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; 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

doi:10.1186/s13059-019-1660-0

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, 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. BergerChun 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

Research output: Contribution to journal › Article › peer-review

66 Scopus citations

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.

Original language	English
Article number	64
Journal	Genome Biology
Volume	20
Issue number	1
DOIs	https://doi.org/10.1186/s13059-019-1660-0
State	Published - Apr 2 2019

Bibliographical note

Publisher Copyright:
© 2019 The Author(s).

Funding

We also acknowledge funding for the project from German Research Foundation (DFG) grants PA 2044/1-1 and SFB 680 project A12 to KAP. Support for specific analyses was provided by the Swiss National Science Foundation with grant 31003A-143936 to EMZ and PP00P3-170664 to RMW; the European Research Council grant ERC-CoG #616346 to AK; DFG grant SFB 680 project A1 to SiR; the National Science Foundation with grant US NSF DEB1257053 to JHW; NIH grant R01GM113230 (NIGMS) to LP; and by NIH grants 5R01GM080203 (NIGMS) and 5R01HG004483 (NHGRI) and by the Director, Office of Science, Office of Basic Energy Sciences, U.S. Department of Energy, Contract No. DE-AC02-05CH11231 to MCMT.

Funders	Funder number
National Institutes of Health (NIH)
U.S. Department of Energy EPSCoR	DE-AC02-05CH11231
U.S. Department of Energy EPSCoR
National Institute of General Medical Sciences	5R01HG004483, 5R01GM080203, R01GM113230
National Institute of General Medical Sciences
National Science Foundation Arctic Social Science Program	DEB1257053
National Science Foundation Arctic Social Science Program

Keywords

Evolution of development
Gene family evolution
Gene structure
Lateral gene transfer
Phytophagy
RNAi
Transcription factors

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Genetics
Cell Biology

Access to Document

10.1186/s13059-019-1660-0

Cite this

Panfilio, K. A., Vargas Jentzsch, I. M., Benoit, J. B., Erezyilmaz, D., Suzuki, Y., Colella, S., Robertson, H. M., Poelchau, M. F., Waterhouse, R. M., Ioannidis, P., Weirauch, M. T., Hughes, D. S. T., Murali, S. C., Werren, J. H., Jacobs, C. G. C., Duncan, E. J., Armisén, D., Vreede, B. M. I., Baa-Puyoulet, P., ... Richards, S. (2019). Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome. Genome Biology, 20(1), Article 64. https://doi.org/10.1186/s13059-019-1660-0

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title = "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 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.",

keywords = "Evolution of development, Gene family evolution, Gene structure, Lateral gene transfer, Phytophagy, RNAi, Transcription factors",

author = "Panfilio, {Kristen A.} and {Vargas Jentzsch}, {Iris M.} and Benoit, {Joshua B.} and Deniz Erezyilmaz and Yuichiro Suzuki and Stefano Colella and Robertson, {Hugh M.} and Poelchau, {Monica F.} and Waterhouse, {Robert M.} and Panagiotis Ioannidis and Weirauch, {Matthew T.} and Hughes, {Daniel S.T.} and Murali, {Shwetha C.} and Werren, {John H.} and Jacobs, {Chris G.C.} and Duncan, {Elizabeth J.} and David Armis{\'e}n and Vreede, {Barbara M.I.} and Patrice Baa-Puyoulet and Berger, {Chlo{\'e} S.} and Chang, {Chun Che} and Hsu Chao and Chen, {Mei Ju M.} and Chen, {Yen Ta} and Childers, {Christopher P.} and Chipman, {Ariel D.} and Cridge, {Andrew G.} and Crumi{\`e}re, {Antonin J.J.} and Dearden, {Peter K.} and Didion, {Elise M.} and Huyen Dinh and Doddapaneni, {Harsha Vardhan} and Amanda Dolan and Shannon Dugan and Extavour, {Cassandra G.} and G{\'e}rard Febvay and Markus Friedrich and Neta Ginzburg and Yi Han and Peter Heger and Holmes, {Christopher J.} and Thorsten Horn and Hsiao, {Yi Min} and Jennings, {Emily C.} and Johnston, {J. Spencer} and Jones, {Tamsin E.} and Jones, {Jeffery W.} and Abderrahman Khila and Stefan Koelzer and Viera Kovacova and Megan Leask and Lee, {Sandra L.} and Lee, {Chien Yueh} and Lovegrove, {MacKenzie R.} and Lu, {Hsiao Ling} and Yong Lu and Moore, {Patricia J.} and Munoz-Torres, {Monica C.} and Muzny, {Donna M.} and Palli, {Subba R.} and Nicolas Parisot and Leslie Pick and Porter, {Megan L.} and Jiaxin Qu and Refki, {Peter N.} and Rose Richter and Rolando Rivera-Pomar and Rosendale, {Andrew J.} and Siegfried Roth and Lena Sachs and Santos, {M. Em{\'i}lia} and Jan Seibert and Essia Sghaier and Shukla, {Jayendra N.} and Stancliffe, {Richard J.} and Olivia Tidswell and Lucila Traverso and {Van Der Zee}, Maurijn and S{\'e}verine Viala and Worley, {Kim C.} and Zdobnov, {Evgeny M.} and Gibbs, {Richard A.} and Stephen Richards",

