Abstract
BackgroundTight regulation of testicular gene expression is a prerequisite for male reproductive success, while differentiation of gene activity in spermatogenesis is important during speciation. Thus, comparison of testicular transcriptomes between closely related species can reveal unique regulatory patterns and shed light on evolutionary constraints separating the species.Methodology/Principal FindingsHere, we compared testicular transcriptomes of two closely related mouse species, Mus musculus and Mus spretus, which diverged more than one million years ago. We analyzed testicular expression using tiling arrays overlapping Chromosomes 2, X, