Abstract
For most organisms, chemosensation is critical for survival and is mediated by large families of chemoreceptor proteins, whose expression must be tuned appropriately to changes in the chemical environment. We asked whether expression of chemoreceptor genes that are clustered in the genome would be regulated independently; whether expression of certain chemoreceptor genes would be especially sensitive to environmental changes; whether groups of chemoreceptor genes undergo coordinated rexpression; and how plastic the expression of chemoreceptor genes is with regard to sex, development, reproductive state, and social context. To answer these questions we used Drosophila melanogaster, because its chemosensory systems are well characterized and both the genotype and environment can be controlled precisely. Using customized cDNA microarrays, we showed that chemoreceptor genes that are clustered in the genome undergo independent transcriptional regulation at different developmental stages and between sexes. Expression of distinct subgroups of chemoreceptor genes is sensitive to reproductive state and social interactions. Furthermore, exposure of flies only to odor of the opposite sex results in altered transcript abundance of chemoreceptor genes. These genes are distinct from those that show transcriptional plasticity when flies are allowed physical contact with same or opposite sex members. We analyzed covariance in transcript abundance of chemosensory genes across all environmental conditions and found that they segregated into 20 relatively small, biologically relevant modules of highly correlated transcripts. This finely pixilated modular organization of the chemosensory subgenome enables fine tuning of the expression of the chemoreceptor repertoire in response to ecologically relevant environmental and physiological conditions.
Highlights
Responses to the chemical environment play an important role in animal survival, as chemical cues direct foraging behavior and food selection, predator avoidance, and, in insects, host plant recognition for oviposition and larval feeding
To assess to what extent transcription of chemosensory genes responds to changing conditions, we constructed cDNA expression arrays that represent 50 Odorant binding protein (Obp), 59 Odorant receptor (Or), and 59 Gustatory receptor (Gr) genes, four genes that encode other antenna-specific proteins, and four control genes
We found enrichment in module 15 of a transcription factor binding site for mirr shared by Obp83g and Obp99b (P = 0.03), in module enrichment of a transcription factor binding site for pros shared by a5 and Or22b (P = 0.01), and in module enrichment of a transcription factor binding site for Abd-B shared by Or49b, Gr64d, and Gr93a (P = 0.00035)
Summary
Responses to the chemical environment play an important role in animal survival, as chemical cues direct foraging behavior and food selection, predator avoidance, and, in insects, host plant recognition for oviposition and larval feeding. As a consequence of the profound importance of chemosensation for survival and reproduction, several large families of chemosensory genes have evolved through repeated processes of gene duplication and diversification [1,2,3,4], including genes that encode odorant receptors (Ors) [4,5,6,7,8], gustatory receptors (Grs) [4,9], and, in insects, odorant binding proteins (Obps) [10,11,12]. A 4 bp insertion in the upstream regulatory region of the D. sechellia Obp57e gene eliminates expression of this odorant binding protein, which elicits avoidance of the Morinda fruit in Drosophila species in which the gene is intact [16]
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