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Sex-biased expression of microRNAs in Drosophila melanogaster.

Marco A - Open Biol (2014)

Bottom Line: As with protein-coding genes, sex-biased microRNAs are associated with the reproductive function.MicroRNAs with sex-biased expression do not preferentially target sex-biased gene transcripts.These results strongly suggest that the sex-biased expression of microRNAs is mainly a consequence of high rates of microRNA emergence in the X chromosome (male bias) or hitchhiked expression by host genes (female bias).

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, University of Essex, Colchester CO4 3SQ, UK.

ABSTRACT
Most animals have separate sexes. The differential expression of gene products, in particular that of gene regulators, is underlying sexual dimorphism. Analyses of sex-biased expression have focused mostly on protein-coding genes. Several lines of evidence indicate that microRNAs, a class of major gene regulators, are likely to have a significant role in sexual dimorphism. This role has not been systematically explored so far. Here, I study the sex-biased expression pattern of microRNAs in the model species Drosophila melanogaster. As with protein-coding genes, sex-biased microRNAs are associated with the reproductive function. Strikingly, contrary to protein-coding genes, male-biased microRNAs are enriched in the X chromosome, whereas female microRNAs are mostly autosomal. I propose that the chromosomal distribution is a consequence of high rates of de novo emergence, and a preference for new microRNAs to be expressed in the testis. I also suggest that demasculinization of the X chromosome may not affect microRNAs. Interestingly, female-biased microRNAs are often encoded within protein-coding genes that are also expressed in females. MicroRNAs with sex-biased expression do not preferentially target sex-biased gene transcripts. These results strongly suggest that the sex-biased expression of microRNAs is mainly a consequence of high rates of microRNA emergence in the X chromosome (male bias) or hitchhiked expression by host genes (female bias).

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Sex-biased microRNAs in Drosophila melanogaster. (a) Heatmap of cross-correlations of all expression datasets analysed. Different experiments are hierarchically clustered. (b) Smear plot of mature microRNA sequences. Grey lines indicate a twofold difference in expression levels between males and females. Red dots are microRNAs with a statistically significant differential expression. (c) MicroRNA transcripts with sex-biased expression, average fold change of their products and their chromosomal location. (d) Frequency plot of sex biases in expression levels for autosomes and the X chromosome.
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RSOB140024F1: Sex-biased microRNAs in Drosophila melanogaster. (a) Heatmap of cross-correlations of all expression datasets analysed. Different experiments are hierarchically clustered. (b) Smear plot of mature microRNA sequences. Grey lines indicate a twofold difference in expression levels between males and females. Red dots are microRNAs with a statistically significant differential expression. (c) MicroRNA transcripts with sex-biased expression, average fold change of their products and their chromosomal location. (d) Frequency plot of sex biases in expression levels for autosomes and the X chromosome.

Mentions: To characterize which microRNAs have a sex-biased expression pattern in D. melanogaster, 13 different small RNA sequencing experiments (including males, females, embryos, ovaries and testes) were cross-compared (see §5). Figure 1a shows the correlation among the expression profiles for all experiments, indicating that the female and male pairs of profiles are highly correlated, despite coming from independent experiments. Thus, pairs of male and female profiles were used as biological replicates to calculate differential expression between sexes. A total of 476 mature microRNAs (two sequences per microRNA precursor) were analysed. Of them, 28 and 37 mature microRNAs showed a significant expression bias in males and females, respectively (figure 1b; see §5). Table 1 includes details of sex-biased microRNAs and their fold change. The expression levels for all analysed mature microRNAs are available in the electronic supplementary material, table S1. As only reads mapping to a single microRNA were taken into account, removing reads mapping to multiple sites may influence our analysis. Hence, I compared the expression levels resulting from unique reads and from multiple matching reads. Four microRNA families were affected by multiple matching reads: mir-983, mir-281, mir-276 and mir-2. The first three did not show any differential expression between sexes. However, the fourth one included two microRNAs, mir-2a-1 and mir-13b-2, which are female-biased. To avoid biases due to multiple matches, the mir-2 family was removed from the subsequent analyses.Table 1.


