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Lack of global meiotic sex chromosome inactivation, and paucity of tissue-specific gene expression on the Drosophila X chromosome.

Mikhaylova LM, Nurminsky DI - BMC Biol. (2011)

Bottom Line: Bioinformatics analysis shows that while tissue-specific genes often bind silencing-associated factors in embryonic and cultured cells, this trend is less prominent for the X-linked genes.Our data show that the global meiotic inactivation of the X chromosome does not occur in Drosophila.This effect, probably caused by dosage compensation counteracting repression of the X-linked genes, may be the cause of the exodus of highly tissue-biased genes to the autosomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Anatomy and Cellular Biology, Tufts University School of Medicine, Boston, USA.

ABSTRACT

Background: Paucity of male-biased genes on the Drosophila X chromosome is a well-established phenomenon, thought to be specifically linked to the role of these genes in reproduction and/or their expression in the meiotic male germline. In particular, meiotic sex chromosome inactivation (MSCI) has been widely considered a driving force behind depletion of spermatocyte-biased X-linked genes in Drosophila by analogy with mammals, even though the existence of global MCSI in Drosophila has not been proven.

Results: Microarray-based study and qRT-PCR analyses show that the dynamics of gene expression during testis development are very similar between X-linked and autosomal genes, with both showing transcriptional activation concomitant with meiosis. However, the genes showing at least ten-fold expression bias toward testis are significantly underrepresented on the X chromosome. Intriguingly, the genes with similar expression bias toward tissues other than testis, even those not apparently associated with reproduction, are also strongly underrepresented on the X. Bioinformatics analysis shows that while tissue-specific genes often bind silencing-associated factors in embryonic and cultured cells, this trend is less prominent for the X-linked genes.

Conclusions: Our data show that the global meiotic inactivation of the X chromosome does not occur in Drosophila. Paucity of testis-biased genes on the X appears not to be linked to reproduction or germline-specific events, but rather reflects a general underrepresentation of tissue-biased genes on this chromosome. Our analyses suggest that the activation/repression switch mechanisms that probably orchestrate the highly-biased expression of tissue-specific genes are generally not efficient on the X chromosome. This effect, probably caused by dosage compensation counteracting repression of the X-linked genes, may be the cause of the exodus of highly tissue-biased genes to the autosomes.

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Paucity of X-linked genes with high expression bias toward testis. The testis::somatic tissue ratio of microarray signal intensities, observed between adult testis and a panel of somatic tissues [24], serves as a measure of testis bias of gene expression and is shown at bottom. Bars indicate proportion of genes up-regulated in testis development in the four bias categories. Orange bars, X-linked genes; blue bars, autosomal genes.
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Figure 3: Paucity of X-linked genes with high expression bias toward testis. The testis::somatic tissue ratio of microarray signal intensities, observed between adult testis and a panel of somatic tissues [24], serves as a measure of testis bias of gene expression and is shown at bottom. Bars indicate proportion of genes up-regulated in testis development in the four bias categories. Orange bars, X-linked genes; blue bars, autosomal genes.

Mentions: Although we did observe numerous X-linked genes increasing their expression during testis development, previous reports showed a paucity of male-biased genes on the X [12-14]. To define the relationship between these two gene categories, we analyzed expression bias of the genes up-regulated in developing testes. Using published gene expression data [27], we compared microarray signals observed with adult testis-derived RNA to the signals obtained with RNA from a variety of somatic sources including accessory glands, brain, head, thoracicoabdominal ganglion, crop, midgut, hindgut, malpigian tubules of adults and larvae, ovary, salivary glands, and carcass. Conservatively, the minimal testis-to-somatic tissue signal ratio across the entire panel of analyzed samples was defined as a measure of bias of gene expression toward testis. This analysis identified about 50% of the autosomal genes up-regulated in testis development as highly testis-biased (minimal testis::somatic tissue signal ratio ≥10) (Figure 3, blue bars). Strikingly, highly-biased genes constitute less than one-quarter of the X-linked genes, and this difference from the autosomal genes is highly significant (χ2 test, P = 3 × 10-10) (Figure 3, orange bars). Apparently, it is the cohort of highly testis-biased genes that is depleted in the pool of the X-linked genes up-regulated in testis development. As a result, on average the X-linked genes show a weaker testis bias of expression than their autosomal counterparts.


