RUDI, a short interspersed element of the V-SINE superfamily widespread in molluscan genomes

Abstract

Short interspersed elements (SINEs) are non-autonomous retrotransposons that are widespread in eukaryotic genomes. They exhibit a chimeric sequence structure consisting of a small RNA-related head, an anonymous body and an AT-rich tail. Although their turnover and de novo emergence is rapid, some SINE elements found in distantly related species retain similarity in certain core segments (or highly conserved domains, HCD). We have characterized a new SINE element named RUDI in the bivalve molluscs Ruditapes decussatus and R. philippinarum and found this element to be widely distributed in the genomes of a number of mollusc species. An unexpected structural feature of RUDI is the HCD domain type V, which was first found in non-amniote vertebrate SINEs and in the SINE from one cnidarian species. In addition to the V domain, the overall sequence conservation pattern of RUDI elements resembles that found in ancient AmnSINE (~310 Myr old) and Au SINE (~320 Myr old) families, suggesting that RUDI might be among the most ancient SINE families. Sequence conservation suggests a monophyletic origin of RUDI. Nucleotide variability and phylogenetic analyses suggest long-term vertical inheritance combined with at least one horizontal transfer event as the most parsimonious explanation for the observed taxonomic distribution.

Adjacent sequences disclose potential for intra-genomic dispersal of satellite DNA repeats and suggest a complex network with transposable elements

“…Fragment D12 (Fig. 1b) harbors one complete DTHS3 monomer which has been split by the insertion of a full-length copy of the SINE element RUDI [44]. Although it was previously reported that RUDI regularly forms TSD sequences upon insertion, they were not found in this case.…”

“…TE-related sequences mostly appear as short segments (44–192 bp) of moderate similarity (between 66% and 84%) to DNA transposons and/or LTR-retrotransposons. An exception is the recently characterized short interspersed element (SINE) named RUDI [44], present as a complete copy in D12. In addition, a search for uncharacterized repeated elements by comparing all sequenced fragments revealed two putative MITEs in D. trunculus , DTCM1 and DTCM2, preliminarily classified based on terminal inverted repeats and target site duplication (TSD).…”

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

“…We therefore propose to rename it as the “Cega” (cephalopod + gastropod) domain. Overall, our study enables a wider and more complete picture of HCD distribution than before ( Gilbert and Labuda 1999 , 2000 ; Ogiwara et al 2002 ; Nishihara et al 2006 , 2016 ; Akasaki et al 2010 ; Piskurek and Jackson 2011 ; Luchetti and Mantovani 2013a ; Luchetti et al 2016 ; Matetovici et al 2016 ).…”

“…Few examples of SINE horizontal transfer have yet been suggested: the SmaI family in coregonid and salmonid fishes ( Hamada et al 1997 ), a SINE shared by reptiles and mammals ( Piskurek and Okada 2007 ), and a RUDI subfamily between distantly related bivalve species ( Luchetti et al 2016 ). We found that Nin and V domain divergence showed a positive correlation with host species split ages, with few deviations suggesting horizontal transfers and/or paralogous lineage comparisons.…”

“…CORE domain dataset: MIR3 ( H. sapiens ), MON1 ( Ornithorhynchus anatinus ), CoeSINE3 ( Latimeria chalumnae ), MIR-Xt ( Xenopus tropicalis ), Bf1SINE1 ( B. floridae ), SINE2-4c_SP ( S. purpuratus ), OR2 ( Octopus vulgaris ); moreover, recently found elements BivaCORE-SINE1 ( Ruditapes decussatus ) and BivaCORE-SINE2 ( Mizuhopecten yessoensis ) have been added ( Nishihara et al 2016 ). The V domain dataset consisted of Dana ( D. rerio ), SINE2-1_XT ( X. tropicalis ), SINE2-1_NV ( N. vectensis ), and SINE2-2_Adi ( Adineta vaga ) and 5 RUDI V-SINEs from Haliotis discus (Gastropoda), Ruditapes philippinarum , Tegillarca granosa , Yoldia limatula (Bivalvia), and Neomenia megatrapezata (Solenogastres) ( Luchetti et al 2016 ). Finally, we also considered the V domain contained in the H. sapiens MER6 DNA transposon ( Smit and Riggs 1996 ).…”