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

[1]  Robert M. Waterhouse,et al.  Evolutionary Dynamics of Immune-Related Genes and Pathways in Disease-Vector Mosquitoes , 2007, Science.

[2]  R. Butlin,et al.  Large gene family expansions and adaptive evolution for odorant and gustatory receptors in the pea aphid, Acyrthosiphon pisum. , 2009, Molecular biology and evolution.

[3]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[4]  Ian Korf,et al.  Gene finding in novel genomes , 2004, BMC Bioinformatics.

[5]  P. Pelosi,et al.  Soluble proteins of chemical communication: an overview across arthropods , 2014, Front. Physiol..

[6]  G. K. Davis,et al.  Genome Sequence of the Pea Aphid Acyrthosiphon pisum , 2010, PLoS biology.

[7]  R. Durbin,et al.  GeneWise and Genomewise. , 2004, Genome research.

[8]  Mark Yandell,et al.  MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects , 2011, BMC Bioinformatics.

[9]  D. Richardson,et al.  Integrative invasion science: model systems, multi-site studies, focused meta-analysis and invasion syndromes. , 2013, The New phytologist.

[10]  J. Ravaux,et al.  Survey of genome size in 28 hydrothermal vent species covering 10 families. , 2009, Genome.

[11]  Inderjit,et al.  Emergent insights from the synthesis of conceptual frameworks for biological invasions. , 2011, Ecology letters.

[12]  Robert D. Finn,et al.  The Pfam protein families database: towards a more sustainable future , 2015, Nucleic Acids Res..

[13]  F. Legeai,et al.  De novo transcriptome assembly of the grapevine phylloxera allows identification of genes differentially expressed between leaf- and root-feeding forms , 2016, BMC Genomics.

[14]  O. Gascuel,et al.  An improved general amino acid replacement matrix. , 2008, Molecular biology and evolution.

[15]  Ana Kozomara,et al.  miRBase: annotating high confidence microRNAs using deep sequencing data , 2013, Nucleic Acids Res..

[16]  Daniel C. Desrosiers,et al.  The ankyrin repeat as molecular architecture for protein recognition , 2004, Protein science : a publication of the Protein Society.

[17]  M. Sedgley,et al.  Interaction between Vitis vinifera and grape phylloxera: changes in root tissue during nodosity formation. , 2004, Annals of botany.

[18]  J. Peccoud,et al.  Fast Evolution and Lineage-Specific Gene Family Expansions of Aphid Salivary Effectors Driven by Interactions with Host-Plants , 2018, Genome biology and evolution.

[19]  Ludovic Cottret,et al.  CycADS: an annotation database system to ease the development and update of BioCyc databases , 2011, Database J. Biol. Databases Curation.

[20]  Toni Gabaldón,et al.  ArthropodaCyc: a CycADS powered collection of BioCyc databases to analyse and compare metabolism of arthropods , 2016, Database J. Biol. Databases Curation.

[21]  G. K. Davis.  Cyclical parthenogenesis and viviparity in aphids as evolutionary novelties. , 2012, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[22]  Mark Blaxter,et al.  BlobTools: Interrogation of genome assemblies , 2017, F1000Research.

[23]  David Posada,et al.  ProtTest: selection of best-fit models of protein evolution , 2005, Bioinform..

[24]  Walter Pirovano,et al.  SSPACE-LongRead: scaffolding bacterial draft genomes using long read sequence information , 2014, BMC Bioinformatics.

[25]  P. Hebert,et al.  Identification of Birds through DNA Barcodes , 2004, PLoS biology.

[26]  N. Moran,et al.  The Dynamics and Time Scale of Ongoing Genomic Erosion in Symbiotic Bacteria , 2009, Science.

[27]  J. Stuart.  Insect effectors and gene-for-gene interactions with host plants. , 2015, Current opinion in insect science.

[28]  A. Nakabachi,et al.  Aphids acquired symbiotic genes via lateral gene transfer , 2009, BMC Biology.

[29]  A. Futschik,et al.  PoPoolation: A Toolbox for Population Genetic Analysis of Next Generation Sequencing Data from Pooled Individuals , 2011, PloS one.

[30]  P. Stadler,et al.  MITOS: improved de novo metazoan mitochondrial genome annotation. , 2013, Molecular phylogenetics and evolution.

[31]  E. Carafoli,et al.  Why Calcium? How Calcium Became the Best Communicator* , 2016, The Journal of Biological Chemistry.

[32]  D. Nelson,et al.  Rhodnius prolixus supergene families of enzymes potentially associated with insecticide resistance. , 2016, Insect biochemistry and molecular biology.

