Genome-enabled insights into the biology of thrips as crop pests

Author:

Rotenberg DorithORCID,Baumann Aaron A.,Ben-Mahmoud Sulley,Christiaens Olivier,Dermauw Wannes,Ioannidis Panagiotis,Jacobs Chris G. C.,Vargas Jentzsch Iris M.,Oliver Jonathan E.,Poelchau Monica F.,Rajarapu Swapna Priya,Schneweis Derek J.,Snoeck Simon,Taning Clauvis N. T.,Wei Dong,Widana Gamage Shirani M. K.,Hughes Daniel S. T.,Murali Shwetha C.,Bailey Samuel T.,Bejerman Nicolas E.,Holmes Christopher J.,Jennings Emily C.,Rosendale Andrew J.,Rosselot Andrew,Hervey Kaylee,Schneweis Brandi A.,Cheng Sammy,Childers Christopher,Simão Felipe A.,Dietzgen Ralf G.,Chao Hsu,Dinh Huyen,Doddapaneni Harsha Vardhan,Dugan Shannon,Han Yi,Lee Sandra L.,Muzny Donna M.,Qu Jiaxin,Worley Kim C.,Benoit Joshua B.,Friedrich Markus,Jones Jeffery W.,Panfilio Kristen A.,Park Yoonseong,Robertson Hugh M.,Smagghe Guy,Ullman Diane E.,van der Zee Maurijn,Van Leeuwen Thomas,Veenstra Jan A.,Waterhouse Robert M.,Weirauch Matthew T.,Werren John H.,Whitfield Anna E.,Zdobnov Evgeny M.,Gibbs Richard A.,Richards Stephen

Abstract

Abstract 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.

Funder

National Human Genome Research Institute

National Science Foundation

Swiss NSF

Research Foundation Flanders

National Institute of Food and Agriculture

Publisher

Springer Science and Business Media LLC

Subject

Cell Biology,Developmental Biology,Plant Science,General Agricultural and Biological Sciences,General Biochemistry, Genetics and Molecular Biology,Physiology,Ecology, Evolution, Behavior and Systematics,Structural Biology,Biotechnology

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