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

Authors :
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]
Apollo - University of Cambridge Repository
Source :
CONICET Digital (CONICET), Consejo Nacional de Investigaciones Científicas y Técnicas, instacron:CONICET, Genome biology, vol. 20, no. 1, pp. 64, Genome biology, vol 20, iss 1, SEDICI (UNLP), Universidad Nacional de La Plata, instacron:UNLP, Genome Biology, Genome Biology, BioMed Central, 2019, 20 (1), pp.64. ⟨10.1186/s13059-019-1660-0⟩, Genome Biology, Vol 20, Iss 1, Pp 1-26 (2019), Genome Biology 1 (20), 26 p.. (2019), Genome Biology, 2019, 20 (1), pp.64. ⟨10.1186/s13059-019-1660-0⟩, Genome Biology, Vol. 20, No 1 (2019) P. 64, Genome Biology, 20, 64. BMC
Publication Year :
2019
Publisher :
BioMed Central, 2019.

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.<br />La lista completa de autores puede verse en el archivo asociado.<br />Facultad de Ciencias Exactas<br />Centro Regional de Estudios Genómicos

Subjects

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

Details

Language :
English
ISSN :
14656906, 1474760X, and 14747596
Database :
OpenAIRE
Journal :
CONICET Digital (CONICET), Consejo Nacional de Investigaciones Científicas y Técnicas, instacron:CONICET, Genome biology, vol. 20, no. 1, pp. 64, Genome biology, vol 20, iss 1, SEDICI (UNLP), Universidad Nacional de La Plata, instacron:UNLP, Genome Biology, Genome Biology, BioMed Central, 2019, 20 (1), pp.64. ⟨10.1186/s13059-019-1660-0⟩, Genome Biology, Vol 20, Iss 1, Pp 1-26 (2019), Genome Biology 1 (20), 26 p.. (2019), Genome Biology, 2019, 20 (1), pp.64. ⟨10.1186/s13059-019-1660-0⟩, Genome Biology, Vol. 20, No 1 (2019) P. 64, Genome Biology, 20, 64. BMC
Accession number :
edsair.doi.dedup.....e2d4b6dffa7d518988ee5b66386abf7d