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 Fernández; Arinder K Arora; Patrice Baa-Puyoulet; Celeste R Banfill; Leticia Bao; Miquel Barberà; Maryem Bouallègue; Anthony Bretaudeau; Jennifer A Brisson; Federica Calevro; Pierre Capy; Olivier Catrice; Thomas Chertemps; Carole Couture; Laurent Delière; Angela E Douglas; Keith Dufault-Thompson; Paula Escuer; Honglin Feng; Astrid Forneck; Toni Gabaldón; Roderic Guigó; Frédérique Hilliou; Silvia Hinojosa-Alvarez; Yi-Min Hsiao; Sylvie Hudaverdian; Emmanuelle Jacquin-Joly; Edward B James; Spencer Johnston; Benjamin Joubard; Gaëlle Le Goff; Gaël Le Trionnaire; Pablo Librado; Shanlin Liu; Eric Lombaert; Hsiao-Ling Lu; Martine Maïbèche; Mohamed Makni; Marina Marcet-Houben; David Martínez-Torres; Camille Meslin; Nicolas Montagné; Nancy A Moran; Daciana Papura; Nicolas Parisot; Yvan Rahbé; Mélanie Ribeiro Lopes; Aida Ripoll-Cladellas; Stéphanie Robin; Céline Roques; Pascale Roux; Julio Rozas; Alejandro Sánchez-Gracia; Jose F Sánchez-Herrero; Didac Santesmasses; Iris Scatoni; Rémy-Félix Serre; Ming Tang; Wenhua Tian; Paul A Umina; Manuella van Munster; Carole Vincent-Monégat; Joshua Wemmer; Alex C C Wilson; Ying Zhang; Chaoyang Zhao; Jing Zhao; Serena Zhao; Xin Zhou; François Delmotte; Denis Tagu

doi:10.1186/s12915-020-00820-5

Back

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

Journal article

Open access

Peer reviewed

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 Fernández, Arinder K Arora, Patrice Baa-Puyoulet, Celeste R Banfill, Leticia Bao, Miquel Barberà, Maryem Bouallègue, …

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

2020-07-23

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

PMID: 32698880

Abstract

Biological Evolution

Genome, Insect - physiology

Animals

Hemiptera - genetics

Adaptation, Biological - genetics

Vitis

Animal Distribution

Introduced Species

Although native to North America, the invasion of the aphid-like grape phylloxera Daktulosphaira vitifoliae across the globe altered the course of grape cultivation. For the past 150 years, viticulture relied on grafting-resistant North American Vitis species 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 of D. vitifoliae as a basic tool to understand host plant manipulation, nutritional endosymbiosis, and enhance global viticulture. 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. 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.

Files and links (1)

url

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

Published (Version of record) Open

Metrics

8 Record Views

32 Times Cited - Web of Science

See more details

InCites Highlights

These are selected metrics from InCites Benchmarking & Analytics tool, related to this output

Collaboration types: Domestic collaboration; International collaboration
Citation topics: 3 Agriculture, Environment & Ecology; 3.4 Crop Science; 3.4.1898 Insect Pests & Fungal Diseases
Web Of Science research areas: Biology
ESI research areas: Biology & Biochemistry

UN Sustainable Development Goals (SDGs)

This output has contributed to the advancement of the following goals:

