) RNA editing is an evolutionarily conserved mechanism that alters RNA sequences at the co-transcriptional or post-transcriptional level. RNA editing is hypothesized to facilitate adaptation in that it expands the transcriptomic and proteomic diversity. However, evidence for adaptation of RNA editing at the whole editome level is still lacking. In this study we systematically identified A-to-I RNA editing sites in female and male brains of three Drosophila species at different temperatures. With evolutionary analysis from different perspectives, we provide lines of evidence to demonstrate that the nonsynonymous editing sites in Drosophila brains are generally adaptive. The signals of adaptation for the editing sites are significantly enriched in genes related to chemical and electrical neurotransmission. We show that the RNA editing events might interplay with gene expression plasticity in temperature stress responses. Furthermore, we demonstrated that the expression level of Adar, together with the expression profiles of a set of genes that have editing sites favored by natural selection, were important in shaping the overall selective patterns of the global editomes at different developmental stages (or tissues) of D. melanogaster. Altogether our results support the hypothesis that A-to-I editing provides a driving force for adaptive evolution in Drosophila from different aspects.
- Published
- 2017