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

BMC Biology

Manuella van Munster¹  Claude Rispe²  Stéphanie Robin³  Anthony Bretaudeau⁴  Fabrice Legeai⁴  Marina Marcet-Houben⁵  Toni Gabaldón⁵  Rosa Fernández⁵  Roderic Guigó⁶  Didac Santesmasses⁶  Aida Ripoll-Cladellas⁶  Jing Zhao⁷  Shanlin Liu⁷  Alejandro Sánchez-Gracia⁸  Julio Rozas⁸  Silvia Hinojosa-Alvarez⁸  Paula Escuer⁸  Jose F. Sánchez-Herrero⁸  Jennifer A. Brisson⁹  Edward B. James^1,10  Celeste R. Banfill^1,10  Alex C. C. Wilson^1,10  Honglin Feng^1,10  Joshua Wemmer^1,11  Wenhua Tian^1,11  Chaoyang Zhao^1,11  Paul D. Nabity^1,11  Keith Dufault-Thompson^1,12  Ying Zhang^1,12  Xin Zhou^1,13  Ming Tang^1,13  Angela E. Douglas^1,14  Arinder K. Arora^1,14  Spencer Johnston^1,15  Nancy A. Moran^1,16  Serena Zhao^1,16  Hsiao-ling Lu^1,17  Leticia Bao^1,18  Iris Scatoni^1,19  Gaël Le Trionnaire^2,20  Denis Tagu^2,20  Sylvie Hudaverdian^2,20  Emmanuelle Jacquin-Joly^2,21  Camille Meslin^2,21  Miquel Barberà^2,22  David Martínez-Torres^2,22  Yi-min Hsiao^2,23  Olivier Catrice^2,24  Pierre Capy^2,25  Pablo Librado^2,26  Rémy-Félix Serre^2,27  Céline Roques^2,27  Daciana Papura^2,28  Pascale Roux^2,28  Carole Couture^2,28  Benjamin Joubard^2,28  Laurent Delière^2,28  François Delmotte^2,28  Paul A. Umina^2,29  Nicolas Montagné^3,30  Thomas Chertemps^3,31  Martine Maïbèche^3,31  Yvan Rahbé^3,32  Mélanie Ribeiro Lopes^3,33  Federica Calevro^3,33  Patrice Baa-Puyoulet^3,33  Nicolas Parisot^3,33  Carole Vincent-Monégat^3,33  Astrid Forneck^3,34  Eric Lombaert^3,35  Gaëlle Le Goff^3,36  Frédérique Hilliou^3,36  Mohamed Makni^3,37  Maryem Bouallègue^3,37 

[1] BGPI, Université Montpellier, CIRAD, INRAE, Montpellier SupAgro;BIOEPAR, INRAE, Oniris;BIPAA IGEPP, Agrocampus Ouest, INRAE, Université de Rennes 1;BIPAA, IGEPP, Agrocampus Ouest, INRAE, Université de Rennes 1;Bioinformatics and Genomics Unit, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology;Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology;China National GeneBank-Shenzhen, BGI-Shenzhen;Departament de Genètica, Microbiologia i Estadística and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona;Department Biol, Univ Rochester;Department of Biology, University of Miami;Department of Botany and Plant Sciences, University of California;Department of Cell and Molecular Biology, College of the Environment and Life Sciences, University of Rhode Island;Department of Entomology, College of Plant Protection, China Agricultural University;Department of Entomology, Cornell University;Department of Entomology, Texas A&M University;Department of Integrative Biology, University of Texas at Austin;Department of Post-Modern Agriculture, MingDao University;Facultad de Agronomía;Facultad de Agronoía;IGEPP, Agrocampus Ouest, INRAE, Université de Rennes 1;INRAE, Institute of Ecology and Environmental Sciences;Institut de Biologia Integrativa de Sistemes, Parc Cientific Universitat de Valencia;Institute of Biotechnology and Department of Entomology, College of Bioresources and Agriculture, National Taiwan University;LIPM, Université de Toulouse, INRAE, CNRS;Laboratoire Evolution, Génomes, Comportement, Ecologie CNRS, Univ. Paris-Sud, IRD, Université Paris-Saclay;Laboratoire d’Anthropobiologie Moléculaire et d’Imagerie de Synthèse, CNRS UMR 5288, Université de Toulouse, Université Paul Sabatier;Plateforme Génomique GeT-PlaGe, Centre INRAE de Toulouse Midi-Pyrénées;SAVE, INRAE, Bordeaux Sciences Agro;School of BioSciences, The University of Melbourne;Sorbonne Université, Institute of Ecology and Environmental Sciences;Sorbonne Université, UPEC, Université Paris 7, INRAE, CNRS, IRD, Institute of Ecology and Environmental Sciences;Univ Lyon, INRAE, INSA-Lyon, CNRS, UCBL, UMR5240 MAP;Univ Lyon, INSA-Lyon, INRAE, BF2I, UMR0203, F-69621;Universität für Bodenkultur (BOKU);Université Côte d’Azur, INRAE, CNRS, ISA;Université Côte d’Azur, INRAE, CNRS, Institut Sophia Agrobiotech;Université de Tunis El Manar, Faculté des Sciences de Tunis, LR01ES05 Biochimie et Biotechnologie;

关键词: Arthropod genomes;    Daktulosphaira vitifoliae;    Gene duplications;    Host plant interactions;    Effectors;    Biological invasions;   

DOI  :  10.1186/s12915-020-00820-5

来源: DOAJ

【 摘 要 】

Abstract Background 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. 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.

【 授权许可】

Unknown