Evidence map›Paper›PMID 30935422›Full record

ArticleGenome biology2019

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

Kristen A Panfilio, Iris M Vargas Jentzsch, Joshua B Benoit, Deniz Erezyilmaz, Yuichiro Suzuki, Stefano Colella, Hugh M Robertson, Monica F Poelchau, Robert M Waterhouse, Panagiotis Ioannidis and 73 more

Abstract read
In one paragraph

Article in Genome biology, 2019. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 71 papers.

0numbers the graph read from it
0cells of the map it votes in
71citing papers in PubMed
–field-weighted citation impact
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

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3 · Its place in the literature

Who cites it

71 citing papers in PubMed.

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11 more citing papers are in PubMed but not listed here.

4 · The record

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5 · Who and what money

Authors and funding

83 authors.

Kristen A PanfilioInstitute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674, Cologne, Germany. kristen.panfilio@alum.swarthmore.edu.ORCID 0000-0002-6417-251X
Iris M Vargas JentzschInstitute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674, Cologne, Germany.ORCID 0000-0003-4527-1560
Joshua B BenoitDepartment of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA.ORCID 0000-0002-4018-3513
Deniz ErezyilmazDepartment of Biochemistry and Cell Biology and Center for Developmental Genetics, Stony Brook University, Stony Brook, NY, 11794, USA.ORCID 0000-0001-8416-8561
Yuichiro SuzukiDepartment of Biological Sciences, Wellesley College, 106 Central St., Wellesley, MA, 02481, USA.ORCID 0000-0002-0957-3564
Stefano ColellaUniv Lyon, INSA-Lyon, INRA, BF2I, UMR0203, F-69621, Villeurbanne, France.ORCID 0000-0003-3139-6055
Hugh M RobertsonDepartment of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA.
Monica F PoelchauNational Agricultural Library, Beltsville, MD, 20705, USA.ORCID 0000-0002-4584-6056
Robert M WaterhouseDepartment of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva, 1211, Geneva, Switzerland.ORCID 0000-0003-4199-9052
Panagiotis IoannidisDepartment of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva, 1211, Geneva, Switzerland.ORCID 0000-0003-0939-6745
Matthew T WeirauchCenter for Autoimmune Genomics and Etiology, Division of Biomedical Informatics, and Division of Developmental Biology, Cincinnati Children's Hospital Medical Center, Department of Pediatrics, College of Medicine, University of Cincinnati, Cincinnati, OH, 45229, USA.ORCID 0000-0001-7977-9122
Daniel S T HughesHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Shwetha C MuraliHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
John H WerrenDepartment of Biology, University of Rochester, Rochester, NY, 14627, USA.ORCID 0000-0001-9353-2070
Chris G C JacobsInstitute of Biology, Leiden University, Sylviusweg 72, 2333 BE, Leiden, Netherlands.ORCID 0000-0002-3128-2288
Elizabeth J DuncanDepartment of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin, 9054, New Zealand.ORCID 0000-0002-1841-504X
David ArmisénInstitut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon, 46 Allée d'Italie, 69364, Lyon, France.
Barbara M I VreedeDepartment of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Givat Ram, 91904, Jerusalem, Israel.ORCID 0000-0002-5023-4601
Patrice Baa-PuyouletUniv Lyon, INSA-Lyon, INRA, BF2I, UMR0203, F-69621, Villeurbanne, France.
Chloé S BergerInstitut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon, 46 Allée d'Italie, 69364, Lyon, France.
Chun-Che ChangDepartment of Entomology/Institute of Biotechnology, College of Bioresources and Agriculture, National Taiwan University, Taipei, Taiwan.ORCID 0000-0002-3586-1607
Hsu ChaoHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Mei-Ju M ChenNational Agricultural Library, Beltsville, MD, 20705, USA.ORCID 0000-0001-7768-8905
Yen-Ta ChenInstitute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674, Cologne, Germany.ORCID 0000-0002-4570-6061
Christopher P ChildersNational Agricultural Library, Beltsville, MD, 20705, USA.ORCID 0000-0002-1253-5550
Ariel D ChipmanDepartment of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Givat Ram, 91904, Jerusalem, Israel.ORCID 0000-0001-6696-840X
Andrew G CridgeDepartment of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin, 9054, New Zealand.ORCID 0000-0002-1399-5188
Antonin J J CrumièreInstitut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon, 46 Allée d'Italie, 69364, Lyon, France.ORCID 0000-0003-2214-2993
Peter K DeardenDepartment of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin, 9054, New Zealand.ORCID 0000-0001-7790-9675
Elise M DidionDepartment of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA.ORCID 0000-0002-4987-8901
Huyen DinhHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.ORCID 0000-0003-0336-0362
Harsha Vardhan DoddapaneniHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.ORCID 0000-0002-2433-633X
Amanda DolanDepartment of Biology, University of Rochester, Rochester, NY, 14627, USA.
Shannon DuganHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.ORCID 0000-0003-1482-816X
Cassandra G ExtavourDepartment of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138, USA.ORCID 0000-0003-2922-5855
Gérard FebvayUniv Lyon, INSA-Lyon, INRA, BF2I, UMR0203, F-69621, Villeurbanne, France.ORCID 0000-0002-0654-2340
