Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum.

Aphid host Aphidius ervi Chemosensory genes DNA methylation loss GC content Lysiphlebus fabarum Parasitoid wasp Toll and Imd pathways Venom proteins de novo genome assembly

Journal

BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258

Informations de publication

Date de publication:
29 May 2020
Historique:
received: 16 01 2020
accepted: 30 04 2020
entrez: 31 5 2020
pubmed: 31 5 2020
medline: 12 1 2021
Statut: epublish

Résumé

Parasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biological control. Their success depends on adapting to develop inside aphids and overcoming both host aphid defenses and their protective endosymbionts. We present the de novo genome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids: Aphidius ervi and Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp) and the most AT-rich reported thus far for any arthropod (GC content: 25.8 and 23.8%). This nucleotide bias is accompanied by skewed codon usage and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and energy efficiency. We identify missing desaturase genes, whose absence may underlie mimicry in the cuticular hydrocarbon profile of L. fabarum. We highlight key gene groups including those underlying venom composition, chemosensory perception, and sex determination, as well as potential losses in immune pathway genes. These findings are of fundamental interest for insect evolution and biological control applications. They provide a strong foundation for further functional studies into coevolution between parasitoids and their hosts. Both genomes are available at https://bipaa.genouest.org.

Sections du résumé

BACKGROUND BACKGROUND
Parasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biological control. Their success depends on adapting to develop inside aphids and overcoming both host aphid defenses and their protective endosymbionts.
RESULTS RESULTS
We present the de novo genome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids: Aphidius ervi and Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp) and the most AT-rich reported thus far for any arthropod (GC content: 25.8 and 23.8%). This nucleotide bias is accompanied by skewed codon usage and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and energy efficiency. We identify missing desaturase genes, whose absence may underlie mimicry in the cuticular hydrocarbon profile of L. fabarum. We highlight key gene groups including those underlying venom composition, chemosensory perception, and sex determination, as well as potential losses in immune pathway genes.
CONCLUSIONS CONCLUSIONS
These findings are of fundamental interest for insect evolution and biological control applications. They provide a strong foundation for further functional studies into coevolution between parasitoids and their hosts. Both genomes are available at https://bipaa.genouest.org.

Identifiants

pubmed: 32471448
doi: 10.1186/s12864-020-6764-0
pii: 10.1186/s12864-020-6764-0
pmc: PMC7257214
doi:

Substances chimiques

Insect Proteins 0
Venoms 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

376

Subventions

Organisme : Fondo Nacional de Desarrollo Científico y Tecnológico
ID : 1130483 and 1170943
Organisme : Agence Nationale de la Recherche
ID : ANR-11-LABX-0028-01
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
ID : PP00P3_123376
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
ID : PP00P3_146341
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
ID : PP00P3_170627
Organisme : Deutsches Forschungsgemeinschaft
ID : GA 661/4-1
Organisme : Deutsche Forschungsgemeinschaft
ID : 1554/3-1

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Auteurs

Alice B Dennis (AB)

Department of Aquatic Ecology, Eawag, 8600, Dübendorf, Switzerland. alicebdennis@gmail.com.
Institute of Integrative Biology, ETH Zürich, 8092, Zürich, Switzerland. alicebdennis@gmail.com.
Institute of Biochemistry and Biology, University of Potsdam, 14476, Potsdam, Germany. alicebdennis@gmail.com.

Gabriel I Ballesteros (GI)

Instituto de Ciencias Biológicas, Universidad de Talca, Talca, Chile.
Centre for Molecular and Functional Ecology in Agroecosystems, Universidad de Talca, Talca, Chile.
Laboratorio de Control Biológico, Instituto de Ciencias Biológicas, Universidad de Talca, Talca, Chile.

Stéphanie Robin (S)

IGEPP, Agrocampus Ouest, INRAE, Université de Rennes, 35650, Le Rheu, France.
Université de Rennes 1, INRIA, CNRS, IRISA, 35000, Rennes, France.

Lukas Schrader (L)

Institute for Evolution and Biodiversity, Universität Münster, Münster, Germany.

Jens Bast (J)

Department of Ecology and Evolution, Université de Lausanne, 1015, Lausanne, Switzerland.
Institute of Zoology, Universität zu Köln, 50674, Köln, Germany.

Jan Berghöfer (J)

Institute for Evolution and Biodiversity, Universität Münster, Münster, Germany.

Leo W Beukeboom (LW)

Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands.

Maya Belghazi (M)

Aix-Marseille Univ, CNRS, INP, Inst Neurophysiopathol, PINT, PFNT, Marseille, France.

Anthony Bretaudeau (A)

IGEPP, Agrocampus Ouest, INRAE, Université de Rennes, 35650, Le Rheu, France.
Université de Rennes 1, INRIA, CNRS, IRISA, 35000, Rennes, France.

