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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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Highly tissue-biased genes show a skewed representation on the X chromosome. The ratio of microarray signal intensities observed between the tissue sample indicated at bottom including midgut, malpigian tubule, accessory gland, salivary gland, head, and ovary and a panel of other tissue samples [24] was used as a measure of tissue bias. The bars correspond to the frequencies of the genes on the X chromosome normalized against the genome averages, and are shown for the genes with at least two-fold expression bias toward indicated tissues (light gray), for the genes with at least five-fold bias (dark gray), and for highly biased genes with at least ten-fold bias (black).
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Figure 4: Highly tissue-biased genes show a skewed representation on the X chromosome. The ratio of microarray signal intensities observed between the tissue sample indicated at bottom including midgut, malpigian tubule, accessory gland, salivary gland, head, and ovary and a panel of other tissue samples [24] was used as a measure of tissue bias. The bars correspond to the frequencies of the genes on the X chromosome normalized against the genome averages, and are shown for the genes with at least two-fold expression bias toward indicated tissues (light gray), for the genes with at least five-fold bias (dark gray), and for highly biased genes with at least ten-fold bias (black).

Mentions: Our gene expression study on developing testes indicated that the paucity of testis-biased genes on the X chromosome is not caused by the spermatocyte-specific events. We therefore hypothesized that the underlying mechanisms may be not restricted to the male meiotic germline and instead could operate in diverse tissues, causing broad effects on tissue-biased expression. To test this suggestion, using the published gene expression dataset [27] we identified genes that show expression bias toward midgut, malpigian tubules, accessory gland, salivary gland, head, and ovary, using the same bioinformatics approach as described above for testis. We further determined whether the frequencies of the identified genes on the X chromosome deviated from the genome averages. We observed that the majority of the analyzed genes show the same trends that the testis-biased genes do: they are underrepresented on the X chromosome, and the higher the expression bias the stronger the underrepresentation (Figure 4). One important exception, however, was the ovary-biased gene set for which both trends were reversed. This finding is consistent with previous reports on the overrepresentation of female- and ovary-biased genes on the X [13,28], and indicates that the genes selectively expressed in the ovary are subject to unique selective pressures, probably owing to their female-beneficial sexually-antagonistic effects [7,29] and/or because of their peculiar regulation, as discussed below.


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)

Highly tissue-biased genes show a skewed representation on the X chromosome. The ratio of microarray signal intensities observed between the tissue sample indicated at bottom including midgut, malpigian tubule, accessory gland, salivary gland, head, and ovary and a panel of other tissue samples [24] was used as a measure of tissue bias. The bars correspond to the frequencies of the genes on the X chromosome normalized against the genome averages, and are shown for the genes with at least two-fold expression bias toward indicated tissues (light gray), for the genes with at least five-fold bias (dark gray), and for highly biased genes with at least ten-fold bias (black).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Highly tissue-biased genes show a skewed representation on the X chromosome. The ratio of microarray signal intensities observed between the tissue sample indicated at bottom including midgut, malpigian tubule, accessory gland, salivary gland, head, and ovary and a panel of other tissue samples [24] was used as a measure of tissue bias. The bars correspond to the frequencies of the genes on the X chromosome normalized against the genome averages, and are shown for the genes with at least two-fold expression bias toward indicated tissues (light gray), for the genes with at least five-fold bias (dark gray), and for highly biased genes with at least ten-fold bias (black).
Mentions: Our gene expression study on developing testes indicated that the paucity of testis-biased genes on the X chromosome is not caused by the spermatocyte-specific events. We therefore hypothesized that the underlying mechanisms may be not restricted to the male meiotic germline and instead could operate in diverse tissues, causing broad effects on tissue-biased expression. To test this suggestion, using the published gene expression dataset [27] we identified genes that show expression bias toward midgut, malpigian tubules, accessory gland, salivary gland, head, and ovary, using the same bioinformatics approach as described above for testis. We further determined whether the frequencies of the identified genes on the X chromosome deviated from the genome averages. We observed that the majority of the analyzed genes show the same trends that the testis-biased genes do: they are underrepresented on the X chromosome, and the higher the expression bias the stronger the underrepresentation (Figure 4). One important exception, however, was the ovary-biased gene set for which both trends were reversed. This finding is consistent with previous reports on the overrepresentation of female- and ovary-biased genes on the X [13,28], and indicates that the genes selectively expressed in the ovary are subject to unique selective pressures, probably owing to their female-beneficial sexually-antagonistic effects [7,29] and/or because of their peculiar regulation, as discussed below.

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