Sex-biased expression of microRNAs in Drosophila melanogaster.

Marco A - Open Biol (2014)

Sex-biased microRNAs in Drosophila melanogaster. (a) Heatmap of cross-correlations of all expression datasets analysed. Different experiments are hierarchically clustered. (b) Smear plot of mature microRNA sequences. Grey lines indicate a twofold difference in expression levels between males and females. Red dots are microRNAs with a statistically significant differential expression. (c) MicroRNA transcripts with sex-biased expression, average fold change of their products and their chromosomal location. (d) Frequency plot of sex biases in expression levels for autosomes and the X chromosome.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4043116&req=5

RSOB140024F1: Sex-biased microRNAs in Drosophila melanogaster. (a) Heatmap of cross-correlations of all expression datasets analysed. Different experiments are hierarchically clustered. (b) Smear plot of mature microRNA sequences. Grey lines indicate a twofold difference in expression levels between males and females. Red dots are microRNAs with a statistically significant differential expression. (c) MicroRNA transcripts with sex-biased expression, average fold change of their products and their chromosomal location. (d) Frequency plot of sex biases in expression levels for autosomes and the X chromosome.
Mentions: To characterize which microRNAs have a sex-biased expression pattern in D. melanogaster, 13 different small RNA sequencing experiments (including males, females, embryos, ovaries and testes) were cross-compared (see §5). Figure 1a shows the correlation among the expression profiles for all experiments, indicating that the female and male pairs of profiles are highly correlated, despite coming from independent experiments. Thus, pairs of male and female profiles were used as biological replicates to calculate differential expression between sexes. A total of 476 mature microRNAs (two sequences per microRNA precursor) were analysed. Of them, 28 and 37 mature microRNAs showed a significant expression bias in males and females, respectively (figure 1b; see §5). Table 1 includes details of sex-biased microRNAs and their fold change. The expression levels for all analysed mature microRNAs are available in the electronic supplementary material, table S1. As only reads mapping to a single microRNA were taken into account, removing reads mapping to multiple sites may influence our analysis. Hence, I compared the expression levels resulting from unique reads and from multiple matching reads. Four microRNA families were affected by multiple matching reads: mir-983, mir-281, mir-276 and mir-2. The first three did not show any differential expression between sexes. However, the fourth one included two microRNAs, mir-2a-1 and mir-13b-2, which are female-biased. To avoid biases due to multiple matches, the mir-2 family was removed from the subsequent analyses.Table 1.

Bottom Line: As with protein-coding genes, sex-biased microRNAs are associated with the reproductive function.MicroRNAs with sex-biased expression do not preferentially target sex-biased gene transcripts.These results strongly suggest that the sex-biased expression of microRNAs is mainly a consequence of high rates of microRNA emergence in the X chromosome (male bias) or hitchhiked expression by host genes (female bias).

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, University of Essex, Colchester CO4 3SQ, UK.

ABSTRACT
Most animals have separate sexes. The differential expression of gene products, in particular that of gene regulators, is underlying sexual dimorphism. Analyses of sex-biased expression have focused mostly on protein-coding genes. Several lines of evidence indicate that microRNAs, a class of major gene regulators, are likely to have a significant role in sexual dimorphism. This role has not been systematically explored so far. Here, I study the sex-biased expression pattern of microRNAs in the model species Drosophila melanogaster. As with protein-coding genes, sex-biased microRNAs are associated with the reproductive function. Strikingly, contrary to protein-coding genes, male-biased microRNAs are enriched in the X chromosome, whereas female microRNAs are mostly autosomal. I propose that the chromosomal distribution is a consequence of high rates of de novo emergence, and a preference for new microRNAs to be expressed in the testis. I also suggest that demasculinization of the X chromosome may not affect microRNAs. Interestingly, female-biased microRNAs are often encoded within protein-coding genes that are also expressed in females. MicroRNAs with sex-biased expression do not preferentially target sex-biased gene transcripts. These results strongly suggest that the sex-biased expression of microRNAs is mainly a consequence of high rates of microRNA emergence in the X chromosome (male bias) or hitchhiked expression by host genes (female bias).

Show MeSH
Related in: MedlinePlus