Jan Buellesbach (J)

Institute for Evolution and Biodiversity, Universität Münster, Münster, Germany.

Elizabeth Cash (E)

Department of Environmental Science, Policy, & Management, University of California, Berkeley, Berkeley, CA, 94720, USA.

Dominique Colinet (D)

Université Côte d'Azur, INRAE, CNRS, ISA, Sophia Antipolis, France.

Zoé Dumas (Z)

Department of Ecology and Evolution, Université de Lausanne, 1015, Lausanne, Switzerland.

Mohammed Errbii (M)

Institute for Evolution and Biodiversity, Universität Münster, Münster, Germany.

Patrizia Falabella (P)

Department of Sciences, University of Basilicata, 85100, Potenza, Italy.

Jean-Luc Gatti (JL)

Université Côte d'Azur, INRAE, CNRS, ISA, Sophia Antipolis, France.

Elzemiek Geuverink (E)

Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands.

Joshua D Gibson (JD)

Department of Environmental Science, Policy, & Management, University of California, Berkeley, Berkeley, CA, 94720, USA.
Department of Biology, Georgia Southern University, Statesboro, GA, 30460, USA.

Corinne Hertaeg (C)

Department of Aquatic Ecology, Eawag, 8600, Dübendorf, Switzerland.
Department of Environmental Systems Sciences, D-USYS, ETH Zürich, Zürich, Switzerland.

Stefanie Hartmann (S)

Institute of Biochemistry and Biology, University of Potsdam, 14476, Potsdam, Germany.

Emmanuelle Jacquin-Joly (E)

INRAE, Sorbonne Université, CNRS, IRD, UPEC, Université Paris Diderot, Institute of Ecology and Environmental Sciences of Paris, iEES-Paris, F-78000, Versailles, France.

Mark Lammers (M)

Institute for Evolution and Biodiversity, Universität Münster, Münster, Germany.

Blas I Lavandero (BI)

Laboratorio de Control Biológico, Instituto de Ciencias Biológicas, Universidad de Talca, Talca, Chile.

Ina Lindenbaum (I)

Institute for Evolution and Biodiversity, Universität Münster, Münster, Germany.

Lauriane Massardier-Galata (L)

Université Côte d'Azur, INRAE, CNRS, ISA, Sophia Antipolis, France.

Camille Meslin (C)

INRAE, Sorbonne Université, CNRS, IRD, UPEC, Université Paris Diderot, Institute of Ecology and Environmental Sciences of Paris, iEES-Paris, F-78000, Versailles, France.

Nicolas Montagné (N)

INRAE, Sorbonne Université, CNRS, IRD, UPEC, Université Paris Diderot, Institute of Ecology and Environmental Sciences of Paris, iEES-Paris, F-78000, Versailles, France.

Nina Pak (N)

Department of Environmental Science, Policy, & Management, University of California, Berkeley, Berkeley, CA, 94720, USA.

Marylène Poirié (M)

Université Côte d'Azur, INRAE, CNRS, ISA, Sophia Antipolis, France.

Rosanna Salvia (R)

Department of Sciences, University of Basilicata, 85100, Potenza, Italy.

Chris R Smith (CR)

Department of Biology, Earlham College, Richmond, IN, 47374, USA.

Denis Tagu (D)

IGEPP, Agrocampus Ouest, INRAE, Université de Rennes, 35650, Le Rheu, France.

Sophie Tares (S)

Université Côte d'Azur, INRAE, CNRS, ISA, Sophia Antipolis, France.

Heiko Vogel (H)

Department of Entomology, Max Planck Institute for Chemical Ecology, Jena, Germany.

Tanja Schwander (T)

Department of Ecology and Evolution, Université de Lausanne, 1015, Lausanne, Switzerland.

Jean-Christophe Simon (JC)

IGEPP, Agrocampus Ouest, INRAE, Université de Rennes, 35650, Le Rheu, France.

Christian C Figueroa (CC)

Instituto de Ciencias Biológicas, Universidad de Talca, Talca, Chile.
Centre for Molecular and Functional Ecology in Agroecosystems, Universidad de Talca, Talca, Chile.

Christoph Vorburger (C)

Department of Aquatic Ecology, Eawag, 8600, Dübendorf, Switzerland.
Institute of Integrative Biology, ETH Zürich, 8092, Zürich, Switzerland.

Fabrice Legeai (F)

IGEPP, Agrocampus Ouest, INRAE, Université de Rennes, 35650, Le Rheu, France.
Université de Rennes 1, INRIA, CNRS, IRISA, 35000, Rennes, France.

Jürgen Gadau (J)

Institute for Evolution and Biodiversity, Universität Münster, Münster, Germany. gadauj@uni-muenster.de.

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