PIF transposable elements domestication and genetic novelty in insects

Abstract

**Please note that the full text is embargoed until 5/17/2024** ABSTRACT: Transposable elements or TEs, are selfish genetic elements that represent a major component of a eukaryotic genome. They are genetic units that can move and amplify within a host genome. Mobilization of these TEs can be harmful to the host genome as they can transpose to new locations and can be a source of disruptions to the genetic information, DNA breakage and ectopic recombination. It has been shown, however, that TE proteins can be domesticated/co-opted and supply functions for major adaptations. There are two broad classes of TEs: Class I or retro-transposable elements and Class II or DNA elements. It has been described that DNA TE proteins are more prone to be co-opted by the host. In Drosophila, the transposase genes from the PIF/Harbinger DNA TE family have been co-opted seven times in several closely related species of Drosophila, and in one case (DPLG7:DPM7) both PIF/Harbinger TE genes (i.e., not only the transposase but also the MADF protein second ORF) were domesticated from the same TE insertion. In the first part of this dissertation work, we explored the abundance of co-domestication of the two ORFs of PIF/Harbinger DNA TEs in insect genomes and the correlation of the presence of MADF proteins with transposase domestication in these genomes. We uncover seven cases of either transposase domestication or co-domestication including cases in mosquito, Lepidoptera and cockroaches. The summary of all instances supports a model where both genes from PIF/Harbinger DNA TEs are often co-domesticated from the same TE insertion after PIF/Harbinger TE invasion and amplification and only after suffer rearrangements and appear at separate locations in the genome. There are also two dissertation chapters where we explored the functions of two domesticated transposases from PIF/Harbinger DNA TE in D. melanogaster: Drosophila PIF Like Gene 2 and 3 (DPLG2 and DPLG3). These DPLGs are old (55 - 192 My old) and independent domestications, under strong purifying selection. We tagged these DPLG proteins and produced null mutants. DPLG2 and DPLG3 localize both in the cytoplasm of some cells and the nucleus of others. Their transport to the nucleus might be regulated. We found support for a role of DPLG3 in germline development during gonadogenesis in both sexes from the null mutant We also explore the change in expression in mutant ovaries of DPLG3 and DPLG2 and that similar genes change expression. Both DPLG2 and DPLG3 might be gene expression regulators and have potentially related neuronal and gonadal functions given their protein localization and mutant phenotypes.