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1. Sawfly Genomes Reveal Evolutionary Acquisitions That Fostered the Mega-Radiation of Parasitoid and Eusocial Hymenoptera

Author

Sebastian Martin, Huyen Dinh, Kim C. Worley, Björn M. von Reumont, Tanja Ziesmann, Elena N. Elpidina, Cameron Gudobba, Alexander G. Martynov, Patrice Baa-Puyoulet, Cornelis J. P. Grimmelikhuijzen, Elizabeth Cash, Olivia R.A. Tidswell, Federica Calevro, Aaron Stahl, Markus Friedrich, Jiaxin Qu, Andrew J. Rosendale, Joshua B. Benoit, Leo W. Beukeboom, Shwetha C. Murali, Mackenzie Lovegrove, Panagiotis Ioannidis, Brenda Oppert, Daniel Dowling, Mei-Ju May Chen, Peter Lesný, Elzemiek Geuverink, Jan Philip Oeyen, Bernhard Misof, Maarten J.M.F. Reijnders, Masatsugu Hatakeyama, Emily C. Jennings, Christoph Mayer, Lucia Vedder, Daisuke S. Yamamoto, Anja Buttstedt, Hsu Chao, Elizabeth J. Duncan, Louis van de Zande, Daniel S.T. Hughes, Monica Munoz-Torres, Erich Bornberg-Bauer, Richard A. Gibbs, Lars Podsiadlowski, Peter K. Dearden, Alexandros G Sotiropoulos, Ralph S. Peters, Nicolas Montagné, Jeanne Wilbrandt, Andrew G. Cridge, Stephen Richards, John H. Werren, Yi Han, Sandra L. Lee, Megumi Sumitani, Victoria C. Moris, Oliver Niehuis, Ewald Große-Wilde, Amanda Dolan, Elise M. Szuter, Nicolas Parisot, Christopher P. Childers, Emmanuelle Jacquin-Joly, Sonja Grath, Panagiotis Provataris, Donna M. Muzny, Thomas Pauli, Joshua D. Gibson, Steffen Klasberg, Frank Hauser, John Skelly, Robert M. Waterhouse, Alexander Donath, Monica F. Poelchau, Shannon Dugan, Bill S. Hansson, Hubert Charles, Harshavardhan Doddapaneni, Malte Petersen, Evgeny M. Zdobnov, Evangelos Tsitlakidis, Christian Pick, Felipe A. Simão, Emma Persyn, Jeffery W. Jones, Lavrov, Dennis, Beukeboom lab, Evolutionary Genetics, Development & Behaviour, Van de Zande lab, 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), Groningen Institute for Evolutionary Life Sciences [Groningen] (GELIFES), University of Groningen [Groningen], Westfälische Wilhelms-Universität Münster (WWU), Biochemistry Department, University of Otago [Dunedin, Nouvelle-Zélande], Max-Planck-Institut für Kernphysik (MPIK), Max-Planck-Gesellschaft, Max Planck Institute for Chemical Ecology, Physiologie de l'Insecte : Signalisation et Communication (PISC), Institut National de la Recherche Agronomique (INRA)-Université Pierre et Marie Curie - Paris 6 (UPMC)-AgroParisTech, Institute for Evolution and Biodiversity (IEB), Department of Chemistry [Vancouver] (UBC Chemistry), University of British Columbia (UBC), Lawrence Berkeley National Laboratory [Berkeley] (LBNL), Human Genome Sequencing Center, Baylor College of Medicine, Baylor College of Medicine (BCM), Baylor University-Baylor University, Center for Molecular Biodiversity Research (ZMB), Zoological Research Museum Alexander Koenig (ZFMK), Department of Biology, Georgetown University, Université de Lausanne (UNIL), Human Genome Sequencing Center [Houston] (HGSC), Grad Sch Life Sci, Div Neurogenet, Tohoku University [Sendai], Department of Genetic Medicine and Development [Geneva], Université de Genève (UNIGE), Zoologisches Forschungsmuseum Alexander Koenig, Center for Molecular Biodiversity Research, Lavrov, Dennis (ed.), 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)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), and Zdobnov, Evgeny

Subjects
AcademicSubjects/SCI01140, 0106 biological sciences, Most recent common ancestor, Male, Vision, Genome, Insect, Gene Dosage, Hymenoptera, JEWEL WASP NASONIA, Receptors, Odorant, 01 natural sciences, Genome, Parasitoid, MULTIPLE SEQUENCE ALIGNMENT, opsin, Receptors, phytophagy, ddc:576.5, Apocrita, Conserved Sequence, 0303 health sciences, [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], HOST LOCATION, Eusociality, ROYAL JELLY PROTEIN, ATHALIA-ROSAE, Sawfly, Odorant, APIS-MELLIFERA, Multigene Family, Insect Proteins, Female, Research Article, Genetics, Ecology, Evolution, Behavior and Systematics, hexamerin, major royal jelly protein, microsynteny, odorant receptor, CHEMORECEPTOR SUPERFAMILY, Genetic Speciation, Biology, 010603 evolutionary biology, Host-Parasite Interactions, 03 medical and health sciences, Ocular, Animals, Amino Acid Sequence, Herbivory, Social Behavior, DRAFT GENOME, Life Below Water, Vision, Ocular, 030304 developmental biology, MODEL SELECTION, Glycoproteins, Orussidae, Evolutionary Biology, fungi, Human Genome, AcademicSubjects/SCI01130, Immunity, biology.organism_classification, MOLECULAR EVOLUTION, Evolutionary biology, DNA Transposable Elements, Biochemistry and Cell Biology, Insect, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis, Developmental Biology
Abstract

The tremendous diversity of Hymenoptera is commonly attributed to the evolution of parasitoidism in the last common ancestor of parasitoid sawflies (Orussidae) and wasp-waisted Hymenoptera (Apocrita). However, Apocrita and Orussidae differ dramatically in their species richness, indicating that the diversification of Apocrita was promoted by additional traits. These traits have remained elusive due to a paucity of sawfly genome sequences, in particular those of parasitoid sawflies. Here, we present comparative analyses of draft genomes of the primarily phytophagous sawfly Athalia rosae and the parasitoid sawfly Orussus abietinus. Our analyses revealed that the ancestral hymenopteran genome exhibited traits that were previously considered unique to eusocial Apocrita (e.g., low transposable element content and activity) and a wider gene repertoire than previously thought (e.g., genes for CO2 detection). Moreover, we discovered that Apocrita evolved a significantly larger array of odorant receptors than sawflies, which could be relevant to the remarkable diversification of Apocrita by enabling efficient detection and reliable identification of hosts.

