title: Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials.
abstract: Syncytins are genes of retroviral origin captured by eutherian mammals, with a role in placentation. Here we show that some marsupials-which are the closest living relatives to eutherian mammals, although they diverged from the latter ∼190 Mya-also possess a syncytin gene. The gene identified in the South American marsupial opossum and dubbed syncytin-Opo1 has all of the characteristic features of a bona fide syncytin gene: It is fusogenic in an ex vivo cell-cell fusion assay; it is specifically expressed in the short-lived placenta at the level of the syncytial feto-maternal interface; and it is conserved in a functional state in a series of Monodelphis species. We further identify a nonfusogenic retroviral envelope gene that has been conserved for >80 My of evolution among all marsupials (including the opossum and the Australian tammar wallaby), with evidence for purifying selection and conservation of a canonical immunosuppressive domain, but with only limited expression in the placenta. This unusual captured gene, together with a third class of envelope genes from recently endogenized retroviruses-displaying strong expression in the uterine glands where retroviral particles can be detected-plausibly correspond to the different evolutionary statuses of a captured retroviral envelope gene, with only syncytin-Opo1 being the present-day bona fide syncytin active in the opossum and related species. This study would accordingly recapitulate the natural history of syncytin exaptation and evolution in a single species, and definitely extends the presence of such genes to all major placental mammalian clades.
authors.affiliation: Unité des Rétrovirus Endogènes et Eléments Rétroïdes des Eucaryotes Supérieurs, CNRS UMR 8122, Institut Gustave Roussy, Villejuif, F-94805, France; Université Paris-Sud, Orsay, F-91405, France; Université Paris Denis Diderot, Sorbonne Paris-Cité, Paris, F-75013, France;
authors.forename: Guillaume
authors.initials: G
authors.lastname: Cornelis
authors.affiliation: Unité des Rétrovirus Endogènes et Eléments Rétroïdes des Eucaryotes Supérieurs, CNRS UMR 8122, Institut Gustave Roussy, Villejuif, F-94805, France; Université Paris-Sud, Orsay, F-91405, France;
authors.forename: Cécile
authors.initials: C
authors.lastname: Vernochet
authors.affiliation: Unité des Rétrovirus Endogènes et Eléments Rétroïdes des Eucaryotes Supérieurs, CNRS UMR 8122, Institut Gustave Roussy, Villejuif, F-94805, France; Université Paris-Sud, Orsay, F-91405, France;
authors.forename: Quentin
authors.initials: Q
authors.lastname: Carradec
authors.affiliation: Unité des Rétrovirus Endogènes et Eléments Rétroïdes des Eucaryotes Supérieurs, CNRS UMR 8122, Institut Gustave Roussy, Villejuif, F-94805, France; Université Paris-Sud, Orsay, F-91405, France;
authors.forename: Sylvie
authors.initials: S
authors.lastname: Souquere
authors.affiliation: Zooparc de Beauval et Beauval Nature, Saint Aignan, F-41110, France;
authors.forename: Baptiste
authors.initials: B
authors.lastname: Mulot
authors.affiliation: Laboratoire de Paléontologie, Phylogénie et Paléobiologie, UMR 5554 CNRS, Université Montpellier II, Montpellier, F-34095, France;
authors.forename: François
authors.initials: F
authors.lastname: Catzeflis
authors.affiliation: LOEWE Biodiversity and Climate Research Center, Frankfurt am Main, D-60325 Germany;
authors.forename: Maria A
authors.initials: MA
authors.lastname: Nilsson
authors.affiliation: Department of Zoology, University of Melbourne, Melbourne, VIC 3010, Australia; and.
authors.forename: Brandon R
authors.initials: BR
authors.lastname: Menzies
authors.affiliation: Department of Zoology, University of Melbourne, Melbourne, VIC 3010, Australia; and.
authors.forename: Marilyn B
authors.initials: MB
authors.lastname: Renfree
authors.affiliation: Unité des Rétrovirus Endogènes et Eléments Rétroïdes des Eucaryotes Supérieurs, CNRS UMR 8122, Institut Gustave Roussy, Villejuif, F-94805, France; Université Paris-Sud, Orsay, F-91405, France;
authors.forename: Gérard
authors.initials: G
authors.lastname: Pierron
authors.affiliation: Systematic Zoology, Humboldt University, 10099 Berlin, Germany.
authors.forename: Ulrich
authors.initials: U
authors.lastname: Zeller
authors.affiliation: Unité des Rétrovirus Endogènes et Eléments Rétroïdes des Eucaryotes Supérieurs, CNRS UMR 8122, Institut Gustave Roussy, Villejuif, F-94805, France; Université Paris-Sud, Orsay, F-91405, France;
authors.forename: Odile
authors.initials: O
authors.lastname: Heidmann
authors.affiliation: Unité des Rétrovirus Endogènes et Eléments Rétroïdes des Eucaryotes Supérieurs, CNRS UMR 8122, Institut Gustave Roussy, Villejuif, F-94805, France; Université Paris-Sud, Orsay, F-91405, France;
authors.forename: Anne
authors.initials: A
authors.lastname: Dupressoir
authors.affiliation: Unité des Rétrovirus Endogènes et Eléments Rétroïdes des Eucaryotes Supérieurs, CNRS UMR 8122, Institut Gustave Roussy, Villejuif, F-94805, France; Université Paris-Sud, Orsay, F-91405, France; heidmann@igr.fr.
authors.forename: Thierry
authors.initials: T
authors.lastname: Heidmann
mesh_terms: D000818:Animals; D005260:Female; D020869:Gene Expression Profiling; D015686:Gene Products, env / Q000235:genetics*; D015752:Genes, env; D017403:In Situ Hybridization; D008394:Marsupialia / Q000145:classification / Q000235:genetics*; D008969:Molecular Sequence Data; D010802:Phylogeny; D010920:Placenta / Q000502:physiology*; D011247:Pregnancy; D011257:Pregnancy Proteins / Q000235:genetics*; D012190:Retroviridae / Q000502:physiology*; D014158:Transcription, Genetic; D014759:Viral Envelope Proteins / Q000235:genetics*
chemical_list: D015686:Gene Products, env; D011257:Pregnancy Proteins; D014759:Viral Envelope Proteins; C405335:syncytin
keywords: endogenous retrovirus; envelope protein; fusogenic activity; marsupials; syncytiotrophoblast