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

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• dc.contributor.author Rispe, Claude
• dc.contributor.author Fernández, Rosa
• dc.contributor.author Gabaldón Estevan, Juan Antonio, 1973-
• dc.contributor.author Guigó Serra, Roderic
• dc.contributor.author Ripoll Cladellas, Aida
• dc.contributor.author Tagu, Denis
• dc.date.accessioned 2020-09-15T06:27:05Z
• dc.date.available 2020-09-15T06:27:05Z
• dc.date.issued 2020
• dc.description.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.
• dc.description.sponsorship This work has been funded by INRAE (France) and by the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement no. 764840 for the ITN IGNITE project. Rosa Fernandez was funded by a Juan de la Cierva-Incorporación Fellowship (Government of Spain, IJCI-2015-26627) and a Marie Skłodowska-Curie Fellowship (747607). Angela Douglas was supported by the US National Institute of Food and Agriculture Grant 12216941. Honglin Feng was supported by a University of Miami Maytag Fellowship, William H. Evoy Graduate Research Support Fund, and a Molecular Biosciences Graduate Research Award from the Department of Biology.
• dc.format.mimetype application/pdf
• dc.identifier.citation Rispe C, Legeai F, Nabity PD, Fernández R, Arora AK, Baa-Puyoulet P et al. The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest. BMC Biol. 2020; 18(1):90. DOI: 10.1186/s12915-020-00820-5
• dc.identifier.doi http://dx.doi.org/10.1186/s12915-020-00820-5
• dc.identifier.issn 1741-7007
• dc.identifier.uri http://hdl.handle.net/10230/45284
• dc.language.iso eng
• dc.publisher BioMed Central
• dc.relation.ispartof BMC Biol. 2020; 18(1):90
• dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/764840
• dc.rights © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data ma
• dc.rights.accessRights info:eu-repo/semantics/openAccess
• dc.rights.uri http://creativecommons.org/licenses/by/4.0/
• dc.subject.keyword Arthropod genomes
• dc.subject.keyword Biological invasions
• dc.subject.keyword Daktulosphaira vitifoliae
• dc.subject.keyword Effectors
• dc.subject.keyword Gene duplications
• dc.subject.keyword Host plant interactions
• dc.title The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest
• dc.type info:eu-repo/semantics/article
• dc.type.version info:eu-repo/semantics/publishedVersion