A12: Publications
A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)
Schoville S.D., Yolanda H.C., Panfilio K.A., Richards S., et al., 31. Jan. 2018, Scientific Reports 8:1931, DOI:10.1038/s41598-018-20154-1
Background
The Colorado potato beetle is one of the most challenging agricultural pests to manage. It has shown a spectacular ability to adapt to a variety of solanaceaeous plants and variable climates during its global invasion, and, notably, to rapidly evolve insecticide resistance. To examine evidence of rapid evolutionary change, and to understand the genetic basis of herbivory and insecticide resistance, we tested for structural and functional genomic changes relative to other arthropod species using genome sequencing, transcriptomics, and community annotation. Two factors that might facilitate rapid evolutionary change include transposable elements, which comprise at least 17% of the genome and are rapidly evolving compared to other Coleoptera, and high levels of nucleotide diversity in rapidly growing pest populations. Adaptations to plant feeding are evident in gene expansions and differential expression of digestive enzymes in gut tissues, as well as expansions of gustatory receptors for bitter tasting. Surprisingly, the suite of genes involved in insecticide resistance is similar to other beetles. Finally, duplications in the RNAi pathway might explain why Leptinotarsa decemlineata has high sensitivity to dsRNA. The L. decemlineata genome provides opportunities to investigate a broad range of phenotypes and to develop sustainable methods to control this widely successful pest.
By land, air, and sea: hemipteran diversity through the genomic lens
Panfilio K.A., Angelini D.R., 24. Dec. 2017, Current Opinion in Insect Science 25:106-115, https://doi.org/10.1016/j.cois.2017.12.005
Background
Thanks to a recent spate of sequencing projects, the Hemiptera are the first hemimetabolous insect order to achieve a critical mass of species with sequenced genomes, establishing the basis for comparative genomics of the bugs. However, as the most speciose hemimetabolous order, there is still a vast swathe of the hemipteran phylogeny that awaits genomic representation across subterranean, terrestrial, and aquatic habitats, and with lineage-specific and developmentally plastic cases of both wing polyphenisms and flightlessness. In this review, we highlight opportunities for taxonomic sampling beyond obvious pest species candidates, motivated by intriguing biological features of certain groups as well as the rich research tradition of ecological, physiological, developmental, and particularly cytogenetic investigation that spans the diversity of the Hemiptera.
Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface
McKenna D.D., Panfilio K.A., Richards S., et al., 11. Nov. 2016, Genome Biology 2016 17:227, https://doi.org/10.1186/s13059-016-1088-8
Background
Relatively little is known about the genomic basis and evolution of wood-feeding in beetles. We undertook genome sequencing and annotation, gene expression assays, studies of plant cell wall degrading enzymes, and other functional and comparative studies of the Asian longhorned beetle, Anoplophora glabripennis, a globally significant invasive species capable of inflicting severe feeding damage on many important tree species. Complementary studies of genes encoding enzymes involved in digestion of woody plant tissues or detoxification of plant allelochemicals were undertaken with the genomes of 14 additional insects, including the newly sequenced emerald ash borer and bull-headed dung beetle.
Results
The Asian longhorned beetle genome encodes a uniquely diverse arsenal of enzymes that can degrade the main polysaccharide networks in plant cell walls, detoxify plant allelochemicals, and otherwise facilitate feeding on woody plants. It has the metabolic plasticity needed to feed on diverse plant species, contributing to its highly invasive nature. Large expansions of chemosensory genes involved in the reception of pheromones and plant kairomones are consistent with the complexity of chemical cues it uses to find host plants and mates.
Conclusions
Amplification and functional divergence of genes associated with specialized feeding on plants, including genes originally obtained via horizontal gene transfer from fungi and bacteria, contributed to the addition, expansion, and enhancement of the metabolic repertoire of the Asian longhorned beetle, certain other phytophagous beetles, and to a lesser degree, other phytophagous insects. Our results thus begin to establish a genomic basis for the evolutionary success of beetles on plants.
