The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest
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.
Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
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BioMed Central
2020-07-23
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Online Access: | http://hdl.handle.net/10261/237064 http://dx.doi.org/10.13039/100005825 http://dx.doi.org/10.13039/501100003329 http://dx.doi.org/10.13039/501100000780 |
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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. |
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European Commission |
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European Commission 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, Fréderique 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-Coisne, Martine Makni, Mohamed Marcet-Houben, Marina Martínez-Torres, David Meslin, Camille Montagné, Nicolas Moran, Nancy A. Papura, Daciana Parisot, Nicolas Rahbé, Yvan Ribeiro Lopes, Mélanie Ripoll-Cladellas, Aida Robin, Stéphanie Roques, Céline Roux, Pascale Rozas, Julio Sánchez-Gracia, Alejandro Sánchez-Herrero, José F. Santesmasses, Didac Scatoni, Iris Serre, Rémy-Félix Tang, Ming Tian, Wenhua Umina, Paul A. Munster, Manuella van Vincent-Monégat, Carole Wemmer, Joshua Wilson, Alex C. C. Zhang, Ying Zhao, Chaoyang Zhao, Jing Zhao, Serena Zhou, Xin Delmotte, François Tagu, Denis |
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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, Fréderique 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-Coisne, Martine Makni, Mohamed Marcet-Houben, Marina Martínez-Torres, David Meslin, Camille Montagné, Nicolas Moran, Nancy A. Papura, Daciana Parisot, Nicolas Rahbé, Yvan Ribeiro Lopes, Mélanie Ripoll-Cladellas, Aida Robin, Stéphanie Roques, Céline Roux, Pascale Rozas, Julio Sánchez-Gracia, Alejandro Sánchez-Herrero, José F. Santesmasses, Didac Scatoni, Iris Serre, Rémy-Félix Tang, Ming Tian, Wenhua Umina, Paul A. Munster, Manuella van Vincent-Monégat, Carole Wemmer, Joshua Wilson, Alex C. C. Zhang, Ying Zhao, Chaoyang Zhao, Jing Zhao, Serena Zhou, Xin Delmotte, François Tagu, Denis |
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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, Fréderique 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-Coisne, Martine Makni, Mohamed Marcet-Houben, Marina Martínez-Torres, David Meslin, Camille Montagné, Nicolas Moran, Nancy A. Papura, Daciana Parisot, Nicolas Rahbé, Yvan Ribeiro Lopes, Mélanie Ripoll-Cladellas, Aida Robin, Stéphanie Roques, Céline Roux, Pascale Rozas, Julio Sánchez-Gracia, Alejandro Sánchez-Herrero, José F. Santesmasses, Didac Scatoni, Iris Serre, Rémy-Félix Tang, Ming Tian, Wenhua Umina, Paul A. Munster, Manuella van Vincent-Monégat, Carole Wemmer, Joshua Wilson, Alex C. C. Zhang, Ying Zhao, Chaoyang Zhao, Jing Zhao, Serena Zhou, Xin Delmotte, François Tagu, Denis The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest |
author_sort |
Rispe, Claude |
title |
The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest |
title_short |
The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest |
title_full |
The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest |
title_fullStr |
The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest |
title_full_unstemmed |
The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest |
title_sort |
genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest |
publisher |
BioMed Central |
publishDate |
2020-07-23 |
url |
http://hdl.handle.net/10261/237064 http://dx.doi.org/10.13039/100005825 http://dx.doi.org/10.13039/501100003329 http://dx.doi.org/10.13039/501100000780 |
work_keys_str_mv |
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dig-ibe-es-10261-2370642021-04-08T01:21:45Z The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest 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, Fréderique 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-Coisne, Martine Makni, Mohamed Marcet-Houben, Marina Martínez-Torres, David Meslin, Camille Montagné, Nicolas Moran, Nancy A. Papura, Daciana Parisot, Nicolas Rahbé, Yvan Ribeiro Lopes, Mélanie Ripoll-Cladellas, Aida Robin, Stéphanie Roques, Céline Roux, Pascale Rozas, Julio Sánchez-Gracia, Alejandro Sánchez-Herrero, José F. Santesmasses, Didac Scatoni, Iris Serre, Rémy-Félix Tang, Ming Tian, Wenhua Umina, Paul A. Munster, Manuella van Vincent-Monégat, Carole Wemmer, Joshua Wilson, Alex C. C. Zhang, Ying Zhao, Chaoyang Zhao, Jing Zhao, Serena Zhou, Xin Delmotte, François Tagu, Denis European Commission Ministerio de Economía y Competitividad (España) National Institute of Food and Agriculture (US) Miami University 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. 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. 2021-04-07T10:40:25Z 2021-04-07T10:40:25Z 2020-07-23 2021-04-07T10:40:25Z artículo http://purl.org/coar/resource_type/c_6501 doi: 10.1186/s12915-020-00820-5 e-issn: 1741-7007 BMC Biology 18: 90 (2020) http://hdl.handle.net/10261/237064 10.1186/s12915-020-00820-5 http://dx.doi.org/10.13039/100005825 http://dx.doi.org/10.13039/501100003329 http://dx.doi.org/10.13039/501100000780 #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/EC/H2020/764840 info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/IJCI-2015-26627 info:eu-repo/grantAgreement/EC/H2020/747607 Publisher's version http://dx.doi.org/10.1186/s12915-020-00820-5 Sí open BioMed Central |