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1. Correction to: The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest

Author

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

Subjects
Physiology, Genome, Insect, Adaptation, Biological, Plant Science, General Biochemistry, Genetics and Molecular Biology, Hemiptera, Structural Biology, Animals, Vitis, Phylloxera, lcsh:QH301-705.5, Ecology, Evolution, Behavior and Systematics, Whole genome sequencing, biology, Correction, Cell Biology, Biological Sciences, biology.organism_classification, Biological Evolution, lcsh:Biology (General), Evolutionary biology, PEST analysis, Adaptation, General Agricultural and Biological Sciences, Introduced Species, Animal Distribution, Biotechnology, Developmental Biology
Abstract

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.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.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.

Published
2020

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

Author

Ying Zhang, Pascale Roux, Alex C.C. Wilson, Celeste R. Banfill, Roderic Guigó, Ming Tang, Carole Vincent-Monégat, Denis Tagu, Claude Rispe, Yi Min Hsiao, Angela E. Douglas, Daciana Papura, Keith Dufault-Thompson, Frédérique Hilliou, Shanlin Liu, Astrid Forneck, Nicolas Montagné, Eric Lombaert, Fabrice Legeai, Julio Rozas, Gaël Le Trionnaire, Yvan Rahbé, Anthony Bretaudeau, Jing Zhao, Silvia Hinojosa-Alvarez, Maryem Bouallègue, Joshua Wemmer, Stéphanie Robin, Jose Francisco Sánchez-Herrero, Pierre Capy, Federica Calevro, Xin Zhou, David Martínez-Torres, Martine Maïbèche, Patrice Baa-Puyoulet, Marina Marcet-Houben, Gaëlle Le Goff, Aida Ripoll-Cladellas, Mélanie Ribeiro Lopes, Wenhua Tian, Hsiao-ling Lu, François Delmotte, Toni Gabaldón, Arinder K. Arora, Paul A Umina, Rémy Félix Serre, Spencer Johnston, Olivier Catrice, Céline Roques, Paul D. Nabity, Serena Zhao, Pablo Librado, Miquel Barberà, Thomas Chertemps, Emmanuelle Jacquin-Joly, Benjamin Joubard, Leticia Bao, Jennifer A. Brisson, Camille Meslin, Honglin Feng, Manuella van Munster, Paula Escuer, Edward B. James, Rosa Fernández, Chaoyang Zhao, Mohamed Makni, Sylvie Hudaverdian, Nancy A. Moran, Iris Scatoni, Nicolas Parisot, Carole Couture, Didac Santesmasses, Laurent Delière, Alejandro Sánchez-Gracia, Biologie, Epidémiologie et analyse de risque en Santé Animale (BIOEPAR), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Scalable, Optimized and Parallel Algorithms for Genomics (GenScale), Inria Rennes – Bretagne Atlantique, Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-GESTION DES DONNÉES ET DE LA CONNAISSANCE (IRISA-D7), Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Université de Bretagne Sud (UBS)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National de Recherche en Informatique et en Automatique (Inria)-École normale supérieure - Rennes (ENS Rennes)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-CentraleSupélec-IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Bretagne Sud (UBS)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-École normale supérieure - Rennes (ENS Rennes)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT), Department of Botany and Plant Sciences [Riverside], University of California [Riverside] (UCR), University of California-University of California, Centre for Genomic Regulation [Barcelona] (CRG), Universitat Pompeu Fabra [Barcelona] (UPF)-Centro Nacional de Analisis Genomico [Barcelona] (CNAG), Institut de Biologia Evolutiva [Barcelona] (IBE / UPF - CSIC), Universitat Pompeu Fabra [Barcelona] (UPF), Cornell University [New York], Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), University of Miami [Coral Gables], Universidad de la República (UDELAR), Universitat de València (UV), Faculté des Sciences Mathématiques, Physiques et Naturelles de Tunis (FST), Université de Tunis El Manar (UTM), University of Rochester [USA], Evolution, génomes, comportement et écologie (EGCE), Institut de Recherche pour le Développement (IRD)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Laboratoire des Interactions Plantes Microbes Environnement (LIPME), Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institut d'écologie et des sciences de l'environnement de Paris (iEES Paris ), Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Centre National de la Recherche Scientifique (CNRS)-Université de Paris (UP)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Santé et agroécologie du vignoble (UMR SAVE), Université de Bordeaux (UB)-Institut des Sciences de la Vigne et du Vin (ISVV)-Ecole Nationale Supérieure des Sciences Agronomiques de Bordeaux-Aquitaine (Bordeaux Sciences Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), University of Rhode Island (URI), Université de Barcelonne, Boyce Thompson Institute [Ithaca], Universität für Bodenkultur Wien [Vienne, Autriche] (BOKU), Center for Genomic Regulation (CRG-UPF), CIBER de Epidemiología y Salud Pública (CIBERESP), Institució Catalana de Recerca i Estudis Avançats (ICREA), Institut Sophia Agrobiotech (ISA), Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Côte d'Azur (UCA), National Taiwan University [Taiwan] (NTU), Chang Gung Memorial Hospital [Taipei] (CGMH), Texas A&M University [College Station], Anthropologie Moléculaire et Imagerie de Synthèse (AMIS), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Beijing Genomics Institute [Shenzhen] (BGI), China Agricultural University (CAU), MingDao University (MDU), University of Texas at Austin [Austin], Trafic et signalisation membranaires chez les bactéries (MTSB), Microbiologie, adaptation et pathogénie (MAP), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS), Biologie et Génétique des Interactions Plante-Parasite (UMR BGPI), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Sciences pour l'environnement (SPE), Centre National de la Recherche Scientifique (CNRS)-Université Pascal Paoli (UPP), Génome et Transcriptome - Plateforme Génomique ( GeT-PlaGe), Plateforme Génome & Transcriptome (GET), Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Brigham & Women’s Hospital [Boston] (BWH), Harvard Medical School [Boston] (HMS), University of California, University of Melbourne, INRAE (France), Juan de la Cierva-Incorporacion Fellowship (Government of Spain) : IJCI-2015-26627, Marie Sklodowska-Curie Fellowship : 747607, US National Institute of Food and Agriculture : 12216941, University of Miami Maytag Fellowship from the Department of Biology, William H. Evoy Graduate Research Support Fund from the Department of Biology, Molecular Biosciences Graduate Research, Award from the Department of Biology, Springer Nature, European Project: 764840,IGNITE, École nationale vétérinaire, agroalimentaire et de l'alimentation Nantes-Atlantique (ONIRIS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Université de Rennes (UR)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-INSTITUT AGRO Agrocampus Ouest, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Université de Rennes (UR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Rennes (UR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique), University of California [Riverside] (UC Riverside), University of California (UC)-University of California (UC), Department of Entomology [CALS], College of Agriculture and Life Sciences [Cornell University] (CALS), Cornell University [New York]-Cornell University [New York], Universidad de la República [Montevideo] (UDELAR), Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Universitat de Barcelona (UB), Universität für Bodenkultur Wien = University of Natural Resources and Life [Vienne, Autriche] (BOKU), Université Nice Sophia Antipolis (1965 - 2019) (UNS), Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut Agro - Montpellier SupAgro, Université Pascal Paoli (UPP)-Centre National de la Recherche Scientifique (CNRS), Université de Toulouse (UT)-Université de Toulouse (UT)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), University of California (UC), Centre National de la Recherche Scientifique (CNRS)-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon, European Commission, Ministerio de Economía y Competitividad (España), National Institute of Food and Agriculture (US), Miami University, Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-INSTITUT AGRO Agrocampus Ouest, Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Rennes 1 (UR1), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPC)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Institut National de la Recherche Agronomique (INRA)-École nationale vétérinaire, agroalimentaire et de l'alimentation Nantes-Atlantique (ONIRIS), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique), and Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique)

