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 Nabity; Rosa Fernández; Arinder Arora; Patrice Baa-Puyoulet; Celeste Banfill; Leticia Bao; Miquel Barberà; Maryem Bouallegue; Anthony Bretaudeau; Jennifer Brisson; Federica Calevro; Pierre Capy; Olivier Catrice; Thomas Chertemps; Carole Couture; Laurent Deliere; Angela 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 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 Martinez-Torres; Camille Meslin; Nicolas Montagné; Nancy Moran; Daciana Papura; Nicolas Parisot; Yvan Rahbé; Mélanie Ribeiro Lopes; Aida Ripoll-Cladellas; Stéphanie Robin; Céline Roques; Celine Lopez-Roques; Pascale Roux; Julio Rozas; Alejandro Sanchez-Gracia; Jose Sánchez-Herrero; Didac Santesmasses; Iris Scatoni; Rémy-Félix Serre; Ming Tang; Wenhua Tian; Paul Umina; Manuella van Munster; Carole Vincent-Monégat; Joshua Wemmer; Alex Wilson; Ying Zhang; Chaoyang Zhao; Jing Zhao; Serena Zhao; Xin Zhou; François Delmotte; Denis Tagu

doi:10.1186/s12915-020-00820-5

Journal articles

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

Claude Rispe ^{1, *} Fabrice Legeai ^{2, 3, *} Paul Nabity ⁴ Rosa Fernández ^{5, 6} Arinder Arora ⁷ Patrice Baa-Puyoulet ⁸ Celeste Banfill ⁹ Leticia Bao ¹⁰ Miquel Barberà ¹¹ Maryem Bouallegue ¹² Anthony Bretaudeau ² Jennifer Brisson ¹³ Federica Calevro ⁸ Pierre Capy ¹⁴ Olivier Catrice ¹⁵ Thomas Chertemps ¹⁶ Carole Couture ¹⁷ Laurent Deliere ¹⁷ Angela Douglas ⁷ Keith Dufault-Thompson ¹⁸ Paula Escuer ¹⁹ Honglin Feng ^{9, 20} Astrid Forneck ²¹ Toni Gabaldón ^{22, 23} Roderic Guigó ²² Frédérique Hilliou ²⁴ Silvia Hinojosa-Alvarez ¹⁹ Yi-Min Hsiao ^{25, 26} Sylvie Hudaverdian ² Emmanuelle Jacquin-Joly ¹⁶ Edward James ⁹ Spencer Johnston ²⁷ Benjamin Joubard ¹⁷ Gaëlle Le Goff ²⁴ Gaël Le Trionnaire ² Pablo Librado ²⁸ Shanlin Liu ^{29, 30} Eric Lombaert ²⁴ Hsiao-Ling Lu ³¹ Martine Maïbèche ¹⁶ Mohamed Makni ¹² Marina Marcet-Houben ⁵ David Martinez-Torres ¹¹ Camille Meslin ¹⁶ Nicolas Montagné ¹⁶ Nancy Moran ³² Daciana Papura ¹⁷ Nicolas Parisot ⁸ Yvan Rahbé ^{33, 34, 35} Mélanie Ribeiro Lopes ⁸ Aida Ripoll-Cladellas ⁵ Stéphanie Robin ² Céline Roques ³⁶ Celine Lopez-Roques ³⁶ Pascale Roux ¹⁷ Julio Rozas ¹⁹ Alejandro Sanchez-Gracia ¹⁹ Jose Sánchez-Herrero ¹⁹ Didac Santesmasses ^{5, 37} Iris Scatoni ¹⁰ Rémy-Félix Serre ³⁶ Ming Tang ³⁰ Wenhua Tian ³⁸ Paul Umina ³⁹ Manuella van Munster ³⁵ Carole Vincent-Monégat ⁸ Joshua Wemmer ³⁸ Alex Wilson ⁹ Ying Zhang ¹⁸ Chaoyang Zhao ³⁸ Jing Zhao ²⁹ Serena Zhao ³² Xin Zhou ³⁰ François Delmotte ^{17, *} Denis Tagu ^{2, *}

* Corresponding author

1 BIOEPAR - Biologie, Epidémiologie et analyse de risque en Santé Animale

2 IGEPP - Institut de Génétique, Environnement et Protection des Plantes

3 GenScale - Scalable, Optimized and Parallel Algorithms for Genomics

Inria Rennes – Bretagne Atlantique , IRISA-D7 - GESTION DES DONNÉES ET DE LA CONNAISSANCE

4 Department of Botany and Plant Sciences [Riverside]

5 CRG - Centre for Genomic Regulation [Barcelona]

6 IBE / UPF - CSIC - Institut de Biologia Evolutiva [Barcelona]

7 Cornell University

8 BF2I - Biologie Fonctionnelle, Insectes et Interactions

9 University of Miami [Coral Gables]

10 Facultad de Agronomía (UDELAR)

11 UV - Universitat de València

12 FST - Faculté des Sciences Mathématiques, Physiques et Naturelles de Tunis

13 University of Rochester [USA]

14 EGCE - Evolution, génomes, comportement et écologie

15 LIPM - Laboratoire des interactions plantes micro-organismes

16 IEES (UMR_7618 / UMR_D_242 / UMR_A_1392 / UM_113) - Institut d'écologie et des sciences de l'environnement de Paris

17 UMR SAVE - Santé et agroécologie du vignoble

18 URI - University of Rhode Island

19 Université de Barcelonne

20 Boyce Thompson Institute [Ithaca]

21 BOKU - Universität für Bodenkultur Wien [Vienne, Autriche]

22 CRG-UPF - Center for Genomic Regulation

23 ICREA - Institució Catalana de Recerca i Estudis Avançats

24 ISA - Institut Sophia Agrobiotech

25 NTU - National Taiwan University [Taiwan]

26 CGMH - Chang Gung Memorial Hospital [Taipei]

27 Texas A&M University [College Station]

28 AMIS - Anthropologie Moléculaire et Imagerie de Synthèse

29 BGI - Beijing Genomics Institute [Shenzhen]

30 CAU - China Agricultural University

31 MDU - MingDao University

32 University of Texas at Austin [Austin]

33 MTSB - Trafic et signalisation membranaires chez les bactéries

MAP - Microbiologie, adaptation et pathogénie

34 MAP - Microbiologie, adaptation et pathogénie

35 UMR BGPI - Biologie et Génétique des Interactions Plante-Parasite

36 GeT PlaGe - GeT PlaGe, Genotoul

37 BWH - Brigham & Women’s Hospital [Boston]

38 UCR - University of California [Riverside]

39 University of Melbourne

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.

Keywords : Arthropod genomes Daktulosphaira vitifoliae Gene duplications Host plant interactions Effectors Biological invasions

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Journal articles

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Life Sciences [q-bio]

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Submitted on : Tuesday, September 29, 2020 - 12:27:28 PM
Last modification on : Monday, February 22, 2021 - 2:32:02 PM

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