Molecular evolution of piggyBac superfamily: from selfishness to domestication

Abstract

The piggyBac transposable element was originally isolated from the cabbage looper moth, Trichoplusia ni, in the 1980s. Despite its early discovery and specificity compared to the other Class II elements, the diversity and evolution of this superfamily have been only partially analyzed. Two main types of elements can be distinguished: the piggyBac-like elements (PBLE) with terminal inverted repeats, untranslated region, and an open reading frame encoding a transposase, and the piggyBac-derived sequences (PGBD), containing a sequence derived from a piggyBac transposase, and which correspond to domesticated elements. To define the distribution, their structural diversity and phylogenetic relationships, analyses were conducted using known PBLE and PGBD sequences to scan databases. From this data mining, numerous new sequences were characterized (50 for PBLE and 396 for PGBD). Structural analyses suggest that four groups of PBLE can be defined according to the presence/absence of sub-terminal repeats. The transposase is characterized by highly variable catalytic domain and C-terminal region. There is no relationship between the structural groups and the phylogeny of these PBLE elements. The PGBD are clearly structured into nine main groups. A new group of domesticated elements is suspected in Neopterygii and the remaining eight previously described elements have been investigated in more detail. In all cases, these sequences are no longer transposable elements, the catalytic domain of the ancestral transposase is not always conserved, but they are under strong purifying selection. The phylogeny of both PBLE and PGBD suggests multiple and independent domestication events of PGBD from different PBLE ancestors.

Structural basis of seamless excision and specific targeting by piggyBac transposase

“…The pB from T. ni is but one member of a larger superfamily of pB-like elements 68 . The superfamily includes piggyBat, one of the very few DNA transposons natively active in vertebrates 69,70 ; domesticated elements such as PiggyMac which play a pivotal role in ciliate nuclear development 71 ; and the larger group of piggyBac-derived (PGBD) proteins 68 . In humans, PGBD proteins have been implicated in premature ovarian failure 72 and childhood tumor development 73 , and the structures here will provide insight into their action.…”

Six domesticated PiggyBac transposases together carry out programmed DNA elimination in Paramecium

“…Transposases from the piggyBac family have repeatedly been domesticated in eukaryotes ( Bouallègue et al, 2017 ). In mammals, five PGBD ( piggyBac -derived) genes have been identified, but their cellular function has so far remained elusive ( Sarkar et al, 2003 ).…”

The Mitonuclear Dimension of Neanderthal and Denisovan Ancestry in Modern Human Genomes

“…Mitonuclear coadaptations are thought to be driven by the rapid evolution of the mitochondrial genome and subsequent coevolutionary responses in nuclear genes that encode mitochondrially targeted proteins (N-mt genes) (Osada and Akashi 2012; Havird et al 2017). Although mitochondria retain their own genome, the vast majority of the >1000 proteins that function in mitochondria are encoded in the nucleus (Gray 2015).…”