Published
2020
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2. Brown marmorated stink bug, Halyomorpha halys (Stål), genome: putative underpinnings of polyphagy, insecticide resistance potential and biology of a top worldwide pest

Author

J. Spencer Johnston, John H. Werren, Hugh M. Robertson, Joshua B. Benoit, Shannon Dugan, Monica Munoz-Torres, Richard A. Gibbs, Kim C. Worley, Raman Bansal, Patrick Masterson, Joshua H. Rhoades, Panagiotis Ioannidis, Christopher P. Childers, Dawn E. Gundersen-Rindal, Yi Han, Brent A. Kronmiller, Alexander G. Martynov, Brenda Oppert, Harshavardhan Doddapaneni, Stephen Richards, Zhijian Jake Tu, Richard W. Hardy, Christopher J. Holmes, Florian Maumus, Shwetha C. Murali, Markus Friedrich, Evgeny M. Zdobnov, Alys M. Cheatle Jarvela, Arun S. Velamuri, Mengyao Chen, Monica F. Poelchau, Matthew T. Weirauch, Michael E. Sparks, Robert M. Waterhouse, Katie Reding, Brantley Hall, Sandra L. Lee, Jiaxin Qu, Jeffery W. Jones, David W. Farrow, Kristen A. Panfilio, Adelaide C. Rhodes, Jackson Wells, Hsu Chao, Donna M. Muzny, Sammy Cheng, Huyen Dinh, David R. Nelson, Leslie Pick, Elena N. Elpidina, Michael B. Blackburn, Rose Richter, Daniel S.T. Hughes, Terence Murphy, Faith Kung, Andrew J. Rosendale, Débora P. Paula, Biochemistry, Ioannidis, Panagiotis, Zdobnov, Evgeny, Department of Biochemistry and Molecular Biology [Houston, TX, USA], The University of Texas Medical School at Houston, Human Genome Sequencing Center [Houston] (HGSC), Baylor College of Medicine (BCM), Baylor University-Baylor University, Human Genome Sequencing Center, Baylor College of Medicine, Interactions Arbres-Microorganismes (IAM), Université de Lorraine (UL)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Unité de Recherche Génomique Info (URGI), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Lawrence Berkeley National Laboratory [Berkeley] (LBNL), National Center for Biotechnology Information (NCBI), University of Tennessee, Department of Biology, Georgetown University, University of Illinois [Chicago] (UIC), University of Illinois System, Université de Lausanne (UNIL), Cincinnati Children's Hospital Medical Center, Department of Genetic Medicine and Development [Geneva], Université de Genève (UNIGE), Invasive Insect Biocontrol and Behavior Laboratory [Beltsville, USA], USDA Agricultural Research Service [Beltsville, Maryland], and USDA-ARS : Agricultural Research Service-USDA-ARS : Agricultural Research Service

Subjects
0106 biological sciences, Integrated pest management, Gene Transfer, Insect, 01 natural sciences, Genome, Medical and Health Sciences, chemoreceptors, Invasive species, invasive species, Insecticide Resistance, Genome Size, ddc:576.5, ComputingMilieux_MISCELLANEOUS, Phylogeny, media_common, 0303 health sciences, biology, Ecology, Biological Sciences, Habitat, Insect Proteins, Brown marmorated stink bug genome, odorant binding proteins, Biotechnology, Research Article, lcsh:QH426-470, Gene Transfer, Horizontal, Bioinformatics, media_common.quotation_subject, lcsh:Biotechnology, 010603 evolutionary biology, Horizontal, Heteroptera, 03 medical and health sciences, lcsh:TP248.13-248.65, Information and Computing Sciences, Genetics, Animals, polyphagy, Brown marmorated stink bug, Ecosystem, 030304 developmental biology, [SDV.GEN]Life Sciences [q-bio]/Genetics, QL, Whole Genome Sequencing, opsins, Human Genome, fungi, 15. Life on land, Pesticide, biology.organism_classification, Pentatomid genomics, lcsh:Genetics, PEST analysis, cathepsins, Introduced Species, xenobiotic detoxification
Abstract

BackgroundHalyomorpha halys(Stål), the brown marmorated stink bug, is a highly invasive insect species due in part to its exceptionally high levels of polyphagy. This species is also a nuisance due to overwintering in human-made structures. It has caused significant agricultural losses in recent years along the Atlantic seaboard of North America and in continental Europe. Genomic resources will assist with determining the molecular basis for this species’ feeding and habitat traits, defining potential targets for pest management strategies.ResultsAnalysis of the 1.15-Gb draft genome assembly has identified a wide variety of genetic elements underpinning the biological characteristics of this formidable pest species, encompassing the roles of sensory functions, digestion, immunity, detoxification and development, all of which likely supportH. halys’ capacity for invasiveness. Many of the genes identified herein have potential for biomolecular pesticide applications.ConclusionsAvailability of theH. halysgenome sequence will be useful for the development of environmentally friendly biomolecular pesticides to be applied in concert with more traditional, synthetic chemical-based controls.

Published
2020
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3. Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome

