%0 Journal Article %J BMC Biol %D 2020 %T Genome-enabled insights into the biology of thrips as crop pests. %A Rotenberg, Dorith %A Baumann, Aaron A %A Ben-Mahmoud, Sulley %A Christiaens, Olivier %A Dermauw, Wannes %A Ioannidis, Panagiotis %A Jacobs, Chris G C %A Vargas Jentzsch, Iris M %A Oliver, Jonathan E %A Poelchau, Monica F %A Rajarapu, Swapna Priya %A Schneweis, Derek J %A Snoeck, Simon %A Taning, Clauvis N T %A Wei, Dong %A Widana Gamage, Shirani M K %A Hughes, Daniel S T %A Murali, Shwetha C %A Bailey, Samuel T %A Bejerman, Nicolas E %A Holmes, Christopher J %A Jennings, Emily C %A Rosendale, Andrew J %A Rosselot, Andrew %A Hervey, Kaylee %A Schneweis, Brandi A %A Cheng, Sammy %A Childers, Christopher %A Simão, Felipe A %A Dietzgen, Ralf G %A Chao, Hsu %A Dinh, Huyen %A Harshavardhan Doddapaneni %A Dugan, Shannon %A Yi Han %A Lee, Sandra L %A Donna M Muzny %A Qu, Jiaxin %A Kim C Worley %A Benoit, Joshua B %A Friedrich, Markus %A Jones, Jeffery W %A Panfilio, Kristen A %A Park, Yoonseong %A Robertson, Hugh M %A Smagghe, Guy %A Ullman, Diane E %A Van der Zee, Maurijn %A Van Leeuwen, Thomas %A Veenstra, Jan A %A Waterhouse, Robert M %A Weirauch, Matthew T %A Werren, John H %A Whitfield, Anna E %A Zdobnov, Evgeny M %A Richard A Gibbs %A Stephen Richards %K Animals %K Crops, Agricultural %K Feeding Behavior %K Food Chain %K Genome, Insect %K Immunity, Innate %K Life History Traits %K Perception %K Phylogeny %K Reproduction %K Thysanoptera %K Transcriptome %X

BACKGROUND: The western flower thrips, Frankliniella occidentalis (Pergande), is a globally invasive pest and plant virus vector on a wide array of food, fiber, and ornamental crops. The underlying genetic mechanisms of the processes governing thrips pest and vector biology, feeding behaviors, ecology, and insecticide resistance are largely unknown. To address this gap, we present the F. occidentalis draft genome assembly and official gene set.

RESULTS: We report on the first genome sequence for any member of the insect order Thysanoptera. Benchmarking Universal Single-Copy Ortholog (BUSCO) assessments of the genome assembly (size = 415.8 Mb, scaffold N50 = 948.9 kb) revealed a relatively complete and well-annotated assembly in comparison to other insect genomes. The genome is unusually GC-rich (50%) compared to other insect genomes to date. The official gene set (OGS v1.0) contains 16,859 genes, of which ~ 10% were manually verified and corrected by our consortium. We focused on manual annotation, phylogenetic, and expression evidence analyses for gene sets centered on primary themes in the life histories and activities of plant-colonizing insects. Highlights include the following: (1) divergent clades and large expansions in genes associated with environmental sensing (chemosensory receptors) and detoxification (CYP4, CYP6, and CCE enzymes) of substances encountered in agricultural environments; (2) a comprehensive set of salivary gland genes supported by enriched expression; (3) apparent absence of members of the IMD innate immune defense pathway; and (4) developmental- and sex-specific expression analyses of genes associated with progression from larvae to adulthood through neometaboly, a distinct form of maturation differing from either incomplete or complete metamorphosis in the Insecta.

CONCLUSIONS: Analysis of the F. occidentalis genome offers insights into the polyphagous behavior of this insect pest that finds, colonizes, and survives on a widely diverse array of plants. The genomic resources presented here enable a more complete analysis of insect evolution and biology, providing a missing taxon for contemporary insect genomics-based analyses. Our study also offers a genomic benchmark for molecular and evolutionary investigations of other Thysanoptera species.

%B BMC Biol %V 18 %P 142 %8 2020 Oct 19 %G eng %N 1 %1 https://www.ncbi.nlm.nih.gov/pubmed/33070780?dopt=Abstract %R 10.1186/s12915-020-00862-9 %0 Journal Article %J Genome Biol %D 2019 %T Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome. %A Panfilio, Kristen A %A Vargas Jentzsch, Iris M %A Benoit, Joshua B %A Erezyilmaz, Deniz %A Suzuki, Yuichiro %A Colella, Stefano %A Robertson, Hugh M %A Poelchau, Monica F %A Waterhouse, Robert M %A Ioannidis, Panagiotis %A Weirauch, Matthew T %A Hughes, Daniel S T %A Murali, Shwetha C %A Werren, John H %A Jacobs, Chris G C %A Duncan, Elizabeth J %A Armisén, David %A Vreede, Barbara M I %A Baa-Puyoulet, Patrice %A Berger, Chloé S %A Chang, Chun-Che %A Chao, Hsu %A Chen, Mei-Ju M %A Chen, Yen-Ta %A Childers, Christopher P %A Chipman, Ariel D %A Cridge, Andrew G %A Crumière, Antonin J J %A Dearden, Peter K %A Didion, Elise M %A Dinh, Huyen %A Harshavardhan Doddapaneni %A Dolan, Amanda %A Dugan, Shannon %A Extavour, Cassandra G %A Febvay, Gérard %A Friedrich, Markus %A Ginzburg, Neta %A Yi Han %A Heger, Peter %A Holmes, Christopher J %A Horn, Thorsten %A Hsiao, Yi-Min %A Jennings, Emily C %A Johnston, J Spencer %A Jones, Tamsin E %A Jones, Jeffery W %A Khila, Abderrahman %A Koelzer, Stefan %A Kovacova, Viera %A Leask, Megan %A Lee, Sandra L %A Lee, Chien-Yueh %A Lovegrove, Mackenzie R %A Lu, Hsiao-Ling %A Lu, Yong %A Moore, Patricia J %A Munoz-Torres, Monica C %A Donna M Muzny %A Palli, Subba R %A Parisot, Nicolas %A Pick, Leslie %A Porter, Megan L %A Qu, Jiaxin %A Refki, Peter N %A Richter, Rose %A Rivera-Pomar, Rolando %A Rosendale, Andrew J %A Roth, Siegfried %A Sachs, Lena %A Santos, M Emília %A Seibert, Jan %A Sghaier, Essia %A Shukla, Jayendra N %A Stancliffe, Richard J %A Tidswell, Olivia %A Traverso, Lucila %A Van der Zee, Maurijn %A Viala, Sèverine %A Kim C Worley %A Zdobnov, Evgeny M %A Richard A Gibbs %A Stephen Richards %K Amino Acid Sequence %K Animals %K CYS2-HIS2 Zinc Fingers %K Evolution, Molecular %K Feeding Behavior %K Gene Dosage %K Gene Expression Profiling %K Gene Transfer, Horizontal %K Genes, Homeobox %K Genome, Insect %K Hemiptera %K Pigmentation %K Smell %K Transcription Factors %X

