Rare horizontal transmission does not hide long-term inheritance of SINE highly conserved domains in the metazoan evolution

Abstract

Transposable elements (TEs) are self-replicating, mobile DNA sequences which constitute a significant fraction of eukaryotic genomes. They are generally considered selfish DNA, as their replication and random insertion may have deleterious effects on genome functionalities, although some beneficial effects and evolutionary potential have been recognized. Short interspersed elements (SINEs) are non-autonomous TEs with a modular structure: a small RNA-related head, a body, and a long interspersed element-related tail. Despite their high turnover rate and de novo emergence, the body may retain highly conserved domains (HCDs) shared among divergent SINE families: in metazoans, at least nine HCD-SINEs have been recognized. Data mining on public molecular databases allowed the retrieval of 16 new HCD-SINE families from cnidarian, molluscs, arthropods, and vertebrates. Tracking the ancestry of HCDs on the metazoan phylogeny revealed that some of them date back to the Radiata–Bilateria split. Moreover, phylogenetic and age versus divergence analyses of the most ancient HCDs suggested that long-term vertical inheritance is the rule, with few horizontal transfer events. We suggest that the evolutionary conservation of HCDs may be linked to their potential to serve as recombination hotspots. This indirectly affects host genomes by maintaining active and diverse SINE lineages, whose insertions may impact (either positively or negatively) on the evolution of the genome.

The conserved 3′ Angio‐domain defines a superfamily of short interspersed nuclear elements (SINEs) in higher plants

“…In particular, incomplete lineage sorting may have led to differences in the SINE populations of related species (Shedlock and Okada, ; Shedlock et al , ; Ray et al , ). This is in accordance with the suggested vertical transmission for the widespread Au SINE in plants and highly conserved SINE domains in animals (Fawcett, ; Luchetti and Mantovani, ). Indeed, a group of 13 Angio‐SINE families shares similarity over their full length and occurs across the wide phylogenetic range of the Angio‐SINEs from the most basal Ranunculales order to evolutionary young rosids and asterids.…”

“…So far, the Au SINE family is the only plant SINE family with a wide taxonomic distribution across distantly related plant families (Yasui et al , ; Fawcett et al , ; Fawcett, ). In contrast to plants, in animal genomes detailed studies on structural relationships between SINE families facilitated their assignment to superfamilies sharing central domains across a wide species range (Luchetti and Mantovani, ). Animal SINE domains with lengths between 30 bp and more than 100 bp have been proposed such as CORE (Gilbert and Labuda, ), V (Ogiwara et al , ), Deu (Nishihara et al , ), and Meta/MESC (Matetovici et al , ; Nishihara et al , ).…”

Editorial The evolutionary consequences of selfish genetic elements

“… Luchetti and Mantovani (2016) investigate the conservation of features across distantly related taxa in one type of transposable element, SINEs (short interspersed nuclear elements). SINE structure includes the head and tail, which carry the key functional components that allow the SINE to jump to new locations, separated by a body domain in between.…”

“…Phylogenetic analysis of this larger dataset strongly contradicts the horizontal transmission theory. Instead, Luchetti and Mantovani (2016) suggest the current distribution of HCDs across the tree of life is mainly the result of vertical transmission—meaning that some HCDs have been conserved reliably in vastly different organisms, for 850 million years. This means that HCDs, despite being part of a selfish, manipulative and damaging genetic element, and moreover being a part of that element that apparently has no function, have nevertheless persisted for as long as many of the fundamental genes that are vital to the biochemistry of most eukaryotic life.…”

“…It is certain that vast numbers of undiscovered selfish elements exist, most functioning in species that have never been screened for such conflicts. Others may be inactive, representing historical conflicts, as seen in many of the transposable elements discussed by Luchetti and Mantovani (2016) . Even systems that have been studied intensively for decades, such as the t haplotype in mice, continue to surprise us with novel discoveries, differences between strains, and controversies ( Auclair et al 2013 ; Sutter and Lindholm 2016 ).…”