The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest
Authors: Rispe Claude , Legeai Fabrice , Nabity Paul D. , Fernández Rosa , Arora Arinder K. , Baa-Puyoulet Patrice , Banfill Celeste R. , Bao Leticia , Barberà Miquel , Bouallègue Maryem , Bretaudeau Anthony , Brisson Jennifer A. , Calevro Federica , Capy Pierre , Catrice Olivier , Chertemps Thomas , Couture Carole , Delière Laurent , Douglas Angela E. , Dufault-Thompson Keith , Escuer Paula , Feng Honglin , Forneck Astrid , Gabaldón Toni , Guigó Roderic , Hilliou Frédérique , Hinojosa-Alvarez Silvia , Hsiao Yi-min , Hudaverdian Sylvie , Jacquin-Joly Emmanuelle , James Edward B. , Johnston Spencer , Joubard Benjamin , Le Goff Gaëlle , Le Trionnaire Gaël , Librado Pablo , Liu Shanlin , Lombaert Eric , Lu Hsiao-ling , Maïbèche Martine , Makni Mohamed , Marcet-Houben Marina , Martínez-Torres David , Meslin Camille , Montagné Nicolas , Moran Nancy A. , Papura Daciana , Parisot Nicolas , Rahbé Yvan , Lopes Mélanie Ribeiro , Ripoll-Cladellas Aida , Robin Stéphanie , Roques Céline , Roux Pascale , Rozas Julio , Sánchez-Gracia Alejandro , Sánchez-Herrero Jose F. , Santesmasses Didac , Scatoni Iris , Serre Rémy-Félix , Tang Ming , Tian Wenhua , Umina Paul A. , van Munster Manuella , Vincent-Monégat Carole , Wemmer Joshua , Wilson Alex C. C. , Zhang Ying , Zhao Chaoyang , Zhao Jing , Zhao Serena , Zhou Xin , Delmotte François , Tagu Denis 
Published: July 2020

Background

Although native to North America, the invasion of the aphid-like grape phylloxeraDaktulosphaira vitifoliaeacross the globe altered the course of grape cultivation. For the past 150 years, viticulture relied on grafting-resistant North AmericanVitisspecies 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 ofD. vitifoliaeas 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.