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.
Digital Object Identifier (DOI)
Funding for genome sequencing, assembly and automated annotation was provided by the National Institutes of Health (NIH) grant U54 HG003273 (NHGRI) to RAG. 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.
All sequence data are publically available at the NCBI, bioproject number PRJNA229125 and in the USDA Ag Data Commons data access system. In addition, assembled scaffolds, gene models, and a browser are available at the National Agricultural Library (https://i5k.nal.usda.gov/Oncopeltus_fasciatus). The OncfaCyc metabolism database is available within the ArthropodaCyc collection (http://arthropodacyc.cycadsys.org/).
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.; Palli, Subba Reddy; and Shukla, Jayendra Nath, "Molecular Evolutionary Trends and Feeding Ecology Diversification in the Hemiptera, Anchored by the Milkweed Bug Genome" (2019). Entomology Faculty Publications. 182.