Transposon Invasion of theParameciumGermline Genome Countered by a Domesticated PiggyBac Transposase and the NHEJ Pathway

Abstract

Sequences related to transposons constitute a large fraction of extant genomes, but insertions within coding sequences have generally not been tolerated during evolution. Thanks to their unique nuclear dimorphism and to their original mechanism of programmed DNA elimination from their somatic nucleus (macronucleus), ciliates are emerging model organisms for the study of the impact of transposable elements on genomes. The germline genome of the ciliateParamecium, located in its micronucleus, contains thousands of short intervening sequences, the IESs, which interrupt 47% of genes. Recent data provided support to the hypothesis that an evolutionary link exists betweenParameciumIESs andTc1/marinertransposons. During development of the macronucleus, IESs are excised precisely thanks to the coordinated action of PiggyMac, a domesticatedpiggyBactransposase, and of the NHEJ double-strand break repair pathway. A PiggyMac homolog is also required for developmentally programmed DNA elimination in another ciliate,Tetrahymena. Here, we present an overview of the life cycle of these unicellular eukaryotes and of the developmentally programmed genome rearrangements that take place at each sexual cycle. We discuss how ancient domestication of apiggyBactransposase might have allowedTc1/marinerelements to spread throughout the germline genome ofParamecium, without strong counterselection against insertion within genes.