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

Abstract 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 ada...

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Main Authors: Alice B. Dennis, Gabriel I. Ballesteros, Stéphanie Robin, Lukas Schrader, Jens Bast, Jan Berghöfer, Leo W. Beukeboom, Maya Belghazi, Anthony Bretaudeau, Jan Buellesbach, Elizabeth Cash, Dominique Colinet, Zoé Dumas, Mohammed Errbii, Patrizia Falabella, Jean-Luc Gatti, Elzemiek Geuverink, Joshua D. Gibson, Corinne Hertaeg, Stefanie Hartmann, Emmanuelle Jacquin-Joly, Mark Lammers, Blas I. Lavandero, Ina Lindenbaum, Lauriane Massardier-Galata, Camille Meslin, Nicolas Montagné, Nina Pak, Marylène Poirié, Rosanna Salvia, Chris R. Smith, Denis Tagu, Sophie Tares, Heiko Vogel, Tanja Schwander, Jean-Christophe Simon, Christian C. Figueroa, Christoph Vorburger, Fabrice Legeai, Jürgen Gadau
Format: Article
Language:English
Published: BMC 2020-05-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-020-6764-0
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author Alice B. Dennis
Gabriel I. Ballesteros
Stéphanie Robin
Lukas Schrader
Jens Bast
Jan Berghöfer
Leo W. Beukeboom
Maya Belghazi
Anthony Bretaudeau
Jan Buellesbach
Elizabeth Cash
Dominique Colinet
Zoé Dumas
Mohammed Errbii
Patrizia Falabella
Jean-Luc Gatti
Elzemiek Geuverink
Joshua D. Gibson
Corinne Hertaeg
Stefanie Hartmann
Emmanuelle Jacquin-Joly
Mark Lammers
Blas I. Lavandero
Ina Lindenbaum
Lauriane Massardier-Galata
Camille Meslin
Nicolas Montagné
Nina Pak
Marylène Poirié
Rosanna Salvia
Chris R. Smith
Denis Tagu
Sophie Tares
Heiko Vogel
Tanja Schwander
Jean-Christophe Simon
Christian C. Figueroa
Christoph Vorburger
Fabrice Legeai
Jürgen Gadau
spellingShingle Alice B. Dennis
Gabriel I. Ballesteros
Stéphanie Robin
Lukas Schrader
Jens Bast
Jan Berghöfer
Leo W. Beukeboom
Maya Belghazi
Anthony Bretaudeau
Jan Buellesbach
Elizabeth Cash
Dominique Colinet
Zoé Dumas
Mohammed Errbii
Patrizia Falabella
Jean-Luc Gatti
Elzemiek Geuverink
Joshua D. Gibson
Corinne Hertaeg
Stefanie Hartmann
Emmanuelle Jacquin-Joly
Mark Lammers
Blas I. Lavandero
Ina Lindenbaum
Lauriane Massardier-Galata
Camille Meslin
Nicolas Montagné
Nina Pak
Marylène Poirié
Rosanna Salvia
Chris R. Smith
Denis Tagu
Sophie Tares
Heiko Vogel
Tanja Schwander
Jean-Christophe Simon
Christian C. Figueroa
Christoph Vorburger
Fabrice Legeai
Jürgen Gadau
Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum
BMC Genomics
Parasitoid wasp
Aphid host
Aphidius ervi
Lysiphlebus fabarum
GC content
de novo genome assembly
author_facet Alice B. Dennis
Gabriel I. Ballesteros
Stéphanie Robin
Lukas Schrader
Jens Bast
Jan Berghöfer
Leo W. Beukeboom
Maya Belghazi
Anthony Bretaudeau
Jan Buellesbach
Elizabeth Cash
Dominique Colinet
Zoé Dumas
Mohammed Errbii
Patrizia Falabella
Jean-Luc Gatti
Elzemiek Geuverink
Joshua D. Gibson
Corinne Hertaeg
Stefanie Hartmann
Emmanuelle Jacquin-Joly
Mark Lammers
Blas I. Lavandero
Ina Lindenbaum
Lauriane Massardier-Galata
Camille Meslin
Nicolas Montagné
Nina Pak
Marylène Poirié
Rosanna Salvia
Chris R. Smith
Denis Tagu
Sophie Tares
Heiko Vogel
Tanja Schwander
Jean-Christophe Simon
Christian C. Figueroa
Christoph Vorburger
Fabrice Legeai
Jürgen Gadau
author_sort Alice B. Dennis
title Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum
title_short Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum
title_full Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum
title_fullStr Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum
title_full_unstemmed Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum
title_sort functional insights from the gc-poor genomes of two aphid parasitoids, aphidius ervi and lysiphlebus fabarum
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2020-05-01
description Abstract 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 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 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 .
