Sex- and tissue-specific profiles of chemosensory gene expression in a herbivorous gall-inducing fly (Diptera: Cecidomyiidae)
Author
Summary, in English
Background: The chemical senses of insects mediate behaviors that are closely linked to survival and reproduction.
The order Diptera contains two model organisms, the vinegar fly Drosophila melanogaster and the mosquito
Anopheles gambiae, whose chemosensory genes have been extensively studied. Representing a third dipteran
lineage with an interesting phylogenetic position, and being ecologically distinct by feeding on plants, the Hessian
fly (Mayetiola destructor Say, Diptera: Cecidomyiidae) genome sequence has recently become available. Among
plant-feeding insects, the Hessian fly is unusual in ‘reprogramming’ the plant to create a superior food and in being the
target of plant resistance genes, a feature shared by plant pathogens. Chemoreception is essential for reproductive
success, including detection of sex pheromone and plant-produced chemicals by males and females, respectively.
Results: We identified genes encoding 122 odorant receptors (OR), 28 gustatory receptors (GR), 39 ionotropic
receptors (IR), 32 odorant binding proteins, and 7 sensory neuron membrane proteins in the Hessian fly genome. We
then mapped Illumina-sequenced transcriptome reads to the genome to explore gene expression in male and female
antennae and terminal abdominal segments. Our results reveal that a large number of chemosensory genes have
up-regulated expression in the antennae, and the expression is in many cases sex-specific. Sex-specific expression is
particularly evident among the Or genes, consistent with the sex-divergent olfactory-mediated behaviors of the adults.
In addition, the large number of Ors in the genome but the reduced set of Grs and divergent Irs suggest that the
short-lived adults rely more on long-range olfaction than on short-range gustation. We also report up-regulated
expression of some genes from all chemosensory gene families in the terminal segments of the abdomen, which
play important roles in reproduction.
Conclusions: We show that a large number of the chemosensory genes in the Hessian fly genome have sex- and
tissue-specific expression profiles. Our findings provide the first insights into the molecular basis of chemoreception in
plant-feeding flies, representing an important advance toward a more complete understanding of olfaction in Diptera
and its links to ecological specialization.
The order Diptera contains two model organisms, the vinegar fly Drosophila melanogaster and the mosquito
Anopheles gambiae, whose chemosensory genes have been extensively studied. Representing a third dipteran
lineage with an interesting phylogenetic position, and being ecologically distinct by feeding on plants, the Hessian
fly (Mayetiola destructor Say, Diptera: Cecidomyiidae) genome sequence has recently become available. Among
plant-feeding insects, the Hessian fly is unusual in ‘reprogramming’ the plant to create a superior food and in being the
target of plant resistance genes, a feature shared by plant pathogens. Chemoreception is essential for reproductive
success, including detection of sex pheromone and plant-produced chemicals by males and females, respectively.
Results: We identified genes encoding 122 odorant receptors (OR), 28 gustatory receptors (GR), 39 ionotropic
receptors (IR), 32 odorant binding proteins, and 7 sensory neuron membrane proteins in the Hessian fly genome. We
then mapped Illumina-sequenced transcriptome reads to the genome to explore gene expression in male and female
antennae and terminal abdominal segments. Our results reveal that a large number of chemosensory genes have
up-regulated expression in the antennae, and the expression is in many cases sex-specific. Sex-specific expression is
particularly evident among the Or genes, consistent with the sex-divergent olfactory-mediated behaviors of the adults.
In addition, the large number of Ors in the genome but the reduced set of Grs and divergent Irs suggest that the
short-lived adults rely more on long-range olfaction than on short-range gustation. We also report up-regulated
expression of some genes from all chemosensory gene families in the terminal segments of the abdomen, which
play important roles in reproduction.
Conclusions: We show that a large number of the chemosensory genes in the Hessian fly genome have sex- and
tissue-specific expression profiles. Our findings provide the first insights into the molecular basis of chemoreception in
plant-feeding flies, representing an important advance toward a more complete understanding of olfaction in Diptera
and its links to ecological specialization.
Publishing year
2014
Language
English
Pages
1-19
Publication/Series
BMC Genomics
Volume
15
Document type
Journal article
Publisher
BioMed Central (BMC)
Topic
- Genetics
Status
Published
Project
- Sex pheromone biosynthesis and odorant receptors in gall midges
Research group
- Pheromone Group
- Molecular Ecology and Evolution Lab
ISBN/ISSN/Other
- ISSN: 1471-2164