title: Genome-defence small RNAs exapted for epigenetic mating-type inheritance.
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.
authors.affiliation: 1] Ecole Normale Supérieure, Institut de Biologie de l'ENS, IBENS; Inserm, U1024; CNRS, UMR 8197 Paris F-75005, France [2] Sorbonne Universités, UPMC Univ., IFD, 4 place Jussieu, 75252 Paris cedex 05, France.
authors.forename: Deepankar Pratap
authors.initials: DP
authors.lastname: Singh
authors.affiliation: 1] Ecole Normale Supérieure, Institut de Biologie de l'ENS, IBENS; Inserm, U1024; CNRS, UMR 8197 Paris F-75005, France [2] Sorbonne Universités, UPMC Univ., IFD, 4 place Jussieu, 75252 Paris cedex 05, France [3] Laboratoire de Biochimie, Unité Mixte de Recherche 8231, École Supérieure de Physique et de Chimie Industrielles, 75231 Paris, France (B.S.); Department of Biology, Indiana University, Bloomington, Indiana 47405, USA (J.-F.G.); INRA, UMR 1061 Unité de Génétique Moléculaire Animale, Université de Limoges, IFR 145, Faculté des Sciences et Techniques, 87060 Limoges, France (K.B.).
authors.forename: Baptiste
authors.initials: B
authors.lastname: Saudemont
authors.affiliation: Ecole Normale Supérieure, Institut de Biologie de l'ENS, IBENS; Inserm, U1024; CNRS, UMR 8197 Paris F-75005, France.
authors.forename: Gérard
authors.initials: G
authors.lastname: Guglielmi
authors.affiliation: CNRS UPR3404 Centre de Génétique Moléculaire, Gif-sur-Yvette F-91198, and Université Paris-Sud, Département de Biologie, Orsay F-91405, France.
authors.forename: Olivier
authors.initials: O
authors.lastname: Arnaiz
authors.affiliation: 1] CNRS UMR5558, Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, 43 boulevard du 11 Novembre 1918, Villeurbanne F-69622, France [2] Laboratoire de Biochimie, Unité Mixte de Recherche 8231, École Supérieure de Physique et de Chimie Industrielles, 75231 Paris, France (B.S.); Department of Biology, Indiana University, Bloomington, Indiana 47405, USA (J.-F.G.); INRA, UMR 1061 Unité de Génétique Moléculaire Animale, Université de Limoges, IFR 145, Faculté des Sciences et Techniques, 87060 Limoges, France (K.B.).
authors.forename: Jean-François
authors.initials: JF
authors.lastname: Goût
authors.affiliation: Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Sławkowska 17, 31-016 Krakow, Poland.
authors.forename: Malgorzata
authors.initials: M
authors.lastname: Prajer
authors.affiliation: Department of Microbiology, Faculty of Biology, St Petersburg State University, Saint Petersburg 199034, Russia.
authors.forename: Alexey
authors.initials: A
authors.lastname: Potekhin
authors.affiliation: Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Sławkowska 17, 31-016 Krakow, Poland.
authors.forename: Ewa
authors.initials: E
authors.lastname: Przybòs
authors.affiliation: CNRS UPR3404 Centre de Génétique Moléculaire, Gif-sur-Yvette F-91198, and Université Paris-Sud, Département de Biologie, Orsay F-91405, France.
authors.forename: Anne
authors.initials: A
authors.lastname: Aubusson-Fleury
authors.affiliation: Ecole Normale Supérieure, Institut de Biologie de l'ENS, IBENS; Inserm, U1024; CNRS, UMR 8197 Paris F-75005, France.
authors.forename: Simran
authors.initials: S
authors.lastname: Bhullar
authors.affiliation: 1] Ecole Normale Supérieure, Institut de Biologie de l'ENS, IBENS; Inserm, U1024; CNRS, UMR 8197 Paris F-75005, France [2] Laboratoire de Biochimie, Unité Mixte de Recherche 8231, École Supérieure de Physique et de Chimie Industrielles, 75231 Paris, France (B.S.); Department of Biology, Indiana University, Bloomington, Indiana 47405, USA (J.-F.G.); INRA, UMR 1061 Unité de Génétique Moléculaire Animale, Université de Limoges, IFR 145, Faculté des Sciences et Techniques, 87060 Limoges, France (K.B.).
authors.forename: Khaled
authors.initials: K
authors.lastname: Bouhouche
authors.affiliation: 1] Sorbonne Universités, UPMC Univ., IFD, 4 place Jussieu, 75252 Paris cedex 05, France [2] Institut Jacques Monod, CNRS, UMR 7592, Université Paris Diderot, Sorbonne Paris Cité, Paris F-75205, France.
authors.forename: Maoussi
authors.initials: M
authors.lastname: Lhuillier-Akakpo
authors.affiliation: Ecole Normale Supérieure, Institut de Biologie de l'ENS, IBENS; Inserm, U1024; CNRS, UMR 8197 Paris F-75005, France.
authors.forename: Véronique
authors.initials: V
authors.lastname: Tanty
authors.affiliation: Ecole Normale Supérieure, Institut de Biologie de l'ENS, IBENS; Inserm, U1024; CNRS, UMR 8197 Paris F-75005, France.
authors.forename: Corinne
authors.initials: C
authors.lastname: Blugeon
authors.affiliation: Commissariat à l'Energie Atomique (CEA), Institut de Génomique (IG), Genoscope, 2 rue Gaston Crémieux, BP5706, 91057 Evry, France.
authors.forename: Adriana
authors.initials: A
authors.lastname: Alberti
authors.affiliation: Commissariat à l'Energie Atomique (CEA), Institut de Génomique (IG), Genoscope, 2 rue Gaston Crémieux, BP5706, 91057 Evry, France.
authors.forename: Karine
authors.initials: K
authors.lastname: Labadie
authors.affiliation: Commissariat à l'Energie Atomique (CEA), Institut de Génomique (IG), Genoscope, 2 rue Gaston Crémieux, BP5706, 91057 Evry, France.
authors.forename: Jean-Marc
authors.initials: JM
authors.lastname: Aury
authors.affiliation: CNRS UPR3404 Centre de Génétique Moléculaire, Gif-sur-Yvette F-91198, and Université Paris-Sud, Département de Biologie, Orsay F-91405, 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 F-75205, France.
authors.forename: Sandra
authors.initials: S
authors.lastname: Duharcourt
authors.affiliation: Ecole Normale Supérieure, Institut de Biologie de l'ENS, IBENS; Inserm, U1024; CNRS, UMR 8197 Paris F-75005, France.
authors.forename: Eric
authors.initials: E
authors.lastname: Meyer
mesh_terms: D004251:DNA Transposable Elements / Q000235:genetics; D044127:Epigenesis, Genetic / Q000235:genetics*; D005786:Gene Expression Regulation; D005796:Genes / Q000235:genetics; D016678:Genome / Q000235:genetics*; D040582:Inheritance Patterns / Q000235:genetics*; D008969:Molecular Sequence Data; D016805:Paramecium tetraurelia / Q000235:genetics* / Q000502:physiology; D011401:Promoter Regions, Genetic / Q000235:genetics; D034741:RNA, Small Interfering / Q000235:genetics*; D012098:Reproduction / Q000235:genetics / Q000502:physiology; D017384:Sequence Deletion / Q000235:genetics
chemical_list: D004251:DNA Transposable Elements; D034741:RNA, Small Interfering