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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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Related in: MedlinePlus

Expression bias of microRNAs and their targets. Box plots of expression bias of gene transcripts targeted by microRNAs with no (0), moderate (−5/5) and large (−10/10) sex-biased expression. Targets are shown for three different target prediction algorithms: (a) TargetScan, (b) DIANA-microT and (c) miRanda.
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RSOB140024F4: Expression bias of microRNAs and their targets. Box plots of expression bias of gene transcripts targeted by microRNAs with no (0), moderate (−5/5) and large (−10/10) sex-biased expression. Targets are shown for three different target prediction algorithms: (a) TargetScan, (b) DIANA-microT and (c) miRanda.

Mentions: Do sex-biased microRNAs also target sex-biased expressed gene transcripts? To explore this question, three different target prediction algorithms were used: TargetScan, miRanda and DIANA-microT (see §5). MicroRNAs were binned by their bias level, and the expression bias of their targets was plotted in figure 4. These boxplots show that there is no tendency of sex-biased microRNAs to target sex-biased transcripts, at least not as a global pattern. I further explored the targets of seven melanogaster-subgroup-specific male-biased microRNAs. For two of them, two of the three prediction algorithms detected a significant association with sex-biased transcripts: mir-985 has a tendency to target female-biased genes, whereas mir-997 significantly targets male-biased genes (electronic supplementary material, table S2). The other associations were not significant and/or supported by only one prediction algorithm. Finally, I investigated whether recently emerged male-biased microRNAs also target evolutionarily young genes. I calculated the ratio between Drosophila-specific and conserved targeted genes for the targets predicted for the three above-mentioned algorithms. Four of seven studied microRNAs showed a tendency to target more conserved genes than expected by chance for at least two algorithms (electronic supplementary material, table S3), among them mir-985. The results here described rely heavily on target prediction algorithms and, therefore, should be taken with caution. However, they suggest that newly emerged microRNAs can potentially target conserved genes, altering regulatory relationships that have been conserved throughout evolution.Figure 4.


Sex-biased expression of microRNAs in Drosophila melanogaster.

Marco A - Open Biol (2014)

Expression bias of microRNAs and their targets. Box plots of expression bias of gene transcripts targeted by microRNAs with no (0), moderate (−5/5) and large (−10/10) sex-biased expression. Targets are shown for three different target prediction algorithms: (a) TargetScan, (b) DIANA-microT and (c) miRanda.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

RSOB140024F4: Expression bias of microRNAs and their targets. Box plots of expression bias of gene transcripts targeted by microRNAs with no (0), moderate (−5/5) and large (−10/10) sex-biased expression. Targets are shown for three different target prediction algorithms: (a) TargetScan, (b) DIANA-microT and (c) miRanda.
Mentions: Do sex-biased microRNAs also target sex-biased expressed gene transcripts? To explore this question, three different target prediction algorithms were used: TargetScan, miRanda and DIANA-microT (see §5). MicroRNAs were binned by their bias level, and the expression bias of their targets was plotted in figure 4. These boxplots show that there is no tendency of sex-biased microRNAs to target sex-biased transcripts, at least not as a global pattern. I further explored the targets of seven melanogaster-subgroup-specific male-biased microRNAs. For two of them, two of the three prediction algorithms detected a significant association with sex-biased transcripts: mir-985 has a tendency to target female-biased genes, whereas mir-997 significantly targets male-biased genes (electronic supplementary material, table S2). The other associations were not significant and/or supported by only one prediction algorithm. Finally, I investigated whether recently emerged male-biased microRNAs also target evolutionarily young genes. I calculated the ratio between Drosophila-specific and conserved targeted genes for the targets predicted for the three above-mentioned algorithms. Four of seven studied microRNAs showed a tendency to target more conserved genes than expected by chance for at least two algorithms (electronic supplementary material, table S3), among them mir-985. The results here described rely heavily on target prediction algorithms and, therefore, should be taken with caution. However, they suggest that newly emerged microRNAs can potentially target conserved genes, altering regulatory relationships that have been conserved throughout evolution.Figure 4.

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