[33]  C. Claudel-Renard,et al.  Enzyme-specific profiles for genome annotation: PRIAM. , 2003, Nucleic acids research.

[34]  B. Roe,et al.  Comparative analysis of detoxification enzymes in Acyrthosiphon pisum and Myzus persicae , 2010, Insect molecular biology.

[35]  Juan Miguel García-Gómez,et al.  BIOINFORMATICS APPLICATIONS NOTE Sequence analysis Manipulation of FASTQ data with Galaxy , 2005 .

[36]  Matko Bosnjak,et al.  REVIGO Summarizes and Visualizes Long Lists of Gene Ontology Terms , 2011, PloS one.

[37]  Oliver Eulenstein,et al.  DupTree: a program for large-scale phylogenetic analyses using gene tree parsimony , 2008, Bioinform..

[38]  R. Feyereisen.  Arthropod CYPomes illustrate the tempo and mode in P450 evolution. , 2011, Biochimica et biophysica acta.

[39]  K. Katoh,et al.  MAFFT version 5: improvement in accuracy of multiple sequence alignment , 2005, Nucleic acids research.

[40]  H. Akaike,et al.  Information Theory and an Extension of the Maximum Likelihood Principle , 1973 .

[41]  Kazutaka Katoh,et al.  Application of the MAFFT sequence alignment program to large data—reexamination of the usefulness of chained guide trees , 2016, Bioinform..

[42]  A. Forneck,et al.  Major Outbreaks in the Nineteenth Century Shaped Grape Phylloxera Contemporary Genetic Structure in Europe , 2019, Scientific Reports.

[43]  Honghe Sun,et al.  The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance , 2016, BMC Biology.

[44]  S. Hogenhout,et al.  Aphid protein effectors promote aphid colonization in a plant species-specific manner. , 2013, Molecular plant-microbe interactions : MPMI.

[45]  P. Nabity,et al.  Phylloxerids share ancestral carotenoid biosynthesis genes of fungal origin with aphids and adelgids , 2017, PloS one.

[46]  I. Hiltpold,et al.  Behaviour and physiology of root herbivores , 2013 .

[47]  Thomas K. F. Wong,et al.  Phylogenomics resolves the timing and pattern of insect evolution , 2014, Science.

[48]  Z. Fei,et al.  Evolutionary conservation of candidate osmoregulation genes in plant phloem sap‐feeding insects , 2016, Insect molecular biology.

[49]  Roderic Guigó,et al.  Selenoprofiles: profile-based scanning of eukaryotic genome sequences for selenoprotein genes , 2010, Bioinform..

[50]  V. Gladyshev,et al.  Adjustments, extinction, and remains of selenocysteine incorporation machinery in the nematode lineage , 2014, RNA.

[51]  Stefan R. Henz,et al.  The genome of Tetranychus urticae reveals herbivorous pest adaptations , 2011, Nature.

[52]  O. Gascuel,et al.  Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. , 2006, Systematic biology.

[53]  Ronan M. T. Fleming,et al.  fastGapFill: efficient gap filling in metabolic networks , 2014, Bioinform..

[54]  C. Robert,et al.  ABC random forests for Bayesian parameter inference , 2016, Bioinform..

[55]  D. Martínez-Torres,et al.  Characterisation, analysis of expression and localisation of circadian clock genes from the perspective of photoperiodism in the aphid Acyrthosiphon pisum. , 2017, Insect biochemistry and molecular biology.

[56]  The genome of Diuraphis noxia, a global aphid pest of small grains , 2015, BMC Genomics.

[57]  T. Flutre,et al.  Considering Transposable Element Diversification in De Novo Annotation Approaches , 2011, PloS one.

[58]  D. Pimentel,et al.  Update on the environmental and economic costs associated with alien-invasive species in the United States , 2005 .

[59]  Ewan Birney,et al.  Automated generation of heuristics for biological sequence comparison , 2005, BMC Bioinformatics.

[60]  Wayne B. Hunter,et al.  Annotation of the Asian Citrus Psyllid Genome Reveals a Reduced Innate Immune System , 2016, Frontiers in physiology.

[61]  R. Guigó,et al.  Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia , 2006, Nature.

[62]  O. Gascuel,et al.  New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. , 2010, Systematic biology.

[63]  J. Rozas,et al.  Genome annotation and comparative analyses of the odorant‐binding proteins and chemosensory proteins in the pea aphid Acyrthosiphon pisum , 2010, Insect molecular biology.

[64]  D. Martínez-Torres,et al.  Pantoea agglomerans‐associated bacteria in grape phylloxera (Daktulosphaira vitifoliae, Fitch) , 2007 .