Author

Shwetha C. Murali, Hsiao-ling Lu, Siegfried Roth, Huyen Dinh, Peter K. Dearden, Barbara M. I. Vreede, M. Emília Santos, Evgeny M. Zdobnov, Viera Kovacova, Christopher J. Holmes, Stefano Colella, Yuichiro Suzuki, Tamsin E. M. Jones, Chun-che Chang, Stefan Koelzer, Jeffery W. Jones, Essia Sghaier, Thorsten Horn, Richard A. Gibbs, Mackenzie Lovegrove, Panagiotis Ioannidis, Lucila Traverso, Subba Reddy Palli, Megan L. Porter, Olivia Tidswell, Peter Nagui Refki, Neta Ginzburg, Rolando Rivera-Pomar, Sandra L. Lee, Chris Jacobs, Cassandra G. Extavour, Jan Seibert, Amanda Dolan, David Armisén, Jayendra Nath Shukla, Kristen A. Panfilio, Christopher P. Childers, Matthew T. Weirauch, Daniel S.T. Hughes, Jiaxin Qu, Kim C. Worley, Hugh M. Robertson, Monica Munoz-Torres, Markus Friedrich, Emily C. Jennings, Elizabeth J. Duncan, Andrew G. Cridge, Hsu Chao, J. Spencer Johnston, Maurijn van der Zee, Mei-Ju May Chen, John H. Werren, Abderrahman Khila, Shannon Dugan, Stephen Richards, Lena Sachs, Joshua B. Benoit, Antonin J.J. Crumière, Nicolas Parisot, Megan Leask, Yen-Ta Chen, Harshavardhan Doddapaneni, Gérard Febvay, Donna M. Muzny, Ariel D. Chipman, Rose Richter, Robert M. Waterhouse, Leslie Pick, Monica F. Poelchau, Patricia J. Moore, Chloé Suzanne Berger, Richard J. Stancliffe, Yi Min Hsiao, Séverine Viala, Chien-Yueh Lee, Yi Han, Iris M. Vargas Jentzsch, Elise M. Didion, Deniz F. Erezyilmaz, Yong Lu, Andrew J. Rosendale, Peter Heger, Patrice Baa-Puyoulet, 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), Institut National de la Recherche Agronomique (INRA)-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), University of Illinois [Chicago] (UIC), University of Illinois System, Department of Biology, Georgetown University, Université de Lausanne (UNIL), Cincinnati Children's Hospital Medical Center, Biochemistry Department, University of Otago [Dunedin, Nouvelle-Zélande], Human Genome Sequencing Center, Baylor College of Medicine, Baylor College of Medicine (BCM), Baylor University-Baylor University, University of Edinburgh, Lawrence Berkeley National Laboratory [Berkeley] (LBNL), Department of Entomology [Lexington], University of Kentucky, Cologne Biocenter, Institute of Developmental Biology, Institute of Developmental Biology, University of Basel (Unibas), Institut de Génomique Fonctionnelle de Lyon (IGFL), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA)-École normale supérieure - Lyon (ENS Lyon), Human Genome Sequencing Center [Houston] (HGSC), Department of Genetic Medicine and Development [Geneva], Université de Genève (UNIGE), United States Department of Health & Human Services National Institutes of Health (NIH) - USA [U54 HG003273], German Research Foundation (DFG) [PA 2044/1 1 SFB 680], Swiss National Science Foundation (SNSF) [31003A_143936, PP00P3_170664], European Research Council grant ERC-CoG [616346], German Research Foundation (DFG) [SFB 680], National Science Foundation (NSF) [US NSF DEB1257053], United States Department of Health & Human Services National Institutes of Health (NIH) - USA [5R01GM080203, 5R01HG004483, R01GM113230], United States Department of Energy (DOE) [DE-AC02-05CH11231], École normale supérieure - Lyon (ENS Lyon)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS), Georgetown University [Washington] (GU), Université de Lausanne = University of Lausanne (UNIL), University of Kentucky (UK), École normale supérieure de Lyon (ENS de Lyon)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Genève = University of Geneva (UNIGE), Panfilio, Kristen A [0000-0002-6417-251X], Vargas Jentzsch, Iris M [0000-0003-4527-1560], Benoit, Joshua B [0000-0002-4018-3513], Erezyilmaz, Deniz [0000-0001-8416-8561], Suzuki, Yuichiro [0000-0002-0957-3564], Colella, Stefano [0000-0003-3139-6055], Poelchau, Monica F [0000-0002-4584-6056], Waterhouse, Robert M [0000-0003-4199-9052], Ioannidis, Panagiotis [0000-0003-0939-6745], Weirauch, Matthew T [0000-0001-7977-9122], Werren, John H [0000-0001-9353-2070], Jacobs, Chris GC [0000-0002-3128-2288], Duncan, Elizabeth J [0000-0002-1841-504X], Vreede, Barbara MI [0000-0002-5023-4601], Chang, Chun-Che [0000-0002-3586-1607], Chen, Mei-Ju M [0000-0001-7768-8905], Chen, Yen-Ta [0000-0002-4570-6061], Childers, Christopher P [0000-0002-1253-5550], Chipman, Ariel D [0000-0001-6696-840X], Cridge, Andrew G [0000-0002-1399-5188], Crumière, Antonin JJ [0000-0003-2214-2993], Dearden, Peter K [0000-0001-7790-9675], Didion, Elise M [0000-0002-4987-8901], Dinh, Huyen [0000-0003-0336-0362], Doddapaneni, Harsha Vardhan [0000-0002-2433-633X], Dugan, Shannon [0000-0003-1482-816X], Extavour, Cassandra G [0000-0003-2922-5855], Febvay, Gérard [0000-0002-0654-2340], Friedrich, Markus [0000-0002-5622-7920], Han, Yi [0000-0001-7605-8979], Holmes, Christopher J [0000-0001-9612-366X], Horn, Thorsten [0000-0001-8181-939X], Hsiao, Yi-Min [0000-0002-1817-0302], Jennings, Emily C [0000-0002-7687-5319], Johnston, J Spencer [0000-0003-4792-2945], Jones, Tamsin E [0000-0002-0027-0858], Khila, Abderrahman [0000-0003-0908-483X], Kovacova, Viera [0000-0003-4581-4254], Lee, Chien-Yueh [0000-0002-4304-974X], Lu, Hsiao-Ling [0000-0002-4029-6470], Moore, Patricia J [0000-0001-9802-7217], Munoz-Torres, Monica C [0000-0001-8430-6039], Muzny, Donna M [0000-0002-3055-0359], Palli, Subba R [0000-0002-0873-3247], Parisot, Nicolas [0000-0001-5217-8415], Pick, Leslie [0000-0002-4505-5107], Porter, Megan L [0000-0001-7985-2887], Qu, Jiaxin [0000-0002-1122-9391], Rivera-Pomar, Rolando [0000-0002-7720-7064], Rosendale, Andrew J [0000-0002-2463-8856], Roth, Siegfried [0000-0001-5772-3558], Shukla, Jayendra N [0000-0003-1589-1929], Stancliffe, Richard J [0000-0002-6972-9655], van der Zee, Maurijn [0000-0002-8728-8646], Worley, Kim C [0000-0002-0282-1000], Richards, Stephen [0000-0001-8959-5466], and Apollo - University of Cambridge Repository

Subjects
gene family evolution, Lineage (evolution), [SDV]Life Sciences [q-bio], Genome, Insect, Gene Transfer, Gene Dosage, Insect, Genome, purl.org/becyt/ford/1 [https], 0302 clinical medicine, CYS2-HIS2 Zinc Fingers, phytophagy, ddc:576.5, lcsh:QH301-705.5, media_common, [SDV.EE]Life Sciences [q-bio]/Ecology, environment, 0303 health sciences, biology, Large milkweed bug, Ecology, Pigmentation, [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], Genes, Homeobox, Biological Sciences, Lygaeidae, Hemiptera, séquence du génome, Smell, evolution of development, TRANSCRIPTION FACTORS, puceron, Biotechnology, lcsh:QH426-470, Gene Transfer, Horizontal, ddc:025.063/570, Evolution, Bioinformatics, media_common.quotation_subject, 1.1 Normal biological development and functioning, Transcription Factors/genetics, Zoology, Amino Acid Sequence, Animals, Evolution, Molecular, Feeding Behavior, Gene Expression Profiling, Hemiptera/genetics, Hemiptera/growth & development, Hemiptera/metabolism, Pigmentation/genetics, Evolution of development, Gene family evolution, Gene structure, Lateral gene transfer, Phytophagy, RNAi, Transcription factors, GENE FAMILY EVOLUTION, Genomics, Biotechnologies, LATERAL GENE TRANSFER, Horizontal, 03 medical and health sciences, Molecular evolution, Underpinning research, [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], Information and Computing Sciences, transcription factors, RNAI, Genetics, Homeobox, GENE STRUCTURE, purl.org/becyt/ford/1.6 [https], SB, Genome size, Ciencias Exactas, 030304 developmental biology, Whole genome sequencing, QL, QH, Research, gene structure, lateral gene transfer, Human Genome, fungi, Molecular, biology.organism_classification, Hemiptera/genetics/growth & development/metabolism, diversité des populations, lcsh:Genetics, [SDV.GEN.GA]Life Sciences [q-bio]/Genetics/Animal genetics, PHYTOPHAGY, lcsh:Biology (General), Genes, Animal ecology, Evolutionary biology, EVOLUTION OF DEVELOPMENT, Evolutionary developmental biology, 030217 neurology & neurosurgery, Environmental Sciences
Abstract

