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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 Paul Nabity 3 Rosa Fernández 4, 5 Arinder Arora 6 Patrice Baa-Puyoulet 7 Celeste Banfill 8 Leticia Bao 9 Miquel Barberà 10 Maryem Bouallegue 11 Anthony Bretaudeau 2 Jennifer Brisson 12 Federica Calevro 7 Pierre Capy 13 Olivier Catrice 14 Thomas Chertemps 15 Carole Couture 16 Laurent Deliere 16 Angela Douglas 6 Keith Dufault-Thompson 17 Paula Escuer 18 Honglin Feng 8, 19 Astrid Forneck 20 Toni Gabaldón 21, 22 Roderic Guigó 21 Frédérique Hilliou 23 Silvia Hinojosa-Alvarez 18 Yi-Min Hsiao 24, 25 Sylvie Hudaverdian 2 Emmanuelle Jacquin-Joly 15 Edward James 8 Spencer Johnston 26 Benjamin Joubard 16 Gaëlle Le Goff 23 Gaël Le Trionnaire 2 Pablo Librado 27 Shanlin Liu 28, 29 Eric Lombaert 23 Hsiao-Ling Lu 30 Martine Maïbèche 15 Mohamed Makni 11 Marina Marcet-Houben 4 David Martinez-Torres 10 Camille Meslin 15 Nicolas Montagné 15 Nancy Moran 31 Daciana Papura 16 Nicolas Parisot 7 Yvan Rahbé 32, 33, 34 Mélanie Ribeiro Lopes 7 Aida Ripoll-Cladellas 4 Stéphanie Robin 2 Céline Roques 35 Celine Lopez-Roques 35 Pascale Roux 16 Julio Rozas 18 Alejandro Sanchez-Gracia 18 Jose Sánchez-Herrero 18 Didac Santesmasses 4, 36 Iris Scatoni 9 Rémy-Félix Serre 35 Ming Tang 29 Wenhua Tian 37 Paul Umina 38 Manuella van Munster 34 Carole Vincent-Monégat 7 Joshua Wemmer 37 Alex Wilson 8 Ying Zhang 17 Chaoyang Zhao 37 Jing Zhao 28 Serena Zhao 31 Xin Zhou 29 François Delmotte 16 Denis Tagu 2
* Auteur correspondant
32 MTSB - Trafic et signalisation membranaires chez les bactéries
MAP - Microbiologie, adaptation et pathogénie
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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Soumis le : mardi 29 septembre 2020 - 12:27:28
Dernière modification le : lundi 16 novembre 2020 - 15:48:02

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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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