Markus FriedrichDepartment of Biological Sciences, Wayne State University, Detroit, MI, 48202, USA.ORCID 0000-0002-5622-7920
Neta GinzburgDepartment of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Givat Ram, 91904, Jerusalem, Israel.
Yi HanHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.ORCID 0000-0001-7605-8979
Peter HegerInstitute for Genetics, University of Cologne, Zülpicher Straße 47a, 50674, Cologne, Germany.
Christopher J HolmesDepartment of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA.ORCID 0000-0001-9612-366X
Thorsten HornInstitute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674, Cologne, Germany.ORCID 0000-0001-8181-939X
Yi-Min HsiaoDepartment of Entomology/Institute of Biotechnology, College of Bioresources and Agriculture, National Taiwan University, Taipei, Taiwan.ORCID 0000-0002-1817-0302
Emily C JenningsDepartment of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA.ORCID 0000-0002-7687-5319
J Spencer JohnstonDepartment of Entomology, Texas A&M University, College Station, TX, 77843, USA.ORCID 0000-0003-4792-2945
Tamsin E JonesDepartment of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138, USA.ORCID 0000-0002-0027-0858
Jeffery W JonesDepartment of Biological Sciences, Wayne State University, Detroit, MI, 48202, USA.
Abderrahman KhilaInstitut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon, 46 Allée d'Italie, 69364, Lyon, France.ORCID 0000-0003-0908-483X
Stefan KoelzerInstitute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674, Cologne, Germany.
Viera KovacovaCECAD, University of Cologne, Cologne, Germany.ORCID 0000-0003-4581-4254
Megan LeaskDepartment of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin, 9054, New Zealand.
Sandra L LeeHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Chien-Yueh LeeNational Agricultural Library, Beltsville, MD, 20705, USA.ORCID 0000-0002-4304-974X
Mackenzie R LovegroveDepartment of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin, 9054, New Zealand.
Hsiao-Ling LuDepartment of Entomology/Institute of Biotechnology, College of Bioresources and Agriculture, National Taiwan University, Taipei, Taiwan.ORCID 0000-0002-4029-6470
Yong LuDepartment of Entomology and Program in Molecular & Cell Biology, University of Maryland, College Park, MD, 20742, USA.
Patricia J MooreDepartment of Entomology, University of Georgia, 120 Cedar St., Athens, GA, 30602, USA.ORCID 0000-0001-9802-7217
Monica C Munoz-TorresEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.ORCID 0000-0001-8430-6039
Donna M MuznyHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.ORCID 0000-0002-3055-0359
Subba R PalliDepartment of Entomology, College of Agriculture, Food and Environment, University of Kentucky, Lexington, KY, 40546, USA.ORCID 0000-0002-0873-3247
Nicolas ParisotUniv Lyon, INSA-Lyon, INRA, BF2I, UMR0203, F-69621, Villeurbanne, France.ORCID 0000-0001-5217-8415
Leslie PickDepartment of Entomology and Program in Molecular & Cell Biology, University of Maryland, College Park, MD, 20742, USA.ORCID 0000-0002-4505-5107
Megan L PorterDepartment of Biology, University of Hawai'i at Mānoa, Honolulu, HI, 96822, USA.ORCID 0000-0001-7985-2887
Jiaxin QuHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.ORCID 0000-0002-1122-9391
Peter N RefkiInstitut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon, 46 Allée d'Italie, 69364, Lyon, France.
Rose RichterDepartment of Biology, University of Rochester, Rochester, NY, 14627, USA.
Rolando Rivera-PomarCentro de Bioinvestigaciones, Universidad Nacional del Noroeste de Buenos Aires, Pergamino, Argentina.ORCID 0000-0002-7720-7064
Andrew J RosendaleDepartment of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA.ORCID 0000-0002-2463-8856
Siegfried RothInstitute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674, Cologne, Germany.ORCID 0000-0001-5772-3558
Lena SachsInstitute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674, Cologne, Germany.
M Emília SantosInstitut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon, 46 Allée d'Italie, 69364, Lyon, France.
Jan SeibertInstitute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674, Cologne, Germany.
Essia SghaierInstitut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon, 46 Allée d'Italie, 69364, Lyon, France.
Jayendra N ShuklaDepartment of Entomology, College of Agriculture, Food and Environment, University of Kentucky, Lexington, KY, 40546, USA.ORCID 0000-0003-1589-1929
Richard J StancliffeArgelander-Institut für Astronomie, Universität Bonn, Auf dem Hügel 71, 53121, Bonn, Germany.ORCID 0000-0002-6972-9655
Olivia TidswellDepartment of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin, 9054, New Zealand.
Lucila TraversoCentro Regional de Estudios Genómicos, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, La Plata, Argentina.
Maurijn van der ZeeInstitute of Biology, Leiden University, Sylviusweg 72, 2333 BE, Leiden, Netherlands.ORCID 0000-0002-8728-8646
Séverine VialaInstitut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon, 46 Allée d'Italie, 69364, Lyon, France.
Kim C WorleyHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.ORCID 0000-0002-0282-1000
Evgeny M ZdobnovDepartment of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva, 1211, Geneva, Switzerland.
Richard A GibbsHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Stephen RichardsHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.ORCID 0000-0001-8959-5466

