Genome-defence small RNAs exapted for epigenetic mating-type inheritance

Deepankar Pratap Singh, Baptiste Saudemont, Gérard Guglielmi, Olivier Arnaiz, Jean-François Goût, Malgorzata Prajer, Alexey Potekhin, Ewa Przybòs, Anne Aubusson-Fleury, Simran Bhullar, Khaled Bouhouche, Maoussi Lhuillier-Akakpo, Véronique Tanty, Corinne Blugeon, Adriana Alberti, Karine Labadie, Jean-Marc Aury, Linda Sperling, Sandra Duharcourt and Eric Meyer ()
Additional contact information
Deepankar Pratap Singh: Ecole Normale Supérieure, Institut de Biologie de l’ENS, IBENS; Inserm, U1024; CNRS, UMR 8197 Paris F-75005, France
Baptiste Saudemont: Ecole Normale Supérieure, Institut de Biologie de l’ENS, IBENS; Inserm, U1024; CNRS, UMR 8197 Paris F-75005, France
Gérard Guglielmi: Ecole Normale Supérieure, Institut de Biologie de l’ENS, IBENS; Inserm, U1024; CNRS, UMR 8197 Paris F-75005, France
Olivier Arnaiz: CNRS UPR3404 Centre de Génétique Moléculaire, Gif-sur-Yvette F-91198, and Université Paris-Sud, Orsay F-91405, France
Jean-François Goût: CNRS UMR5558, Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, 43 boulevard du 11 Novembre 1918, Villeurbanne F-69622, France
Malgorzata Prajer: Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Sławkowska 17, 31-016 Krakow, Poland
Alexey Potekhin: Faculty of Biology, St Petersburg State University, Saint Petersburg 199034, Russia
Ewa Przybòs: Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Sławkowska 17, 31-016 Krakow, Poland
Anne Aubusson-Fleury: CNRS UPR3404 Centre de Génétique Moléculaire, Gif-sur-Yvette F-91198, and Université Paris-Sud, Orsay F-91405, France
Simran Bhullar: Ecole Normale Supérieure, Institut de Biologie de l’ENS, IBENS; Inserm, U1024; CNRS, UMR 8197 Paris F-75005, France
Khaled Bouhouche: Ecole Normale Supérieure, Institut de Biologie de l’ENS, IBENS; Inserm, U1024; CNRS, UMR 8197 Paris F-75005, France
Maoussi Lhuillier-Akakpo: Sorbonne Universités, UPMC Univ., IFD, 4 place Jussieu, 75252 Paris cedex 05, France
Véronique Tanty: Ecole Normale Supérieure, Institut de Biologie de l’ENS, IBENS; Inserm, U1024; CNRS, UMR 8197 Paris F-75005, France
Corinne Blugeon: Ecole Normale Supérieure, Institut de Biologie de l’ENS, IBENS; Inserm, U1024; CNRS, UMR 8197 Paris F-75005, France
Adriana Alberti: Commissariat à l’Energie Atomique (CEA), Institut de Génomique (IG), Genoscope, 2 rue Gaston Crémieux, BP5706, 91057 Evry, France
Karine Labadie: Commissariat à l’Energie Atomique (CEA), Institut de Génomique (IG), Genoscope, 2 rue Gaston Crémieux, BP5706, 91057 Evry, France
Jean-Marc Aury: Commissariat à l’Energie Atomique (CEA), Institut de Génomique (IG), Genoscope, 2 rue Gaston Crémieux, BP5706, 91057 Evry, France
Linda Sperling: CNRS UPR3404 Centre de Génétique Moléculaire, Gif-sur-Yvette F-91198, and Université Paris-Sud, Orsay F-91405, France
Sandra Duharcourt: Institut Jacques Monod, CNRS, UMR 7592, Université Paris Diderot, Sorbonne Paris Cité, Paris F-75205, France
Eric Meyer: Ecole Normale Supérieure, Institut de Biologie de l’ENS, IBENS; Inserm, U1024; CNRS, UMR 8197 Paris F-75005, France

Nature, 2014, vol. 509, issue 7501, 447-452

Abstract: Abstract In the ciliate Paramecium, transposable elements and their single-copy remnants are deleted during the development of somatic macronuclei from germline micronuclei, at each sexual generation. Deletions are targeted by scnRNAs, small RNAs produced from the germ line during meiosis that first scan the maternal macronuclear genome to identify missing sequences, and then allow the zygotic macronucleus to reproduce the same deletions. Here we show that this process accounts for the maternal inheritance of mating types in Paramecium tetraurelia, a long-standing problem in epigenetics. Mating type E depends on expression of the transmembrane protein mtA, and the default type O is determined during development by scnRNA-dependent excision of the mtA promoter. In the sibling species Paramecium septaurelia, mating type O is determined by coding-sequence deletions in a different gene, mtB, which is specifically required for mtA expression. These independently evolved mechanisms suggest frequent exaptation of the scnRNA pathway to regulate cellular genes and mediate transgenerational epigenetic inheritance of essential phenotypic polymorphisms.

Date: 2014
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DOI: 10.1038/nature13318

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