Weapons exchange in the battle between transposable elements and their host

Weapons exchange in the battle between transposable elements and their host

The inactivation of transposable elements within genomes is insured by multiple epigenetic mechanisms. Olivier Mathieu's team has identified two genes required for repressing many transposable elements through a new molecular pathway independent of the main epigenetic modifications. Surprisingly, these genes could themselves have derived from transposable elements. This reveals that domestication of transposable elements by flowering plants’ genomes would have allowed emergence of a new mechanism to control activity of these invasive sequences. This study is published in Nature Communications (Ikeda et al., 2017).

Transposable elements are mobile DNA sequences capable of duplicating within genomes by integrating into new chromosomal positions. These elements represent a significant fraction of most eukaryotic genomes, contributing for example about 50% of the human genome, a fraction which can reach more than 80% for plant genomes such as maize. Although transposable elements contribute significantly to genome evolution, their mobilization could also generate mutations deleterious to the host survival; such potentiality has led to the establishment of multiple, overlapping epigenetic mechanisms, that allow the host genome to strictly control the transcriptional activity of these elements.

Epigenetic marks include chemical, reversible chromatin modifications that can be stably inherited through cell divisions. Thus, several silencing pathways repress the expression of the transposable elements through imposition and maintenance on these elements of a high level of DNA methylation. In the plant model Arabidopsis thaliana, such targeting of DNA hypermethylation depends in part on small interfering RNAs and correlates with other epigenetic changes affecting histones, such as methylation of lysine 9 (H3K9me2) or Lysine 27 (H3K27me1) of histone H3. The juxtaposition of these marks is associated with the implementation of "closed" heterochromatic structures in which the highly condensed chromatin is not permissive to transcription. The archetype of this compact structure is visible at pericentromeric regions of the chromosomes, where a large fraction of the transposable elements of the genome are located.

Through a genetic approach, the team of Olivier Mathieu has just highlighted a novel regulatory pathway contributing to the inactivation of transposable elements. The transcriptional deregulation observed in the kumonosu (kun) mutant do not rely on small interfering RNAs and is largely independent of DNA methylation and other epigenetic marks commonly associated with heterochromatin. In this study, Ikeda et al. demonstrate that the kun phenotype is linked to a single mutation in the MAIL1 gene and that a highly homologous, MAIN gene is also required for silencing, probably via the formation of MAIL1-MAIN heterodimers. Although the molecular mechanism of the MAIL1 / MAIN pathway remains to be defined, this complex appears necessary for proper condensation of heterochromatin; the absence of one of these factors then correlates with structural and functional defects of pericentromeric regions, associated with transcriptional reactivation of many transposable elements.

The MAIL1 / MAIN proteins contain only one conserved domain, called "Plant Mobile Domain". Phylogenetic analysis suggests that this domain was originally present in transposable elements and that it was then "captured" by the host genome for its own benefit. This domestication event took place in the common ancestor of flowering plants and paradoxically led to the emergence of a new class of genes whose function is to restrict the autonomy of transposable elements. These data underscore the extraordinary ability of the genome to adapt and develop new strategies to stop invasion and control the proliferation of potentially deleterious elements.

Reference

Arabidopsis proteins with a transposon-related domain act in gene silencing.

Ikeda Y., Pélissier T., Bourguet P., BeckerC., Pouch-PélissierM.N., PogorelcnikR., WeingartnerM., WeigelD., DeragonJ.M. and Mathieu O.

Nat. Commun. 2017 May 3; 8, 15122. doi: 10.1038/ncomms15122

This work has been highlighted on the CNRS website (in French)

http://www.cnrs.fr/insb/recherche/parutions/articles2017/t-pelissier.html

Contacts:

Thierry Pelissier  (thierry.pelissier@uca.fr)

Olivier Mathieu   (olivier.mathieru.uca.fr)

Last modified: 05/15/2017