[65]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[66]  Chris Mungall,et al.  A Chado case study: an ontology-based modular schema for representing genome-associated biological information , 2007, ISMB/ECCB.

[67]  Joaquín Dopazo,et al.  FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes , 2004, Bioinform..

[68]  A. Briscoe,et al.  Insect cryptochromes: gene duplication and loss define diverse ways to construct insect circadian clocks. , 2007, Molecular biology and evolution.

[69]  D. Simberloff.  Non-native invasive species and novel ecosystems , 2015, F1000prime reports.

[70]  S. Komatsu,et al.  Molecular cloning of a novel calcium-binding protein in the secreted saliva of the green rice leafhopper Nephotettix cincticeps. , 2012, Insect biochemistry and molecular biology.

[71]  Peer Bork,et al.  Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees , 2016, Nucleic Acids Res..

[72]  P. Bork,et al.  ETE 3: Reconstruction, Analysis, and Visualization of Phylogenomic Data , 2016, Molecular biology and evolution.

[73]  Claudia M. A. Carareto,et al.  Genome of Rhodnius prolixus, an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection , 2015, Proceedings of the National Academy of Sciences.

[74]  W. Jonckheere,et al.  Salivary proteins of spider mites suppress defenses in Nicotiana benthamiana and promote mite reproduction. , 2016, The Plant journal : for cell and molecular biology.

[75]  J. Bennetzen,et al.  A unified classification system for eukaryotic transposable elements , 2007, Nature Reviews Genetics.

[76]  P. Nabity.  Insect-induced plant phenotypes: Revealing mechanisms through comparative genomics of galling insects and their hosts. , 2016, American journal of botany.

[77]  Akiyasu C. Yoshizawa,et al.  KAAS: an automatic genome annotation and pathway reconstruction server , 2007, Environmental health perspectives.

[78]  Z. Heng,et al.  Selectivity of Phylloxera viticola Fitch (Homoptera: Phylloxeridae) to grape with different resistance and the identification of grape root volatiles. , 2009 .

[79]  W. F. Tjallingii,et al.  Molecular sabotage of plant defense by aphid saliva , 2007, Proceedings of the National Academy of Sciences.

[80]  Markus Krummenacker,et al.  The MetaCyc database of metabolic pathways and enzymes , 2017, Nucleic acids research.

[81]  M. Banfield,et al.  Effector gene birth in plant parasitic nematodes: Neofunctionalization of a housekeeping glutathione synthetase gene , 2018, PLoS genetics.

[82]  Roderic Guigó,et al.  Computational identification of the selenocysteine tRNA (tRNASec) in genomes , 2017, PLoS Comput. Biol..

[83]  Julian Chen,et al.  Identification and Expression Analysis of Candidate Odorant-Binding Protein and Chemosensory Protein Genes by Antennal Transcriptome of Sitobion avenae , 2016, PloS one.

[84]  O Gascuel,et al.  BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. , 1997, Molecular biology and evolution.

[85]  S. Riaz,et al.  Population Structure, Diversity and Reproductive Mode of the Grape Phylloxera (Daktulosphaira vitifoliae) across Its Native Range , 2017, PloS one.

[86]  P. Oliveira,et al.  Rhodnius prolixus: Identification of missing components of the IMD immune signaling pathway and functional characterization of its role in eliminating bacteria , 2019, PloS one.

[87]  P. Sunnucks,et al.  Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). , 1996, Molecular biology and evolution.

[88]  Peter D. Karp,et al.  Pathway Tools version 19.0 update: software for pathway/genome informatics and systems biology , 2016, Briefings Bioinform..

[89]  Peter D. Karp,et al.  Pathway Tools version 13.0: integrated software for pathway/genome informatics and systems biology , 2015, Briefings Bioinform..

[90]  M. Carrete,et al.  The extent, frequency and ecological functions of food wasting by parrots , 2019, Scientific Reports.

[91]  Lawrence S. Hon,et al.  Soybean Aphid Biotype 1 Genome: Insights into the invasive biology and adaptive evolution of a major agricultural pest. , 2020, Insect biochemistry and molecular biology.

[92]  P. Falabella,et al.  Molecular Basis of Alarm Pheromone Detection in Aphids , 2017, Current Biology.

[93]  K. Borden.  RING domains: master builders of molecular scaffolds? , 2000, Journal of molecular biology.

[94]  J. Rozas,et al.  Comparative Genomics Reveals Thousands of Novel Chemosensory Genes and Massive Changes in Chemoreceptor Repertories across Chelicerates , 2018, Genome biology and evolution.