topic Parasitoid wasp
Aphid host
Aphidius ervi
Lysiphlebus fabarum
GC content
de novo genome assembly
url http://link.springer.com/article/10.1186/s12864-020-6764-0
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spelling doaj-9aa15e0959b849d98488571e8f04baa72020-11-25T03:46:31ZengBMCBMC Genomics1471-21642020-05-0121112710.1186/s12864-020-6764-0Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarumAlice B. Dennis0Gabriel I. Ballesteros1Stéphanie Robin2Lukas Schrader3Jens Bast4Jan Berghöfer5Leo W. Beukeboom6Maya Belghazi7Anthony Bretaudeau8Jan Buellesbach9Elizabeth Cash10Dominique Colinet11Zoé Dumas12Mohammed Errbii13Patrizia Falabella14Jean-Luc Gatti15Elzemiek Geuverink16Joshua D. Gibson17Corinne Hertaeg18Stefanie Hartmann19Emmanuelle Jacquin-Joly20Mark Lammers21Blas I. Lavandero22Ina Lindenbaum23Lauriane Massardier-Galata24Camille Meslin25Nicolas Montagné26Nina Pak27Marylène Poirié28Rosanna Salvia29Chris R. Smith30Denis Tagu31Sophie Tares32Heiko Vogel33Tanja Schwander34Jean-Christophe Simon35Christian C. Figueroa36Christoph Vorburger37Fabrice Legeai38Jürgen Gadau39Department of Aquatic Ecology, EawagInstituto de Ciencias Biológicas, Universidad de TalcaIGEPP, Agrocampus Ouest, INRAE, Université de RennesInstitute for Evolution and Biodiversity, Universität MünsterDepartment of Ecology and Evolution, Université de LausanneInstitute for Evolution and Biodiversity, Universität MünsterGroningen Institute for Evolutionary Life Sciences, University of GroningenAix-Marseille Univ, CNRS, INP, Inst Neurophysiopathol, PINT, PFNTIGEPP, Agrocampus Ouest, INRAE, Université de RennesInstitute for Evolution and Biodiversity, Universität MünsterDepartment of Environmental Science, Policy, & Management, University of California, BerkeleyUniversité Côte d’Azur, INRAE, CNRS, ISADepartment of Ecology and Evolution, Université de LausanneInstitute for Evolution and Biodiversity, Universität MünsterDepartment of Sciences, University of BasilicataUniversité Côte d’Azur, INRAE, CNRS, ISAGroningen Institute for Evolutionary Life Sciences, University of GroningenDepartment of Environmental Science, Policy, & Management, University of California, BerkeleyDepartment of Aquatic Ecology, EawagInstitute of Biochemistry and Biology, University of PotsdamINRAE, Sorbonne Université, CNRS, IRD, UPEC, Université Paris Diderot, Institute of Ecology and Environmental Sciences of Paris, iEES-ParisInstitute for Evolution and Biodiversity, Universität MünsterLaboratorio de Control Biológico, Instituto de Ciencias Biológicas, Universidad de TalcaInstitute for Evolution and Biodiversity, Universität MünsterUniversité Côte d’Azur, INRAE, CNRS, ISAINRAE, Sorbonne Université, CNRS, IRD, UPEC, Université Paris Diderot, Institute of Ecology and Environmental Sciences of Paris, iEES-ParisINRAE, Sorbonne Université, CNRS, IRD, UPEC, Université Paris Diderot, Institute of Ecology and Environmental Sciences of Paris, iEES-ParisDepartment of Environmental Science, Policy, & Management, University of California, BerkeleyUniversité Côte d’Azur, INRAE, CNRS, ISADepartment of Sciences, University of BasilicataDepartment of Biology, Earlham CollegeIGEPP, Agrocampus Ouest, INRAE, Université de RennesUniversité Côte d’Azur, INRAE, CNRS, ISADepartment of Entomology, Max Planck Institute for Chemical EcologyDepartment of Ecology and Evolution, Université de LausanneIGEPP, Agrocampus Ouest, INRAE, Université de RennesInstituto de Ciencias Biológicas, Universidad de TalcaDepartment of Aquatic Ecology, EawagIGEPP, Agrocampus Ouest, INRAE, Université de RennesInstitute for Evolution and Biodiversity, Universität MünsterAbstract 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 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 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 .http://link.springer.com/article/10.1186/s12864-020-6764-0Parasitoid waspAphid hostAphidius erviLysiphlebus fabarumGC contentde novo genome assembly