note = "Publisher Copyright: {\textcopyright} 2019 The Author(s).",

year = "2019",

month = apr,

day = "2",

doi = "10.1186/s13059-019-1660-0",

language = "English",

volume = "20",

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Panfilio, KA, Vargas Jentzsch, IM, Benoit, JB, Erezyilmaz, D, Suzuki, Y, Colella, S, Robertson, HM, Poelchau, MF, Waterhouse, RM, Ioannidis, P, Weirauch, MT, Hughes, DST, Murali, SC, Werren, JH, Jacobs, CGC, Duncan, EJ, Armisén, D, Vreede, BMI, Baa-Puyoulet, P, Berger, CS, Chang, CC, Chao, H, Chen, MJM, Chen, YT, Childers, CP, Chipman, AD, Cridge, AG, Crumière, AJJ, Dearden, PK, Didion, EM, Dinh, H, Doddapaneni, HV, Dolan, A, Dugan, S, Extavour, CG, Febvay, G, Friedrich, M, Ginzburg, N, Han, Y, Heger, P, Holmes, CJ, Horn, T, Hsiao, YM, Jennings, EC, Johnston, JS, Jones, TE, Jones, JW, Khila, A, Koelzer, S, Kovacova, V, Leask, M, Lee, SL, Lee, CY, Lovegrove, MR, Lu, HL, Lu, Y, Moore, PJ, Munoz-Torres, MC, Muzny, DM, Palli, SR, Parisot, N, Pick, L, Porter, ML, Qu, J, Refki, PN, Richter, R, Rivera-Pomar, R, Rosendale, AJ, Roth, S, Sachs, L, Santos, ME, Seibert, J, Sghaier, E, Shukla, JN, Stancliffe, RJ, Tidswell, O, Traverso, L, Van Der Zee, M, Viala, S, Worley, KC, Zdobnov, EM, Gibbs, RA & Richards, S 2019, 'Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome', Genome Biology, vol. 20, no. 1, 64. https://doi.org/10.1186/s13059-019-1660-0

TY - JOUR

T1 - Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome

AU - Panfilio, Kristen A.

AU - Vargas Jentzsch, Iris M.

AU - Benoit, Joshua B.

AU - Erezyilmaz, Deniz

AU - Suzuki, Yuichiro

AU - Colella, Stefano

AU - Robertson, Hugh M.

AU - Poelchau, Monica F.

AU - Waterhouse, Robert M.

AU - Ioannidis, Panagiotis

AU - Weirauch, Matthew T.

AU - Hughes, Daniel S.T.

AU - Murali, Shwetha C.

AU - Werren, John H.

AU - Jacobs, Chris G.C.

AU - Duncan, Elizabeth J.

AU - Armisén, David

AU - Vreede, Barbara M.I.

AU - Baa-Puyoulet, Patrice

AU - Berger, Chloé S.

AU - Chang, Chun Che

AU - Chao, Hsu

AU - Chen, Mei Ju M.

AU - Chen, Yen Ta

AU - Childers, Christopher P.

AU - Chipman, Ariel D.

AU - Cridge, Andrew G.

AU - Crumière, Antonin J.J.

AU - Dearden, Peter K.

AU - Didion, Elise M.

AU - Dinh, Huyen

AU - Doddapaneni, Harsha Vardhan

AU - Dolan, Amanda

AU - Dugan, Shannon

AU - Extavour, Cassandra G.

AU - Febvay, Gérard

AU - Friedrich, Markus

AU - Ginzburg, Neta

AU - Han, Yi

AU - Heger, Peter

AU - Holmes, Christopher J.

AU - Horn, Thorsten

AU - Hsiao, Yi Min

AU - Jennings, Emily C.

AU - Johnston, J. Spencer

AU - Jones, Tamsin E.

AU - Jones, Jeffery W.

AU - Khila, Abderrahman

AU - Koelzer, Stefan

AU - Kovacova, Viera

AU - Leask, Megan

AU - Lee, Sandra L.

AU - Lee, Chien Yueh

AU - Lovegrove, MacKenzie R.

AU - Lu, Hsiao Ling

AU - Lu, Yong

AU - Moore, Patricia J.

AU - Munoz-Torres, Monica C.

AU - Muzny, Donna M.

AU - Palli, Subba R.

AU - Parisot, Nicolas

AU - Pick, Leslie

AU - Porter, Megan L.

AU - Qu, Jiaxin

AU - Refki, Peter N.

AU - Richter, Rose

AU - Rivera-Pomar, Rolando

AU - Rosendale, Andrew J.

AU - Roth, Siegfried

AU - Sachs, Lena

AU - Santos, M. Emília

AU - Seibert, Jan

AU - Sghaier, Essia

AU - Shukla, Jayendra N.

AU - Stancliffe, Richard J.

AU - Tidswell, Olivia

AU - Traverso, Lucila

AU - Van Der Zee, Maurijn

AU - Viala, Séverine

AU - Worley, Kim C.

AU - Zdobnov, Evgeny M.

AU - Gibbs, Richard A.

AU - Richards, Stephen

PY - 2019/4/2

Y1 - 2019/4/2

N2 - 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.

AB - 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.

KW - Evolution of development

KW - Gene family evolution

KW - Gene structure

KW - Lateral gene transfer

KW - Phytophagy

KW - RNAi

KW - Transcription factors

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UR - http://www.scopus.com/inward/citedby.url?scp=85063784440&partnerID=8YFLogxK

U2 - 10.1186/s13059-019-1660-0

DO - 10.1186/s13059-019-1660-0

M3 - Article

C2 - 30935422

AN - SCOPUS:85063784440

SN - 1474-7596

VL - 20

JO - Genome Biology

JF - Genome Biology

IS - 1

M1 - 64

ER -

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

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

Access to Document

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