[95]  R. Guigó,et al.  Correction to: The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest , 2020, BMC Biology.

[96]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[97]  Toni Gabaldón,et al.  trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses , 2009, Bioinform..

[98]  L. Riddiford,et al.  Structure and expression of a Manduca sexta larval cuticle gene homologous to Drosophila cuticle genes. , 1988, Journal of molecular biology.

[99]  Susan J. Brown,et al.  A Massive Expansion of Effector Genes Underlies Gall-Formation in the Wheat Pest Mayetiola destructor , 2015, Current Biology.

[100]  P. Nabity,et al.  Plant manipulation through gall formation constrains amino acid transporter evolution in sap-feeding insects , 2017, BMC Evolutionary Biology.

[101]  Jinian Feng,et al.  Identification and Expression Profiling of Odorant-Binding Proteins and Chemosensory Proteins of Daktulosphaira vitifoliae (Hemiptera: Phylloxeridae) , 2017, Journal of Economic Entomology.

[102]  Florian Odronitz,et al.  Scipio: Using protein sequences to determine the precise exon/intron structures of genes and their orthologs in closely related species , 2008, BMC Bioinformatics.

[103]  Hong Luo,et al.  Understanding and identifying amino acid repeats , 2014, Briefings Bioinform..

[104]  J. Granett,et al.  Biology and management of grape phylloxera. , 2001, Annual review of entomology.

[105]  K. Denby,et al.  Insect Gallers and Their Plant Hosts: From Omics Data to Systems Biology , 2016, International journal of molecular sciences.

[106]  Martin Kollmar,et al.  A novel hybrid gene prediction method employing protein multiple sequence alignments , 2011, Bioinform..

[107]  J. Granett,et al.  Population Diversity of Grape Phylloxera in California and Evidence for Sexual Reproduction , 2017, American Journal of Enology and Viticulture.

[108]  Wei Qian,et al.  Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. , 2000, Molecular biology and evolution.

[109]  Bernardo J. Clavijo,et al.  Rapid transcriptional plasticity of duplicated gene clusters enables a clonally reproducing aphid to colonise diverse plant species , 2017, Genome Biology.

[110]  Erik L. L. Sonnhammer,et al.  Kalign – an accurate and fast multiple sequence alignment algorithm , 2005, BMC Bioinformatics.

[111]  Monica C Munoz-Torres,et al.  Web Apollo: a web-based genomic annotation editing platform , 2013, Genome Biology.

[112]  D. Werck-Reichhart,et al.  Cytochromes P450: a success story , 2000, Genome Biology.

[113]  D. Downie.  Locating the sources of an invasive pest, grape phylloxera, using a mitochondrial DNA gene genealogy , 2002, Molecular ecology.

[114]  Publisher's Note , 2018, Anaesthesia.

[115]  M. Banfield.  Perturbation of host ubiquitin systems by plant pathogen/pest effector proteins , 2014, Cellular microbiology.

[116]  Paul Cox,et al.  A survey of , 1989 .

[117]  Keith Dufault-Thompson,et al.  PSAMM: A Portable System for the Analysis of Metabolic Models , 2016, PLoS Comput. Biol..

[118]  Suzanna E Lewis,et al.  JBrowse: a dynamic web platform for genome visualization and analysis , 2016, Genome Biology.

[119]  J. Bähler,et al.  Rapidly regulated genes are intron poor. , 2008, Trends in genetics : TIG.

[120]  V. Gladyshev,et al.  Selenoproteins: molecular pathways and physiological roles. , 2014, Physiological reviews.

[121]  C. E. Hjelmen,et al.  Genome Size Estimation and Quantitative Cytogenetics in Insects. , 2018, Methods in molecular biology.

[122]  Iain M. Wallace,et al.  M-Coffee: combining multiple sequence alignment methods with T-Coffee , 2006, Nucleic acids research.

[123]  R. Ewan,et al.  E3 ubiquitin ligases and plant innate immunity. , 2009, Journal of experimental botany.

[124]  Matthew Fraser,et al.  InterProScan 5: genome-scale protein function classification , 2014, Bioinform..

[125]  X. Martini,et al.  Innate immune system capabilities of the Asian citrus psyllid, Diaphorina citri. , 2017, Journal of invertebrate pathology.

[126]  W. Pirovano,et al.  Toward almost closed genomes with GapFiller , 2012, Genome Biology.

[127]  D. Tagu,et al.  Cuticular proteins and seasonal photoperiodism in aphids. , 2010, Insect biochemistry and molecular biology.

[128]  E. Campbell,et al.  Invertebrate aquaporins: a review , 2008, Journal of Comparative Physiology B.

