BMC Biology (2020-07-01)

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 Baa-Puyoulet,
  • Celeste R. Banfill,
  • Leticia Bao,
  • Miquel 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-Alvarez,
  • Yi-min Hsiao,
  • Sylvie Hudaverdian,
  • Emmanuelle Jacquin-Joly,
  • Edward B. James,
  • Spencer Johnston,
  • Benjamin Joubard,
  • Gaëlle Le Goff,
  • Gaël Le Trionnaire,
  • Pablo Librado,
  • Shanlin Liu,
  • Eric Lombaert,
  • Hsiao-ling Lu,
  • Martine Maïbèche,
  • Mohamed Makni,
  • Marina Marcet-Houben,
  • David Martínez-Torres,
  • Camille Meslin,
  • Nicolas Montagné,
  • Nancy A. Moran,
  • Daciana Papura,
  • Nicolas Parisot,
  • Yvan Rahbé,
  • Mélanie Ribeiro Lopes,
  • Aida Ripoll-Cladellas,
  • Stéphanie Robin,
  • Céline Roques,
  • Pascale Roux,
  • Julio Rozas,
  • Alejandro Sánchez-Gracia,
  • Jose F. Sánchez-Herrero,
  • Didac Santesmasses,
  • Iris 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 Zhao,
  • Xin Zhou,
  • François Delmotte,
  • Denis Tagu

Journal volume & issue
Vol. 18, no. 1
pp. 1 – 25


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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.