Subjects
0106 biological sciences, Fil·loxera, Physiology, [SDV]Life Sciences [q-bio], Introduced species, Plant Science, 01 natural sciences, Genome, Gene duplications, Structural Biology, Vitis, lcsh:QH301-705.5, ComputingMilieux_MISCELLANEOUS, 2. Zero hunger, 0303 health sciences, education.field_of_study, Host plant interactions, Endosymbiosis, biology, food and beverages, Biological Sciences, Biological Evolution, General Agricultural and Biological Sciences, Rootstock, Infection, Daktulosphaira vitifoliae, Biotechnology, Research Article, Population, 010603 evolutionary biology, General Biochemistry, Genetics and Molecular Biology, Hemiptera, 03 medical and health sciences, Genetics, Insect pests, Animals, Plagues d'insectes, Adaptation, Biological invasions, Genomes, education, Phylloxera, Ecology, Evolution, Behavior and Systematics, 030304 developmental biology, Obligate, Human Genome, Viticultura, Cell Biology, 15. Life on land, biology.organism_classification, Biological, Effectors, Climate Action, lcsh:Biology (General), 13. Climate action, Evolutionary biology, Arthropod genomes, Introduced Species, Insect, Animal Distribution, Developmental Biology
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., 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.

Published
2020

3. Genome-Wide Screen for Saccharomyces cerevisiae Genes Contributing to Opportunistic Pathogenicity in an Invertebrate Model Host

Author

Kaitlyn L. Norman, Lucas A. Michelotti, Sujal Phadke, Timothy Y. James, Anuj Kumar, Calum J. Maclean, Serena Zhao, and Emmi A. Mueller

Subjects
0301 basic medicine, Genotype, bulk segregant analysis, Quantitative Trait Loci, 030106 microbiology, Saccharomyces cerevisiae, Virulence, Investigations, Moths, Quantitative trait locus, Biology, QH426-470, medicine.disease_cause, 03 medical and health sciences, pseudohyphae, Cell Wall, medicine, Genetics, Animals, Molecular Biology, Gene, Alleles, Genetics (clinical), 2. Zero hunger, Mutation, Innate immune system, hybrid, Molecular Sequence Annotation, barseq, biology.organism_classification, Phenotype, Immunity, Innate, Yeast, Mitochondria, virulence, Gene Ontology, 030104 developmental biology, Larva, Host-Pathogen Interactions, Tyrosine, Genome, Fungal, Genome-Wide Association Study
Abstract

Environmental opportunistic pathogens can exploit vulnerable hosts through expression of traits selected for in their natural environments. Pathogenicity is itself a complicated trait underpinned by multiple complex traits, such as thermotolerance, morphology, and stress response. The baker’s yeast, Saccharomyces cerevisiae, is a species with broad environmental tolerance that has been increasingly reported as an opportunistic pathogen of humans. Here we leveraged the genetic resources available in yeast and a model insect species, the greater waxmoth Galleria mellonella, to provide a genome-wide analysis of pathogenicity factors. Using serial passaging experiments of genetically marked wild-type strains, a hybrid strain was identified as the most fit genotype across all replicates. To dissect the genetic basis for pathogenicity in the hybrid isolate, bulk segregant analysis was performed which revealed eight quantitative trait loci significantly differing between the two bulks with alleles from both parents contributing to pathogenicity. A second passaging experiment with a library of deletion mutants for most yeast genes identified a large number of mutations whose relative fitness differed in vivovs.in vitro, including mutations in genes controlling cell wall integrity, mitochondrial function, and tyrosine metabolism. Yeast is presumably subjected to a massive assault by the innate insect immune system that leads to melanization of the host and to a large bottleneck in yeast population size. Our data support that resistance to the innate immune response of the insect is key to survival in the host and identifies shared genetic mechanisms between S. cerevisiae and other opportunistic fungal pathogens.

