Evolution of Gene Structural Complexity: An Alternative-Splicing-Based Model Accounts for Intron-Containing Retrogenes  

Abstract

The structure of eukaryotic genes evolves extensively by intron loss or gain. Previous studies have revealed two models for gene structure evolution through the loss of introns: RNA-based gene conversion, dubbed the Fink model and retroposition model. However, retrogenes that experienced both intron loss and intron-retaining events have been ignored; evolutionary processes responsible for the variation in complex exon-intron structure were unknown. We detected hundreds of retroduplicationderived genes in human (Homo sapiens), fly (Drosophila melanogaster), rice (Oryza sativa), and Arabidopsis (Arabidopsis thaliana) and categorized them either as duplicated genes that have all introns lost or as duplicated genes that have at least lost one and retained one intron compared with the parental copy (intron-retaining [IR] type). Our new model attributes intron retention alternative splicing to the generation of these IR-type gene pairs. We presented 25 parental genes that have an intron retention isoform and have retained introns in the same locations in the IR-type duplicate genes, which directly support our hypothesis. Our alternative-splicing-based model in conjunction with the retroposition and Fink models can explain the IR-type gene observed. We discovered a greater percentage of IR-type genes in plants than in animals, which may be due to the abundance of intron retention cases in plants. Given the prevalence of intron retention in plants, this new model gives a support that plant genomes have very complex gene structures.

LINE-1-like retrotransposons contribute to RNA-based gene duplication in dicots

“…Interestingly, this retroCNV encodes one intron inherited from its parental gene ( Supplementary Fig. S2C ), which is consistent with pervasive intron retention events in plants due to alternative splicing 24 25 . In contrast, no LTR retrotransposons were associated with the other three retroCNVs.…”

Functional divergence of diterpene syntheses in the medicinal plant Salvia miltiorrhiza Bunge

“…Group II CPS/KSL genes, including SmCPS1, SmCPS3, SmCPS4, SmKSL1, OsCPS2, OsCPS4, OsKSL5, OsKSL6, OsKSL8, and OsKSL10, show diverged sequences and genomic architecture. In particular, intron loss (Zhang et al, 2014) relative to the conserved group I genes are often observed. For example, SmCPS1 has lost the 10th and 12th introns, SmCPS4 the 5th intron, and SmCPS3 the first four introns, while OsCPS2 has lost the 2nd and 3rd introns, and OsKSL5, OsKSL6, OsKSL8, and OsKSL10 all have lost the last intron (Supplemental Fig.…”

PlantRGDB: A Database of Plant Retrocopied Genes

“…In plants, hundreds of retrocopies have been found in Arabidopsis (Zhang et al 2005, Benovoy and Drouin 2006, Zhu et al 2016, rice (Wang et al 2006, Sakai et al 2011, Populus (Zhu et al 2009) and green algae (Jakalski et al 2016) via genome-wide analysis. These studies provide further support for the importance of retroposition in genome evolution (Zhang et al 2014).…”