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


Claude Rispe, INRAE
Fabrice Legeai, Universite de Rennes 1
Paul D. Nabity, University of California, Riverside
Rosa Fernández, Barcelona Institute of Science and Technology (BIST)
Arinder K. Arora, Cornell University
Patrice Baa-Puyoulet, Institut National des Sciences Appliquées de Lyon
Celeste R. Banfill, University of Miami
Leticia Bao, Universidad de la Republica
Miquel Barberà, Universitat de València
Maryem Bouallègue, Université de Tunis El Manar, Faculté des Sciences de Tunis
Anthony Bretaudeau, Universite de Rennes 1
Jennifer A. Brisson, University of Rochester
Federica Calevro, Institut National des Sciences Appliquées de Lyon
Pierre Capy, Evolution, Génomes, Comportement et Ecologie
Olivier Catrice, Université Fédérale Toulouse Midi-Pyrénées
Thomas Chertemps, Sorbonne Universite
Carole Couture, Santé et Agroécologie du Vignoble
Laurent Delière, Santé et Agroécologie du Vignoble
Angela E. Douglas, Cornell University
Keith Dufault-Thompson, University of Rhode Island
Paula Escuer, Universitat de Barcelona
Honglin Feng, University of Miami
Astrid Forneck, Universitat fur Bodenkultur Wien
Toni Gabaldón, Barcelona Institute of Science and Technology (BIST)
Roderic Guigó, Barcelona Institute of Science and Technology (BIST)
Frédérique Hilliou, Université Côte d'Azur
Silvia Hinojosa-Alvarez, Universitat de Barcelona
Yi Min Hsiao, National Taiwan University
Sylvie Hudaverdian, Universite de Rennes 1
Emmanuelle Jacquin-Joly, Institut d'Ecologie et des Sciences de l'Environnement de Paris (IEES Paris)

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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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BMC Biology