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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 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, * 
* Corresponding author
3 GenScale - Scalable, Optimized and Parallel Algorithms for Genomics
33 MTSB - Trafic et signalisation membranaires chez les bactéries
MAP - Microbiologie, adaptation et pathogénie
38 GeT-PlaGe - Génome et Transcriptome - Plateforme Génomique
GET - Plateforme Génome & Transcriptome, INRAE - Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement : US 1426
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.
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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, BioMed Central, 2020, 18 (1), pp.90. ⟨10.1186/s12915-020-00820-5⟩. ⟨hal-02917617⟩



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