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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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The autosomal and the X-linked tissue-biased genes show different patterns of chromatin modifications. The frequencies of binding targets for the proteins indicated at the bottom were calculated among the X-linked (orange) and autosomal (blue) tissue-biased genes. The sets of genes showing at least two-fold expression bias toward the indicated tissues (such as testis, midgut, accessory gland, salivary gland, malpigian tubule, and ovary) were generated from the genome-wide expression data [24]. Protein binding genes were defined using chromatin immunoprecipitation and DamID data [29,30] with arbitrarily set thresholds. Bars show relative increase or decrease in binding target frequency within analyzed gene sets as compared to the entire genome.
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Figure 6: The autosomal and the X-linked tissue-biased genes show different patterns of chromatin modifications. The frequencies of binding targets for the proteins indicated at the bottom were calculated among the X-linked (orange) and autosomal (blue) tissue-biased genes. The sets of genes showing at least two-fold expression bias toward the indicated tissues (such as testis, midgut, accessory gland, salivary gland, malpigian tubule, and ovary) were generated from the genome-wide expression data [24]. Protein binding genes were defined using chromatin immunoprecipitation and DamID data [29,30] with arbitrarily set thresholds. Bars show relative increase or decrease in binding target frequency within analyzed gene sets as compared to the entire genome.

Mentions: We inquired whether the tissue-biased gene activation generally correlates with binding of repressor proteins in the 'non-target' embryonic and cultured cells, and whether such correlation differs between the X chromosome and autosomes. For this analysis, we calculated the relative enrichment with chromatin proteins for the genes that show more than two-fold expression bias toward testis, midgut, accessory gland, salivary gland, malpigian tubule, and ovary. The tissue expression bias was determined using the same approach as described above for the analysis of tissue-biased gene frequencies on chromosomes. Using arbitrarily-set thresholds to define the categories of bound versus non-bound genes for each of the analyzed chromatin proteins [30,31], we determined the frequencies of bound genes in the sets of tissue-biased genes on the X chromosome and autosomes and normalized them to the frequencies of bound genes in the entire genome. The study included nine repressor proteins and eight activators that showed the strongest 'inverse' correlations in previous analysis. The resulting graphs (Figure 6) show whether the X-linked (orange bars) or autosomal (blue bars) genes bind repressors or activators in embryos and cultured cells with a frequency different from the genome average (defined as 1.0).


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)

The autosomal and the X-linked tissue-biased genes show different patterns of chromatin modifications. The frequencies of binding targets for the proteins indicated at the bottom were calculated among the X-linked (orange) and autosomal (blue) tissue-biased genes. The sets of genes showing at least two-fold expression bias toward the indicated tissues (such as testis, midgut, accessory gland, salivary gland, malpigian tubule, and ovary) were generated from the genome-wide expression data [24]. Protein binding genes were defined using chromatin immunoprecipitation and DamID data [29,30] with arbitrarily set thresholds. Bars show relative increase or decrease in binding target frequency within analyzed gene sets as compared to the entire genome.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: The autosomal and the X-linked tissue-biased genes show different patterns of chromatin modifications. The frequencies of binding targets for the proteins indicated at the bottom were calculated among the X-linked (orange) and autosomal (blue) tissue-biased genes. The sets of genes showing at least two-fold expression bias toward the indicated tissues (such as testis, midgut, accessory gland, salivary gland, malpigian tubule, and ovary) were generated from the genome-wide expression data [24]. Protein binding genes were defined using chromatin immunoprecipitation and DamID data [29,30] with arbitrarily set thresholds. Bars show relative increase or decrease in binding target frequency within analyzed gene sets as compared to the entire genome.
Mentions: We inquired whether the tissue-biased gene activation generally correlates with binding of repressor proteins in the 'non-target' embryonic and cultured cells, and whether such correlation differs between the X chromosome and autosomes. For this analysis, we calculated the relative enrichment with chromatin proteins for the genes that show more than two-fold expression bias toward testis, midgut, accessory gland, salivary gland, malpigian tubule, and ovary. The tissue expression bias was determined using the same approach as described above for the analysis of tissue-biased gene frequencies on chromosomes. Using arbitrarily-set thresholds to define the categories of bound versus non-bound genes for each of the analyzed chromatin proteins [30,31], we determined the frequencies of bound genes in the sets of tissue-biased genes on the X chromosome and autosomes and normalized them to the frequencies of bound genes in the entire genome. The study included nine repressor proteins and eight activators that showed the strongest 'inverse' correlations in previous analysis. The resulting graphs (Figure 6) show whether the X-linked (orange bars) or autosomal (blue bars) genes bind repressors or activators in embryos and cultured cells with a frequency different from the genome average (defined as 1.0).

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