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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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Evolutionary origin of sex-biased microRNA transcripts. Phylogenetic tree of Drosophila melanogaster and other animal groups. MicroRNAs emerging at a given lineage were shown over the relevant branches. For microRNA clusters, only the first microRNA is shown in the figure over the branch at which the oldest microRNA emerged. Red microRNAs are female-biased and blue are male-biased.
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RSOB140024F3: Evolutionary origin of sex-biased microRNA transcripts. Phylogenetic tree of Drosophila melanogaster and other animal groups. MicroRNAs emerging at a given lineage were shown over the relevant branches. For microRNA clusters, only the first microRNA is shown in the figure over the branch at which the oldest microRNA emerged. Red microRNAs are female-biased and blue are male-biased.

Mentions: There are two possible ways a gene may become sex-biased. First, a gene can acquire sex-biased expression. Second, a new gene appears (either de novo or by the duplication of an existing gene) having from the very beginning a sex-biased expression. Figure 3 shows the evolutionary origin of sex-biased microRNAs. Most male-biased microRNAs emerged within the Drosophila lineage, with only two exceptions: mir-993 and mir-283/304/12. These are indeed the least biased of all of the microRNAs. Thus, microRNAs with a strong male bias are evolutionarily young. By contrast, the evolutionary origin of female-biased microRNA families is diverse, and there are both old and young microRNAs. Among the old microRNAs, we have the mir-92, mir-184 and mir-9 families, which are conserved even in chordates. Interestingly, there are no D. melanogaster-specific microRNAs with a clear female-biased expression (contrary to the case of male-biased microRNAs). There are, however, two female-biased microRNAs which appeared in the Drosophila genus lineage: mir-314 and the mir-310–mir-313 cluster.Figure 3.


Sex-biased expression of microRNAs in Drosophila melanogaster.

Marco A - Open Biol (2014)

Evolutionary origin of sex-biased microRNA transcripts. Phylogenetic tree of Drosophila melanogaster and other animal groups. MicroRNAs emerging at a given lineage were shown over the relevant branches. For microRNA clusters, only the first microRNA is shown in the figure over the branch at which the oldest microRNA emerged. Red microRNAs are female-biased and blue are male-biased.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

RSOB140024F3: Evolutionary origin of sex-biased microRNA transcripts. Phylogenetic tree of Drosophila melanogaster and other animal groups. MicroRNAs emerging at a given lineage were shown over the relevant branches. For microRNA clusters, only the first microRNA is shown in the figure over the branch at which the oldest microRNA emerged. Red microRNAs are female-biased and blue are male-biased.
Mentions: There are two possible ways a gene may become sex-biased. First, a gene can acquire sex-biased expression. Second, a new gene appears (either de novo or by the duplication of an existing gene) having from the very beginning a sex-biased expression. Figure 3 shows the evolutionary origin of sex-biased microRNAs. Most male-biased microRNAs emerged within the Drosophila lineage, with only two exceptions: mir-993 and mir-283/304/12. These are indeed the least biased of all of the microRNAs. Thus, microRNAs with a strong male bias are evolutionarily young. By contrast, the evolutionary origin of female-biased microRNA families is diverse, and there are both old and young microRNAs. Among the old microRNAs, we have the mir-92, mir-184 and mir-9 families, which are conserved even in chordates. Interestingly, there are no D. melanogaster-specific microRNAs with a clear female-biased expression (contrary to the case of male-biased microRNAs). There are, however, two female-biased microRNAs which appeared in the Drosophila genus lineage: mir-314 and the mir-310–mir-313 cluster.Figure 3.

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