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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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Related in: MedlinePlus

Comparison of global transcriptome expression profiles. The overall expression levels of the 27 029 genes predicted from the four transcriptomes were compared using Jensen-Shannon (JS) distance (A) and principle component analysis (B), both indicating the high similarity between the male and female antennal transcriptomes. In (B), PC 1 and PC 2 explained 55.8% and 32.2% respectively of the overall gene expression level variation in the four transcriptomes (black dots represent the predicted genes). Both the direction and length (length = within-transcriptome variation) of the eigenvectors (red arrows) show that the male and female antennal transcriptomes had highly similar variation in expression levels, both in relation to PC 1 and PC 2. In contrast, the variation in expression levels differed between the two terminal abdominal transcriptomes, which were also different from the two antennal transcriptomes (as indicated by the different lengths and directions of the eigenvectors). The difference between transcriptomes was explained (mainly) by the expression variation encompassed by PC 2 (i.e. as shown by the position of the four arrow heads). In addition, 1:1 plots (dashed line = 1:1 relationship) in combination with linear regression analyses (blue solid lines) were used to compare transcriptomes pair-wise. The female and male terminal abdomen both had an overall higher expression of the predicted genes compared to the antennae of females (C) and males (D), respectively. As indicated by the slope coefficients and relatively low R2 values, the expression did not follow a 1:1 relationship in these comparisons. In contrast, expression in the male antennae was similar to that in the female antennae, following a close to 1:1 relationship (E). Finally, the female terminal abdomen had an overall higher expression than the male terminal abdomen, i.e. the relationship between the two transcriptomes was relatively far from 1:1 (F).
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Figure 1: Comparison of global transcriptome expression profiles. The overall expression levels of the 27 029 genes predicted from the four transcriptomes were compared using Jensen-Shannon (JS) distance (A) and principle component analysis (B), both indicating the high similarity between the male and female antennal transcriptomes. In (B), PC 1 and PC 2 explained 55.8% and 32.2% respectively of the overall gene expression level variation in the four transcriptomes (black dots represent the predicted genes). Both the direction and length (length = within-transcriptome variation) of the eigenvectors (red arrows) show that the male and female antennal transcriptomes had highly similar variation in expression levels, both in relation to PC 1 and PC 2. In contrast, the variation in expression levels differed between the two terminal abdominal transcriptomes, which were also different from the two antennal transcriptomes (as indicated by the different lengths and directions of the eigenvectors). The difference between transcriptomes was explained (mainly) by the expression variation encompassed by PC 2 (i.e. as shown by the position of the four arrow heads). In addition, 1:1 plots (dashed line = 1:1 relationship) in combination with linear regression analyses (blue solid lines) were used to compare transcriptomes pair-wise. The female and male terminal abdomen both had an overall higher expression of the predicted genes compared to the antennae of females (C) and males (D), respectively. As indicated by the slope coefficients and relatively low R2 values, the expression did not follow a 1:1 relationship in these comparisons. In contrast, expression in the male antennae was similar to that in the female antennae, following a close to 1:1 relationship (E). Finally, the female terminal abdomen had an overall higher expression than the male terminal abdomen, i.e. the relationship between the two transcriptomes was relatively far from 1:1 (F).

Mentions: The expression levels of the 27 029 genes predicted by Cufflinks were used for global transcriptome profiling. Transcriptomes were compared pair-wise, i.e. male antennae vs. female antennae; male terminal abdomen vs. female terminal abdomen; male antennae vs. male terminal abdomen; and female antennae vs. female terminal abdomen. The male and female antennal transcriptomes had very similar global expression profiles, whereas male and female terminal abdomens were more different, both from each other as well as from the two antennal transcriptomes (Figure 1). When divergence based on FPKM values was analyzed using Jensen-Shannon (JS) distance, male and female antennae showed a low level of differentiation (a JS distance of only ca. 0.09). In contrast, the distances in all other pair-wise comparisons were larger, ranging from ca. 0.15 to 0.19 (Figure 1A). The global expression profile similarity between male and female antennae, and their distinctiveness from the other transcriptomes were confirmed in a principle component analysis (Figure 1B), and in pair-wise regression analyses. The latter analyses indicated that the female and male terminal abdominal segments had an overall higher expression than the female and male antennae, respectively (female antennae vs. female terminal abdomen: regression slope coefficient = 0.57, R2 = 0.51, Figure 1C; male antennae vs. male terminal abdomen: slope = 0.78, R2 = 0.64, Figure 1D). The male antennae had a similar global expression profile as the female antennae, as shown by a close to 1:1 relationship between the expression levels (slope = 0.97, R2 = 0.90, Figure 1E). In general, higher expression was found in the female terminal abdomen as compared to the male terminal abdomen (slope = 0.66, R2 = 0.61, Figure 1F).


