Transcriptomics reveal the molecular underpinnings of chemosensory proteins in  Chlorops oryzae

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Abstract

Background

Chemosensory proteins are a family of insect-specific chemical sensors that sense specific chemical cues and regulate insect behavior. Chemosensory proteins have been identified and analyzed in many insect species, such as Drosophila melanogaster, Bactrocera dorsalis and Calliphora stygia. This research has revealed that these proteins play a crucial role in insect orientation, predation and oviposition. However, little is known about the chemosensory proteins of Chlorops oryzae, a major pest of rice crops throughout Asia.

Results

Comparative transcription analysis of the genes of Chlorops oryzae larvae, pupae and adults identified a total of 104 chemosensory genes, including 25 odorant receptors (ORs), 26 odorant-binding proteins (OBPs), 19 ionotropic receptors (IRs), 23 gustatory receptors (GRs) and 11 sensory neuron membrane proteins (SNMPs). The sequences of these candidate chemosensory genes were confirmed and used to construct phylogenetic trees. Quantitative real-time PCR (qRT-PCR) confirmed that the expression of candidate OR genes in different developmental stages was consistent with the fragments per kilobase per million fragments (FPKM) values of differentially expressed genes (DEGs).

Conclusions

The identification of chemosensory genes in C. oryzae provides a foundation for the investigation of the function of chemosensory proteins in this species, which, in turn, could allow the development of new, improved methods of controlling this pest.

Electronic supplementary material

The online version of this article (10.1186/s12864-018-5315-4) contains supplementary material, which is available to authorized users.

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Most cited references 69

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L E M Vet, M Dicke (1992)

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Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels.

Dieter Wicher, Ronny Schäfer, René Bauernfeind … (2008)

From worm to man, many odorant signals are perceived by the binding of volatile ligands to odorant receptors that belong to the G-protein-coupled receptor (GPCR) family. They couple to heterotrimeric G-proteins, most of which induce cAMP production. This second messenger then activates cyclic-nucleotide-gated ion channels to depolarize the olfactory receptor neuron, thus providing a signal for further neuronal processing. Recent findings, however, have challenged this concept of odorant signal transduction in insects, because their odorant receptors, which lack any sequence similarity to other GPCRs, are composed of conventional odorant receptors (for example, Or22a), dimerized with a ubiquitously expressed chaperone protein, such as Or83b in Drosophila. Or83b has a structure akin to GPCRs, but has an inverted orientation in the plasma membrane. However, G proteins are expressed in insect olfactory receptor neurons, and olfactory perception is modified by mutations affecting the cAMP transduction pathway. Here we show that application of odorants to mammalian cells co-expressing Or22a and Or83b results in non-selective cation currents activated by means of an ionotropic and a metabotropic pathway, and a subsequent increase in the intracellular Ca(2+) concentration. Expression of Or83b alone leads to functional ion channels not directly responding to odorants, but being directly activated by intracellular cAMP or cGMP. Insect odorant receptors thus form ligand-gated channels as well as complexes of odorant-sensing units and cyclic-nucleotide-activated non-selective cation channels. Thereby, they provide rapid and transient as well as sensitive and prolonged odorant signalling.

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A spatial map of olfactory receptor expression in the Drosophila antenna.

L B Vosshall, H Amrein, P S Morozov … (1999)

Insects provide an attractive system for the study of olfactory sensory perception. We have identified a novel family of seven transmembrane domain proteins, encoded by 100 to 200 genes, that is likely to represent the family of Drosophila odorant receptors. Members of this gene family are expressed in topographically defined subpopulations of olfactory sensory neurons in either the antenna or the maxillary palp. Sensory neurons express different complements of receptor genes, such that individual neurons are functionally distinct. The isolation of candidate odorant receptor genes along with a genetic analysis of olfactory-driven behavior in insects may ultimately afford a system to understand the mechanistic link between odor recognition and behavior.

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Author and article information

Contributors

Lin Qiu: qiulin@hunau.edu.cn

Shunjie Tao: 1374633020@qq.com

Hualiang He: hhl_1234@126.com

Wenbing Ding: dingwenb119@hunau.edu.cn

Youzhi Li: liyouzhi@hunau.edu.cn

Journal

Journal ID (nlm-ta): BMC Genomics

Journal ID (iso-abbrev): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2164

Publication date (Electronic): 7 December 2018

Publication date PMC-release: 7 December 2018

Publication date Collection: 2018

Volume: 19

Electronic Location Identifier: 890

Affiliations

[1 ]GRID grid.257160.7, Hunan Provincial Key Laboratory for Biology and Control of Plant Diseases and Insect Pests, College of Plant Protection, , Hunan Agricultural University, ; Changsha, 410128 China

[2 ]Hunan Provincial Engineering & Technology Research Center for Biopesticide and Formulation Processing, Changsha, 410128 China

Article

Publisher ID: 5315

DOI: 10.1186/s12864-018-5315-4

PMC ID: 6286535

PubMed ID: 30526496

SO-VID: d3948b6e-6905-49bc-ac04-362db397879c

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 19 July 2018

Date accepted : 27 November 2018

Funding

Funded by: Hunan Provincial Science and Technology Department (CN)

Award ID: 2018NK2094

Award Recipient : Youzhi Li

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: chlorops oryzae,transcriptome,chemosensory genes,olfactory receptors,expression profiling

Data availability:

ScienceOpen disciplines: Genetics

Keywords: chlorops oryzae, transcriptome, chemosensory genes, olfactory receptors, expression profiling

Transcriptomics reveal the molecular underpinnings of chemosensory proteins in Chlorops oryzae

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Genes & Diseases

Most cited references 69

Ecology of Infochemical Use by Natural Enemies in a Tritrophic Context

Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels.

A spatial map of olfactory receptor expression in the Drosophila antenna.

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