Background: The Hemiptera (aphids, cicadas, and true bugs) are a key insect order, with high diversity for feeding ecology and excellent experimental tractability for molecular genetics. Building upon recent sequencing of hemipteran pests such as phloem-feeding aphids and blood-feeding bed bugs, we present the genome sequence and comparative analyses centered on the milkweed bug Oncopeltus fasciatus, a seed feeder of the family Lygaeidae. Results: The 926-Mb Oncopeltus genome is well represented by the current assembly and official gene set. We use our genomic and RNA-seq data not only to characterize the protein-coding gene repertoire and perform isoform-specific RNAi, but also to elucidate patterns of molecular evolution and physiology. We find ongoing, lineage-specific expansion and diversification of repressive C2H2 zinc finger proteins. The discovery of intron gain and turnover specific to the Hemiptera also prompted the evaluation of lineage and genome size as predictors of gene structure evolution. Furthermore, we identify enzymatic gains and losses that correlate with feeding biology, particularly for reductions associated with derived, fluid nutrition feeding. Conclusions: With the milkweed bug, we now have a critical mass of sequenced species for a hemimetabolous insect order and close outgroup to the Holometabola, substantially improving the diversity of insect genomics. We thereby define commonalities among the Hemiptera and delve into how hemipteran genomes reflect distinct feeding ecologies. Given Oncopeltus’s strength as an experimental model, these new sequence resources bolster the foundation for molecular research and highlight technical considerations for the analysis of medium-sized invertebrate genomes., La lista completa de autores puede verse en el archivo asociado., Facultad de Ciencias Exactas, Centro Regional de Estudios Genómicos

Published
2019
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4. Gene Ages, Nomenclatures, and Functional Diversification of the Methuselah/Methuselah-Like GPCR Family inDrosophilaandTribolium

Author

Jeffery W. Jones and Markus Friedrich

Subjects
0301 basic medicine, Genetics, Subfamily, biology, fungi, Methuselah, biology.organism_classification, 03 medical and health sciences, 030104 developmental biology, 0302 clinical medicine, Evolutionary biology, Melanogaster, Molecular Medicine, Gene family, Animal Science and Zoology, Drosophila melanogaster, Clade, Gene, Drosophila, 030217 neurology & neurosurgery, Ecology, Evolution, Behavior and Systematics, Developmental Biology
Abstract

Affecting lifespan regulation and oxidative stress resistance, the G-protein coupled receptor (GPCR) gene methuselah (mth) plays important roles in the life history of Drosophila melanogaster. Substantial progress has been made in elucidating the molecular pathways by which mth affects these traits, yet conflicting ideas exist as to how old these genetic interactions are as well as how old the mth gene itself is. Root to these issues is the complex gene family history of the Mth/Mthl GPCR family, which experienced independent expansions in a variety of animal clades, leading to at least six subfamilies in insects. Within insects, drosophilid flies stand out by possessing up to three times more Mth/Mthl receptors due to the expansion of a single subfamily, the mth superclade subfamily, which contains an even younger subfamily introduced here as the melanogaster subgroup subfamily. As a result, most of the 16 Mth/Mthl receptors of D. melanogaster are characterized by n:1 orthology relationships to singleton mth superclade homologs in nondrosophilid species. This challenge is exacerbated by the inconsistent naming of Mth/Mthl orthologs across species. To consolidate this situation, we review established ortholog relationships among insect Mth/Mthl receptors, clarify the gene nomenclatures in two important satellite model species, the fruit fly relative D. virilis and the red flour beetle Tribolium castaneum, and discuss the genetic and functional evolution of the D. melanogaster Mth GPCR.

Published
2016
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5. The Toxicogenome of Hyalella azteca: A Model for Sediment Ecotoxicology and Evolutionary Toxicology

Author

J. Spencer Johnston, John H. Werren, Mei-Ju May Chen, Shwetha C. Murali, Joshua B. Benoit, Kaley M. Major, Alexandra Mechler-Hickson, Jiaxin Qu, Hsu Chao, Shuai Chen, Michael A. D. Goodisman, René Feyereisen, Nicholas Mathers, Sandra L. Lee, Daniel S.T. Hughes, Andrew J. Rosendale, Karl M. Glastad, Christopher P. Childers, Joseph H. Vineis, Chris D. Vulpe, Huyen Dinh, Yi Han, Bonnie J. Blalock, Peter A. Bain, Jennifer L. Bowen, Carol Eunmi Lee, Simone Hasenbein, Padrig Tuck, Kim C. Worley, Shannon Dugan, Donna M. Muzny, Hugo Ochoa-Acuña, Gary A. Wellborn, Faith N. Lambert, Helen C. Poynton, Mark E. Smith, Adam D. Biales, Austin R. Manny, Monica Munoz-Torres, Jeffery W. Jones, Andrew G. Cridge, Richard A. Gibbs, Hugh M. Robertson, Stephen Richards, Monica F. Poelchau, Markus Friedrich, Harshavardhan Doddapaneni, John K. Colbourne, Yu-Yu Lin, and Maria S. Sepúlveda

Subjects
0301 basic medicine, Species complex, Geologic Sediments, Amphipoda, Ecotoxicology, Genome, Article, 03 medical and health sciences, chemistry.chemical_compound, Toxicity Tests, Environmental Chemistry, Animals, biology, Ecology, Hyalella azteca, General Chemistry, biology.organism_classification, Major gene, Azteca, 030104 developmental biology, chemistry, North America, Water Pollutants, Chemical, Toxicant
Abstract