Funding

The Human Genome Sequencing CenterU54HG003273 · NHGRI · BAYLOR COLLEGE OF MEDICINE · PI GIBBS, RICHARD A · 2004 to 2015
$341.3M
Web-based visualization of coronavirus genomes and proteinsR01HG004483 · NHGRI · UNIVERSITY OF CALIFORNIA BERKELEY · PI Ian H Holmes · 2007 to 2026
$9.3M
Novel Web-based Tools for Collaborative Community-Driven Genome Feature AnnotatioR01GM080203 · NIGMS · UNIVERSITY OF CALIFORNIA BERKELEY · PI Ian H Holmes · 2007 to 2026
$8.5M
Functional evolution of segmentation gene regulatory networks in insectsR01GM113230 · NIGMS · UNIV OF MARYLAND, COLLEGE PARK · PI Leslie Pick · 2015 to 2026
$3.7M
NHGRI NIH HHS R01 HG004483NHGRI NIH HHS U54 HG003273NIGMS NIH HHS R01 GM080203NIGMS NIH HHS R01 GM113230
6 · The paper itself

Abstract

backgroundThe 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.

resultsThe 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.

conclusionsWith 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.

Indexed as

Evolution, MolecularGenome, InsectAmino Acid SequenceAnimalsCYS2-HIS2 Zinc FingersFeeding BehaviorGene DosageGene Expression ProfilingGenes, HomeoboxGene Transfer, HorizontalHemipteraPigmentationSmellTranscription FactorsTranscription FactorsEvolution of developmentGene family evolutionGene structureLateral gene transferPhytophagyRNAiTranscription factors

Identifiers

PMID30935422
PMCPMC6444547

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