Source: InCites

Details

Title: The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest
Creators: Claude Rispe - BIOEPAR, INRAE, Oniris, Nantes, France. claude.rispe@inrae.fr
Fabrice Legeai - BIPAA, IGEPP, Agrocampus Ouest, INRAE, Université de Rennes 1, 35650, Le Rheu, France. fabrice.legeai@inrae.fr
Paul D Nabity - Department of Botany and Plant Sciences, University of California, Riverside, USA
Rosa Fernández - Present address: Institute of Evolutionary Biology (CSIC-UPF), Passeig marítim de la Barceloneta 37-49, 08003, Barcelona, Spain
Arinder K Arora - Department of Entomology, Cornell University, Ithaca, NY, 14853, USA
Patrice Baa-Puyoulet - Univ Lyon, INSA-Lyon, INRAE, BF2I, UMR0203, F-69621, Villeurbanne, France
Celeste R Banfill - Department of Biology, University of Miami, Coral Gables, FL, 33146, USA
Leticia Bao - Facultad de Agronomía, Montevideo, Uruguay
Miquel Barberà - Institut de Biologia Integrativa de Sistemes, Parc Cientific Universitat de Valencia, C/ Catedrático José Beltrán n° 2, 46980, Paterna, València, Spain
Maryem Bouallègue - Université de Tunis El Manar, Faculté des Sciences de Tunis, LR01ES05 Biochimie et Biotechnologie, 2092, Tunis, Tunisia
Anthony Bretaudeau - BIPAA, IGEPP, Agrocampus Ouest, INRAE, Université de Rennes 1, 35650, Le Rheu, France
Jennifer A Brisson - Department Biol, Univ Rochester, Rochester, NY, 14627, USA
Federica Calevro - Univ Lyon, INSA-Lyon, INRAE, BF2I, UMR0203, F-69621, Villeurbanne, France
Pierre Capy - Laboratoire Evolution, Génomes, Comportement, Ecologie CNRS, Univ. Paris-Sud, IRD, Université Paris-Saclay, Gif-sur-Yvette, France
Olivier Catrice - LIPM, Université de Toulouse, INRAE, CNRS, Castanet-Tolosan, France
Thomas Chertemps - Sorbonne Université, UPEC, Université Paris 7, INRAE, CNRS, IRD, Institute of Ecology and Environmental Sciences, Paris, France
Carole Couture - SAVE, INRAE, Bordeaux Sciences Agro, Villenave d'Ornon, France
Laurent Delière - SAVE, INRAE, Bordeaux Sciences Agro, Villenave d'Ornon, France
Angela E Douglas - Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY, 14853, USA
Keith Dufault-Thompson - Department of Cell and Molecular Biology, College of the Environment and Life Sciences, University of Rhode Island, Kingston, RI, USA
Paula Escuer - Departament de Genètica, Microbiologia i Estadística and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, 08028, Barcelona, Spain
Honglin Feng - Current affiliation: Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, USA
Astrid Forneck - Universität für Bodenkultur (BOKU), Vienna, Austria
Toni Gabaldón - Institució Catalana de Recerca i Estudis Avançats (ICREA), Pg. Lluís Companys 23, 08010, Barcelona, Spain
Roderic Guigó - Universitat Pompeu Fabra (UPF), Barcelona, Spain
Frédérique Hilliou - Université Côte d'Azur, INRAE, CNRS, Institut Sophia Agrobiotech, Sophia-Antipolis, France
Silvia Hinojosa-Alvarez - Departament de Genètica, Microbiologia i Estadística and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, 08028, Barcelona, Spain
Yi-Min Hsiao - Present affiliation: Bone and Joint Research Center, Chang Gung Memorial Hospital, Taoyuan, Taiwan
Sylvie Hudaverdian - IGEPP, Agrocampus Ouest, INRAE, Université de Rennes 1, 35650, Le Rheu, France
Emmanuelle Jacquin-Joly - INRAE, Institute of Ecology and Environmental Sciences, Versailles, France
Edward B James - Department of Biology, University of Miami, Coral Gables, FL, 33146, USA
Spencer Johnston - Department of Entomology, Texas A&M University, College Station, TX, 77843, USA
Benjamin Joubard - SAVE, INRAE, Bordeaux Sciences Agro, Villenave d'Ornon, France
Gaëlle Le Goff - Université Côte d'Azur, INRAE, CNRS, Institut Sophia Agrobiotech, Sophia-Antipolis, France
Gaël Le Trionnaire - IGEPP, Agrocampus Ouest, INRAE, Université de Rennes 1, 35650, Le Rheu, France
Pablo Librado - Laboratoire d'Anthropobiologie Moléculaire et d'Imagerie de Synthèse, CNRS UMR 5288, Université de Toulouse, Université Paul Sabatier, Toulouse, France
Shanlin Liu - Department of Entomology, College of Plant Protection, China Agricultural University, Beijing, 100193, People's Republic of China
Eric Lombaert - Université Côte d'Azur, INRAE, CNRS, ISA, Sophia Antipolis, France
Hsiao-Ling Lu - Department of Post-Modern Agriculture, MingDao University, Changhua, Taiwan
Martine Maïbèche - Sorbonne Université, UPEC, Université Paris 7, INRAE, CNRS, IRD, Institute of Ecology and Environmental Sciences, Paris, France
