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. 2010 Dec;186(4):1475-85.
doi: 10.1534/genetics.110.123166. Epub 2010 Sep 24.

Natural variation, functional pleiotropy and transcriptional contexts of odorant binding protein genes in Drosophila melanogaster

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Natural variation, functional pleiotropy and transcriptional contexts of odorant binding protein genes in Drosophila melanogaster

Gunjan H Arya et al. Genetics. 2010 Dec.

Abstract

How functional diversification affects the organization of the transcriptome is a central question in systems genetics. To explore this issue, we sequenced all six Odorant binding protein (Obp) genes located on the X chromosome, four of which occur as a cluster, in 219 inbred wild-derived lines of Drosophila melanogaster and tested for associations between genetic and phenotypic variation at the organismal and transcriptional level. We observed polymorphisms in Obp8a, Obp19a, Obp19b, and Obp19c associated with variation in olfactory responses and polymorphisms in Obp19d associated with variation in life span. We inferred the transcriptional context, or "niche," of each gene by identifying expression polymorphisms where genetic variation in these Obp genes was associated with variation in expression of transcripts genetically correlated to each Obp gene. All six Obp genes occupied a distinct transcriptional niche. Gene ontology enrichment analysis revealed associations of different Obp transcriptional niches with olfactory behavior, synaptic transmission, detection of signals regulating tissue development and apoptosis, postmating behavior and oviposition, and nutrient sensing. Our results show that diversification of the Obp family has organized distinct transcriptional niches that reflect their acquisition of additional functions.

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Figures

F<sc>igure</sc> 1.—
Figure 1.—
Phenotypic variation in mean olfactory responses to benzaldehyde (A), acetophenone (B), hexanol (C), hexanal (D), and longevity (E) among 219 inbred wild-derived lines of D. melanogaster. Mean phenotypic values for each line and sex are given in Table S1. Genetic correlations among the traits are listed in Table S5.
F<sc>igure</sc> 2.—
Figure 2.—
Associations between polymorphisms in Obp8a, Obp18a, Obp19a, Obp19b, Obp19c, and Obp19d and variation in olfactory responses and longevity. The red horizontal line represents the significance threshold determined by Bonferroni correction for the number of markers tested. The arrow indicates an association with a marker in Obp19a and variation in response to acetophenone that does not pass the Bonferroni correction but does pass the significance threshold determined by permutation. The diagrams below the graphs indicate the degree of linkage disequilibrium between markers, as measured by r2. The structures of the genes and positions of the polymorphic markers are indicated schematically with red boxes representing 5′-untranslated regions, blue boxes showing exons, and white boxes showing 3′-untranslated regions. For each marker, a circle indicates a single-nucleotide polymorphism (SNP) and a triangle indicates an indel.
F<sc>igure</sc> 3.—
Figure 3.—
Transcript abundance comparisons between genotypic classes of Obp8a and Obp19b. Transcript levels were measured by RT–PCR of five lines with high and five lines with low response scores to hexanol. Data are standardized to Gapdh and presented as averaged normalized CT values. Note that averaged normalized CT values are inversely proportional to transcript abundance. (A) Transcript levels of Obp8a in lines homozygous for the deletion (D) or insertion (I) polymorphisms at I281D, measured for males and females separately. (B) Transcript levels of Obp19b in lines homozygous for alternative alleles (G and T) at T1100G, measured for sexes pooled. Red bars indicate higher olfactory response values, and blue bars indicate lower olfactory response values.
F<sc>igure</sc> 4.—
Figure 4.—
Transcriptional niches of six Obp genes. The diagrams depict transcriptional niches of genetically correlated transcripts associated with polymorphisms after accounting for sexual dimorphism in Obp8a (A), Obp18a (B), Obp19a (C), Obp19b (D), Obp19c (E), and Obp19d (F). Black arrows indicate a marker–transcript association of P ≤ 0.00001, dark gray arrows indicate P ≤ 0.0001, and light gray arrows indicate P ≤ 0.001. Transcripts that are significantly associated with a phenotype after regression analysis (P < 0.01) are in colors other than light gray (dark blue, starvation resistance; maroon, copulation latency; green, longevity; purple, response to hexanol; turquoise, response to hexanal; orange, response to benzaldehyde; light blue, response to acetophenone). Transcript profiles and phenotypic values for starvation stress resistance and copulation latency were published previously (Ayroles et al. 2009). See also Table S4.
F<sc>igure</sc> 5.—
Figure 5.—
Characterization of transcriptional niches. (A) Gene ontology categories enriched within Obp-centered transcriptional niches (P < 0.05). Data are based on level 4 of the DAVID analysis (Dennis et al. 2003). GO categories in the same color font are related in the GO hierarchy (black font indicates unrelated categories). (B) Expression of Obp8a, Obp18a, Obp19a, Obp19b, Obp19c, and Obp19d in different fly tissues according to FlyAtlas (Chintapalli et al. 2007). (C) Expression of transcripts in niches associated with Obp8a, Obp18a, Obp19a, Obp19b, Obp19c, and Obp19d in different fly tissues according to FlyAtlas (Chintapalli et al. 2007).

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