[129]  Yang Liu,et al.  Molecular Characterization of the Aphis gossypii Olfactory Receptor Gene Families , 2014, PloS one.

[130]  Stephen P. Ficklin,et al.  Tripal v1.1: a standards-based toolkit for construction of online genetic and genomic databases , 2013, Database J. Biol. Databases Curation.

[131]  Björn Canbäck,et al.  ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences , 2008, Bioinform..

[132]  Y. Carton,et al.  Une coopération exemplaire entre entomologistes enançais et américains pendant la crise du Phylloxera en France (1868–1895) , 2007 .

[133]  S. Sawyer.  Statistical tests for detecting gene conversion. , 1989, Molecular biology and evolution.

[134]  Paramvir S. Dehal,et al.  FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments , 2010, PloS one.

[135]  Casey M. Bergman,et al.  Combined Evidence Annotation of Transposable Elements in Genome Sequences , 2005, PLoS Comput. Biol..

[136]  Margarita C. Theodoropoulou,et al.  CutProtFam-Pred: detection and classification of putative structural cuticular proteins from sequence alone, based on profile hidden Markov models. , 2014, Insect biochemistry and molecular biology.

[137]  N. Moran,et al.  Diversification of genes for carotenoid biosynthesis in aphids following an ancient transfer from a fungus. , 2012, Molecular biology and evolution.

[138]  Ziheng Yang.  PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[139]  Daniel J. Blankenberg,et al.  Galaxy: a platform for interactive large-scale genome analysis. , 2005, Genome research.

[140]  Salvador Capella-Gutiérrez,et al.  PhylomeDB v4: zooming into the plurality of evolutionary histories of a genome , 2013, Nucleic Acids Res..

[141]  D. Martínez-Torres,et al.  Identification of the prothoracicotropic hormone (Ptth) coding gene and localization of its site of expression in the pea aphid Acyrthosiphon pisum , 2017, Insect molecular biology.

[142]  D. Higgins,et al.  Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega , 2011, Molecular systems biology.

[143]  Thomas E. Smith,et al.  Gene Family Evolution in the Pea Aphid Based on Chromosome-Level Genome Assembly , 2019, Molecular biology and evolution.

[144]  Anthony Bretaudeau,et al.  Galaxy Genome Annotation project: Integrating Galaxy and GMOD for genome annotation , 2018 .

[145]  T. Cortés,et al.  Identification and characterization of circadian clock genes in the pea aphid Acyrthosiphon pisum , 2010, Insect molecular biology.

[146]  P. Buchner.  Endosymbiosis of Animals with Plant Microorganisms , 1965 .

[147]  P. Nabity,et al.  Secretory RING finger proteins function as effectors in a grapevine galling insect , 2019, BMC Genomics.

[148]  S. Reed,et al.  Ubiquitin ligases and cell cycle control. , 2013, Annual review of biochemistry.

[149]  N. Moran,et al.  Bacterial Genes in the Aphid Genome: Absence of Functional Gene Transfer from Buchnera to Its Host , 2010, PLoS genetics.

[150]  O. Gascuel,et al.  SMS: Smart Model Selection in PhyML , 2017, Molecular biology and evolution.

[151]  M. B. Ponsen.  A histological description of the alimentary tract and related organs of Phylloxeridae (Homoptera, Aphidoidea) , 1997 .

[152]  Jinyang Zhao,et al.  Genome sequencing of the sweetpotato whitefly Bemisia tabaci MED/Q , 2017, GigaScience.

[153]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[154]  Colleen J Doherty,et al.  Circadian control of global gene expression patterns. , 2010, Annual review of genetics.

[155]  A. Banerjee,et al.  Long-Run Health Impacts of Income Shocks: Wine and Phylloxera in Nineteenth-Century France , 2010, The Review of Economics and Statistics.

[156]  Jean-Michel Claverie,et al.  Phylogeny.fr: robust phylogenetic analysis for the non-specialist , 2008, Nucleic Acids Res..

[157]  Charles E. Chapple,et al.  Relaxation of Selective Constraints Causes Independent Selenoprotein Extinction in Insect Genomes , 2008, PloS one.

[158]  Dan Graur,et al.  Heads or tails: a simple reliability check for multiple sequence alignments. , 2007, Molecular biology and evolution.

[159]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[160]  Ashley D. Yates,et al.  Whole genome sequence of the soybean aphid, Aphis glycines. , 2017, Insect biochemistry and molecular biology.

[161]  O. Collin,et al.  AphidBase: a centralized bioinformatic resource for annotation of the pea aphid genome , 2010, Insect molecular biology.