Published
2018

4. Laboulbeniales (Ascomycota) of the Boston Harbor Islands II (and Other Localities): Species Parasitizing Carabidae, and the Laboulbenia flagellata Species Complex

Author

Danny Haelewaters, Donald H. Pfister, Gerrit Gort, Serena Zhao, Michał Gorczak, Kevin Bao, and André De Kesel

Subjects
0106 biological sciences, Morphometrics, Species complex, biology, 010604 marine biology & hydrobiology, Laboulbeniales, Zoology, PE&RC, biology.organism_classification, Wiskundige en Statistische Methoden - Biometris, 010603 evolutionary biology, 01 natural sciences, Laboulbenia, Genus, Pterostichus, Agonum, Oxypselaphus, Life Science, Mathematical and Statistical Methods - Biometris, Ecology, Evolution, Behavior and Systematics
Abstract

This paper presents 13 new records of Laboulbenialean parasites on ground beetles (Coleoptera, Carabidae) from the Boston Harbor Islands National Recreation Area in Massachusetts: Laboulbenia anoplogenii, L. casnoniae, L. clivinalis, L. egens, L. filifera, L. flagellata, L. inflata, L. macrotheca, L. pedicellata, L. terminalis, L. variabilis, L. vulgaris, and Peyritschiella geminata. Laboulbenia clivinalis and L. egens are new country records for the US. Moreover, we present additional localities for L. casnoniae, L. clivinalis, L. filifera, L. flagellata, L. inflata, L. pedicellata, L. variabilis, and L. vulgaris. The following new country records are presented: Laboulbenia clivinalis, L. filifera, and L. variabilis from Canada; L. flagellata from the Democratic Republic of the Congo; L. pedicellata from Ukraine; L. vulgaris from Croatia and Slovenia (and the first undoubtful record from Slovakia). Laboulbenia flagellata was found on 11 host species in the genera Agonum, Oxypselaphus, Patrobus, Platynus, and Pterostichus. Using this abundant material, we performed morphometrics to test the hypothesis that L. flagellata is a species complex. Specimens cannot be separated based on host genus (Agonum, Pterostichus). One parameter is significant between Pterostichus mutus and each of the 4 Agonum species after applying a strong Bonferroni P-value correction: H1T, the ratio of height of cell I (HC1) to total thallus length (TTL). In addition, we collected fresh material to be able to add a molecular phylogenetic component to test said hypothesis. We generated ITS and nrLSU ribosomal sequences of several species of Laboulbenia, including isolates of L. flagellata from multiple hosts. Phylogenetic inference of the concatenated dataset shows that L. flagellata isolates from 3 host species form 2 distinct clades, providing support for our hypothesis. We also show that L. coneglianensis is separate from L. flagellata, unequivocally ending a long-standing taxonomic debate. Finally, examination of Roland Thaxter's 1891-1932 slides led to the designation of lectotypes for L. macrothecia, L. terminalis, and P. geminata.

Published
2019

5. Large wildlife removal drives immune defence increases in rodents

Author

Hillary S. Young, Kristofer M. Helgen, Serena Zhao, Kari E. Veblen, Douglas J. McCauley, Rodolfo Dirzo, Charles L. Nunn, Vanessa O. Ezenwa, and Paul W. Snyder

Subjects
0106 biological sciences, Functional ecology, Rodent, Ecology, Defaunation, 010604 marine biology & hydrobiology, Ecoimmunology, Wildlife, Biology, biology.organism_classification, 010603 evolutionary biology, 01 natural sciences, Invasive species, biology.animal, Exclosure, Saccostomus mearnsi, Ecology, Evolution, Behavior and Systematics
Abstract

