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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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Comparison of expression profiles of the 228 chemosensory genes. Expression level profiles of the 228 genes involved in olfaction or taste in the four tissues were compared using (A) Jensen-Shannon (JS) distance, and (B) principle component analysis. In contrast to the global analysis (Figure 1), the female and male terminal abdomen tissues had the most similar expression profiles, whereas the male and female antennae were more different from each other. In (B), PC 1 and PC 2 explained 66.0% and 20.1% respectively of the overall expression level variation among the chemosensory genes in the four tissues. Both the direction and length (length = within-transcriptome variation) of the eigenvectors (red arrows) indicate that the chemosensory genes (black dots) in the male and female terminal abdominal tissues 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 male and female antennae, and these tissues were also different from the terminal abdominal tissues (as indicated by differences in length and direction of the eigenvectors). The difference in expression of the chemosensory genes between the four tissues was explained (mainly) by the 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) indicate an overall up-regulation of expression of the 228 genes in the antennae of both sexes, compared to the female (C) or male terminal abdomen (D), respectively. The antennae of males and females expressed many of these genes differently (E). Overall, the female and male terminal abdomen had low expression of these genes and the expression was closer to a 1:1 relationship than in the other pair-wise comparisons (F).
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Figure 2: Comparison of expression profiles of the 228 chemosensory genes. Expression level profiles of the 228 genes involved in olfaction or taste in the four tissues were compared using (A) Jensen-Shannon (JS) distance, and (B) principle component analysis. In contrast to the global analysis (Figure 1), the female and male terminal abdomen tissues had the most similar expression profiles, whereas the male and female antennae were more different from each other. In (B), PC 1 and PC 2 explained 66.0% and 20.1% respectively of the overall expression level variation among the chemosensory genes in the four tissues. Both the direction and length (length = within-transcriptome variation) of the eigenvectors (red arrows) indicate that the chemosensory genes (black dots) in the male and female terminal abdominal tissues 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 male and female antennae, and these tissues were also different from the terminal abdominal tissues (as indicated by differences in length and direction of the eigenvectors). The difference in expression of the chemosensory genes between the four tissues was explained (mainly) by the 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) indicate an overall up-regulation of expression of the 228 genes in the antennae of both sexes, compared to the female (C) or male terminal abdomen (D), respectively. The antennae of males and females expressed many of these genes differently (E). Overall, the female and male terminal abdomen had low expression of these genes and the expression was closer to a 1:1 relationship than in the other pair-wise comparisons (F).

Mentions: In contrast to the global comparison where the male and female antennal transcriptomes demonstrated the most similar expression profiles, the female and male terminal abdomens had the most similar profiles when only the 228 chemosensory-related genes were included (Figure 2A, B). Regression analysis demonstrated a close to 1:1 relationship between the expression levels of the chemosensory genes in the two terminal abdominal tissues (regression slope coefficient = 0.98, R2 = 0.80, Figure 2F), although the overall expression level was low in these tissues. Most of the chemosensory genes had the highest expression in the female or male antennae as compared to the female or male terminal abdomens (female antennae vs. female terminal abdomen: slope = 1.35, R2 = 0.42, Figure 2C; male antennae vs. male terminal abdomen: slope = 1.42, R2 = 0.53, Figure 2D), respectively, although a few genes had higher expression in the terminal abdominal tissues (see below for details). In contrast to the global analysis, the expression profiles of the male and female antennal tissues were clearly different when only the 228 genes related to chemosensation were included in the analysis (slope = 0.80, R2 = 0.60, Figure 2E). FPKM values for the chemosensory genes in the four tissues are presented in Additional file6.


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 expression profiles of the 228 chemosensory genes. Expression level profiles of the 228 genes involved in olfaction or taste in the four tissues were compared using (A) Jensen-Shannon (JS) distance, and (B) principle component analysis. In contrast to the global analysis (Figure 1), the female and male terminal abdomen tissues had the most similar expression profiles, whereas the male and female antennae were more different from each other. In (B), PC 1 and PC 2 explained 66.0% and 20.1% respectively of the overall expression level variation among the chemosensory genes in the four tissues. Both the direction and length (length = within-transcriptome variation) of the eigenvectors (red arrows) indicate that the chemosensory genes (black dots) in the male and female terminal abdominal tissues 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 male and female antennae, and these tissues were also different from the terminal abdominal tissues (as indicated by differences in length and direction of the eigenvectors). The difference in expression of the chemosensory genes between the four tissues was explained (mainly) by the 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) indicate an overall up-regulation of expression of the 228 genes in the antennae of both sexes, compared to the female (C) or male terminal abdomen (D), respectively. The antennae of males and females expressed many of these genes differently (E). Overall, the female and male terminal abdomen had low expression of these genes and the expression was closer to a 1:1 relationship than in the other pair-wise comparisons (F).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Comparison of expression profiles of the 228 chemosensory genes. Expression level profiles of the 228 genes involved in olfaction or taste in the four tissues were compared using (A) Jensen-Shannon (JS) distance, and (B) principle component analysis. In contrast to the global analysis (Figure 1), the female and male terminal abdomen tissues had the most similar expression profiles, whereas the male and female antennae were more different from each other. In (B), PC 1 and PC 2 explained 66.0% and 20.1% respectively of the overall expression level variation among the chemosensory genes in the four tissues. Both the direction and length (length = within-transcriptome variation) of the eigenvectors (red arrows) indicate that the chemosensory genes (black dots) in the male and female terminal abdominal tissues 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 male and female antennae, and these tissues were also different from the terminal abdominal tissues (as indicated by differences in length and direction of the eigenvectors). The difference in expression of the chemosensory genes between the four tissues was explained (mainly) by the 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) indicate an overall up-regulation of expression of the 228 genes in the antennae of both sexes, compared to the female (C) or male terminal abdomen (D), respectively. The antennae of males and females expressed many of these genes differently (E). Overall, the female and male terminal abdomen had low expression of these genes and the expression was closer to a 1:1 relationship than in the other pair-wise comparisons (F).
Mentions: In contrast to the global comparison where the male and female antennal transcriptomes demonstrated the most similar expression profiles, the female and male terminal abdomens had the most similar profiles when only the 228 chemosensory-related genes were included (Figure 2A, B). Regression analysis demonstrated a close to 1:1 relationship between the expression levels of the chemosensory genes in the two terminal abdominal tissues (regression slope coefficient = 0.98, R2 = 0.80, Figure 2F), although the overall expression level was low in these tissues. Most of the chemosensory genes had the highest expression in the female or male antennae as compared to the female or male terminal abdomens (female antennae vs. female terminal abdomen: slope = 1.35, R2 = 0.42, Figure 2C; male antennae vs. male terminal abdomen: slope = 1.42, R2 = 0.53, Figure 2D), respectively, although a few genes had higher expression in the terminal abdominal tissues (see below for details). In contrast to the global analysis, the expression profiles of the male and female antennal tissues were clearly different when only the 228 genes related to chemosensation were included in the analysis (slope = 0.80, R2 = 0.60, Figure 2E). FPKM values for the chemosensory genes in the four tissues are presented in Additional file6.

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