Candidates for chemosensory genes identified in the Chinese citrus fly,  Bactrocera minax,  through a transcriptomic analysis

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Abstract

Background

The males of many Bactrocera species (Diptera: Tephritidae) respond strongly to plant-derived chemicals (male lures) and can be divided into cue lure/raspberry ketone (CL/RK) responders, methyl eugenol (ME) responders and non-responders. Representing a non-responders, Bactrocera minax display unique olfactory sensory characteristics compared with other Bactrocera species. The chemical senses of insects mediate behaviors that are associated with survival and reproduction. Here, we report the generation of transcriptomes from antennae and the rectal glands of both male and female adults of B. minax using Illumina sequencing technology, and annotated gene families potentially responsible for chemosensory.

Results

We developed four transcriptomes from different tissues of B. minax and identified a set of candidate genes potentially responsible for chemosensory by analyzing the transcriptomic data. The candidates included 40 unigenes coding for odorant receptors (ORs), 30 for ionotropic receptors (IRs), 17 for gustatory receptors (GRs), three for sensory neuron membrane proteins (SNMPs), 33 for odorant-binding proteins (OBPs), four for chemosensory proteins (CSPs). Sex- and tissue-specific expression profiles for candidate chemosensory genes were analyzed via transcriptomic data analyses, and expression profiles of all ORs and antennal IRs were investigated by real-time quantitative PCR (RT-qPCR). Phylogenetic analyses were also conducted on gene families and paralogs from other insect species together.

Conclusions

A large number of chemosensory genes were identified from transcriptomic data. Identification of these candidate genes and their expression profiles in various tissues provide useful information for future studies towards revealing their function in B. minax.

Electronic supplementary material

The online version of this article (10.1186/s12864-019-6022-5) contains supplementary material, which is available to authorized users.

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Most cited references 54

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Insect olfactory receptors are heteromeric ligand-gated ion channels.

Koji Sato, Maurizio Pellegrino, Takao Nakagawa … (2008)

In insects, each olfactory sensory neuron expresses between one and three ligand-binding members of the olfactory receptor (OR) gene family, along with the highly conserved and broadly expressed Or83b co-receptor. The functional insect OR consists of a heteromeric complex of unknown stoichiometry but comprising at least one variable odorant-binding subunit and one constant Or83b family subunit. Insect ORs lack homology to G-protein-coupled chemosensory receptors in vertebrates and possess a distinct seven-transmembrane topology with the amino terminus located intracellularly. Here we provide evidence that heteromeric insect ORs comprise a new class of ligand-activated non-selective cation channels. Heterologous cells expressing silkmoth, fruitfly or mosquito heteromeric OR complexes showed extracellular Ca2+ influx and cation-non-selective ion conductance on stimulation with odorant. Odour-evoked OR currents are independent of known G-protein-coupled second messenger pathways. The fast response kinetics and OR-subunit-dependent K+ ion selectivity of the insect OR complex support the hypothesis that the complex between OR and Or83b itself confers channel activity. Direct evidence for odorant-gated channels was obtained by outside-out patch-clamp recording of Xenopus oocyte and HEK293T cell membranes expressing insect OR complexes. The ligand-gated ion channel formed by an insect OR complex seems to be the basis for a unique strategy that insects have acquired to respond to the olfactory environment.

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Two chemosensory receptors together mediate carbon dioxide detection in Drosophila.

Walton Jones, Pelin Cayirlioglu, Ilona Grunwald Kadow … (2007)

