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

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

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.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.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.

Journal: Genome biology
DOI: 10.1186/s13059-019-1660-0
Year: 2019

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