The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest

Claude Rispe; Fabrice Legeai; Paul D. Nabity; Rosa Fernandez; Arinder K. Arora; Patrice Baa-Puyoulet; Celeste R. Banfill; Leticia Bao; Miquel Barbera; Maryem Bouallegue; Anthony Bretaudeau; Jennifer A. Brisson; Federica Calevro; Pierre Capy; Olivier Catrice; Thomas Chertemps; Carole Couture; Laurent Deliere; Angela E. Douglas; Keith Dufault-Thompson; Paula Escuer; Honglin Feng; Astrid Forneck; Toni Gabaldon; Roderic Guigo; Frederique Hilliou; Silvia Hinojosa-Alvarez; Yi-Min Hsiao; Sylvie Hudaverdian; Emmanuelle Jacquin-Joly; Edward B. James; Spencer Johnston; Benjamin Joubard; Gaelle Le Goff; Gael Le Trionnaire; Pablo Librado; Shanlin Liu; Eric Lombaert; Hsiao-Ling Lu; Martine Maibeche; Mohamed Makni; Marina Marcet-Houben; David Martinez-Torres; Camille Meslin; Nicolas Montagne; Nancy A. Moran; Daciana Papura; Nicolas Parisot; Yvan Rahbe; Melanie Ribeiro Lopes; Aida Ripoll-Cladellas; Stephanie Robin; Celine Roques; Pascale Roux; Julio Rozas; Alejandro Sanchez-Gracia; Jose F. Sanchez-Herrero; Didac Santesmasses; Iris Scatoni; Remy-Felix Serre; Ming Tang; Wenhua Tian; Paul A. Umina; Manuella van Munster; Carole Vincent-Monegat; Joshua Wemmer; Alex C. C. Wilson; Ying Zhang; Chaoyang Zhao; Jing Zhao; Serena Zhao; Xin Zhou; Francois Delmotte; Denis Tagu

doi:10.1186/s12915-020-00820-5

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The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest

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The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest

Claude Rispe, Fabrice Legeai, Paul D. Nabity, Rosa Fernandez, Arinder K. Arora, Patrice Baa-Puyoulet, Celeste R. Banfill, Leticia Bao, Miquel Barbera, Maryem Bouallegue, …

BMC biology, Vol.18(1), pp.90-25

23/07/2020

DOI: https://doi.org/10.1186/s12915-020-00820-5

PMID: 32698880

Résumé

Biology

Life Sciences & Biomedicine

Life Sciences & Biomedicine - Other Topics

Science & Technology

Background Although native to North America, the invasion of the aphid-like grape phylloxeraDaktulosphaira vitifoliaeacross the globe altered the course of grape cultivation. For the past 150 years, viticulture relied on grafting-resistant North AmericanVitisspecies as rootstocks, thereby limiting genetic stocks tolerant to other stressors such as pathogens and climate change. Limited understanding of the insect genetics resulted in successive outbreaks across the globe when rootstocks failed. Here we report the 294-Mb genome ofD. vitifoliaeas a basic tool to understand host plant manipulation, nutritional endosymbiosis, and enhance global viticulture. Results Using a combination of genome, RNA, and population resequencing, we found grape phylloxera showed high duplication rates since its common ancestor with aphids, but similarity in most metabolic genes, despite lacking obligate nutritional symbioses and feeding from parenchyma. Similarly, no enrichment occurred in development genes in relation to viviparity. However, phylloxera evolved > 2700 unique genes that resemble putative effectors and are active during feeding. Population sequencing revealed the global invasion began from the upper Mississippi River in North America, spread to Europe and from there to the rest of the world. Conclusions The grape phylloxera genome reveals genetic architecture relative to the evolution of nutritional endosymbiosis, viviparity, and herbivory. The extraordinary expansion in effector genes also suggests novel adaptations to plant feeding and how insects induce complex plant phenotypes, for instance galls. Finally, our understanding of the origin of this invasive species and its genome provide genetics resources to alleviate rootstock bottlenecks restricting the advancement of viticulture.

