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

被引：71

作者：

Panfilio, Kristen A. ^{[1
,2
]}

Jentzsch, Iris M. Vargas ^{[1
]}

Benoit, Joshua B. ^{[3
]}

Erezyilmaz, Deniz ^{[4
,5
,47
,48
]}

Suzuki, Yuichiro ^{[6
]}

Colella, Stefano ^{[7
,8
]}

Robertson, Hugh M. ^{[9
]}

Poelchau, Monica F. ^{[10
]}

Waterhouse, Robert M. ^{[11
,12
,13
]}

Ioannidis, Panagiotis ^{[11
,12
]}

Weirauch, Matthew T. ^{[14
,15
]}

Hughes, Daniel S. T. ^{[16
]}

Murali, Shwetha C. ^{[16
,17
,18
]}

Werren, John H. ^{[19
]}

Jacobs, Chris G. C. ^{[20
,21
]}

Duncan, Elizabeth J. ^{[22
,23
]}

Armisen, David ^{[24
]}

Vreede, Barbara M. I. ^{[25
]}

Baa-Puyoulet, Patrice ^{[7
]}

Berger, Chloe S. ^{[24
]}

Chang, Chun-che ^{[26
,50
]}

Chao, Hsu ^{[16
]}

Chen, Mei-Ju M. ^{[10
]}

Chen, Yen-Ta ^{[1
]}

Childers, Christopher P. ^{[10
]}

Chipman, Ariel D. ^{[25
]}

Cridge, Andrew G. ^{[22
]}

Crumiere, Antonin J. J. ^{[24
]}

Dearden, Peter K. ^{[22
]}

Didion, Elise M. ^{[3
]}

Huyen Dinh ^{[16
]}

Doddapaneni, Harsha Vardhan ^{[16
]}

Dolan, Amanda ^{[19
,27
]}

Dugan, Shannon ^{[16
]}

Extavour, Cassandra G. ^{[28
,29
]}

Febvay, Gerard ^{[7
]}

Friedrich, Markus ^{[30
]}

Ginzburg, Neta ^{[25
]}

Han, Yi ^{[16
]}

Heger, Peter ^{[31
]}

Holmes, Christopher J. ^{[3
]}

Horn, Thorsten ^{[1
]}

Hsiao, Yi-min ^{[26
,50
]}

Jennings, Emily C. ^{[3
]}

Johnston, J. Spencer ^{[32
]}

Jones, Tamsin E. ^{[28
]}

Jones, Jeffery W. ^{[30
]}

Khila, Abderrahman ^{[24
]}

Koelzer, Stefan ^{[1
]}

Kovacova, Viera ^{[33
]}

机构：

[1] Univ Cologne, Inst Zool Dev Biol, Zulpicher Str 47b, D-50674 Cologne, Germany

[2] Univ Warwick, Sch Life Sci, Gibbet Hill Campus, Coventry CV4 7AL, W Midlands, England

[3] Univ Cincinnati, Dept Biol Sci, Cincinnati, OH 45221 USA

[4] SUNY Stony Brook, Dept Biochem & Cell Biol, Stony Brook, NY 11794 USA

[5] SUNY Stony Brook, Ctr Dev Genet, Stony Brook, NY 11794 USA

[6] Wellesley Coll, Dept Biol Sci, 106 Cent St, Wellesley, MA 02481 USA

[7] Univ Lyon, INSA Lyon, INRA, BF2I,UMR0203, F-69621 Villeurbanne, France

[8] Univ Montpellier, SupAgro, INRA, LSTM,IRD,CIRAD, Montpellier, France

[9] Univ Illinois, Dept Entomol, Urbana, IL 61801 USA

[10] Natl Agr Lib, Beltsville, MD 20705 USA

[11] Univ Geneva, Dept Genet Med & Dev, CH-1211 Geneva, Switzerland

[12] Univ Geneva, Swiss Inst Bioinformat, CH-1211 Geneva, Switzerland

[13] Univ Lausanne, Dept Ecol & Evolut, CH-1015 Lausanne, Switzerland

[14] Univ Cincinnati, Coll Med, Ctr Autoimmune Genom & Etiol, Div Biomed Informat, Cincinnati, OH 45229 USA

[15] Univ Cincinnati, Coll Med, Cincinnati Childrens Hosp, Dept Pediat,Med Ctr,Div Dev Biol, Cincinnati, OH 45229 USA

[16] Baylor Coll Med, Dept Human & Mol Genet, Human Genome Sequencing Ctr, One Baylor Plaza, Houston, TX 77030 USA

