Retrotransposons evolution and impact on lncRNA and protein coding genes in pigs

Cai Chen,Klaus Wimmers,Dan Shen,Wei Wang,Jiude Mao,Yali Wang,Kui Li,Chengyi Song,Saisai Wang,Bo Gao,Xiaoyan Wang

doi:10.1186/s13100-019-0161-8

Abstract

BackgroundRetrotransposons are the major determinants of genome sizes and they have shaped both genes and genomes in mammalian organisms, but their overall activity, diversity, and evolution dynamics, particularly their impact on protein coding and lncRNA genes in pigs remain largely unknown.ResultsIn the present study, we performed de novo detection of retrotransposons in pigs by using multiple pipelines, four distinct families of pig-specific L1 s classified into 51 distinct subfamilies and representing four evolution models and three expansion waves of pig-specific SINEs represented by three distinct families were identified. ERVs were classified into 18 families and found two most “modern” subfamilies in the pig genome. The transposition activity of pig L1 was verified by experiment, the sense and antisense promoter activities of young L1 5′UTRs and ERV LTRs and expression profiles of young retrotransposons in multiple tissues and cell lines were also validated. Furthermore, retrotransposons had an extensive impact on lncRNA and protein coding genes at both the genomic and transcriptomic levels. Most protein coding and lncRNA (> 80%) genes contained retrotransposon insertions, and about half of protein coding genes (44.30%) and one-fourth (24.13%) of lncRNA genes contained the youngest retrotransposon insertions. Nearly half of protein coding genes (43.78%) could generate chimeric transcripts with retrotransposons. Significant distribution bias of retrotransposon composition, location, and orientation in lncRNA and protein coding genes, and their transcripts, were observed.ConclusionsIn the current study, we characterized the classification and evolution profile of retrotransposons in pigs, experimentally proved the transposition activity of the young pig L1 subfamily, characterized the sense and antisense expression profiles and promoter activities of young retrotransposons, and investigated their impact on lncRNA and protein coding genes by defining the mobilome landscapes at the genomic and transcriptomic levels. These findings help provide a better understanding of retrotransposon evolution in mammal and their impact on the genome and transcriptome.

Highlights

Retrotransposons are the major determinants of genome sizes and they have shaped both genes and genomes in mammalian organisms, but their overall activity, diversity, and evolution dynamics, their impact on protein coding and lncRNA genes in pigs remain largely unknown
Four distinct families of pig-specific L1 s representing four evolution models A total of 4154 L1 elements were identified by MGEScan-non-long terminal repeats (LTRs), and they were aligned against the pig genome by Blat with an extension of 2500 bp of 5′ UTR and 200 bp of 3′UTR to get the full lengths of the elements
We found that the retrotransposition activity of pig and human L1 s were cell-specific; weak retrotransposition activity of pig and human chimeric L1 was observed in porcine kidney (PK15) cells, whereas human L1 did not work in the PK15 cell line (Fig. 3b and c)

Summary

Introduction

Retrotransposons are the major determinants of genome sizes and they have shaped both genes and genomes in mammalian organisms, but their overall activity, diversity, and evolution dynamics, their impact on protein coding and lncRNA genes in pigs remain largely unknown. Transposable elements (TEs), referred to as the mobilome, are DNA sequences that have the ability to integrate into the genome at a new site within their cell of origin. They can be divided into retrotransposons and DNA transposons based on their diverse structures and. TEs contribute substantially to the evolution of the genome at the DNA level, and they can undergo “molecular domestication” [10, 11]; at least 50 genes have been domesticated from mobile elements in the human genome [12]. TEs tend to enrich in the lncRNAs of human, mice, and zebrafish [26, 27], and retrotransposons make a strong contribution to lncRNA evolution, structure, and function in mammalian organisms [28]

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Conclusion