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

Julien Bischerour,Mireille Bétermier,Olivier Arnaiz,Aditi Singh,Linda Sperling,Mariusz Nowacki,Vinciane Régnier,Nathalie Mathy,Estienne Swart,Emeline Dubois,Cyril Denby Wilkes,Simran Bhullar

doi:10.7554/elife.37927

Julien Bischerour, Mireille Bétermier + Show 10 more

Open Access

https://doi.org/10.7554/elife.37927

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Journal: eLife	Publication Date: Sep 18, 2018
Citations: 49	License type: CC BY 4.0

Affiliation: University of Paris-Saclay, University of Bern

Abstract

The domestication of transposable elements has repeatedly occurred during evolution and domesticated transposases have often been implicated in programmed genome rearrangements, as remarkably illustrated in ciliates. In Paramecium, PiggyMac (Pgm), a domesticated PiggyBac transposase, carries out developmentally programmed DNA elimination, including the precise excision of tens of thousands of gene-interrupting germline Internal Eliminated Sequences (IESs). Here, we report the discovery of five groups of distant Pgm-like proteins (PgmLs), all able to interact with Pgm and essential for its nuclear localization and IES excision genome-wide. Unlike Pgm, PgmLs lack a conserved catalytic site, suggesting that they rather have an architectural function within a multi-component excision complex embedding Pgm. PgmL depletion can increase erroneous targeting of residual Pgm-mediated DNA cleavage, indicating that PgmLs contribute to accurately position the complex on IES ends. DNA rearrangements in Paramecium constitute a rare example of a biological process jointly managed by six distinct domesticated transposases.

Highlights

The mobility of DNA transposons is ensured by their self-encoded transposase
The first domain (PF13843 or DDE_Tnp1_7) encompasses the RNase H fold-related catalytic domain found in DD(D/E) transposases
Using a Hidden Markov Model (HMM) search, we discovered that nine putative Pgm-related proteins, hereafter designated as PiggyMac-like (PgmL) proteins, are encoded by the P. tetraurelia somatic genome (Supplementary file 2)

Summary

Introduction

The mobility of DNA transposons is ensured by their self-encoded transposase (reviewed in Hickman and Dyda, 2015). Several instances of domesticated DD(D/E) transposases have been reported, some of which still exhibit at least partial catalytic activity. The Transib-originating Rag protein catalyzes V(D)J recombination of vertebrate immunoglobulin genes (Kapitonov and Jurka, 2005; Huang et al, 2016); SETMAR, a partially active domesticated mariner transposase, is involved in DNA double-strand break repair in primates (Liu et al, 2007; Kim et al, 2014); a3, domesticated from a hAT transposon, and Kat, domesticated from a Mutator-like element, carry out mating type switching in the yeast Kluyveromyces lactis (Barsoum et al, 2010; Rajaei et al, 2014). CENP-B, related to mariner elements, serves as a centromere-binding factor, but its ancestral catalytic domain is no longer required for its function (Mateo and Gonzalez, 2014)

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