Recurrent domestication by Lepidoptera of genes from their parasites mediated by Bracoviruses

Autor: Gasmi, Laila, BOULAIN, Hélène, Gauthier, Jérémy, Hua-Van, Aurélie, Musset, Karine, Jakubowska, Agata K., Aury, Jean-Marc, Volkoff, Anne Nathalie, Huguet, Elisabeth, Herrero, Salvador, Drezen, Jean-Michel
Přispěvatelé: Department of Genetics, Universitat de València (UV), Estructura de Recerca Interdisciplinar en Biotecnologia i Biomedicina (ERI BIOTECMED), Institut de recherche sur la biologie de l'insecte UMR7261 (IRBI), Université de Tours (UT)-Centre National de la Recherche Scientifique (CNRS), Évolution, génomes, comportement et écologie (EGCE), Université Paris-Sud - Paris 11 (UP11)-IRD-Centre National de la Recherche Scientifique (CNRS), Genoscope - Centre national de séquençage [Evry] (GENOSCOPE), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM), Spanish Ministry for Science and Technology : AGL2011-30352-C02-02, AGL2014-57752-C02-2R, Université de Tours-Centre National de la Recherche Scientifique (CNRS), Laboratoire Evolution, Génomes, Comportement, Ecologie, CNRS/Université Paris-Sud UMR9191, IRD UMR247, Université Paris-Sud - Paris 11 (UP11), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay, Université de Montpellier (UM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Institut National de la Recherche Agronomique (INRA), Centre National de la Recherche Scientifique (CNRS)-IRD-Université Paris-Sud - Paris 11 (UP11)
Jazyk: angličtina
Rok vydání: 2015
Předmět:
Zdroj: PLoS Genetics
PLoS Genetics, 2015, 11 (9), 32 p. ⟨10.1371/journal.pgen.1005470⟩
PLoS Genetics, Public Library of Science, 2015, 11 (9), 32 p. ⟨10.1371/journal.pgen.1005470⟩
PLoS Genetics, Vol 11, Iss 9, p e1005470 (2015)
Plos Genetics 9 (11), 32 p.. (2015)
ISSN: 1553-7390
1553-7404
DOI: 10.1371/journal.pgen.1005470⟩
Popis: Bracoviruses are symbiotic viruses associated with tens of thousands of species of parasitic wasps that develop within the body of lepidopteran hosts and that collectively parasitize caterpillars of virtually every lepidopteran species. Viral particles are produced in the wasp ovaries and injected into host larvae with the wasp eggs. Once in the host body, the viral DNA circles enclosed in the particles integrate into lepidopteran host cell DNA. Here we show that bracovirus DNA sequences have been inserted repeatedly into lepidopteran genomes, indicating this viral DNA can also enter germline cells. The original mode of Horizontal Gene Transfer (HGT) unveiled here is based on the integrative properties of an endogenous virus that has evolved as a gene transfer agent within parasitic wasp genomes for ≈100 million years. Among the bracovirus genes thus transferred, a phylogenetic analysis indicated that those encoding C-type-lectins most likely originated from the wasp gene set, showing that a bracovirus-mediated gene flux exists between the 2 insect orders Hymenoptera and Lepidoptera. Furthermore, the acquisition of bracovirus sequences that can be expressed by Lepidoptera has resulted in the domestication of several genes that could result in adaptive advantages for the host. Indeed, functional analyses suggest that two of the acquired genes could have a protective role against a common pathogen in the field, baculovirus. From these results, we hypothesize that bracovirus-mediated HGT has played an important role in the evolutionary arms race between Lepidoptera and their pathogens.
Author Summary Eukaryotes are generally thought to evolve mainly through the modification of existing genetic information. However, evidence of horizontal gene transfer (HGT) in eukaryotes-the accidental acquisition of a novel gene from another species, allowing acquisition of novel traits—is now recognized as an important factor in their evolution. We show here that in several lineages, lepidopteran genomes have acquired genes from a bracovirus that is symbiotically used by parasitic wasps to inhibit caterpillar host immune defences. Integration of parts of the viral genome into host caterpillar DNA strongly suggests that integration can sporadically occur in the germline, leading to the production of lepidopteran lineages that harbor bracovirus sequences. Moreover, some of the transferred bracovirus genes reported here originate from the wasp genome, demonstrating that a gene flux exists between the two insect orders Hymenoptera and Lepidoptera that diverged ≈300 MYA. As bracovirus gene organisation has evolved to allow expression in Lepidoptera, these transferred genes can be readily domesticated. Additionally, we present functional analyses suggesting that some of the acquired genes confer to caterpillars a protection toward baculovirus, a very common pathogen in the field. This phenomenon may have implications for understanding how caterpillars acquire resistance against baculoviruses used in biological control.
Databáze: OpenAIRE
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