Lack of global meiotic sex chromosome inactivation, and paucity of tissue-specific gene expression on the Drosophila X chromosome.

Mikhaylova LM, Nurminsky DI - BMC Biol. (2011)

Paucity of X-linked genes with high expression bias toward testis. The testis::somatic tissue ratio of microarray signal intensities, observed between adult testis and a panel of somatic tissues [24], serves as a measure of testis bias of gene expression and is shown at bottom. Bars indicate proportion of genes up-regulated in testis development in the four bias categories. Orange bars, X-linked genes; blue bars, autosomal genes.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3104377&req=5

Figure 3: Paucity of X-linked genes with high expression bias toward testis. The testis::somatic tissue ratio of microarray signal intensities, observed between adult testis and a panel of somatic tissues [24], serves as a measure of testis bias of gene expression and is shown at bottom. Bars indicate proportion of genes up-regulated in testis development in the four bias categories. Orange bars, X-linked genes; blue bars, autosomal genes.
Mentions: Although we did observe numerous X-linked genes increasing their expression during testis development, previous reports showed a paucity of male-biased genes on the X [12-14]. To define the relationship between these two gene categories, we analyzed expression bias of the genes up-regulated in developing testes. Using published gene expression data [27], we compared microarray signals observed with adult testis-derived RNA to the signals obtained with RNA from a variety of somatic sources including accessory glands, brain, head, thoracicoabdominal ganglion, crop, midgut, hindgut, malpigian tubules of adults and larvae, ovary, salivary glands, and carcass. Conservatively, the minimal testis-to-somatic tissue signal ratio across the entire panel of analyzed samples was defined as a measure of bias of gene expression toward testis. This analysis identified about 50% of the autosomal genes up-regulated in testis development as highly testis-biased (minimal testis::somatic tissue signal ratio ≥10) (Figure 3, blue bars). Strikingly, highly-biased genes constitute less than one-quarter of the X-linked genes, and this difference from the autosomal genes is highly significant (χ2 test, P = 3 × 10-10) (Figure 3, orange bars). Apparently, it is the cohort of highly testis-biased genes that is depleted in the pool of the X-linked genes up-regulated in testis development. As a result, on average the X-linked genes show a weaker testis bias of expression than their autosomal counterparts.

Bottom Line: Bioinformatics analysis shows that while tissue-specific genes often bind silencing-associated factors in embryonic and cultured cells, this trend is less prominent for the X-linked genes.Our data show that the global meiotic inactivation of the X chromosome does not occur in Drosophila.This effect, probably caused by dosage compensation counteracting repression of the X-linked genes, may be the cause of the exodus of highly tissue-biased genes to the autosomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Anatomy and Cellular Biology, Tufts University School of Medicine, Boston, USA.

ABSTRACT

Background: Paucity of male-biased genes on the Drosophila X chromosome is a well-established phenomenon, thought to be specifically linked to the role of these genes in reproduction and/or their expression in the meiotic male germline. In particular, meiotic sex chromosome inactivation (MSCI) has been widely considered a driving force behind depletion of spermatocyte-biased X-linked genes in Drosophila by analogy with mammals, even though the existence of global MCSI in Drosophila has not been proven.

Results: Microarray-based study and qRT-PCR analyses show that the dynamics of gene expression during testis development are very similar between X-linked and autosomal genes, with both showing transcriptional activation concomitant with meiosis. However, the genes showing at least ten-fold expression bias toward testis are significantly underrepresented on the X chromosome. Intriguingly, the genes with similar expression bias toward tissues other than testis, even those not apparently associated with reproduction, are also strongly underrepresented on the X. Bioinformatics analysis shows that while tissue-specific genes often bind silencing-associated factors in embryonic and cultured cells, this trend is less prominent for the X-linked genes.

Conclusions: Our data show that the global meiotic inactivation of the X chromosome does not occur in Drosophila. Paucity of testis-biased genes on the X appears not to be linked to reproduction or germline-specific events, but rather reflects a general underrepresentation of tissue-biased genes on this chromosome. Our analyses suggest that the activation/repression switch mechanisms that probably orchestrate the highly-biased expression of tissue-specific genes are generally not efficient on the X chromosome. This effect, probably caused by dosage compensation counteracting repression of the X-linked genes, may be the cause of the exodus of highly tissue-biased genes to the autosomes.

Show MeSH
Related in: MedlinePlus