Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome
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 b...
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Format: | Article |
Language: | English |
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BMC
2019-04-01
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Series: | Genome Biology |
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Online Access: | http://link.springer.com/article/10.1186/s13059-019-1660-0 |
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English |
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author |
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 Matthew T. Weirauch Daniel S. T. Hughes Shwetha C. Murali John H. Werren Chris G. C. Jacobs Elizabeth J. Duncan David Armisén Barbara M. I. Vreede Patrice Baa-Puyoulet Chloé S. Berger Chun-che Chang Hsu Chao Mei-Ju M. Chen Yen-Ta Chen Christopher P. Childers Ariel D. Chipman Andrew G. Cridge Antonin J. J. Crumière Peter K. Dearden Elise M. Didion Huyen Dinh Harsha Vardhan Doddapaneni Amanda Dolan Shannon Dugan Cassandra G. Extavour Gérard Febvay Markus Friedrich Neta Ginzburg Yi Han Peter Heger Christopher J. Holmes Thorsten Horn Yi-min Hsiao Emily C. Jennings J. Spencer Johnston Tamsin E. Jones Jeffery W. Jones Abderrahman Khila Stefan Koelzer Viera Kovacova Megan Leask Sandra L. Lee Chien-Yueh Lee Mackenzie R. Lovegrove Hsiao-ling Lu Yong Lu Patricia J. Moore Monica C. Munoz-Torres Donna M. Muzny Subba R. Palli Nicolas Parisot Leslie Pick Megan L. Porter Jiaxin Qu Peter N. Refki Rose Richter Rolando Rivera-Pomar Andrew J. Rosendale Siegfried Roth Lena Sachs M. Emília Santos Jan Seibert Essia Sghaier Jayendra N. Shukla Richard J. Stancliffe Olivia Tidswell Lucila Traverso Maurijn van der Zee Séverine Viala Kim C. Worley Evgeny M. Zdobnov Richard A. Gibbs Stephen Richards |
spellingShingle |
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 Matthew T. Weirauch Daniel S. T. Hughes Shwetha C. Murali John H. Werren Chris G. C. Jacobs Elizabeth J. Duncan David Armisén Barbara M. I. Vreede Patrice Baa-Puyoulet Chloé S. Berger Chun-che Chang Hsu Chao Mei-Ju M. Chen Yen-Ta Chen Christopher P. Childers Ariel D. Chipman Andrew G. Cridge Antonin J. J. Crumière Peter K. Dearden Elise M. Didion Huyen Dinh Harsha Vardhan Doddapaneni Amanda Dolan Shannon Dugan Cassandra G. Extavour Gérard Febvay Markus Friedrich Neta Ginzburg Yi Han Peter Heger Christopher J. Holmes Thorsten Horn Yi-min Hsiao Emily C. Jennings J. Spencer Johnston Tamsin E. Jones Jeffery W. Jones Abderrahman Khila Stefan Koelzer Viera Kovacova Megan Leask Sandra L. Lee Chien-Yueh Lee Mackenzie R. Lovegrove Hsiao-ling Lu Yong Lu Patricia J. Moore Monica C. Munoz-Torres Donna M. Muzny Subba R. Palli Nicolas Parisot Leslie Pick Megan L. Porter Jiaxin Qu Peter N. Refki Rose Richter Rolando Rivera-Pomar Andrew J. Rosendale Siegfried Roth Lena Sachs M. Emília Santos Jan Seibert Essia Sghaier Jayendra N. Shukla Richard J. Stancliffe Olivia Tidswell Lucila Traverso Maurijn van der Zee Séverine Viala Kim C. Worley Evgeny M. Zdobnov Richard A. Gibbs Stephen Richards Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome Genome Biology Phytophagy Transcription factors Gene structure Lateral gene transfer RNAi Gene family evolution |
author_facet |
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 Matthew T. Weirauch Daniel S. T. Hughes Shwetha C. Murali John H. Werren Chris G. C. Jacobs Elizabeth J. Duncan David Armisén Barbara M. I. Vreede Patrice Baa-Puyoulet Chloé S. Berger Chun-che Chang Hsu Chao Mei-Ju M. Chen Yen-Ta Chen Christopher P. Childers Ariel D. Chipman Andrew G. Cridge Antonin J. J. Crumière Peter K. Dearden Elise M. Didion Huyen Dinh Harsha Vardhan Doddapaneni Amanda Dolan Shannon Dugan Cassandra G. Extavour Gérard Febvay Markus Friedrich Neta Ginzburg Yi Han Peter Heger Christopher J. Holmes Thorsten Horn Yi-min Hsiao Emily C. Jennings J. Spencer Johnston Tamsin E. Jones Jeffery W. Jones Abderrahman Khila Stefan Koelzer Viera Kovacova Megan Leask Sandra L. Lee Chien-Yueh Lee Mackenzie R. Lovegrove Hsiao-ling Lu Yong Lu Patricia J. Moore Monica C. Munoz-Torres Donna M. Muzny Subba R. Palli Nicolas Parisot Leslie Pick Megan L. Porter Jiaxin Qu Peter N. Refki Rose Richter Rolando Rivera-Pomar Andrew J. Rosendale Siegfried Roth Lena Sachs M. Emília Santos Jan Seibert Essia Sghaier Jayendra N. Shukla Richard J. Stancliffe Olivia Tidswell Lucila Traverso Maurijn van der Zee Séverine Viala Kim C. Worley Evgeny M. Zdobnov Richard A. Gibbs Stephen Richards |