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)

Comparison of global transcriptome expression profiles. The overall expression levels of the 27 029 genes predicted from the four transcriptomes were compared using Jensen-Shannon (JS) distance (A) and principle component analysis (B), both indicating the high similarity between the male and female antennal transcriptomes. In (B), PC 1 and PC 2 explained 55.8% and 32.2% respectively of the overall gene expression level variation in the four transcriptomes (black dots represent the predicted genes). Both the direction and length (length = within-transcriptome variation) of the eigenvectors (red arrows) show that the male and female antennal transcriptomes had highly similar variation in expression levels, both in relation to PC 1 and PC 2. In contrast, the variation in expression levels differed between the two terminal abdominal transcriptomes, which were also different from the two antennal transcriptomes (as indicated by the different lengths and directions of the eigenvectors). The difference between transcriptomes was explained (mainly) by the expression variation encompassed by PC 2 (i.e. as shown by the position of the four arrow heads). In addition, 1:1 plots (dashed line = 1:1 relationship) in combination with linear regression analyses (blue solid lines) were used to compare transcriptomes pair-wise. The female and male terminal abdomen both had an overall higher expression of the predicted genes compared to the antennae of females (C) and males (D), respectively. As indicated by the slope coefficients and relatively low R2 values, the expression did not follow a 1:1 relationship in these comparisons. In contrast, expression in the male antennae was similar to that in the female antennae, following a close to 1:1 relationship (E). Finally, the female terminal abdomen had an overall higher expression than the male terminal abdomen, i.e. the relationship between the two transcriptomes was relatively far from 1:1 (F).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Comparison of global transcriptome expression profiles. The overall expression levels of the 27 029 genes predicted from the four transcriptomes were compared using Jensen-Shannon (JS) distance (A) and principle component analysis (B), both indicating the high similarity between the male and female antennal transcriptomes. In (B), PC 1 and PC 2 explained 55.8% and 32.2% respectively of the overall gene expression level variation in the four transcriptomes (black dots represent the predicted genes). Both the direction and length (length = within-transcriptome variation) of the eigenvectors (red arrows) show that the male and female antennal transcriptomes had highly similar variation in expression levels, both in relation to PC 1 and PC 2. In contrast, the variation in expression levels differed between the two terminal abdominal transcriptomes, which were also different from the two antennal transcriptomes (as indicated by the different lengths and directions of the eigenvectors). The difference between transcriptomes was explained (mainly) by the expression variation encompassed by PC 2 (i.e. as shown by the position of the four arrow heads). In addition, 1:1 plots (dashed line = 1:1 relationship) in combination with linear regression analyses (blue solid lines) were used to compare transcriptomes pair-wise. The female and male terminal abdomen both had an overall higher expression of the predicted genes compared to the antennae of females (C) and males (D), respectively. As indicated by the slope coefficients and relatively low R2 values, the expression did not follow a 1:1 relationship in these comparisons. In contrast, expression in the male antennae was similar to that in the female antennae, following a close to 1:1 relationship (E). Finally, the female terminal abdomen had an overall higher expression than the male terminal abdomen, i.e. the relationship between the two transcriptomes was relatively far from 1:1 (F).
Mentions: The expression levels of the 27 029 genes predicted by Cufflinks were used for global transcriptome profiling. Transcriptomes were compared pair-wise, i.e. male antennae vs. female antennae; male terminal abdomen vs. female terminal abdomen; male antennae vs. male terminal abdomen; and female antennae vs. female terminal abdomen. The male and female antennal transcriptomes had very similar global expression profiles, whereas male and female terminal abdomens were more different, both from each other as well as from the two antennal transcriptomes (Figure 1). When divergence based on FPKM values was analyzed using Jensen-Shannon (JS) distance, male and female antennae showed a low level of differentiation (a JS distance of only ca. 0.09). In contrast, the distances in all other pair-wise comparisons were larger, ranging from ca. 0.15 to 0.19 (Figure 1A). The global expression profile similarity between male and female antennae, and their distinctiveness from the other transcriptomes were confirmed in a principle component analysis (Figure 1B), and in pair-wise regression analyses. The latter analyses indicated that the female and male terminal abdominal segments had an overall higher expression than the female and male antennae, respectively (female antennae vs. female terminal abdomen: regression slope coefficient = 0.57, R2 = 0.51, Figure 1C; male antennae vs. male terminal abdomen: slope = 0.78, R2 = 0.64, Figure 1D). The male antennae had a similar global expression profile as the female antennae, as shown by a close to 1:1 relationship between the expression levels (slope = 0.97, R2 = 0.90, Figure 1E). In general, higher expression was found in the female terminal abdomen as compared to the male terminal abdomen (slope = 0.66, R2 = 0.61, Figure 1F).

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