Blood-feeding insects, including the malaria mosquito Anopheles gambiae, use highly specialized and sensitive olfactory systems to locate their hosts. This is accomplished by detecting and following plumes of volatile host emissions, which include carbon dioxide (CO2). CO2 is sensed by a population of olfactory sensory neurons in the maxillary palps of mosquitoes and in the antennae of the more genetically tractable fruitfly, Drosophila melanogaster. The molecular identity of the chemosensory CO2 receptor, however, remains unknown. Here we report that CO2-responsive neurons in Drosophila co-express a pair of chemosensory receptors, Gr21a and Gr63a, at both larval and adult life stages. We identify mosquito homologues of Gr21a and Gr63a, GPRGR22 and GPRGR24, and show that these are co-expressed in A. gambiae maxillary palps. We show that Gr21a and Gr63a together are sufficient for olfactory CO2-chemosensation in Drosophila. Ectopic expression of Gr21a and Gr63a together confers CO2 sensitivity on CO2-insensitive olfactory neurons, but neither gustatory receptor alone has this function. Mutant flies lacking Gr63a lose both electrophysiological and behavioural responses to CO2. Knowledge of the molecular identity of the insect olfactory CO2 receptors may spur the development of novel mosquito control strategies designed to take advantage of this unique and critical olfactory pathway. This in turn could bolster the worldwide fight against malaria and other insect-borne diseases.

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Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems.

Ana F. Silbering, Raphael Rytz, Yael Grosjean … (2011)

To sense myriad environmental odors, animals have evolved multiple, large families of divergent olfactory receptors. How and why distinct receptor repertoires and their associated circuits are functionally and anatomically integrated is essentially unknown. We have addressed these questions through comprehensive comparative analysis of the Drosophila olfactory subsystems that express the ionotropic receptors (IRs) and odorant receptors (ORs). We identify ligands for most IR neuron classes, revealing their specificity for select amines and acids, which complements the broader tuning of ORs for esters and alcohols. IR and OR sensory neurons exhibit glomerular convergence in segregated, although interconnected, zones of the primary olfactory center, but these circuits are extensively interdigitated in higher brain regions. Consistently, behavioral responses to odors arise from an interplay between IR- and OR-dependent pathways. We integrate knowledge on the different phylogenetic and developmental properties of these receptors and circuits to propose models for the functional contributions and evolution of these distinct olfactory subsystems.

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Author and article information

Contributors

Zhongzhen Wu: zhongzhen_wu@163.com

Cong Kang: kangcong1123@163.com

Mengqiu Qu: qumengqiu@163.com

Junlong Chen: 15112009071@163.com

Mingshun Chen: mchen@ksu.edu

Shuying Bin: binsuying@163.com

Jintian Lin: linjtian@163.com

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): 14 August 2019

Publication date PMC-release: 14 August 2019

Publication date Collection: 2019

Volume: 20

Electronic Location Identifier: 646

Affiliations

[1 ]GRID grid.449900.0, Guang Zhou City Key Laboratory of Subtropical Fruit Tree Outbreak Control, , Zhongkai University of Agriculture and Engineering, ; Guangzhou, 510225 People’s Republic of China

[2 ]ISNI 0000 0001 0737 1259, GRID grid.36567.31, Department of Entomology, , Kansas State University, ; Manhattan, KS 66506 USA

Article

Publisher ID: 6022

DOI: 10.1186/s12864-019-6022-5

PMC ID: 6693287

PubMed ID: 31412763

SO-VID: bc1718c8-9940-4895-8bd1-39658ad67eb8

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 : 14 January 2019

Date accepted : 9 August 2019

Funding

Funded by: Guang Zhou City Key Laboratory of Subtropical Fruit Tree Outbreak Control

Award ID: 201805010008

Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;

Award ID: 31572011

Funded by: Serious Pest and Disease Mechanism and Sustainable Control Innovation Team of Guangdong Province

Award ID: 2017KCXTD018

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: bactrocera minax,gene expression,transcriptome,chemosensory genes

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ScienceOpen disciplines: Genetics

Keywords: bactrocera minax, gene expression, transcriptome, chemosensory genes

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Candidates for chemosensory genes identified in the Chinese citrus fly, Bactrocera minax, through a transcriptomic analysis

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Abstract

Background

Results

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G3: Genes|Genomes|Genetics

Most cited references 54

Insect olfactory receptors are heteromeric ligand-gated ion channels.

Two chemosensory receptors together mediate carbon dioxide detection in Drosophila.

Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems.

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