Origin of exon skipping-rich transcriptomes in animals driven by evolution of gene architecture

Genome Biology
Xavier Grau-BovéManuel Irimia

Abstract

Alternative splicing, particularly through intron retention and exon skipping, is a major layer of pre-translational regulation in eukaryotes. While intron retention is believed to be the most prevalent mode across non-animal eukaryotes, animals have unusually high rates of exon skipping. However, when and how this high prevalence of exon skipping evolved is unknown. Since exon skipping can greatly expand proteomes, answering these questions sheds light on the evolution of higher organismal complexity in metazoans. We used RNA-seq data to quantify exon skipping and intron retention frequencies across 65 eukaryotic species, with particular focus on early branching animals and unicellular holozoans. We found that only bilaterians have significantly increased their exon skipping frequencies compared to all other eukaryotic groups. Unlike in other eukaryotes, however, exon skipping in nearly all animals, including non-bilaterians, is strongly enriched for frame-preserving sequences, suggesting that exon skipping involvement in proteome expansion predated the increase in frequency. We also identified architectural features consistently associated with higher exon skipping rates within all studied eukaryotic genomes. Remarkably, thes...Continue Reading

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Citations

Jan 26, 2020·Drug Metabolism and Disposition : the Biological Fate of Chemicals·Andrew J AnnaloraPatrick L Iversen
Aug 9, 2019·International Journal of Molecular Sciences·Shi-Yi ChenSong-Jia Lai
Aug 21, 2020·G3 : Genes - Genomes - Genetics·Manishi PandeySusan K Dutcher
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Jan 12, 2021·The Journal of Biological Chemistry·Jesse SundarVisvanathan Ramamurthy
Aug 15, 2021·Genome Biology·Evangelos D KarousisOliver Mühlemann
Aug 22, 2021·Genome Biology·Yamile MárquezManuel Irimia
Nov 25, 2021·Microbiology and Molecular Biology Reviews : MMBR·Máté VirághLászló G Nagy
Dec 11, 2021·Frontiers in Molecular Biosciences·Tülay KarakulakAbdullah Kahraman

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Methods Mentioned

BETA
RNA-seq

Software Mentioned

TREE
R MASS library
fitdistr
IQ
PIC
hmmsearch
Orthofinder
Bedtools
R mosaic
FASTX Toolkit

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