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Titre: The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest
Créateurs - sans rôle: Claude Rispe - Oniris, INRAE, BIOEPAR, Nantes, France
Fabrice Legeai - Univ Rennes 1, INRAE, Agrocampus Ouest, BIPAA,IGEPP, F-35650 Le Rheu, France
Paul D. Nabity - Univ Calif Riverside, Dept Bot & Plant Sci, Riverside, CA 92521 USA
Rosa Fernandez - Barcelona Inste Sci & Technol, Bioinformat & Genom Unit, Ctr Genom Regulat CRG, Dr Aiguader 88, Barcelona 08003, Spain
Arinder K. Arora - Cornell Univ, Dept Entomol, Ithaca, NY 14853 USA
Patrice Baa-Puyoulet - Univ Lyon, INSA Lyon, INRAE, BF2I,UMR0203, F-69621 Villeurbanne, France
Celeste R. Banfill - Univ Miami, Dept Biol, Coral Gables, FL 33146 USA
Leticia Bao - Fac Agron, Montevideo, Uruguay
Miquel Barbera - Inst Biol Integrat Sistemes, Parc Cient Univ Valencia, Valencia 46980, Spain
Maryem Bouallegue - Univ Tunis El Manar, LR01ES05 Biochim & Biotechnol, Fac Sci Tunis, Tunis 2092, Tunisia
Anthony Bretaudeau - Univ Rennes 1, INRAE, Agrocampus Ouest, BIPAA,IGEPP, F-35650 Le Rheu, France
Jennifer A. Brisson - Univ Rochester, Dept Biol, Rochester, NY 14627 USA
Federica Calevro - Univ Lyon, INSA Lyon, INRAE, BF2I,UMR0203, F-69621 Villeurbanne, France
Pierre Capy - Univ Paris Saclay, Univ Paris Sud, Lab Evolut Genomes Comportement Ecol, CNRS,IRD, Gif Sur Yvette, France
Olivier Catrice - Univ Toulouse, CNRS, INRAE, LIPM, Castanet Tolosan, France
Thomas Chertemps - Sorbonne Univ, UPEC, Univ Paris 7, INRAE,CNRS,IRD,Inst Ecol & Environm Sci, Paris, France
Carole Couture - Bordeaux Sci Agro, INRAE, SAVE, Villenave Dornon, France
Laurent Deliere - Bordeaux Sci Agro, INRAE, SAVE, Villenave Dornon, France
Angela E. Douglas - Cornell Univ, Dept Entomol, Ithaca, NY 14853 USA
Keith Dufault-Thompson - Univ Rhode Isl, Coll Environm & Life Sci, Dept Cell & Mol Biol, Kingston, RI 02881 USA
Paula Escuer - Univ Barcelona, Dept Genet Microbiol & Estat, Barcelona 08028, Spain
Honglin Feng - Univ Miami, Dept Biol, Coral Gables, FL 33146 USA
Astrid Forneck - Univ Bodenkultur BOKU, Vienna, Austria
Toni Gabaldon - Barcelona Inste Sci & Technol, Bioinformat & Genom Unit, Ctr Genom Regulat CRG, Dr Aiguader 88, Barcelona 08003, Spain
Roderic Guigo - Barcelona Inst Sci & Technol, Ctr Genom Regulat CRG, Barcelona, Spain
Frederique Hilliou - Univ Cote Azur, Inst Sophia Agrobiotech, INRAE, CNRS, Sophia Antipolis, France
Silvia Hinojosa-Alvarez - Univ Barcelona, Dept Genet Microbiol & Estat, Barcelona 08028, Spain
Yi-Min Hsiao - Natl Taiwan Univ, Coll Bioresources & Agr, Inst Biotechnol, Taipei, Taiwan
Sylvie Hudaverdian - Université de Rennes
Emmanuelle Jacquin-Joly - Inste Ecol & Environm Sci, INRAE, Versailles, France
Edward B. James - Univ Miami, Dept Biol, Coral Gables, FL 33146 USA
Spencer Johnston - Texas A&M Univ, Dept Entomol, College Stn, TX 77843 USA
Benjamin Joubard - Bordeaux Sci Agro, INRAE, SAVE, Villenave Dornon, France
Gaelle Le Goff - Univ Cote dAzur, Inst Sophia Agrobiotech, INRAE, CNRS, Sophia Antipolis, France
Gael Le Trionnaire - Université de Rennes
Pablo Librado - Univ Paul Sabatier, Univ Toulouse, CNRS UMR 5288, Lab Anthropobiol Mol & Imagerie Synth, Toulouse, France
Shanlin Liu - BGI Shenzhen, China Natl GeneBank Shenzhen, Shenzhen 518083, Guangdong, Peoples R China
Eric Lombaert - Univ Cote dAzur, INRAE, ISA, CNRS, Sophia Antipolis, France
Hsiao-Ling Lu - MingDao Univ, Dept Postmodern Agr, Changhua, Taiwan
Martine Maibeche - Sorbonne Univ, UPEC, Univ Paris 7, INRAE,CNRS,IRD,Inst Ecol & Environm Sci, Paris, France
Mohamed Makni - Univ Tunis El Manar, LR01ES05 Biochim & Biotechnol, Fac Sci Tunis, Tunis 2092, Tunisia