Author(s): Young, HS; Dirzo, R; Helgen, KM; Mccauley, DJ; Nunn, CL; Snyder, P; Veblen, KE; Zhao, S; Ezenwa, VO | Abstract: Anthropogenic disturbances involving land use change, climate disruption, pollution and invasive species have been shown to impact immune function of wild animals. These immune changes have direct impacts on the fitness of impacted animals and, also, potentially indirect effects on other species and on ecological processes, notably involving the spread of infectious disease. Here, we investigate whether the selective loss of large wildlife can also drive changes in immune function of other consumer species. Using a long-standing large-scale exclosure experiment in East Africa, we investigated the effects of selective removal of large wildlife on multiple measures of immune function in the dominant small rodent in the system, the East African pouched mouse, Saccostomus mearnsi. We find support for a general increase in immune function in landscapes where large wildlife has been removed, but with some variation across immune parameters. These changes may be mediated in part by increased pathogen pressure in plots where large wildlife has been removed due to major increases in rodent density in such plots, but other factors such as changes in food resources are also likely involved. Overall, our research reveals that the elimination of large-bodied wildlife - now recognized as another major form of global anthropogenic change - may have cascading effects on immune health, with the potential for these effects to also impact disease dynamics in ecological communities. Lay Summary Functional Ecology

Published
2015

6. Parasites of Harmonia axyridis: current research and perspectives

Author

Danny Haelewaters, Eric W. Riddick, Regina G. Kleespies, Paul S. van Wielink, Walter P. Pfliegler, David I. Shapiro-Ilan, Piotr Ceryngier, Ted E. Cottrell, C. Lidwien Raak-van den Berg, Tove Steenberg, Lukáš Fiedler, Katie M. Murray, Helen Hesketh, John E. Losey, Rebecca R. Smyth, Helen E. Roy, Ingrid A. Minnaar, André De Kesel, Zihua Zhao, Sandra Viglášová, Annette Herz, Oldřich Nedvěd, Cang Hui, Susana Clusella-Trullas, and Serena Zhao

Subjects
0106 biological sciences, Entomology, Harmonia axyridis, Range (biology), Ecology (disciplines), Biological pest control, Coccipolipus hippodamiae, Biológiai tudományok, 010603 evolutionary biology, 01 natural sciences, Természettudományok, Parasites, Laboratory of Entomology, Enemy release hypothesis, biology, Host (biology), Ecology, Parasitylenchus bifurcatus, Hesperomyces virescens, PE&RC, Laboratorium voor Entomologie, biology.organism_classification, 010602 entomology, Animal ecology, Insect Science, Coccinellidae, 017-4067, Agronomy and Crop Science
Abstract

Harmonia axyridis (Coleoptera: Coccinellidae) has been introduced widely for biological control of agricultural pests. Harmonia axyridis has established in four continents outside of its native range in Asia and it is considered an invasive alien species (IAS). Despite a large body of work on invasion ecology, establishment mechanisms of IAS and their interactions with natural enemies remain open questions. Parasites, defined as multicellular organisms that do not directly kill the host, could potentially play an important role in regulating host populations. This study presents a review of the parasites of H. axyridis, discussing their distributions and effects on host populations across the host’s native and invasive range. These parasites are: Hesperomyces virescens Thaxt. fungi, Coccipolipus hippodamiae (McDaniel and Morrill) mites, and Parasitylenchus bifurcatus Poinar and Steenberg nematodes.

Published
2017

7. Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade

Author

Luís Felipe Toledo, Cláudia Maris Ferreira, Conrado Augusto Vieira, Lisa M. Schloegel, Christina A. Cuomo, Joyce E. Longcore, Peter Daszak, Timothy Y. James, Sasha E. Greenspan, Catherine Wangen, Marcio Hipolito, Maria Lee, Serena Zhao, and Angela J. Davies

Subjects
Amphibian, biology, Lithobates, Fungal genetics, Zoology, biology.organism_classification, Bullfrog, biology.animal, Genetics, Emerging infectious disease, Chytridiomycosis, Internal transcribed spacer, Ecology, Evolution, Behavior and Systematics, Panzootic
Abstract

