Rapid evolution of mammalian X-linked testis microRNAs - PubMed (original) (raw)

Comparative Study

Rapid evolution of mammalian X-linked testis microRNAs

Xuejiang Guo et al. BMC Genomics. 2009.

Abstract

Background: MicroRNAs (miRNAs), which are small, non-coding RNAs approximately 21-nucleotides in length, have become a major focus of research in molecular biology. Mammalian miRNAs are proposed to regulate approximately 30% of all protein-coding genes. Previous studies have focused on highly conserved miRNAs, but nonconserved miRNAs represent a potentially important source of novel functionalities during evolution.

Results: An analysis of the chromosome distribution of miRNAs showed higher densities of miRNAs on the X chromosome compared to the average densities on autosomes in all eight mammalian species analyzed. The distribution pattern did not, however, apply well to species beyond mammals. In addition, by comparing orthologous human and mouse miRNAs, we found that X-linked miRNAs had higher substitution rates than autosomal miRNAs. Since the highest proportion of X-linked miRNAs were found in mouse testis, we tested the hypothesis that testis miRNAs are evolving faster on the X chromosome than on autosomes. Mature X-linked testis miRNAs had an average substitution rate between mouse and human that was almost 25-fold higher than mature testis miRNAs on autosomes. In contrast, for mature miRNAs with precursors not expressed in testis, no significant difference in the substitution rate between the X chromosome and autosomes was found. Among mammals, the rapid evolution of X-linked testis miRNAs was also observed in rodents and primates.

Conclusion: The rapid evolution of X-linked testis miRNAs implies possible important male reproductive functions and may contribute to speciation in mammals.

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Figures

Figure 1

Figure 1

Density distribution of miRNAs across chromosomes among species. Densities of miRNAs on the X chromosome and autosomes are shown for different species, except for chicken, where the Z chromosome is used instead of X. Densities are shown as number of miRNAs per megabase of DNA. The ratios of densities between the X chromosome and autosomes are shown in brackets. Mammals in the species tree on the left are shaded in grey.

Figure 2

Figure 2

Comparison of substitution rates for genome-wide miRNAs between human and mouse by chromosomes. Substitution rate differences of genome-wide mature miRNAs and precursor miRNAs between the X chromosome and autosomes are shown. Substitution rates were calculated from orthologous sequences of human and mouse using the Kimura 2-parameter model. All comparisons showed significant differences (**, p < 0.01).

Figure 3

Figure 3

Proportion of mature X-linked mouse miRNAs by tissues. miRNA data are from the mammalian microRNA expression atlas based on the small RNA library sequencing by Landgraf et al. [8]. The numbers of X-linked miRNAs cloned in corresponding tissues are shown in brackets.

Figure 4

Figure 4

Comparison of substitution rates in testis and non-testis mature miRNAs across chromosomes. Differences in substitution rates of mature miRNAs on the X chromosome and autosomes are shown. Substitution rates were calculated from orthologous sequences of human and mouse using the Kimura 2-parameter model. For non-testis mature miRNAs, miRNAs with precursors not expressed in mouse testis were used. Comparisons with significant differences are shown with ** (p < 0.01).

Figure 5

Figure 5

Comparison of substitution rates for testis and non-testis precusor miRNAs across chromosomes. Differences in substitution rates for precursor miRNAs on the X chromosome and autosomes, as well as their four parts, were compared. For testis precursor miRNAs, substitution rate comparisons were performed for human and mouse orthologs (A), for mouse and rat (C), and for human and macaque (E). The same analysis was performed for precursor miRNAs not expressed in testis (B, D and F, respectively). The names used are: precursor, precursor miRNA; ustem, upper stem region; loop, terminal loop; bseg, basal segments. Significant differences are indicated with * (p < 0.05) or ** (p < 0.01).

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