Marina Marcet-Houben - Barcelona Inste Sci & Technol, Bioinformat & Genom Unit, Ctr Genom Regulat CRG, Dr Aiguader 88, Barcelona 08003, Spain
David Martinez-Torres - Inst Biol Integrat Sistemes, Parc Cient Univ Valencia, Valencia 46980, Spain
Camille Meslin - Inste Ecol & Environm Sci, INRAE, Versailles, France
Nicolas Montagne - Sorbonne Univ, Inste Ecol & Environm Sci, Paris, France
Nancy A. Moran - Univ Texas Austin, Dept Integrat Biol, Austin, TX 78712 USA
Daciana Papura - Bordeaux Sci Agro, INRAE, SAVE, Villenave Dornon, France
Nicolas Parisot - Univ Lyon, INSA Lyon, INRAE, BF2I,UMR0203, F-69621 Villeurbanne, France
Yvan Rahbe - Institut National des Sciences Appliquées de Lyon
Melanie Ribeiro Lopes - Univ Lyon, INSA Lyon, INRAE, BF2I,UMR0203, F-69621 Villeurbanne, France
Aida Ripoll-Cladellas - Barcelona Inst Sci & Technol, Ctr Genom Regulat CRG, Barcelona, Spain
Stephanie Robin - Univ Rennes 1, BIPAA IGEPP, Agrocampus Ouest, INRAE, F-35650 Le Rheu, France
Celine Roques - Ctr INRAE Toulouse Midi Pyrenees, Plateforme Genom GeT PlaGe, 24 Chemin Borde Rouge,CS 52627, F-31326 Castanet Tolosan, France
Pascale Roux - Bordeaux Sci Agro, INRAE, SAVE, Villenave Dornon, France
Julio Rozas - Univ Barcelona, Dept Genet Microbiol & Estat, Barcelona 08028, Spain
Alejandro Sanchez-Gracia - Univ Barcelona, Dept Genet Microbiol & Estat, Barcelona 08028, Spain
Jose F. Sanchez-Herrero - Univ Barcelona, Dept Genet Microbiol & Estat, Barcelona 08028, Spain
Didac Santesmasses - Barcelona Inst Sci & Technol, Ctr Genom Regulat CRG, Barcelona, Spain
Iris Scatoni - Fac Agronoia, Montevideo, Uruguay
Remy-Felix Serre - Ctr INRAE Toulouse Midi Pyrenees, Plateforme Genom GeT PlaGe, 24 Chemin Borde Rouge,CS 52627, F-31326 Castanet Tolosan, France
Ming Tang - China Agr Univ, Coll Plant Protect, Dept Entomol, Beijing 100193, Peoples R China
Wenhua Tian - Univ Calif Riverside, Dept Bot & Plant Sci, Riverside, CA 92521 USA
Paul A. Umina - Univ Melbourne, Sch BioSci, Parkville, Vic, Australia
Manuella van Munster - Institut Agro Montpellier
Carole Vincent-Monegat - Univ Lyon, INSA Lyon, INRAE, BF2I,UMR0203, F-69621 Villeurbanne, France
Joshua Wemmer - Univ Calif Riverside, Dept Bot & Plant Sci, Riverside, CA 92521 USA
Alex C. C. Wilson - Univ Miami, Dept Biol, Coral Gables, FL 33146 USA
Ying Zhang - Univ Rhode Isl, Coll Environm & Life Sci, Dept Cell & Mol Biol, Kingston, RI 02881 USA
Chaoyang Zhao - Univ Calif Riverside, Dept Bot & Plant Sci, Riverside, CA 92521 USA
Jing Zhao - BGI Shenzhen, China Natl GeneBank Shenzhen, Shenzhen 518083, Guangdong, Peoples R China
Serena Zhao - Univ Texas Austin, Dept Integrat Biol, Austin, TX 78712 USA
Xin Zhou - China Agr Univ, Coll Plant Protect, Dept Entomol, Beijing 100193, Peoples R China
Francois Delmotte - Bordeaux Sci Agro, INRAE, SAVE, Villenave Dornon, France
Denis Tagu - Univ Rennes 1, IGEPP, Agrocampus Ouest, INRAE, F-35650 Le Rheu, France
Détails de publication: BMC biology, Vol.18(1), pp.90-25
Éditeur: Springer Nature
Nombre de pages: 25
Note de subvention: Molecular Biosciences Graduate Research Award from the Department of Biology 12216941 / US National Institute of Food and Agriculture University of Miami Maytag Fellowship from the Department of Biology IJCI-2015-26627 / Juan de la Cierva-Incorporacion Fellowship (Government of Spain) 747607 / Marie Curie Actions (MSCA); Marie Curie Actions 764840 / European Union; European Union (EU) 747607 / Marie Sklodowska-Curie Fellowship INRAE (France) William H. Evoy Graduate Research Support Fund from the Department of Biology
Identifiants: 99148093709311
Unité académique: Plant Health Institute of Montpellier - PHIM
Langue: English
Type de ressource: Journal article