author_sort |
Kristen A. Panfilio |
title |
Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome |
title_short |
Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome |
title_full |
Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome |
title_fullStr |
Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome |
title_full_unstemmed |
Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome |
title_sort |
molecular evolutionary trends and feeding ecology diversification in the hemiptera, anchored by the milkweed bug genome |
publisher |
BMC |
series |
Genome Biology |
issn |
1474-760X |
publishDate |
2019-04-01 |
description |
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. |
topic |
Phytophagy Transcription factors Gene structure Lateral gene transfer RNAi Gene family evolution |
url |
http://link.springer.com/article/10.1186/s13059-019-1660-0 |
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doaj-2e808ce5942240759a02b40723087a762020-11-25T01:31:37ZengBMCGenome Biology1474-760X2019-04-0120112610.1186/s13059-019-1660-0Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genomeKristen A. Panfilio0Iris M. Vargas Jentzsch1Joshua B. Benoit2Deniz Erezyilmaz3Yuichiro Suzuki4Stefano Colella5Hugh M. Robertson6Monica F. Poelchau7Robert M. Waterhouse8Panagiotis Ioannidis9Matthew T. Weirauch10Daniel S. T. Hughes11Shwetha C. Murali12John H. Werren13Chris G. C. Jacobs14Elizabeth J. Duncan15David Armisén16Barbara M. I. Vreede17Patrice Baa-Puyoulet18Chloé S. Berger19Chun-che Chang20Hsu Chao21Mei-Ju M. Chen22Yen-Ta Chen23Christopher P. Childers24Ariel D. Chipman25Andrew G. Cridge26Antonin J. J. Crumière27Peter K. Dearden28Elise M. Didion29Huyen Dinh30Harsha Vardhan Doddapaneni31Amanda Dolan32Shannon Dugan33Cassandra G. Extavour34Gérard Febvay35Markus Friedrich36Neta Ginzburg37Yi Han38Peter Heger39Christopher J. Holmes40Thorsten Horn41Yi-min Hsiao42Emily C. Jennings43J. Spencer Johnston44Tamsin E. Jones45Jeffery W. Jones46Abderrahman Khila47Stefan Koelzer48Viera Kovacova49Megan Leask50Sandra L. Lee51Chien-Yueh Lee52Mackenzie R. Lovegrove53Hsiao-ling Lu54Yong Lu55Patricia J. Moore56Monica C. Munoz-Torres57Donna M. Muzny58Subba R. Palli59Nicolas Parisot60Leslie Pick61Megan L. Porter62Jiaxin Qu63Peter N. Refki64Rose Richter65Rolando Rivera-Pomar66Andrew J. Rosendale67Siegfried Roth68Lena Sachs69M. Emília Santos70Jan Seibert71Essia Sghaier72Jayendra N. Shukla73Richard J. Stancliffe74Olivia Tidswell75Lucila Traverso76Maurijn van der Zee77Séverine Viala78Kim C. Worley79Evgeny M. Zdobnov80Richard A. Gibbs81Stephen Richards82Institute for Zoology: Developmental Biology, University of CologneInstitute for Zoology: Developmental Biology, University of CologneDepartment of Biological Sciences, University of CincinnatiDepartment of Biochemistry and Cell Biology and Center for Developmental Genetics, Stony Brook UniversityDepartment of Biological Sciences, Wellesley CollegeUniv Lyon, INSA-Lyon, INRA, BF2I, UMR0203Department of Entomology, University of Illinois at Urbana-ChampaignNational Agricultural LibraryDepartment of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of GenevaDepartment of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of GenevaCenter 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 CincinnatiHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of MedicineHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of MedicineDepartment of Biology, University of RochesterInstitute of Biology, Leiden UniversityDepartment of Biochemistry and Genomics Aotearoa, University of OtagoInstitut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de LyonDepartment of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of JerusalemUniv Lyon, INSA-Lyon, INRA, BF2I, UMR0203Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de LyonDepartment of Entomology/Institute of Biotechnology, College of Bioresources and Agriculture, National Taiwan UniversityHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of MedicineNational Agricultural LibraryInstitute for Zoology: Developmental Biology, University of CologneNational Agricultural LibraryDepartment of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of JerusalemDepartment of Biochemistry and Genomics Aotearoa, University of OtagoInstitut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de LyonDepartment of Biochemistry and Genomics Aotearoa, University of OtagoDepartment of Biological Sciences, University of CincinnatiHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of MedicineHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of MedicineDepartment of Biology, University of RochesterHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of MedicineDepartment of Organismic and Evolutionary Biology, Harvard UniversityUniv Lyon, INSA-Lyon, INRA, BF2I, UMR0203Department of Biological Sciences, Wayne State UniversityDepartment of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of JerusalemHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of MedicineInstitute for Genetics, University of CologneDepartment of Biological Sciences, University of CincinnatiInstitute for Zoology: Developmental Biology, University of CologneDepartment of Entomology/Institute of Biotechnology, College of Bioresources and Agriculture, National Taiwan UniversityDepartment of Biological Sciences, University of CincinnatiDepartment of Entomology, Texas A&M UniversityDepartment of Organismic and Evolutionary Biology, Harvard UniversityDepartment of Biological Sciences, Wayne State UniversityInstitut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de LyonInstitute for Zoology: Developmental Biology, University of CologneCECAD, University of CologneDepartment of Biochemistry and Genomics Aotearoa, University of OtagoHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of MedicineNational Agricultural LibraryDepartment of Biochemistry and Genomics Aotearoa, University of OtagoDepartment of Entomology/Institute of Biotechnology, College of Bioresources and Agriculture, National Taiwan UniversityDepartment of Entomology and Program in Molecular & Cell Biology, University of MarylandDepartment of Entomology, University of GeorgiaEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National LaboratoryHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of MedicineDepartment of Entomology, College of Agriculture, Food and Environment, University of KentuckyUniv Lyon, INSA-Lyon, INRA, BF2I, UMR0203Department of Entomology and Program in Molecular & Cell Biology, University of MarylandDepartment of Biology, University of Hawai’i at MānoaHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of MedicineInstitut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de LyonDepartment of Biology, University of RochesterCentro de Bioinvestigaciones, Universidad Nacional del Noroeste de Buenos AiresDepartment of Biological Sciences, University of CincinnatiInstitute for Zoology: Developmental Biology, University of CologneInstitute for Zoology: Developmental Biology, University of CologneInstitut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de LyonInstitute for Zoology: Developmental Biology, University of CologneInstitut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de LyonDepartment of Entomology, College of Agriculture, Food and Environment, University of KentuckyArgelander-Institut für Astronomie, Universität BonnDepartment of Biochemistry and Genomics Aotearoa, University of OtagoCentro Regional de Estudios Genómicos, Facultad de Ciencias Exactas, Universidad Nacional de La PlataInstitute of Biology, Leiden UniversityInstitut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de LyonHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of MedicineDepartment of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of GenevaHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of MedicineHuman Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of MedicineAbstract 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.http://link.springer.com/article/10.1186/s13059-019-1660-0PhytophagyTranscription factorsGene structureLateral gene transferRNAiGene family evolution |