Evolutionary dynamics of the LTR retrotransposons roo and rooA inferred from twelve complete Drosophila genomes

Abstract

BackgroundRoo is the most abundant retrotransposon in the fruit fly Drosophila melanogaster. Its evolutionary origins and dynamics are thus of special interest for understanding the evolutionary history of Drosophila genome organization. We here study the phylogenetic distribution and evolution of roo, and its highly diverged relative rooA in 12 completely sequenced genomes of the genus Drosophila.ResultsWe identify a total of 164 roo copies, 57 of which were previously unidentified copies that occur in 9 of the 12 genomes. Additionally we find 66 rooA copies in four genomes and remnants of this element in two additional genomes. We further increased the number of elements by searching for individual roo/rooA sequence domains. Most of our roo and rooA elements have been recently inserted. Most elements within a genome are highly similar. A comparison of the phylogenetic tree of our roo and rooA elements shows that the split between roo and rooA took place early in Drosophila evolution. Furthermore there is one incongruency between the species tree and the phylogenetic tree of the roo element. This incongruency regards the placement of elements from D. mojavensis, which are more closely related to D. melanogaster than elements from D. willistoni.ConclusionWithin genomes, the evolutionary dynamics of roo and rooA range from recent transpositional activity to slow decay and extinction. Among genomes, the balance of phylogenetic evidence, sequence divergence distribution, and the occurrence of solo-LTR elements suggests an origin of roo/rooA within the Drosophila clade. We discuss the possibility of a horizontal gene transfer of roo within this clade.

Unique transposon landscapes are pervasive acrossDrosophila melanogastergenomes

“…However, in all the DGRP strains, the roo retrotransposon stands out as the sole TE family with large numbers of novel insertions and high proportions of piRNAs directed against it. Although we do not have a mechanistic explanation for roo's exceptionally high number of new insertions and high levels of roo piRNAs in DGRP flies, this result may be related to roo's high transposition rate ( 73 , 74 ) and possible horizontal transfer of roo between different Drosophilid species ( 75 ).…”

Adaptive evolution of an essential telomere protein restricts telomeric retrotransposons

“…Dynamic telomeric retrotransposon evolution across Drosophila challenges the textbook view of these retrotransposons as obedient telomere elongation factors that, after an ancient domestication event, serve only the host’s interests ( Pardue and DeBaryshe, 2008 ). Instead, Drosophila telomeric retrotransposons evolve rapidly, reminiscent of classic ‘undomesticated’ selfish mobile elements that parasitize host genomes to elevate copy number ( de la Chaux and Wagner, 2009 ; Dias et al, 2015 ; Yang and Barbash, 2008 ).…”

Phylogeny of the GenusDrosophila

“…Transposable and other repetitive elements, each of which can be major determinants of genome size, have also been studied using the whole-genome approach. The evolutionary dynamics of the hAT transposable element ( de Freitas Ortiz and Loreto 2009 ; de Freitas Ortiz et al 2010 ), LTR retrotransposons roo and rooA ( de la Chaux and Wagner 2009 ), and DINE-1 transposable elements ( Yang and Barbash 2008 ) have been examined. In addition, amino acid repeats and microRNAs have been studied in genomes across the genus Drosophila ( Huntley and Clark 2007 ; Stark et al 2007a ).…”