Hyalella azteca is a cryptic species complex of epibenthic amphipods of interest to ecotoxicology and evolutionary biology. It is the primary crustacean used in North America for sediment toxicity testing and an emerging model for molecular ecotoxicology. To provide molecular resources for sediment quality assessments and evolutionary studies, we sequenced, assembled, and annotated the genome of the H. azteca U.S. Lab Strain. The genome quality and completeness is comparable with other ecotoxicological model species. Through targeted investigation and use of gene expression data sets of H. azteca exposed to pesticides, metals, and other emerging contaminants, we annotated and characterized the major gene families involved in sequestration, detoxification, oxidative stress, and toxicant response. Our results revealed gene loss related to light sensing, but a large expansion in chemoreceptors, likely underlying sensory shifts necessary in their low light habitats. Gene family expansions were also noted for cytochrome P450 genes, cuticle proteins, ion transporters, and include recent gene duplications in the metal sequestration protein, metallothionein. Mapping of differentially expressed transcripts to the genome significantly increased the ability to functionally annotate toxicant responsive genes. The H. azteca genome will greatly facilitate development of genomic tools for environmental assessments and promote an understanding of how evolution shapes toxicological pathways with implications for environmental and human health.

Published
2018

6. Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle-plant interface

Author

Seung-Joon Ahn, Michael A. D. Goodisman, Evgeny M. Zdobnov, Lorna B Cohen, David R. Lance, Seunggwan Shin, Scott M. Geib, Robert M. Waterhouse, Honghu Quan, Christian Silva, Stephen Richards, Subba Reddy Palli, Jiaxin Qu, Shwetha C. Murali, Shannon Dugan, Iris M. Vargas Jentzsch, Hsu Chao, Daniel S.T. Hughes, Duane D. McKenna, Kelli Hoover, Hugh M. Robertson, Robert F. Mitchell, Anna K. Childers, Joshua B. Benoit, Deanna Arsala, Panagiotis Ioannidis, Christopher P. Childers, Richard L. Roehrdanz, Yi Han, Donna M. Muzny, Stephanie Haddad, J. Spencer Johnston, Huyen Dinh, John H. Werren, Andrew J. Rosendale, Yannick Pauchet, André Busch, Chien Yueh Lee, Heath Blackmon, Daniel Pers, Joseph P. Rinehart, Ann M. Ray, Markus Friedrich, Amanda Dolan, Jeffery P. Demuth, Harshavardhan Doddapaneni, George D. Yocum, Han Lin, Erin D. Scully, Jeffery W. Jones, Kim C. Worley, David R. Nelson, Tiffany Bledsoe, Bernarda Calla, Julia H. Bowsher, Monica F. Poelchau, Dave J. Clarke, Leslie A. Kuhn, Jeremy A. Lynch, Sandra L. Lee, Jian J. Duan, Karl M. Glastad, Alex S. Torson, Richard A. Gibbs, Kristen A. Panfilio, Armin P. Moczek, and Roy Kirsch

Subjects
0301 basic medicine, Chemoperception, Gene Transfer, Horizontal, Xylophagy, Genome, Insect, Introduced species, Phytophagy, Genome, Invasive species, Host-Parasite Interactions, Trees, Evolution, Molecular, 03 medical and health sciences, Emerald ash borer, Botany, Animals, ddc:576.5, Dung beetle, biology, Research, fungi, food and beverages, Sequence Analysis, DNA, Horizontal gene transfer, 15. Life on land, biology.organism_classification, Coleoptera, 030104 developmental biology, Evolutionary biology, Larva, Glycoside hydrolase, Anoplophora, Introduced Species, Detoxification, Functional divergence, Woody plant
Abstract

Background Relatively little is known about the genomic basis and evolution of wood-feeding in beetles. We undertook genome sequencing and annotation, gene expression assays, studies of plant cell wall degrading enzymes, and other functional and comparative studies of the Asian longhorned beetle, Anoplophora glabripennis, a globally significant invasive species capable of inflicting severe feeding damage on many important tree species. Complementary studies of genes encoding enzymes involved in digestion of woody plant tissues or detoxification of plant allelochemicals were undertaken with the genomes of 14 additional insects, including the newly sequenced emerald ash borer and bull-headed dung beetle. Results The Asian longhorned beetle genome encodes a uniquely diverse arsenal of enzymes that can degrade the main polysaccharide networks in plant cell walls, detoxify plant allelochemicals, and otherwise facilitate feeding on woody plants. It has the metabolic plasticity needed to feed on diverse plant species, contributing to its highly invasive nature. Large expansions of chemosensory genes involved in the reception of pheromones and plant kairomones are consistent with the complexity of chemical cues it uses to find host plants and mates. Conclusions Amplification and functional divergence of genes associated with specialized feeding on plants, including genes originally obtained via horizontal gene transfer from fungi and bacteria, contributed to the addition, expansion, and enhancement of the metabolic repertoire of the Asian longhorned beetle, certain other phytophagous beetles, and to a lesser degree, other phytophagous insects. Our results thus begin to establish a genomic basis for the evolutionary success of beetles on plants. Electronic supplementary material The online version of this article (doi:10.1186/s13059-016-1088-8) contains supplementary material, which is available to authorized users.

Published
2016

7. Dramatic Expansion and Developmental Expression Diversification of the Methuselah Gene Family During Recent Drosophila Evolution

Author

Denise N. Bronner, Jeffery W. Jones, Markus Friedrich, Zahabiya Husain, Dana A. Hallal, Rami Zein, Mark F A VanBerkum, Jason Caravas, and Meghna V. Patel

Subjects
Genetics, animal structures, biology, Phylogenetic tree, fungi, Methuselah, biology.organism_classification, Imaginal disc, Molecular Medicine, Subfunctionalization, Gene family, Animal Science and Zoology, Clade, Gene, Drosophila, Ecology, Evolution, Behavior and Systematics, Developmental Biology
Abstract

Functional studies of the methuselah/methuselah-like (mth/mthl) gene family have focused on the founding member mth, but little is known regarding the developmental functions of this receptor or any of its paralogs. We undertook a comprehensive analysis of developmental expression and sequence divergence in the mth/mthl gene family. Using in situ hybridization techniques, we detect expression of six genes (mthl1, 5, 9, 11, 13, and 14) in the embryo during gastrulation and development of the gut, heart, and lymph glands. Four receptors (mthl3, 4, 6, and 8) are expressed in the larval central nervous system, imaginal discs, or both, and two receptors (mthl10 and mth) are expressed in both embryos and larvae. Phylogenetic analysis of all mth/mthl genes in five Drosophila species, mosquito and flour beetle structured the mth/mthl family into several subclades. mthl1, 5, and 14 are present in most species, each forming a separate clade. A newly identified Drosophila mthl gene (CG31720; herein mthl15) formed another ancient clade. The remaining Drosophila receptors, including mth, are members of a large “superclade” that diversified relatively recently during dipteran evolution, in many cases within the melanogaster subgroup. Comparing the expression patterns of the mth/mthl “superclade” paralogs to the embryonic expression of the singleton ortholog in Tribolium suggests both subfunctionalization and acquisition of novel functionalities. Taken together, our findings shed novel light on mth as a young member of an adaptively evolving developmental gene family. J. Exp. Zool. (Mol. Dev. Evol.) 318B:368-387, 2012. © 2012 Wiley Periodicals, Inc.

