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Frequent co-domestication of PIF-like transposable element proteins in insects


Authors:
Fatema ruma 1; Dragomira N. Markova 1; Claudio Casola 2; Ayda Mirsalehi 1; Esther Betran 1

Affiliations:
1) University of Texas at Arlington; 2) Texas A&M University

Keywords:
a. genome evolution; m. computational models

Transposable elements (TEs) are genetic units that move and amplify within a host genome. In recent years, an increasing number of studies have shown that one of the most direct contributions of TEs to their host is through the process of ‘molecular domestication’ whereby the genes normally encoded by and serving the replication of a TE are co-opted by the host genome to create new gene(s) with cellular function. Thus, TE proteins are an important contributor to the emergence of novel host proteins. Despite the relative abundance of RNA TEs in eukaryotic genomes, DNA TE proteins and most notably their transposase, responsible for the excision and movement of the elements within the host genome, are generally considered to be more likely to be co-opted by the host than any other TE-derived protein. We have been studying four domesticated transposases from the PIF/Harbinger DNA family of TEs in Drosophila melanogaster, named Drosophila PIF Like Genes (DPLGs). So far, all PIF transposable elements known in plants and animals distinguish themselves from traditional DNA transposons by the presence of two independent transcription units. One encodes a protein representing the catalytic transposase, while the other encodes a protein with a MADF domain. We hypothesize that MADF proteins, a big gene family of regulatory proteins in D. melanogaster, to be derived from the same transposable elements. We also hypothesize that there should often be co-domestications of transposase and MADF proteins because the transposase translocates to the nucleus by the MADF protein. This is true for HARBI1 and NAIF1 in humans, DPLG7 and DPM7 in Drosophila and two co-domestications in Arabidopsis (ALP1 and ALP2 and HPD1 and HPD2). To provide further support to this co-domestication model, we investigated numerous insect species genomes for additional evidence of PIF TE domestication events and explore the co-domestication of the MADF protein from the same TE insertion. We present evidence of at least five PIF TE domestication events in insects: two co-domestication of both transposase and MADF proteins in Anopheles (Diptera) and one transposase only domestication event and one co-domestication event Lepidoptera, and one transposase only domestication event in cockroaches (Blattodeae). Thus, our results show that domestication of PIF transposases is frequently accompanied by the co-domestication of a cognate MADF protein potentially for regulatory functions further supporting the common origin of both PIF proteins.