Unique features of the bed bug, a global human ectoparasite, identified through genome sequencing
Benoit JB, Adelman ZN, Reinhardt K, Dolan A, Poelchau M, Jennings EC, Szuter EM, Hagan RW, Gujar H, Shukla JN, Zhu F, Mohan M, Nelson DR, Rosendale AJ, Derst C, Resnik V, Wernig S, Menegazzi P, Wegener C, Peschel N, Hendershot JM, Blenau W, Predel R, Johnston PR, Ioannidis P, Waterhouse RM, Nauen R, Schorn C, Ott MC, Maiwald F, Johnston JS, Gondhalekar AD, Scharf ME, Peterson BF, Raje KR, Hottel BA, Armisén D, Crumière AJ, Refki PN, Santos ME, Sghaier E, Viala S, Khila A, Ahn SJ, Childers C, Lee CY, Lin H, Hughes DS, Duncan EJ, Murali SC, Qu J, Dugan S, Lee SL, Chao H, Dinh H, Han Y, Doddapaneni H, Worley KC, Muzny DM, Wheeler D, Panfilio KA, Vargas Jentzsch IM, Vargo EL, Booth W, Friedrich M, Weirauch MT, Anderson MA, Jones JW, Mittapalli O, Zhao C, Zhou JJ, Evans JD, Attardo GM, Robertson HM, Zdobnov EM, Ribeiro JM, Gibbs RA, Werren JH, Palli SR, Schal C, Richards S, Nat. Commun. (2016), doi: 10.1038/ncomms10165
The bed bug, Cimex lectularius, has re-established itself as a ubiquitous human ectoparasite throughout much of the world during the past two decades. This global resurgence is likely linked to increased international travel and commerce in addition to widespread insecticide resistance. Analyses of the C. lectularius sequenced genome (650 Mb) and 14,220 predicted protein-coding genes provide a comprehensive representation of genes that are linked to traumatic insemination, a reduced chemosensory repertoire of genes related to obligate hematophagy, host-symbiont interactions, and several mechanisms of insecticide resistance. In addition, we document the presence of multiple putative lateral gene transfer events. Genome sequencing and annotation establish a solid foundation for future research on mechanisms of insecticide resistance, human-bed bug and symbiont-bed bug associations, and unique features of bed bug biology that contribute to the unprecedented success of C. lectularius as a human ectoparasite.
Dynamic BMP signaling polarized by Toll patterns the dorsoventral axis in a hemimetabolous insect.
Sachs, L., Chen, Y.-T., Drechsler, A., Lynch, J.A., Panfilio, K.A., Lässig, M., Berg, J., and Roth, S. 2015 - eLife 4: e05502.
Toll-dependent patterning of the dorsoventral axis in Drosophila represents one of the best understood gene regulatory networks. However, its evolutionary origin has remained elusive. Outside the insects Toll is not known for a patterning function, but rather for a role in pathogen defense. Here, we show that in the milkweed bug Oncopeltus fasciatus, whose lineage split from Drosophila's more than 350 million years ago, Toll is only required to polarize a dynamic BMP signaling network. A theoretical model reveals that this network has self-regulatory properties and that shallow Toll signaling gradients are sufficient to initiate axis formation. Such gradients can account for the experimentally observed twinning of insect embryos upon egg fragmentation and might have evolved from a state of uniform Toll activity associated with protecting insect eggs against pathogens.
The iBeetle large-scale RNAi screen reveals gene functions for insect development and physiology
Schmitt-Engel, C., Schultheis, D., Schwirz, J., Ströhlein, N., Troelenberg, N., Majumdar, U., Dao, Van Anh, Grossmann, D., Richter, T., Tech, M., Dönitz, J., Gerischer, L., Theis, M., Schild, I., Trauner, J., Koniszewski, N.D.B., Küster, E., Kittelmann, S., Hu, Y., Lehmann, S., Siemanowski, J., Ulrich, J., Panfilio, K.A., Schröder, R., Morgenstern, B., Stanke, M., Buchhholz, F., Frasch, M., Roth, S., Wimmer, Ernst A., Schoppmeier, M., Klingler, M., and Bucher, G. 2015 - Nat. Commun. 6: 7822
Genetic screens are powerful tools to identify the genes required for a given biological process. However, for technical reasons, comprehensive screens have been restricted to very few model organisms. Therefore, although deep sequencing is revealing the genes of ever more insect species, the functional studies predominantly focus on candidate genes previously identified in Drosophila, which is biasing research towards conserved gene functions. RNAi screens in other organisms promise to reduce this bias. Here we present the results of the iBeetle screen, a large-scale, unbiased RNAi screen in the red flour beetle, Tribolium castaneum, which identifies gene functions in embryonic and postembryonic development, physiology and cell biology. The utility of Tribolium as a screening platform is demonstrated by the identification of genes involved in insect epithelial adhesion. This work transcends the restrictions of the candidate gene approach and opens fields of research not accessible in Drosophila.
Evolution of epithelial morphogenesis: phenotypic integration across multiple levels of biological
organization
Horn, T., Hilbrant, M., and Panfilio, K.A., 2015 Front. Genet. 6: 303
Morphogenesis involves the dynamic reorganization of cell and tissue shapes to create the
three-dimensional body. Intriguingly, different species have evolved different morphogenetic
processes to achieve the same general outcomes during embryonic development. How are meaningful
comparisons between species made, and where do the differences lie? In this Perspective, we argue
that examining the evolution of embryonic morphogenesis requires the simultaneous consideration of
different levels of biological organization: (1) genes, (2) cells, (3) tissues, and (4) the entire
egg, or other gestational context. To illustrate the importance of integrating these levels, we use
the extraembryonic epithelia of insects—a lineage-specific innovation and evolutionary hotspot—as an
exemplary case study. We discuss how recent functional data, primarily from RNAi experiments
targeting the Hox3/Zen and U-shaped group transcription factors, provide insights into developmental
processes at all four levels. Comparisons of these data from several species both challenge and
inform our understanding of homology, in assessing how the process of epithelial morphogenesis has
itself evolved.
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