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Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization.

ABSTRACT: Endogenous viruses form an important proportion of eukaryote genomes and a source of novel functions. How large DNA viruses integrated into a genome evolve when they confer a benefit to their host, however, remains unknown. Bracoviruses are essential for the parasitism success of parasitoid wasps, into whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome at a chromosomal scale, that bracovirus genes colonized all ten chromosomes of Cotesia congregata. Most form clusters of genes involved in particle production or parasitism success. Genomic comparison with another wasp, Microplitis demolitor, revealed that these clusters were already established ~53 mya and thus belong to remarkably stable genomic structures, the architectures of which are evolutionary constrained. Transcriptomic analyses highlight temporal synchronization of viral gene expression without resulting in immune gene induction, suggesting that no conflicts remain between ancient symbiotic partners when benefits to them converge.

SUBMITTER: Gauthier J

PROVIDER: S-EPMC7822920 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization.

Gauthier Jérémy J Boulain Hélène H van Vugt Joke J F A JJFA Baudry Lyam L Persyn Emma E Aury Jean-Marc JM Noel Benjamin B Bretaudeau Anthony A Legeai Fabrice F Warris Sven S Chebbi Mohamed A MA Dubreuil Géraldine G Duvic Bernard B Kremer Natacha N Gayral Philippe P Musset Karine K Josse Thibaut T Bigot Diane D Bressac Christophe C Moreau Sébastien S Periquet Georges G Harry Myriam M Montagné Nicolas N Boulogne Isabelle I Sabeti-Azad Mahnaz M Maïbèche Martine M Chertemps Thomas T Hilliou Frédérique F Siaussat David D Amselem Joëlle J Luyten Isabelle I Capdevielle-Dulac Claire C Labadie Karine K Merlin Bruna Laís BL Barbe Valérie V de Boer Jetske G JG Marbouty Martial M Cônsoli Fernando Luis FL Dupas Stéphane S Hua-Van Aurélie A Le Goff Gaelle G Bézier Annie A Jacquin-Joly Emmanuelle E Whitfield James B JB Vet Louise E M LEM Smid Hans M HM Kaiser Laure L Koszul Romain R Huguet Elisabeth E Herniou Elisabeth A EA Drezen Jean-Michel JM

Communications biology 20210122 1

Endogenous viruses form an important proportion of eukaryote genomes and a source of novel functions. How large DNA viruses integrated into a genome evolve when they confer a benefit to their host, however, remains unknown. Bracoviruses are essential for the parasitism success of parasitoid wasps, into whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome at a chromosomal scale, that bracovirus genes colonized all ten chromosomes of Cot ...[more]

PMID: 33483589

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Project description:The parasitoid wasp Venturia canescens is an important biological control agent of stored products moth pests and serves as a model to study the function and evolution of domesticated endogenous viruses (DEVs). The DEVs discovered in V. canescens are known as virus-like particles (VcVLPs), which are produced using nudivirus-derived components and incorporate wasp-derived virulence proteins instead of packaged nucleic acids. Previous studies of virus-derived components in the V. canescens genome identified 53 nudivirus-like genes organized in six gene clusters and several viral pseudogenes, but how VcVLP genes are organized among wasp chromosomes following their integration in the ancestral wasp genome is largely unknown. Here, we present a chromosomal scale genome of V. canescens consisting of 11 chromosomes and 56 unplaced small scaffolds. The genome size is 290.8 Mbp with a N50 scaffold size of 24.99 Mbp. A high-quality gene set including 11,831 protein-coding genes were produced using RNA-Seq data as well as publicly available peptide sequences from related Hymenoptera. A manual annotation of genes of viral origin produced 61 intact and 19 pseudogenized nudivirus-derived genes. The genome assembly revealed that two previously identified clusters were joined into a single cluster and a total of 5 gene clusters comprising of 60 intact nudivirus-derived genes were located in three chromosomes. In contrast, pseudogenes are dispersed among 8 chromosomes with only 4 pseudogenes associated with nudivirus gene clusters. The architecture of genes encoding VcVLP components suggests it originates from a recent virus acquisition and there is a link between the processes of dispersal and pseudogenization. This high-quality genome assembly and annotation represents the first chromosome-scale assembly for parasitoid wasps associated with VLPs, and is publicly available in the National Center for Biotechnology Information Genome and RefSeq databases, providing a valuable resource for future studies of DEVs in parasitoid wasps.

Dataset Information

Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization.

Publications

Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization.

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