Tissue-specific transcriptomics, chromosomal localization, and phylogeny of chemosensory and odorant binding proteins from the red flour beetle Tribolium castaneum reveal subgroup specificities for olfaction or more general functions

Dippel, Stefan; Oberhofer, Georg; Kahnt, Jörg; Gerischer, Lizzy; Opitz, Lennart; Schachtner, Joachim; Stanke, Mario; Schütz, Stefan; Wimmer, Ernst A.; Angeli, Sergio

doi:10.1186/1471-2164-15-1141

Cited by 107 publications

(132 citation statements)

References 110 publications

(158 reference statements)

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“…On the basis of distinctive structural features and phylogenetic relationships, we identified four main subgroups of OBPs: classic, antenna binding protein II (ABPII), plus‐C, and minus‐C (Figure ). In accordance with previous phylogenetic analyses (Andersson et al., ; Dippel et al., ), we could show that the basal OBP group seems to be the classic, whereas all other groups were internal clades of this subfamily. In our tree, the subgroups ABPIIs and minus‐C OPBs appeared to have independent origins.…”

Section: Resultssupporting

confidence: 93%

“…Even five more minus‐C OBP genes were found being upregulated in the birch feeders’ legs compared to the willow feeders’ legs. Although OBPs are also found in the legs and antennae of other beetles (Dippel et al., ), they could fulfill different functions in the two organs. This scenario could also be true for the high expression of Clap OBP20 found in the Finnish WFP, a result opposing the data from the Kazakh WFP.…”

Section: Discussionmentioning

confidence: 99%

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A subset of chemosensory genes differs between two populations of a specialized leaf beetle after host plant shift

Wang

Pentzold

Kunert

et al. 2018

Ecology and Evolution

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Due to its fundamental role in shaping host selection behavior, we have analyzed the chemosensory repertoire of Chrysomela lapponica. This specialized leaf beetle evolved distinct populations which shifted from the ancestral host plant, willow (Salix sp., Salicaceae), to birch (Betula rotundifolia, Betulaceae). We identified 114 chemosensory candidate genes in adult C. lapponica: 41 olfactory receptors (ORs), eight gustatory receptors, 17 ionotropic receptors, four sensory neuron membrane proteins, 32 odorant binding proteins (OBPs), and 12 chemosensory proteins (CSP) by RNA‐seq. Differential expression analyses in the antennae revealed significant upregulation of one minus‐C OBP (Clap OBP27) and one CSP (Clap CSP12) in the willow feeders. In contrast, one OR (Clap OR17), four minus‐C OBPs (Clap OBP02, 07, 13, 20), and one plus‐C OBP (Clap OBP32) were significantly upregulated in birch feeders. The differential expression pattern in the legs was more complex. To narrow down putative ligands acting as cues for host discrimination, the relative abundance and diversity of volatiles of the two host plant species were analyzed. In addition to salicylaldehyde (willow‐specific), both plant species differed mainly in their emission rate of terpenoids such as (E,E)‐α‐farnesene (high in willow) or 4,8‐dimethylnona‐1,3,7‐triene (high in birch). Qualitatively, the volatiles were similar between willow and birch leaves constituting an “olfactory bridge” for the beetles. Subsequent structural modeling of the three most differentially expressed OBPs and docking studies using 22 host volatiles indicated that ligands bind with varying affinity. We suggest that the evolution of particularly minus‐C OBPs and ORs in C. lapponica facilitated its host plant shift via chemosensation of the phytochemicals from birch as novel host plant.

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Section: Resultssupporting

confidence: 93%

Section: Discussionmentioning

confidence: 99%

A subset of chemosensory genes differs between two populations of a specialized leaf beetle after host plant shift

Wang

Pentzold

Kunert

et al. 2018

Ecology and Evolution

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“…The OBP data set comprised OBPs from Tr. castaneum (Dippel et al ., ), Ac. pisum (Zhou et al ., ), Bl.…”

Section: Methodsmentioning

confidence: 99%

“…germanica (Niu et al ., ), Tr. castaneum (Dippel et al ., ), Ac. pisum (Zhou et al ., ), D. melanogaster (Vieira & Rozas, ), Bo.…”

Section: Methodsmentioning

confidence: 99%

Identification of odorant‐binding and chemosensory protein genes and the ligand affinity of two of the encoded proteins suggest a complex olfactory perception system in Periplaneta americana

