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Dosage Compensation and the Distribution of Sex-Biased Gene Expression in Drosophila: Considerations and Genomic Constraints - PubMed

Dosage Compensation and the Distribution of Sex-Biased Gene Expression in Drosophila: Considerations and Genomic Constraints

Miguel Gallach et al. J Mol Evol. 2016 May.

Abstract

Several studies in Drosophila have shown a paucity of male-biased genes (i.e., genes that express higher in males than in females) on the X chromosome. Dosage compensation (DC) is a regulatory mechanism of gene expression triggered in males that hypertranscribes the X-linked genes to the level of transcription in females. There are currently two different hypotheses about the effects of DC on the distribution of male-biased genes: (1) it might limit male-expression level, or (2) it might interfere with the male upregulation of gene expression. Here, we used previously published gene expression datasets to reevaluate both hypotheses and introduce a mutually exclusive prediction that helped us to reject the hypothesis that the paucity of male-biased genes in the X chromosome is due to a limit in the male-expression level. Our analysis also uncovers unanticipated details about how DC interferes with the genomic distribution of both, male-biased and female-biased genes. We suggest that DC actually interferes with female downregulation of gene expression and not male upregulation, as previously suggested.

Keywords: Dosage compensation; Drosophila; Sex-biased gene expression; X chromosome.

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Figures

Fig. 1
Fig. 1

Percentages of genes with high, medium and low expression levels located in bound (black) and unbound regions (gray) of the X chromosome. Expression data correspond to whole flies (first row a–c), gonadectomized flies (second row d–f), and gonads (third row g–i). All dataset comparisons (dashed lines) and paired comparisons (continuous lines) were tested against the distribution of unbiased genes using a Chi squared test with 5 and 1 degrees of freedom, respectively. H, M and L refer to high, medium and low gene expression, respectively. B and UB refers to bound and unbound genes, respectively. P < 0.05 (asterisk), P < 0.01 (double asterisk), and P < 0.001 (triple asterisk). Data from Parisi et al. (2003)

Fig. 2
Fig. 2

Male/female expression ratio for X-linked genes and autosomal genes. Only male-biased genes are considered. Wilcoxon rank-sum test was performed for each pair of data. P < 0.001, each

Fig. 3
Fig. 3

Expression level of male-biased genes (blue), female-biased genes (red) and unbiased genes (gray) located in bound regions (B), unbound regions (U) and autosomes (A). Paired comparisons were tested using the Wilcoxon rank-sum test. Only significant comparisons are indicated. P < 0.05 (asterisk), P < 0.01 (double asterisk), and P < 0.001 (triple asterisk) (Color figure online)

Fig. 4
Fig. 4

Correlation between the sex bias level in the sex with higher expression and the gene expression level in the opposite sex. In gonadectomized flies (soma, first four panels) only male-biased genes located in the autosomes correlate with the expression level in females: the lower the expression level in females, the higher the difference between males and females. This effect is however minimal compared to gonads (last four panels), where genes linked to the autosomes that express low in females reach the highest male-biased levels. In addition, it can be seen that the effect of the gene expression level in the opposite sex over the sex bias level is insignificant for genes bound (dots) and unbound by the DCC (open squares). Blue dots male-biased genes. Red dots female-biased genes. Black lines correspond to the fitted functions (Color figure online)

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