The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest
Claude Rispe, Fabrice Legeai, Paul D. Nabity, Rosa Fernández, Arinder K. Arora, Patrice Bâa-Puyoulet, Celeste R. Banfill, Leticia Bao, Miquel Aguilar Barberà, Maryem Bouallègue, Anthony Bretaudeau, Jennifer A. Brisson, Federica Calevro, Pierre Capy, Olivier Catrice, Thomas Chertemps, Carole Couture, Laurent Delière, Angela E. Douglas, Keith Dufault‐Thompson, Paula Escuer, Honglin Feng, Astrid Forneck, Toni Gabaldón, Roderic Guigó, Frédérique Hilliou, Silvia Hinojosa‐Álvarez, Yi-Min Hsiao, Sylvie Hudaverdian, Emmanuelle Jacquin‐Joly, Edward James, Spencer Johnston, Benjamin Joubard, Gaëlle Le Goff, Gaël Le Trionnaire, Pablo Librado, Shanlin Liu, Éric Lombaert, Hsiao-ling Lu, Martine Maı̈bèche, Mohamed Makni, Marina Marcet‐Houben, David R. Martinez, Camille Meslin, Nicolas Montagné, Nancy A. Moran, Daciana Papura, Nicolas Parisot, Yvan Rahbé, Mélanie Ribeiro Lopes, Aida Ripoll-Cladellas, Stephanie Stephanie, Céline Lopez‐Roques, Pascale Roux, Julio Rozas, Alejandro Sánchez‐Gracia, José Francisco Sánchez-Herrero, Didac Santesmasses, Iris B. Scatoni, Rémy-Félix Serre, Ming Tang, Wenhua Tian, Paul A. Umina, Manuella van Munster, Carole Vincent-Monégat, Joshua Wemmer, Alex C. C. Wilson, Ying Zhang, Chaoyang Zhao, Jing Zhao, Serena Y. Zhao, Xin Zhou, François Delmotte, Denis Tagu
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.