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

Claude Rispe (1) , Fabrice Legeai (2, 3) , Paul Nabity (4) , Rosa Fernández (5, 6) , Arinder Arora (7) , Patrice Baa-Puyoulet (8) , Celeste Banfill (9) , Leticia Bao (10) , Miquel Barberà (11) , Maryem Bouallegue (12) , Anthony Bretaudeau (2) , Jennifer A. Brisson (13) , Federica Calevro (8) , Pierre Capy (14) , Olivier Catrice (15) , Thomas Chertemps (16) , Carole Couture (17) , Laurent Deliere (17) , Angela Douglas (7) , Keith Dufault-Thompson (18) , Paula Escuer (19) , Honglin Feng (9, 20) , Astrid Forneck (21) , Toni Gabaldón (22, 23) , Roderic Guigó (22) , Frédérique Hilliou (24) , Silvia Hinojosa-Alvarez (19) , Yi-Min Hsiao (25, 26) , Sylvie Hudaverdian (2) , Emmanuelle Jacquin-Joly (16) , Edward James (9) , Spencer J. Johnston (27) , Benjamin Joubard (17) , Gaëlle Le Goff (24) , Gaël Le Trionnaire (2) , Pablo Librado (28) , Shanlin Liu (29, 30) , Eric Lombaert (24) , Hsiao-Ling Lu (31) , Martine Maïbèche (16) , Mohamed Makni (12) , Marina Marcet-Houben (5) , David Martinez-Torres (11) , Camille Meslin (16) , Nicolas Montagné (16) , Nancy Moran (32) , Daciana Papura (17) , Nicolas Parisot (8) , Yvan Rahbé (33, 34, 35, 36, 37) , Mélanie Ribeiro Lopes (8) , Aida Ripoll-Cladellas (5) , Stéphanie Robin (2) , Céline Roques (38) , Celine Lopez-Roques (38) , Pascale Roux (17) , Julio Rozas (19) , Alejandro Sanchez-Gracia (19) , Jose Sánchez-Herrero (19) , Didac Santesmasses (5, 39) , Iris Scatoni (10) , Rémy-Félix Serre (38) , Ming Tang (30) , Wenhua Tian (40) , Paul Umina (41) , Manuella van Munster (35) , Carole Vincent-Monégat (8) , Joshua Wemmer (40) , Alex Wilson (9) , Ying Zhang (18) , Chaoyang Zhao (40) , Jing Zhao (29) , Serena Zhao (32) , Xin Zhou (30) , François Delmotte (17) , Denis Tagu (2)

1 BIOEPAR - Biologie, Epidémiologie et analyse de risque en Santé Animale
2 IGEPP - Institut de Génétique, Environnement et Protection des Plantes
3 GenScale - Scalable, Optimized and Parallel Algorithms for Genomics
4 Department of Botany and Plant Sciences [Riverside]
5 CRG - Centre for Genomic Regulation - Centre de Regulació Genòmica [Barcelona]
6 IBE - Institut de Biologia Evolutiva [Barcelona]
7 Department of Entomology [CALS]
8 BF2I - Biologie Fonctionnelle, Insectes et Interactions
9 University of Miami [Coral Gables]
10 UDELAR - Universidad de la República [Montevideo]
11 UV - Universitat de València
12 FST - Faculté des Sciences Mathématiques, Physiques et Naturelles de Tunis
13 University of Rochester [USA]
14 EGCE - Evolution, génomes, comportement et écologie
15 LIPME - Laboratoire des Interactions Plantes Microbes Environnement
16 iEES Paris - Institut d'écologie et des sciences de l'environnement de Paris
17 UMR SAVE - Santé et agroécologie du vignoble
18 URI - University of Rhode Island
19 UB - Universitat de Barcelona
20 Boyce Thompson Institute [Ithaca]
21 BOKU - Universität für Bodenkultur Wien = University of Natural Resources and Life [Vienne, Autriche]
22 CRG-UPF - Center for Genomic Regulation
23 ICREA - Institució Catalana de Recerca i Estudis Avançats = Catalan Institution for Research and Advanced Studies
24 ISA - Institut Sophia Agrobiotech
25 NTU - National Taiwan University [Taiwan]
26 CGMH - Chang Gung Memorial Hospital [Taipei]
27 Texas A&M University [College Station]
28 AMIS - Anthropologie Moléculaire et Imagerie de Synthèse
29 BGI - Beijing Genomics Institute [Shenzhen]
30 CAU - China Agricultural University
31 MDU - MingDao University
32 University of Texas at Austin [Austin]
33 MTSB - Trafic et signalisation membranaires chez les bactéries
34 MAP - Microbiologie, adaptation et pathogénie
35 UMR BGPI - Biologie et Génétique des Interactions Plante-Parasite
36 INRAE - Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement
37 SPE - Sciences pour l'environnement
38 GeT-PlaGe - Génome et Transcriptome - Plateforme Génomique
39 BWH - Brigham & Women’s Hospital [Boston]
40 UC Riverside - University of California [Riverside]
41 University of Melbourne

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.

Il existe une correction à cet article : DOI : 10.1186/s12915-020-00864-7; clé UT : 000570626800001; PubMed ID: 32917281

Mots clés: Biological invasions; Arthropod genomes; Daktulosphaira vitifoliae; Gene duplications; Host plant interactions; Effectors

Domaines: Sciences du Vivant [q-bio]

Claude Rispe, Fabrice Legeai, Paul Nabity, Rosa Fernández, Arinder Arora, et al.. The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest. BMC Biology, 2020, 18 (1), pp.90. ⟨10.1186/s12915-020-00820-5⟩. ⟨hal-02917617⟩