Mohamed Makni - Université de Tunis El Manar, Faculté des Sciences de Tunis, LR01ES05 Biochimie et Biotechnologie, 2092, Tunis, Tunisia
Marina Marcet-Houben - Bioinformatics and Genomics Unit, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader, 88, 08003, Barcelona, Spain
David Martínez-Torres - Institut de Biologia Integrativa de Sistemes, Parc Cientific Universitat de Valencia, C/ Catedrático José Beltrán n° 2, 46980, Paterna, València, Spain
Camille Meslin - INRAE, Institute of Ecology and Environmental Sciences, Versailles, France
Nicolas Montagné - Sorbonne Université, Institute of Ecology and Environmental Sciences, Paris, France
Nancy A Moran - Department of Integrative Biology, University of Texas at Austin, Austin, USA
Daciana Papura - SAVE, INRAE, Bordeaux Sciences Agro, Villenave d'Ornon, France
Nicolas Parisot - Univ Lyon, INSA-Lyon, INRAE, BF2I, UMR0203, F-69621, Villeurbanne, France
Yvan Rahbé - Univ Lyon, INRAE, INSA-Lyon, CNRS, UCBL, UMR5240 MAP, F-69622, Villeurbanne, France
Mélanie Ribeiro Lopes - Univ Lyon, INSA-Lyon, INRAE, BF2I, UMR0203, F-69621, Villeurbanne, France
Aida Ripoll-Cladellas - Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
Stéphanie Robin - BIPAA IGEPP, Agrocampus Ouest, INRAE, Université de Rennes 1, 35650, Le Rheu, France
Céline Roques - Plateforme Génomique GeT-PlaGe, Centre INRAE de Toulouse Midi-Pyrénées, 24 Chemin de Borde Rouge, Auzeville, CS 52627, 31326, Castanet-Tolosan Cedex, France
Pascale Roux - SAVE, INRAE, Bordeaux Sciences Agro, Villenave d'Ornon, France
Julio Rozas - Departament de Genètica, Microbiologia i Estadística and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, 08028, Barcelona, Spain
Alejandro Sánchez-Gracia - Departament de Genètica, Microbiologia i Estadística and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, 08028, Barcelona, Spain
Jose F Sánchez-Herrero - Departament de Genètica, Microbiologia i Estadística and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, 08028, Barcelona, Spain
Didac Santesmasses - Division of Genetics, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, 02115, USA
Iris Scatoni - Facultad de Agronoía, Montevideo, Uruguay
Rémy-Félix Serre - Plateforme Génomique GeT-PlaGe, Centre INRAE de Toulouse Midi-Pyrénées, 24 Chemin de Borde Rouge, Auzeville, CS 52627, 31326, Castanet-Tolosan Cedex, France
Ming Tang - Department of Entomology, College of Plant Protection, China Agricultural University, Beijing, 100193, People's Republic of China
Wenhua Tian - Department of Botany and Plant Sciences, University of California, Riverside, USA
Paul A Umina - School of BioSciences, The University of Melbourne, Parkville, VIC, Australia
Manuella van Munster - BGPI, Université Montpellier, CIRAD, INRAE, Montpellier SupAgro, Montpellier, France
Carole Vincent-Monégat - Univ Lyon, INSA-Lyon, INRAE, BF2I, UMR0203, F-69621, Villeurbanne, France
Joshua Wemmer - Department of Botany and Plant Sciences, University of California, Riverside, USA
Alex C C Wilson - Department of Biology, University of Miami, Coral Gables, FL, 33146, USA
Ying Zhang - Department of Cell and Molecular Biology, College of the Environment and Life Sciences, University of Rhode Island, Kingston, RI, USA
Chaoyang Zhao - Department of Botany and Plant Sciences, University of California, Riverside, USA
Jing Zhao - BGI-Shenzhen, Shenzhen, 518083, Guangdong Province, People's Republic of China
Serena Zhao - Department of Integrative Biology, University of Texas at Austin, Austin, USA
Xin Zhou - Department of Entomology, College of Plant Protection, China Agricultural University, Beijing, 100193, People's Republic of China
François Delmotte - SAVE, INRAE, Bordeaux Sciences Agro, Villenave d'Ornon, France. francois.delmotte@inrae.fr
Denis Tagu - IGEPP, Agrocampus Ouest, INRAE, Université de Rennes 1, 35650, Le Rheu, France. denis.tagu@inrae.fr
Publication Details: BMC biology, Vol.18(1), pp.90-90
Grant note: IJCI-2015-26627 / Doctorate Fellowship Foundation of Nanjing Forestry University (CN) 747607 / H2020 Marie Skłodowska-Curie Actions 764840 / H2020 Marie Skłodowska-Curie Actions 12216941 / US National Institute for Food and Agriculture
Academic Unit: College of A&S; A&S - Biology
Language: English
Resource Type: Journal article
PMID: 32698880
Record Identifier: 991031600428002976