Published
2012
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8. Unique features of a global human ectoparasite identified through sequencing of the bed bug genome

Author

Fang Zhu, Warren Booth, Zach N. Adelman, Benjamin A. Hottel, Huyen Dinh, Sebastian Wernig, Ameya D. Gondhalekar, Han Lin, Donna M. Muzny, Reinhard Predel, Abderrahman Khila, Antonin J.J. Crumière, Hugh M. Robertson, Christopher P. Childers, Monica F. Poelchau, Peter Nagui Refki, Klaus Reinhardt, Frank Maiwald, Jay D. Evans, Shwetha C. Murali, Kim C. Worley, Sandra L. Lee, Jing-Jiang Zhou, Stephen Richards, Amanda Dolan, Markus Friedrich, Corinna Schorn, Edward L. Vargo, Emily C. Jennings, Robert M. Waterhouse, Elise M. Szuter, Jeffery W. Jones, Iris M. Vargas Jentzsch, Andrew J. Rosendale, Elizabeth J. Duncan, José M. C. Ribeiro, Shannon Dugan, Nicolai Peschel, Yi Han, David Armisén, Christian Derst, Subba Reddy Palli, David A. Wheeler, Kapil R. Raje, Paul R. Johnston, Maria Emilia Santos, Kristen A. Panfilio, Mark-Christoph Ott, Chaoyang Zhao, Matthew T. Weirauch, Chien-Yueh Lee, Jacob M. Hendershot, Hemant Gujar, Valentina Resnik, Panagiotis Ioannidis, David R. Nelson, Coby Schal, M. Mohan, Evgeny M. Zdobnov, Joshua B. Benoit, Ralf Nauen, Omprakash Mittapalli, Pamela Menegazzi, Séverine Viala, Brittany F. Peterson, Harshavardhan Doddapaneni, Essia Sghaier, Richard W. Hagan, Michael E. Scharf, Christian Wegener, Daniel S.T. Hughes, Seung-Joon Ahn, J. Spencer Johnston, John H. Werren, Richard A. Gibbs, Wolfgang Blenau, Michelle A. E. Anderson, Jiaxin Qu, Hsu Chao, Jayendra Nath Shukla, Geoffrey M. Attardo, Ioannidis, Panagiotis, Waterhouse, Robert, Zdobnov, Evgeny, Entomology, and Massachusetts Institute of Technology. Computer Science and Artificial Intelligence Laboratory

Subjects
0301 basic medicine, Traumatic insemination, Bedbugs, Insecticides, Gene Transfer, General Physics and Astronomy, Ectoparasitic Infestations, Genome, Insecticide Resistance, Bed bug, Phylogenomics, ddc:576.5, Genetics, Multidisciplinary, Host-Parasite Interactions/genetics, Bedbugs/genetics, Biological sciences, Cimex lectularius, Sequence Analysis, Biotechnology, animal structures, Gene Transfer, Horizontal, Hematophagy, Science, Biology, Article, General Biochemistry, Genetics and Molecular Biology, DNA sequencing, Horizontal, Host-Parasite Interactions, 03 medical and health sciences, ddc:570, parasitic diseases, Insecticide Resistance/genetics, Animals, Humans, Obligate, Human Genome, fungi, Gene Transfer, Horizontal/genetics, General Chemistry, DNA, Feeding Behavior, Sequence Analysis, DNA, biology.organism_classification, 030104 developmental biology, Good Health and Well Being, Evolutionary biology
Abstract

The bed bug, Cimex lectularius, has re-established itself as a ubiquitous human ectoparasite throughout much of the world during the past two decades. This global resurgence is likely linked to increased international travel and commerce in addition to widespread insecticide resistance. Analyses of the C. lectularius sequenced genome (650 Mb) and 14,220 predicted protein-coding genes provide a comprehensive representation of genes that are linked to traumatic insemination, a reduced chemosensory repertoire of genes related to obligate hematophagy, host–symbiont interactions, and several mechanisms of insecticide resistance. In addition, we document the presence of multiple putative lateral gene transfer events. Genome sequencing and annotation establish a solid foundation for future research on mechanisms of insecticide resistance, human–bed bug and symbiont–bed bug associations, and unique features of bed bug biology that contribute to the unprecedented success of C. lectularius as a human ectoparasite., The bed bug, Cimex lectularius, is a ubiquitous human ectoparasite with global distribution. Here, the authors sequence the genome of the bed bug and identify reductions in chemosensory genes, expansion of genes associated with blood digestion and genes linked to pesticide resistance.

