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

Panfilio, Kristen A.; Vargas Jentzsch, Iris M.; Benoit, Joshua B.; Erezyilmaz, Deniz; Suzuki, Yuichiro; Colella, Stefano; Robertson, Hugh M.; Poelchau, Monica F.; Waterhouse, Robert M.; Ioannidis, Panagiotis; Weirauch, Matthew T.; Hughes, Daniel S. T.; Murali, Shwetha C.; Werren, John H.; Jacobs, Chris G. C.; Duncan, Elizabeth J.; Armisén, David; Vreede, Barbara M. I.; Baa-Puyoulet, Patrice; Berger, Chloé S.; Chang, Chun-che; Chao, Hsu; Chen, Mei-Ju M.; Chen, Yen-Ta; Childers, Christopher P.; Chipman, Ariel D.; Cridge, Andrew G.; Crumière, Antonin J. J.; Dearden, Peter K.; Didion, Elise M.; Dinh, Huyen; Doddapaneni, Harsha Vardhan; Dolan, Amanda; Dugan, Shannon; Extavour, Cassandra G.; Febvay, Gérard; Friedrich, Markus; Ginzburg, Neta; Han, Yi; Heger, Peter; Holmes, Christopher J.; Horn, Thorsten; Hsiao, Yi-min; Jennings, Emily C.; Johnston, J. Spencer; Jones, Tamsin E.; Jones, Jeffery W.; Khila, Abderrahman; Koelzer, Stefan; Kovacova, Viera; Leask, Megan; Lee, Sandra L.; Lee, Chien-Yueh; Lovegrove, Mackenzie R.; Lu, Hsiao-ling; Lu, Yong; Moore, Patricia J.; Munoz-Torres, Monica C.; Muzny, Donna M.; Palli, Subba R.; Parisot, Nicolas; Pick, Leslie; Porter, Megan L.; Qu, Jiaxin; Refki, Peter N.; Richter, Rose; Rivera-Pomar, Rolando; Rosendale, Andrew J.; Roth, Siegfried; Sachs, Lena; Santos, M. Emília; Seibert, Jan; Sghaier, Essia; Shukla, Jayendra N.; Stancliffe, Richard J.; Tidswell, Olivia; Traverso, Lucila; van der Zee, Maurijn; Viala, Séverine; Worley, Kim C.; Zdobnov, Evgeny M.; Gibbs, Richard A.; Richards, Stephen

doi:10.1186/s13059-019-1660-0

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

Journal Article · 02 April 2019 · Genome Biology (Online)

DOI: https://doi.org/10.1186/s13059-019-1660-0 · OSTI ID:1618997

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Univ. of Cologne (Germany); Univ. of Warwich, Coventry (United Kingdom)
Univ. of Cologne (Germany)
Univ. of Cincinnati, OH (United States)
Stony Brook Univ., NY (United States); Univ. of Oxford (United Kingdom)
Wellesley College, MA (United States)
Univ. Lyon, Villeurbanne (France); Univ. of Montpellier (France)
Univ. of Illinois at Urbana-Champaign, IL (United States)
National Agricultural Library, Beltsville, MD (United States)
Univ. of Geneva (Switzerland); Univ. of Lausanne (Switzerland)
Univ. of Geneva (Switzerland)
Baylor College of Medicine, Houston, TX (United States)
Baylor College of Medicine, Houston, TX (United States); Univ. of Washington, Seattle, WA (United States)
Univ. of Rochester, NY (United States)
Leiden Univ. (Netherlands); Max Planck Inst. for Chemical Ecology, Jena (Germany)
Univ. of Otago, Dunedin (New Zealand); Univ. of Leeds (United Kingdom)
Univ. of Lyon (France); Univ. Claude Bernard Lyon 1 (France); Ecole Normale Superieure de Lyon (France)
Univ. of Jerusalem (Israel)
Univ. Lyon, Villeurbanne (France)
National Taiwan Univ., Taipei (Taiwan)
Univ. of Otago, Dunedin (New Zealand)
Univ. of Rochester, NY (United States); Rochester Inst. of Technology, NY (United States)
Harvard Univ., Cambridge, MA (United States)
Wayne State Univ., Detroit, MI (United States)
Texas A & M Univ., College Station, TX (United States)
Univ. of Maryland, College Park, MD (United States)
Univ. of Georgia, Athens, GA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Univ. of Kentucky, Lexington, KY (United States)
Univ. of Hawaii at Manoa, Honolulu, HI (United States)
Univ. of Lyon (France); Univ. Claude Bernard Lyon 1 (France); Ecole Normale Superieure de Lyon (France); Max-Planck-Inst. für Evolutionsbiologie, Plon (Germany)
Univ. of Rochester, NY (United States); Earthworks Inst., Rochester, NY (United States)
Univ. Nacional del Noroeste de Buenos Aires, Pergamino (Argentina)
Univ. of Kentucky, Lexington, KY (United States); Centra Univ. of Rajasthan (CURAJ), Ajmer (India)
Univ. Bonn, (Germany); Univ. of Hull (United Kingdom)
Univ. of Otago, Dunedin (New Zealand); Univ. of Cambridge (United Kingdom)
Univ. Nacional de La Plata (Argentina)
Leiden Univ. (Netherlands)

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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); German Research Foundation (DFG); European Research Council (ERC); Swiss National Science Foundation (SNSF); National Science Foundation (NSF)

Grant/Contract Number:: AC02-05CH11231; U54 HG003273; PA 2044/1-1; 31003A_143936; PPOOP3_170664; ERC-CoG#616346; SFB 680; DEB1257053; R01GM113230; 5R01GM080203; 5R01HG004483

OSTI ID:: 1618997

Alternate ID(s):: OSTI ID: 1630609

Journal Information:: Genome Biology (Online), Vol. 20, Issue 1; ISSN 1474-760X

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 59 works

Citation information provided by
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Figures / Tables (13)

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
phytophagy
transcription factors
gene strucutre
lateral gene transfer
RNAi
gene family evolution
evolution of development

Additional file 1: of Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome Panfilio, Kristen; Jentzsch, Iris Vargas; Benoit, Joshua https://doi.org/10.6084/m9.figshare.7936430 The current record is supplemented by this text	text	January 2019
Additional file 2: of Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome Panfilio, Kristen; Jentzsch, Iris Vargas; Benoit, Joshua https://doi.org/10.6084/m9.figshare.7936448.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 2: of Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome Panfilio, Kristen; Jentzsch, Iris Vargas; Benoit, Joshua https://doi.org/10.6084/m9.figshare.7936448 The current record is supplemented by this dataset	dataset	January 2019
Additional file 3: of Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome Panfilio, Kristen; Jentzsch, Iris Vargas; Benoit, Joshua https://doi.org/10.6084/m9.figshare.7936460.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 3: of Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome Panfilio, Kristen; Jentzsch, Iris Vargas; Benoit, Joshua https://doi.org/10.6084/m9.figshare.7936460 The current record is supplemented by this dataset	dataset	January 2019
Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome Panfilio, Kristen; Jentzsch, Iris Vargas; Benoit, Joshua https://doi.org/10.6084/m9.figshare.c.4455548 The current record is supplemented by this collection	collection	January 2019
Additional file 1: of Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome Panfilio, Kristen; Jentzsch, Iris Vargas; Benoit, Joshua https://doi.org/10.6084/m9.figshare.7936430.v1 The current record is supplemented by this text	text	January 2019
Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome Panfilio, Kristen; Jentzsch, Iris Vargas; Benoit, Joshua https://doi.org/10.6084/m9.figshare.c.4455548.v1 The current record is supplemented by this collection	collection	January 2019