1. Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome
- Author
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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