Published
2016

9. The whole genome sequence of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species

Author

Jiaxin Qu, Hsu Chao, Kostas Bourtzis, John P. Cavanaugh, Mosè Manni, Shannon Dugan, Angela Meccariello, John H. Werren, Panagiota Koskinioti, Miguel González-Guzmán, Ludvik M. Gomulski, Markus Friedrich, Hugh M. Robertson, Patrick Schreiner, Grazia Savini, Daniel S.T. Hughes, Yi Han, Georgios Georgakilas, Richard A. Gibbs, Giuseppe Saccone, Terence Murphy, Jeffery W. Jones, Paolo Siciliano, Kim C. Worley, Huyen Dinh, Pedro Castañera, Ernst A. Wimmer, Sarah D. Giers, Shwetha C. Murali, Antigone Zacharopoulou, Andrew J. Rosendale, Donna M. Muzny, Harshavardhan Doddapaneni, Félix Ortego, Alfred M. Handler, Monica Munoz-Torres, Christopher P. Childers, Pedro Hernández-Crespo, Dimitra Karagkouni, Maria D. Paraskevopoulou, Francesca Scolari, Joshua B. Benoit, Ingrid Curril, Sheina B. Sim, Ioannis S. Vlachos, Marco Salvemini, George Tsiamis, Amanda Dolan, Andrew E. Rosselot, Peter Arensburger, Stephen Richards, Kostas D. Mathiopoulos, Martin Reczko, Ana Guillem-Amat, Georg Oberhofer, Scott M. Geib, Alexie Papanicolaou, Enric Ureña, Monica F. Poelchau, Giuliano Gasperi, Anna R. Malacrida, Marc F. Schetelig, Sandra L. Lee, Artemis G. Hatzigeorgiou, Peter W. Atkinson, National Institute of Food and Agriculture (US), Papanicolaou, Alexie, Schetelig, Marc F, Arensburger, Peter, Atkinson, Peter W, Benoit, Joshua B, Bourtzis, Kosta, Castañera, Pedro, Cavanaugh, John P, Chao, Hsu, Childers, Christopher, Curril, Ingrid, Dinh, Huyen, Doddapaneni, Harshavardhan, Dolan, Amanda, Dugan, Shannon, Friedrich, Marku, Gasperi, Giuliano, Geib, Scott, Georgakilas, Georgio, Gibbs, Richard A, Giers, Sarah D, Gomulski, Ludvik M, González Guzmán, Miguel, Guillem Amat, Ana, Han, Yi, Hatzigeorgiou, Artemis G, Hernández Crespo, Pedro, Hughes, Daniel S. T, Jones, Jeffery W, Karagkouni, Dimitra, Koskinioti, Panagiota, Lee, Sandra L, Malacrida, Anna R, Manni, Mosè, Mathiopoulos, Kosta, Meccariello, Angela, Murali, Shwetha C, Murphy, Terence D, Muzny, Donna M, Oberhofer, Georg, Ortego, Félix, Paraskevopoulou, Maria D, Poelchau, Monica, Qu, Jiaxin, Reczko, Martin, Robertson, Hugh M, Rosendale, Andrew J, Rosselot, Andrew E, Saccone, Giuseppe, Salvemini, Marco, Savini, Grazia, Schreiner, Patrick, Scolari, Francesca, Siciliano, Paolo, Sim, Sheina B, Tsiamis, George, Ureña, Enric, Vlachos, Ioannis S, Werren, John H, Wimmer, Ernst A, Worley, Kim C, Zacharopoulou, Antigone, Richards, Stephen, and Handler, Alfred M.

Subjects
Mediterranean climate, 0301 basic medicine, Integrated pest management, Gene family evolution, Insect invasiveness, 05 Environmental Sciences, Genome, Insect, Genome, Animals, Genetically Modified, Sterile insect technique, Insect invasivene, 0302 clinical medicine, Genetics & Heredity, 2. Zero hunger, Genetics, biology, genome sequence, Mediterranean fruit fly, highly invasive pest species, High-Throughput Nucleotide Sequencing, Ceratitis capitata, Biological Evolution, 3. Good health, Tephritid genomics, Medfly genome, GERM-LINE TRANSFORMATION, Host adaptation, Erratum, Life Sciences & Biomedicine, DIPTERA TEPHRITIDAE, Bioinformatics, TRANSPOSABLE ELEMENT, Zoology, Insect orthology, PROGRAMMED CELL-DEATH, BACTERIA-BINDING PROTEIN, 03 medical and health sciences, Molecular evolution, Medfly integrated pest management (IPM), Animals, Humans, Pest Control, Biological, Drosophila, Whole genome sequencing, 08 Information And Computing Sciences, Science & Technology, ANASTREPHA-SUSPENSA, Research, fungi, Molecular Sequence Annotation, 06 Biological Sciences, biology.organism_classification, ANOPHELES-GAMBIAE, MOLECULAR EVOLUTION, Chromosomal synteny, 030104 developmental biology, Biotechnology & Applied Microbiology, DROSOPHILA-MELANOGASTER, PEST analysis, Insect adaptation, SEMINAL FLUID PROTEINS, Introduced Species, 030217 neurology & neurosurgery, Adaptive evolution
Abstract

31 p.-11 fig.-2 tab.+ Erratum (2 p.) Papanikolaou, Alexie et al., Background: The Mediterranean fruit fly (medfly), Ceratitis capitata, is a major destructive insect pest due to its broad host range, which includes hundreds of fruits and vegetables. It exhibits a unique ability to invade and adapt to ecological niches throughout tropical and subtropical regions of the world, though medfly infestations have been prevented and controlled by the sterile insect technique (SIT) as part of integrated pest management programs (IPMs). The genetic analysis and manipulation of medfly has been subject to intensive study in an effort to improve SIT efficacy and other aspects of IPM control., Results: The 479 Mb medfly genome is sequenced from adult flies from lines inbred for 20 generations. A highquality assembly is achieved having a contig N50 of 45.7 kb and scaffold N50 of 4.06 Mb. In-depth curation of more than 1800 messenger RNAs shows specific gene expansions that can be related to invasiveness and host adaptation, including gene families for chemoreception, toxin and insecticide metabolism, cuticle proteins, opsins, and aquaporins. We identify genes relevant to IPM control, including those required to improve SIT., Conclusions: The medfly genome sequence provides critical insights into the biology of one of the most serious and widespread agricultural pests. This knowledge should significantly advance the means of controlling the size and invasive potential of medfly populations. Its close relationship to Drosophila, and other insect species important to agriculture and human health, will further comparative functional and structural studies of insect genomes that should broaden our understanding of gene family evolution, Support of this project was provided by the U.S. Department of Agriculture(USDA), Agricultural Research Service (ARS), Animal and Plant Health Inspection Service (APHIS), and National Institute of Food and Agriculture(NIFA)-Biotechnology Risk Assessment Grants Program (grant #2011-39211-30769 to AMH) for funding the initial phase of this project, and to the National Institutes of Health (NIH)-National Human Genome Research Institute (NHGRI) for funding the medfly genome sequencing, assembly and Maker 2.0 automated annotation as part of the i5K 30 genome pilot project (grant #U54 HG003273 to RAG). The NIH Intramural Research Program, National Library of Medicine funded the NCBI Gnomon annotation and the USDA-National Agricultural Library (NAL) provided support for the WebApollo curation website, with support for manual curation training (to MM-T) provided by NIGMS (grant #5R01GM080203),NHGRI (grant #5R01HG004483), and the U.S. Department of Energy(contract #DE-AC02-05CH11231). Support was provided for: toxin metabolism and insecticide resistance gene studies from MINECO,Spain (AGL2013-42632-R to FO and PH-C); microRNAs, horizontal gene transfer and bacterial contaminant studies from the European Social Fund and National Strategic Reference Framework-THALES (MIS375869 to KB, GT, AGH, and KM) and the U.S. National Science Foundation(DEB 1257053 to JHW); cuticle protein gene studies from USDA-NIFA(grant #2016-67012-24652 to AJR); sex-determination studies from L.R. Campania (grant 5/02, 2008 to GS); male reproduction and sexual differentiation studies from the FAO/IAEA (Technical Contract No: 16966 to GGa) and Cariplo IMPROVE (to FS); and programmed cell death gene studies and genomic data analysis (to MFS) from the Emmy Noether program, DFG(SCHE 1833/1-1) and the LOEWE Center for Insect Biotechnology & Bioresources grant of the Hessen State Ministry of Higher Education, Research and the Arts(HMWK), Germany and from the USDA-NIFA-Biotechnology Risk Assessment Grants Program (grant #2015-33522-24094 to AMH).