Zhang

et al. 2017

Insect Molecular Biology

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The American cockroach (Periplaneta americana) is an urban pest with a precise chemosensory system that helps it achieve complex physiological behaviours, including locating food and mating. However, its chemosensory mechanisms have not been well studied. Here, we identified 71 putative odorant carrier protein genes in P. americana, including 57 new odorant-binding proteins (OBPs) and 11 chemosensory proteins (CSPs). To identify their physiological functions, we investigated their tissue expression patterns in antennae, mouthparts, legs, and the remainder of the body of both sexes, and determined that most of these genes were expressed in chemosensory organs. A phylogenetic tree showed that the putative pheromone-binding proteins of P. americana were in different clades from those of moths. Two genes, PameOBP24 and PameCSP7, were expressed equally in antennae of both sexes and highly expressed amongst the OBPs and CSPs. These genes were expressed in Escherichia coli and the resultant proteins were purified. The binding affinities of 74 common odorant compounds were tested with recombinant PameOBP24 and PameCSP7. Both proteins bound a variety of ligands. Our findings provide a foundation for future research into the chemosensory mechanisms of P. americana and help in identifying potential target genes for managing this pest.

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“…Another prominent alternative for chemical fumigants is plant natural products, such as plant essential oils. Plant natural products are known for their properties of low residue formation, high selectivity, and difficulty to generate cross-resistance, etc [8]. It is mainly because of their complex constituents and novel modes of action against insects [9].…”

Section: Introductionmentioning

confidence: 99%

Insecticidal Activity of Melaleuca alternifolia Essential Oil and RNA-Seq Analysis of Sitophilus zeamais Transcriptome in Response to Oil Fumigation

et al. 2016

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BackgroundThe cereal weevil, Sitophilus zeamais is one of the most destructive pests of stored cereals worldwide. Frequent use of fumigants for managing stored-product insects has led to the development of resistance in insects. Essential oils from aromatic plants including the tea oil plant, Melaleuca alternifolia may provide environmentally friendly alternatives to currently used pest control agents. However, little is known about molecular events involved in stored-product insects in response to plant essential oil fumigation.ResultsM. alternifolia essential oil was shown to possess the fumigant toxicity against S. zeamais. The constituent, terpinen-4-ol was the most effective compound for fumigant toxicity. M. alternifolia essential oil significantly inhibited the activity of three enzymes in S. zeamais, including two detoxifying enzymes, glutathione S-transferase (GST), and carboxylesterase (CarE), as well as a nerve conduction enzyme, acetylcholinesterase (AChE). Comparative transcriptome analysis of S. zeamais through RNA-Seq identified a total of 3,562 differentially expressed genes (DEGs), of which 2,836 and 726 were up-regulated and down-regulated in response to M. alternifolia essential oil fumigation, respectively. Based on gene ontology (GO) analysis, the majority of DEGs were involved in insecticide detoxification and mitochondrial function. Furthermore, an abundance of DEGs mapped into the metabolism pathway in the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway database were associated with respiration and metabolism of xenobiotics, including cytochrome P450s, CarEs, GSTs, and ATP-binding cassette transporters (ABC transporters). Some DEGs mapped into the proteasome and phagosome pathway were found to be significantly enriched. These results led us to propose a model of insecticide action that M. alternifolia essential oil likely directly affects the hydrogen carrier to block the electron flow and interfere energy synthesis in mitochondrial respiratory chain.ConclusionThis is the first study to perform a comparative transcriptome analysis of S. zeamais in response to M. alternifolia essential oil fumigation. Our results provide new insights into the insecticidal mechanism of M. alternifolia essential oil fumigation against S. zeamais and eventually contribute to the management of this important agricultural pest.

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Tissue-specific transcriptomics, chromosomal localization, and phylogeny of chemosensory and odorant binding proteins from the red flour beetle Tribolium castaneum reveal subgroup specificities for olfaction or more general functions

Cited by 107 publications

References 110 publications

A subset of chemosensory genes differs between two populations of a specialized leaf beetle after host plant shift

A subset of chemosensory genes differs between two populations of a specialized leaf beetle after host plant shift

Identification of odorant‐binding and chemosensory protein genes and the ligand affinity of two of the encoded proteins suggest a complex olfactory perception system in Periplaneta americana

Insecticidal Activity of Melaleuca alternifolia Essential Oil and RNA-Seq Analysis of Sitophilus zeamais Transcriptome in Response to Oil Fumigation

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