title: Local effect of enhancer of zeste-like reveals cooperation of epigenetic and cis-acting determinants for zygotic genome rearrangements.
abstract: In the ciliate Paramecium tetraurelia, differentiation of the somatic nucleus from the zygotic nucleus is characterized by massive and reproducible deletion of transposable elements and of 45,000 short, dispersed, single-copy sequences. A specific class of small RNAs produced by the germline during meiosis, the scnRNAs, are involved in the epigenetic regulation of DNA deletion but the underlying mechanisms are poorly understood. Here, we show that trimethylation of histone H3 (H3K27me3 and H3K9me3) displays a dynamic nuclear localization that is altered when the endonuclease required for DNA elimination is depleted. We identified the putative histone methyltransferase Ezl1 necessary for H3K27me3 and H3K9me3 establishment and show that it is required for correct genome rearrangements. Genome-wide analyses show that scnRNA-mediated H3 trimethylation is necessary for the elimination of long, repeated germline DNA, while single copy sequences display differential sensitivity to depletion of proteins involved in the scnRNA pathway, Ezl1- a putative histone methyltransferase and Dcl5- a protein required for iesRNA biogenesis. Our study reveals cis-acting determinants, such as DNA length, also contribute to the definition of germline sequences to delete. We further show that precise excision of single copy DNA elements, as short as 26 bp, requires Ezl1, suggesting that development specific H3K27me3 and H3K9me3 ensure specific demarcation of very short germline sequences from the adjacent somatic sequences.
authors.affiliation: Institut Jacques Monod, CNRS, UMR 7592, Université Paris Diderot, Sorbonne Paris Cité, Paris, France; Sorbonne Universités, UPMC Univ., IFD, Paris, France.
authors.forename: Maoussi
authors.initials: M
authors.lastname: Lhuillier-Akakpo
authors.affiliation: Institut Jacques Monod, CNRS, UMR 7592, Université Paris Diderot, Sorbonne Paris Cité, Paris, France.
authors.forename: Andrea
authors.initials: A
authors.lastname: Frapporti
authors.affiliation: CNRS UPR3404 Centre de Génétique Moléculaire, Gif-sur-Yvette, France; Département de Biologie, Université Paris-Sud, Orsay, France.
authors.forename: Cyril
authors.initials: C
authors.lastname: Denby Wilkes
authors.affiliation: Institut Jacques Monod, CNRS, UMR 7592, Université Paris Diderot, Sorbonne Paris Cité, Paris, France.
authors.forename: Mélody
authors.initials: M
authors.lastname: Matelot
authors.affiliation: Institut Jacques Monod, CNRS, UMR 7592, Université Paris Diderot, Sorbonne Paris Cité, Paris, France; Institut Universitaire de France, Paris, France.
authors.forename: Michel
authors.initials: M
authors.lastname: Vervoort
authors.affiliation: CNRS UPR3404 Centre de Génétique Moléculaire, Gif-sur-Yvette, France; Département de Biologie, Université Paris-Sud, Orsay, France.
authors.forename: Linda
authors.initials: L
authors.lastname: Sperling
authors.affiliation: Institut Jacques Monod, CNRS, UMR 7592, Université Paris Diderot, Sorbonne Paris Cité, Paris, France.
authors.forename: Sandra
authors.initials: S
authors.lastname: Duharcourt
mesh_terms: D004251:DNA Transposable Elements; D044127:Epigenesis, Genetic; D015321:Gene Rearrangement; D018503:Genome, Protozoan; D006657:Histones / Q000378:metabolism; D048648:Macronucleus; D008745:Methylation; D016805:Paramecium tetraurelia / Q000145:classification / Q000235:genetics* / Q000378:metabolism; D010802:Phylogeny; D011123:Polyploidy; D054730:Protein Interaction Domains and Motifs; D021381:Protein Transport; D015800:Protozoan Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D017384:Sequence Deletion; D015053:Zygote / Q000378:metabolism*
chemical_list: D004251:DNA Transposable Elements; D006657:Histones; D015800:Protozoan Proteins