Published
2016

10. Genome sequence of the tsetse fly (Glossina morsitans): vector of African trypanosomiasis

Author

George F. Obiero, Victor Chukwudi Osamor, Atsushi Toyoda, Apollo Simon Peter Balyeidhusa, Cheolho Sim, Paul O. Mireji, Jelle Caers, Serap Aksoy, Irene Omedo, Jan Van Den Abbeele, Lucien Manga, Wanqi Hu, Daniel Lawson, Tadashi Imanishi, Sing-Hoi Sze, Jeffery W. Jones, Sumir Panji, Erich Loza Telleria, Mandy Sanders, Joy J. Winzerling, Dawn L. Geiser, Atway R. Msangi, Joshua B. Benoit, Sandy J. Macdonald, Junichi Watanabe, James Cotton, Francesca Scolari, Steven G. Nyanjom, Linda M. Field, George Githinji, Vineet K. Sharma, José M. C. Ribeiro, Furaha Mramba, Stella Lehane, Shuhua Fu, Marco Falchetto, Imna I. Malele, Michael A. Riehle, Tulika P. Srivastava, Hugh M. Robertson, Immo A. Hansen, Mmule Makgamathe, Caleb K. Kibet, Philippe Solano, Alan Christoffels, Yoshihiro Kawahara, Megan E. Meuti, Nicola Mulder, Patrick Wincker, Gerd Gäde, Zahra Jalali Sefid Dashti, Heather G. Marco, Sheila C. Ommeh, Veronika Michalkova, Cher-Pheng Ooi, Geoffrey M. Attardo, Oliver Manangwa, David L. Denlinger, Alistair C. Darby, Todd D. Taylor, Daniel S.T. Hughes, Mark Wamalwa, Michael W. Gaunt, Daphne Q.-D. Pham, Rosaline W. Macharia, Chinyere K. Okoro, Lee R. Haines, Masahira Hattori, Markus Friedrich, Jingwen Wang, Aaron A. Baumann, Jing-Jiang Zhou, Martin Aslett, Judith H. Willis, Deirdre Walshe, Justin T. Peyton, Alvaro Acosta-Serrano, Loyce M. Okedi, Ludvik M. Gomulski, Johnson Kinyua, Daniel K. Masiga, Mathurin Koffi, J.J.O. Koekemoer, Corey L. Brelsfoard, Gordon William Harkins, Geoffrey H. Siwo, Guy Caljon, Michael A. Quail, Grace Murilla, Anna K. Snyder, Adele Kruger, Gavin H. Thomas, Anna R. Malacrida, Patrick P. Abila, Liliane Schoofs, Rosemary Bateta, Martin T. Swain, Michael J. Lehane, Richard Gregory, Kostas Bourtzis, Brian L. Weiss, Eleanor J Stanley, Zhijian Tu, Matthew Berriman, Winston Hide, David P. Price, Yutaka Suzuki, Maxwell J. Scott, Aaron M. Tarone, Joanna E. Auma, Johnson O. Ouma, Christiane Hertz-Fowler, Alia Benkahla, Karyn Megy, Sophie Ravel, Noboru Inoue, Feziwe Mpondo, Sarah Mwangi, Yeya T. Touré, Florence N. Wamwiri, Clair Rose, Neil D. Rawlings, George Tsiamis, Thiago Luiz, Peter Arensburger, Mario Jonas, Wesley C. Warren, Rita V. M. Rio, Richard K. Wilson, Heikki Lehväslaiho, Denis M. Larkin, Urvashi N. Ramphul, Qirui Zhang, Dawn Stephens, Neil Hall, Kevin K. Marucha, Ryuichi Sakate, Institut de Recherche pour le Développement (IRD [France-Sud]), Genoscope - Centre national de séquençage [Evry] (GENOSCOPE), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Laboratoire de Parasitologie Médicale, Biotechnologies et Biomolécules (LR11IPT06), Institut Pasteur de Tunis, and Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)

Subjects
MESH: Sequence Analysis, DNA, MESH: Insect Vectors/physiology, Genome, Insect, MESH: Insect Vectors/genetics, Genes, Insect, MESH: Genes, Insect, Genome, MESH: Insect Vectors/microbiology, Salivary Glands, MESH: Genome, Insect, 0302 clinical medicine, African trypanosomiasis, MESH: Animals, Genetics, MESH: Salivary Glands/physiology, 0303 health sciences, Multidisciplinary, MESH: Symbiosis, biology, Microbiota, Reproduction, MESH: Tsetse Flies/genetics, MESH: Tsetse Flies/parasitology, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, Blood, MESH: Feeding Behavior, MESH: Insect Proteins/physiology, Insect Proteins, Wolbachia, MESH: Trypanosoma/physiology, Female, Trypanosoma, Tsetse Flies, MESH: Tsetse Flies/microbiology, MESH: Trypanosomiasis, African/transmission, 030231 tropical medicine, Molecular Sequence Data, Sensation, MESH: Wolbachia/physiology, MESH: Molecular Sequence Annotation, Article, MESH: Sensation/genetics, 03 medical and health sciences, medicine, MESH: Blood, MESH: Microbiota, Animals, MESH: Reproduction/genetics, Symbiosis, Gene, 030304 developmental biology, Whole genome sequencing, MESH: Insect Vectors/parasitology, MESH: Molecular Sequence Data, MESH: Insect Proteins/genetics, MESH: Salivary Glands/parasitology, Tsetse fly, Molecular Sequence Annotation, Feeding Behavior, Sequence Analysis, DNA, biology.organism_classification, medicine.disease, Insect Vectors, Trypanosomiasis, African, Vector (epidemiology), MESH: Tsetse Flies/physiology, MESH: Wolbachia/genetics, Trypanosomiasis, MESH: Female
Abstract

Africa's Bane Tsetse are blood-feeding, fast-flying flies that transmit a range of Trypanosoma spp. protozoan pathogens, which cause sleeping sickness in humans and their nagana in their livestock. The International Glossina Genome Initiative (p. 380 ) sequenced the genome of Glossina morsitans and identified the genes for many attributes of the tsetse's remarkable biology, including viviparity and the expression of analogs of mammalian milk proteins. Tsetse are host to several specific symbionts that appear to synthesize essential nutrients for the fly and also to hitherto undiscovered parasitoid-derived viruses. Deeper exploration of this genome will reveal what makes these fly species so host- and trypanosome specific.

Published
2014
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