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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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Related in: MedlinePlus

Lack of global X-chromosome inactivation in developing testes. Expression of X-linked (orange) and autosomal (blue) genes was measured as signal intensity of corresponding microarray probes, after normalization. cDNAs hybridized to the microarrays were isolated from testes of either feeding (f) or wandering (w) larvae grown for the indicated number of days at 18°C. The analysis traces the first wave of germline differentiation; pupation indicative of the meiotic divisions occurred at day 11.
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Figure 2: Lack of global X-chromosome inactivation in developing testes. Expression of X-linked (orange) and autosomal (blue) genes was measured as signal intensity of corresponding microarray probes, after normalization. cDNAs hybridized to the microarrays were isolated from testes of either feeding (f) or wandering (w) larvae grown for the indicated number of days at 18°C. The analysis traces the first wave of germline differentiation; pupation indicative of the meiotic divisions occurred at day 11.

Mentions: To further support our findings by extending them to the majority of X-linked genes, we analyzed the global trends of X-linked gene expression during testis development using gene microarrays. To improve the resolution of the analysis, we cultured larvae at a lower temperature (18°C) and collected testes from feeding larvae at fourth, fifth, sixth and seventh days of development (Figure 2 dLf), and from wandering larvae at days seven and ten, just before the onset of pupation at days 11 to 12 (Figure 2, dLw). Throughout larval testis development, we did not find appreciable differences in expression between the X chromosome and autosomes (Figure 2, orange versus blue bars) or any substantial reduction in X-linked gene expression (Figure 2, orange bars), strengthening the hypothesis that the X chromosome is not affected by global MSCI in Drosophila, contrary to mammalian spermatogenesis.


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)

Lack of global X-chromosome inactivation in developing testes. Expression of X-linked (orange) and autosomal (blue) genes was measured as signal intensity of corresponding microarray probes, after normalization. cDNAs hybridized to the microarrays were isolated from testes of either feeding (f) or wandering (w) larvae grown for the indicated number of days at 18°C. The analysis traces the first wave of germline differentiation; pupation indicative of the meiotic divisions occurred at day 11.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Lack of global X-chromosome inactivation in developing testes. Expression of X-linked (orange) and autosomal (blue) genes was measured as signal intensity of corresponding microarray probes, after normalization. cDNAs hybridized to the microarrays were isolated from testes of either feeding (f) or wandering (w) larvae grown for the indicated number of days at 18°C. The analysis traces the first wave of germline differentiation; pupation indicative of the meiotic divisions occurred at day 11.
Mentions: To further support our findings by extending them to the majority of X-linked genes, we analyzed the global trends of X-linked gene expression during testis development using gene microarrays. To improve the resolution of the analysis, we cultured larvae at a lower temperature (18°C) and collected testes from feeding larvae at fourth, fifth, sixth and seventh days of development (Figure 2 dLf), and from wandering larvae at days seven and ten, just before the onset of pupation at days 11 to 12 (Figure 2, dLw). Throughout larval testis development, we did not find appreciable differences in expression between the X chromosome and autosomes (Figure 2, orange versus blue bars) or any substantial reduction in X-linked gene expression (Figure 2, orange bars), strengthening the hypothesis that the X chromosome is not affected by global MSCI in Drosophila, contrary to mammalian spermatogenesis.

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