Global amphibian declines are linked with the presence of specific, highly virulent genotypes of the emerging fungal disease chytridiomycosis caused by Batrachochytrium dendrobatidis (Bd) known as the global panzootic lineage (Bd-GPL). The global trade in amphibians for human consumption is suspected to have facilitated emergence of the disease, but evidence to support this is largely lacking. Here, we investigated the role the Lithobates catesbeianus (North American bullfrog) trade in spreading Bd genotypes by comparing strains associated with L. catesbeianus to a global panel using 36 sequenced loci from multiple chromosomal regions. Most bullfrogs were infected with Bd-GPL genotypes, but we also detected novel, highly divergent Bd genotypes (Bd-Brazil) from a live bullfrog in a US market and from native Brazilian anurans in the Atlantic Forest where bullfrogs are widely farmed. Sexual reproduction was also detected for the first time in Bd in the form of a hybrid genotype between the Bd-GPL and Bd-Brazil lineages in the Atlantic Forest. Despite the demonstration that ribosomal RNA types in Bd fail to undergo concerted evolution (over 20 sequence types may be found in a single strain), the Bd-GPL and Bd-Brazil lineages form largely separate clusters of related internal transcribed spacer (ITS) RNA sequences. Using ITS sequences, we then demonstrate the presence of Bd-Brazil in Japan, primarily on invasive L. catesbeianus. The finding that Bd is capable of sexual reproduction between panzootic and endemic genotypes emphasizes the risk of international wildlife trade as a source of additional Bd epizootics owing to hybridization.

Published
2012

8. Laboulbeniales (Ascomycota) of the Boston Harbor Islands I: Species Parasitizing Coccinellidae and Staphylinidae, with Comments on Typification

Author

Rebecca E. Handlin, Brian D. Farrell, André De Kesel, Danny Haelewaters, Serena Zhao, Donald H. Pfister, and Isabel R. Royer

Subjects
Laboulbenia, biology, Ecology, Laboulbeniales, Typification, Coccinellidae, Parasitism, Taxonomy (biology), Type locality, biology.organism_classification, Protea, Ecology, Evolution, Behavior and Systematics
Abstract

This paper, based on a recent comprehensive sampling of insects, is the first report of Laboulbeniales from the New England region since the 1930s. We present 7 new records of laboulbenialean parasites on Staphylinidae (rove beetles) and Coccinellidae (lady beetles) from the Boston Harbor Islands National Recreation Area. These are Clonophoro- myces nipponicus Terada & I.I. Tav., Hesperomyces virescens Thaxt., Ilyomyces cf. mairei F. Picard, Laboulbenia philonthi Thaxt., Peyritschiella protea Thaxt., Stichomyces conoso- matis Thaxt., and Teratomyces actobii Thaxt. One of these parasite species, C. nipponicus, has not been found previously outside of its type locality in Japan. Examination of Roland Thaxter's 1891-1932 slides led to the designation of lectotypes for L. philonthi, P. protea, S. conosomatis, and T. actobii. The following synonymy is established: Teratomyces brevi- caulis Thaxt. = T. actobii. In addition, we discovered new localities for H. virescens (from Canada, Cuba, Guatemala, and Japan) and L. philonthi (from Canada, Grenada, Panama, Trinidad, and Venezuela).

Published
2015

9. Erratum to: Hesperomyces virescens (Fungi, Ascomycota, Laboulbeniales) attacking Harmonia axyridis (Coleoptera, Coccinellidae) in its native range

Author

Richard Comont, Danny Haelewaters, Serena Zhao, and Donald H. Pfister

Subjects
Multidisciplinary, biology, Obligate, Ascomycota, Range (biology), Laboulbeniales, Botany, Coccinellidae, biology.organism_classification, Hesperomyces virescens, Harmonia axyridis, Invasive species
Abstract

This study intended to find data on obligate ectoparasitic Laboulbeniales (Fungi, Ascomycota) on Chinese Harmonia axyridis (Coleoptera, Coccinellidae). After having screened over four thousand dried specimens of H. axyridis and close relatives, we present the first (historical) record of Chinese H. axyridis infected with Hesperomyces virescens. We suggest that H. virescens is a historically globally distributed species and hypothesize that (native) infection was lost when H. axyridis was introduced in North America.

Published
2014

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