[17] Univ Washington, Sch Med, Dept Genome Sci, Seattle, WA 98195 USA

[18] Univ Washington, Howard Hughes Med Inst, Seattle, WA 98195 USA

[19] Univ Rochester, Dept Biol, Rochester, NY 14627 USA

[20] Leiden Univ, Inst Biol, Sylviusweg 72, NL-2333 BE Leiden, Netherlands

[21] Max Planck Inst Chem Ecol, Hans Knoll Str 8, D-07745 Jena, Germany

[22] Univ Otago, Dept Biochem & Genom Aotearoa, Dunedin 9054, New Zealand

[23] Univ Leeds, Fac Biol Sci, Sch Biol, Leeds LS2 9JT, W Yorkshire, England

[24] Univ Claude Bernard Lyon 1, Univ Lyon, Inst Genom Fonct Lyon, CNRS,UMR 5242,Ecole Normale Super Lyon, 46 Allee Italie, F-69364 Lyon, France

[25] Hebrew Univ Jerusalem, Alexander Silberman Inst Sci, Dept Ecol Evolut & Behav, Edmond J Safra Campus, IL-91904 Jerusalem, Israel

[26] Natl Taiwan Univ, Dept Entomol, Inst Biotechnol, Coll Bioresources & Agr, Taipei, Taiwan

[27] Rochester Inst Technol, Sch Life Sci, Rochester, NY 14623 USA

[28] Harvard Univ, Dept Organism & Evolutionary Biol, 26 Oxford St, Cambridge, MA 02138 USA

[29] Harvard Univ, Dept Mol & Cellular Biol, 26 Oxford St, Cambridge, MA 02138 USA

[30] Wayne State Univ, Dept Biol Sci, Detroit, MI 48202 USA

[31] Univ Cologne, Inst Genet, Zulpicher Str 47a, D-50674 Cologne, Germany

[32] Texas A&M Univ, Dept Entomol, College Stn, TX 77843 USA

[33] Univ Cologne, CECAD, Cologne, Germany

[34] Univ Maryland, Dept Entomol, College Pk, MD 20742 USA

[35] Univ Maryland, Program Mol & Cell Biol, College Pk, MD 20742 USA

[36] Univ Georgia, Dept Entomol, 120 Cedar St, Athens, GA 30602 USA

[37] Lawrence Berkeley Natl Lab, Environm Genom & Syst Biol Div, Berkeley, CA USA

[38] Univ Kentucky, Coll Agr Food & Environm, Dept Entomol, Lexington, KY 40546 USA

[39] Univ Hawaii Manoa, Dept Biol, Honolulu, HI 96822 USA

[40] Max Planck Inst Evolutionsbiol, Dept Evolutionary Genet, August Thienemann Str 2, D-24306 Plon, Germany

[41] Earthworks Inst, 185 Caroline St, Rochester, NY 14620 USA

[42] Univ Nacl Noroeste Buenos Aires, Ctr Bioinvest, Pergamino, Argentina

[43] Cent Univ Rajasthan CURAJ, Dept Biotechnol, NH-8, Ajmer, India

[44] Univ Bonn, Argelander Inst Astron, Hugel 71, D-53121 Bonn, Germany

[45] Univ Cambridge, Dept Zool, Cambridge CB2 3DT, England

[46] Univ Nacl La Plata, Fac Ciencias Exactas, Ctr Reg Estudios, La Plata, Buenos Aires, Argentina

[47] Univ Oxford, Dept Physiol Anat & Genet, Oxford OX1 3SR, England

[48] Univ Oxford, Ctr Neural Circuits & Behav, Oxford OX1 3SR, England

[49] Univ Hull, Dept Math & Phys, EA Milne Ctr Astrophys, Kingston Upon Hull HU6 7RX, N Humberside, England

[50] Natl Taiwan Univ, Res Ctr Dev Biol & Regenerat Med, Taipei, Taiwan

来源：

GENOME BIOLOGY | 2019年 / 20卷 / 1期

基金：

美国国家科学基金会; 瑞士国家科学基金会; 欧洲研究理事会; 美国国家卫生研究院;

关键词：

Phytophagy; Transcription factors; Gene structure; Lateral gene transfer; RNAi; Gene family evolution; Evolution of development; DE-NOVO IDENTIFICATION; ONCOPELTUS-FASCIATUS; PEA APHID; DROSOPHILA-MELANOGASTER; ACYRTHOSIPHON-PISUM; ADAPTIVE EVOLUTION; INSECT; GENE; FAMILY; INSIGHTS;

D O I：

10.1186/s13059-019-1660-0

中图分类号：

Q81 [生物工程学（生物技术）]; Q93 [微生物学];

学科分类号：

071005 ; 0836 ; 090102 ; 100705 ;

摘要：

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.

引用

页数：26

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