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Sex- and tissue-specific profiles of chemosensory gene expression in a herbivorous gall-inducing fly (Diptera: Cecidomyiidae).

Andersson MN, Videvall E, Walden KK, Harris MO, Robertson HM, Löfstedt C - BMC Genomics (2014)

Bottom Line: 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.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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, Lund University, Lund SE-223 62, Sweden. martin_n.andersson@biol.lu.se.

ABSTRACT

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.

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Expression profiles of the genes coding for ionotropic receptors (IR) in M. destructor. Expression levels of the Ir genes in the four transcriptomes represented as heat plots based on log-transformed FPKM values. Zero expression is represented by the lightest yellow color. Suffixes to gene names are explained in the Methods section.
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Figure 5: Expression profiles of the genes coding for ionotropic receptors (IR) in M. destructor. Expression levels of the Ir genes in the four transcriptomes represented as heat plots based on log-transformed FPKM values. Zero expression is represented by the lightest yellow color. Suffixes to gene names are explained in the Methods section.

Mentions: Twelve of the identified Ir genes (all divergent) were not expressed, whereas all the antennal Ir genes showed expression in at least one of the analyzed tissues (Figure 5; Additional file6). Larger numbers of Ir genes were expressed in the antennal tissues as compared to the terminal abdominal tissues (Table 1). The gene for the broadly occurring co-receptor IR25a had the highest expression of all the MdIr genes. Expression of this gene was high in the antennae of both sexes and in the male terminal abdomen.


Sex- and tissue-specific profiles of chemosensory gene expression in a herbivorous gall-inducing fly (Diptera: Cecidomyiidae).

Andersson MN, Videvall E, Walden KK, Harris MO, Robertson HM, Löfstedt C - BMC Genomics (2014)

Expression profiles of the genes coding for ionotropic receptors (IR) in M. destructor. Expression levels of the Ir genes in the four transcriptomes represented as heat plots based on log-transformed FPKM values. Zero expression is represented by the lightest yellow color. Suffixes to gene names are explained in the Methods section.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4230025&req=5

Figure 5: Expression profiles of the genes coding for ionotropic receptors (IR) in M. destructor. Expression levels of the Ir genes in the four transcriptomes represented as heat plots based on log-transformed FPKM values. Zero expression is represented by the lightest yellow color. Suffixes to gene names are explained in the Methods section.
Mentions: Twelve of the identified Ir genes (all divergent) were not expressed, whereas all the antennal Ir genes showed expression in at least one of the analyzed tissues (Figure 5; Additional file6). Larger numbers of Ir genes were expressed in the antennal tissues as compared to the terminal abdominal tissues (Table 1). The gene for the broadly occurring co-receptor IR25a had the highest expression of all the MdIr genes. Expression of this gene was high in the antennae of both sexes and in the male terminal abdomen.

Bottom Line: 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.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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, Lund University, Lund SE-223 62, Sweden. martin_n.andersson@biol.lu.se.

ABSTRACT

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.

Show MeSH
Related in: MedlinePlus