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.

%B Genome Biol %V 20 %P 64 %8 2019 Apr 02 %G eng %N 1 %1 https://www.ncbi.nlm.nih.gov/pubmed/30935422?dopt=Abstract %R 10.1186/s13059-019-1660-0 %0 Journal Article %J BMC Genomics %D 2018 %T The genome of the water strider Gerris buenoi reveals expansions of gene repertoires associated with adaptations to life on the water. %A Armisén, David %A Rajakumar, Rajendhran %A Friedrich, Markus %A Benoit, Joshua B %A Robertson, Hugh M %A Panfilio, Kristen A %A Ahn, Seung-Joon %A Poelchau, Monica F %A Chao, Hsu %A Dinh, Huyen %A Harshavardhan Doddapaneni %A Dugan, Shannon %A Richard A Gibbs %A Hughes, Daniel S T %A Yi Han %A Lee, Sandra L %A Murali, Shwetha C %A Donna M Muzny %A Qu, Jiaxin %A Worley, Kim C %A Munoz-Torres, Monica %A Abouheif, Ehab %A Bonneton, François %A Chen, Travis %A Chiang, Li-Mei %A Childers, Christopher P %A Cridge, Andrew G %A Crumière, Antonin J J %A Decaras, Amelie %A Didion, Elise M %A Duncan, Elizabeth J %A Elpidina, Elena N %A Favé, Marie-Julie %A Finet, Cédric %A Jacobs, Chris G C %A Cheatle Jarvela, Alys M %A Jennings, Emily C %A Jones, Jeffery W %A Lesoway, Maryna P %A Lovegrove, Mackenzie R %A Martynov, Alexander %A Oppert, Brenda %A Lillico-Ouachour, Angelica %A Rajakumar, Arjuna %A Refki, Peter Nagui %A Rosendale, Andrew J %A Santos, Maria Emilia %A Toubiana, William %A Van der Zee, Maurijn %A Vargas Jentzsch, Iris M %A Lowman, Aidamalia Vargas %A Viala, Sèverine %A Richards, Stephen %A Khila, Abderrahman %K Adaptation, Physiological %K Animals %K Evolution, Molecular %K Genome %K Genomics %K Heteroptera %K Insect Proteins %K Phenotype %K Phylogeny %X

BACKGROUND: Having conquered water surfaces worldwide, the semi-aquatic bugs occupy ponds, streams, lakes, mangroves, and even open oceans. The diversity of this group has inspired a range of scientific studies from ecology and evolution to developmental genetics and hydrodynamics of fluid locomotion. However, the lack of a representative water strider genome hinders our ability to more thoroughly investigate the molecular mechanisms underlying the processes of adaptation and diversification within this group.

RESULTS: Here we report the sequencing and manual annotation of the Gerris buenoi (G. buenoi) genome; the first water strider genome to be sequenced thus far. The size of the G. buenoi genome is approximately 1,000 Mb, and this sequencing effort has recovered 20,949 predicted protein-coding genes. Manual annotation uncovered a number of local (tandem and proximal) gene duplications and expansions of gene families known for their importance in a variety of processes associated with morphological and physiological adaptations to a water surface lifestyle. These expansions may affect key processes associated with growth, vision, desiccation resistance, detoxification, olfaction and epigenetic regulation. Strikingly, the G. buenoi genome contains three insulin receptors, suggesting key changes in the rewiring and function of the insulin pathway. Other genomic changes affecting with opsin genes may be associated with wavelength sensitivity shifts in opsins, which is likely to be key in facilitating specific adaptations in vision for diverse water habitats.

CONCLUSIONS: Our findings suggest that local gene duplications might have played an important role during the evolution of water striders. Along with these findings, the sequencing of the G. buenoi genome now provides us the opportunity to pursue exciting research opportunities to further understand the genomic underpinnings of traits associated with the extreme body plan and life history of water striders.

%B BMC Genomics %V 19 %P 832 %8 2018 Nov 21 %G eng %N 1 %1 https://www.ncbi.nlm.nih.gov/pubmed/30463532?dopt=Abstract %R 10.1186/s12864-018-5163-2