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Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes.

Ellegren H, Hultin-Rosenberg L, Brunström B, Dencker L, Kultima K, Scholz B - BMC Biol. (2007)

Bottom Line: The distribution of male-to-female fold-change values for Z chromosome genes is wide and has a mean of 1.4-1.6, which is consistent with absence of dosage compensation and sex-specific feedback regulation of gene expression at individual loci.Intriguingly, without global dosage compensation, the female chicken has significantly lower expression levels of Z-linked compared to autosomal genes, which is not the case in male birds.The pronounced sex difference in gene expression is likely to contribute to sexual dimorphism among birds, and potentially has implication to avian sex determination.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Evolutionary Biology, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, Sweden. Hans.Ellegren@ebc.uu.se

ABSTRACT

Background: The contrasting dose of sex chromosomes in males and females potentially introduces a large-scale imbalance in levels of gene expression between sexes, and between sex chromosomes and autosomes. In many organisms, dosage compensation has thus evolved to equalize sex-linked gene expression in males and females. In mammals this is achieved by X chromosome inactivation and in flies and worms by up- or down-regulation of X-linked expression, respectively. While otherwise widespread in systems with heteromorphic sex chromosomes, the case of dosage compensation in birds (males ZZ, females ZW) remains an unsolved enigma.

Results: Here, we use a microarray approach to show that male chicken embryos generally express higher levels of Z-linked genes than female birds, both in soma and in gonads. The distribution of male-to-female fold-change values for Z chromosome genes is wide and has a mean of 1.4-1.6, which is consistent with absence of dosage compensation and sex-specific feedback regulation of gene expression at individual loci. Intriguingly, without global dosage compensation, the female chicken has significantly lower expression levels of Z-linked compared to autosomal genes, which is not the case in male birds.

Conclusion: The pronounced sex difference in gene expression is likely to contribute to sexual dimorphism among birds, and potentially has implication to avian sex determination. Importantly, this report, together with a recent study of sex-biased expression in somatic tissue of chicken, demonstrates the first example of an organism with a lack of global dosage compensation, providing an unexpected case of a viable system with large-scale imbalance in gene expression between sexes.

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Similar levels of male and female autosomal, and male but not female Z-linked, gene expression. Histograms of mean log2 hybridization intensities for all genes, and unbiased genes (<1.2 fold-change), in (a) soma and (b) gonads. Male autosomal genes are shown in blue and female genes in red, whereas Z-linked genes in males are shown in yellow and in females in green. Error bars correspond to 95% confidence intervals.
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Figure 4: Similar levels of male and female autosomal, and male but not female Z-linked, gene expression. Histograms of mean log2 hybridization intensities for all genes, and unbiased genes (<1.2 fold-change), in (a) soma and (b) gonads. Male autosomal genes are shown in blue and female genes in red, whereas Z-linked genes in males are shown in yellow and in females in green. Error bars correspond to 95% confidence intervals.

Mentions: It is of interest to specifically study the expression levels of sexually unbiased genes on the Z chromosome because this could potentially indicate how differences in sex-linked gene dose are being dealt with. Unbiased Z chromosome genes are expressed at lower levels than unbiased autosomal genes, for somatic tissue significantly so (≈ 1.8 times higher expression on autosomes than on the Z chromosome, p < 0.001) (Figure 4). This suggests that for unbiased Z-linked genes the major mechanism for sex-specific regulation is reduction of male expression. Furthermore, a number of gene ontology (GO) terms are significantly over-represented among unbiased Z chromosome genes (Additional file 5), while other terms are over-represented among those that are sex-biased (Additional file 6). For instance, genes with equal expression in males and females are in all tissues enriched for basic cellular functions such as regulation of metabolism and physiological processes.


Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes.

Ellegren H, Hultin-Rosenberg L, Brunström B, Dencker L, Kultima K, Scholz B - BMC Biol. (2007)

Similar levels of male and female autosomal, and male but not female Z-linked, gene expression. Histograms of mean log2 hybridization intensities for all genes, and unbiased genes (<1.2 fold-change), in (a) soma and (b) gonads. Male autosomal genes are shown in blue and female genes in red, whereas Z-linked genes in males are shown in yellow and in females in green. Error bars correspond to 95% confidence intervals.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2099419&req=5

Figure 4: Similar levels of male and female autosomal, and male but not female Z-linked, gene expression. Histograms of mean log2 hybridization intensities for all genes, and unbiased genes (<1.2 fold-change), in (a) soma and (b) gonads. Male autosomal genes are shown in blue and female genes in red, whereas Z-linked genes in males are shown in yellow and in females in green. Error bars correspond to 95% confidence intervals.
Mentions: It is of interest to specifically study the expression levels of sexually unbiased genes on the Z chromosome because this could potentially indicate how differences in sex-linked gene dose are being dealt with. Unbiased Z chromosome genes are expressed at lower levels than unbiased autosomal genes, for somatic tissue significantly so (≈ 1.8 times higher expression on autosomes than on the Z chromosome, p < 0.001) (Figure 4). This suggests that for unbiased Z-linked genes the major mechanism for sex-specific regulation is reduction of male expression. Furthermore, a number of gene ontology (GO) terms are significantly over-represented among unbiased Z chromosome genes (Additional file 5), while other terms are over-represented among those that are sex-biased (Additional file 6). For instance, genes with equal expression in males and females are in all tissues enriched for basic cellular functions such as regulation of metabolism and physiological processes.

Bottom Line: The distribution of male-to-female fold-change values for Z chromosome genes is wide and has a mean of 1.4-1.6, which is consistent with absence of dosage compensation and sex-specific feedback regulation of gene expression at individual loci.Intriguingly, without global dosage compensation, the female chicken has significantly lower expression levels of Z-linked compared to autosomal genes, which is not the case in male birds.The pronounced sex difference in gene expression is likely to contribute to sexual dimorphism among birds, and potentially has implication to avian sex determination.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Evolutionary Biology, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, Sweden. Hans.Ellegren@ebc.uu.se

ABSTRACT

Background: The contrasting dose of sex chromosomes in males and females potentially introduces a large-scale imbalance in levels of gene expression between sexes, and between sex chromosomes and autosomes. In many organisms, dosage compensation has thus evolved to equalize sex-linked gene expression in males and females. In mammals this is achieved by X chromosome inactivation and in flies and worms by up- or down-regulation of X-linked expression, respectively. While otherwise widespread in systems with heteromorphic sex chromosomes, the case of dosage compensation in birds (males ZZ, females ZW) remains an unsolved enigma.

Results: Here, we use a microarray approach to show that male chicken embryos generally express higher levels of Z-linked genes than female birds, both in soma and in gonads. The distribution of male-to-female fold-change values for Z chromosome genes is wide and has a mean of 1.4-1.6, which is consistent with absence of dosage compensation and sex-specific feedback regulation of gene expression at individual loci. Intriguingly, without global dosage compensation, the female chicken has significantly lower expression levels of Z-linked compared to autosomal genes, which is not the case in male birds.

Conclusion: The pronounced sex difference in gene expression is likely to contribute to sexual dimorphism among birds, and potentially has implication to avian sex determination. Importantly, this report, together with a recent study of sex-biased expression in somatic tissue of chicken, demonstrates the first example of an organism with a lack of global dosage compensation, providing an unexpected case of a viable system with large-scale imbalance in gene expression between sexes.

Show MeSH
Related in: MedlinePlus