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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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Phylogenetic relationships of the odorant receptors (OR) and their expression profiles in M. destructor. A distance-corrected neighbor-joining tree (bootstrap consensus, topology only) based on M. destructor OR amino acid sequences and rooted by MdORCO. The tree was constructed using Mega 5 after multiple sequence alignment in ClustalX. Numbers on branches indicate bootstrap support (1000 iterations) and are only displayed if >70 and on major branches. Expression levels of the Or genes in the four transcriptomes are represented in a heat plot 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 3: Phylogenetic relationships of the odorant receptors (OR) and their expression profiles in M. destructor. A distance-corrected neighbor-joining tree (bootstrap consensus, topology only) based on M. destructor OR amino acid sequences and rooted by MdORCO. The tree was constructed using Mega 5 after multiple sequence alignment in ClustalX. Numbers on branches indicate bootstrap support (1000 iterations) and are only displayed if >70 and on major branches. Expression levels of the Or genes in the four transcriptomes are represented in a heat plot 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: Based on our annotation, the current assembly of the Hessian fly genome contains 122 Or genes, including a gene for the conserved co-receptor ORCO and six pseudogenes. Our transcriptome analysis showed that 99 of the Or genes were expressed in at least one of the analyzed tissues. Thus, almost 20% (23 genes) of the Or genes were not expressed (i.e. genes with less than 10 mapped read-pairs were regarded as having no or biologically insignificant expression). A substantially larger number of Or genes were represented by reads in the female antennae (94 Or genes) as compared to in the male antennae (64 Or genes) (Table 1). Thus, while a large proportion (77%) of the Or genes in the genome was expressed in the antennae of the female, only ca. half (52%) of them were expressed in the antennae of the male. Female and male terminal abdomens expressed 24 and 30 Or genes, respectively, including Orco (Table 1). Thus, relatively large numbers of Or genes were expressed outside of the main olfactory organ in both sexes, although the expression level was low in general (Figure 3; Additional file6). The Orco gene had the highest level of expression in both sexes, followed by Or116 for which the FPKM value in the male antennae was 90% of the FPKM value for Orco.


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)

Phylogenetic relationships of the odorant receptors (OR) and their expression profiles in M. destructor. A distance-corrected neighbor-joining tree (bootstrap consensus, topology only) based on M. destructor OR amino acid sequences and rooted by MdORCO. The tree was constructed using Mega 5 after multiple sequence alignment in ClustalX. Numbers on branches indicate bootstrap support (1000 iterations) and are only displayed if >70 and on major branches. Expression levels of the Or genes in the four transcriptomes are represented in a heat plot 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 3: Phylogenetic relationships of the odorant receptors (OR) and their expression profiles in M. destructor. A distance-corrected neighbor-joining tree (bootstrap consensus, topology only) based on M. destructor OR amino acid sequences and rooted by MdORCO. The tree was constructed using Mega 5 after multiple sequence alignment in ClustalX. Numbers on branches indicate bootstrap support (1000 iterations) and are only displayed if >70 and on major branches. Expression levels of the Or genes in the four transcriptomes are represented in a heat plot 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: Based on our annotation, the current assembly of the Hessian fly genome contains 122 Or genes, including a gene for the conserved co-receptor ORCO and six pseudogenes. Our transcriptome analysis showed that 99 of the Or genes were expressed in at least one of the analyzed tissues. Thus, almost 20% (23 genes) of the Or genes were not expressed (i.e. genes with less than 10 mapped read-pairs were regarded as having no or biologically insignificant expression). A substantially larger number of Or genes were represented by reads in the female antennae (94 Or genes) as compared to in the male antennae (64 Or genes) (Table 1). Thus, while a large proportion (77%) of the Or genes in the genome was expressed in the antennae of the female, only ca. half (52%) of them were expressed in the antennae of the male. Female and male terminal abdomens expressed 24 and 30 Or genes, respectively, including Orco (Table 1). Thus, relatively large numbers of Or genes were expressed outside of the main olfactory organ in both sexes, although the expression level was low in general (Figure 3; Additional file6). The Orco gene had the highest level of expression in both sexes, followed by Or116 for which the FPKM value in the male antennae was 90% of the FPKM value for Orco.

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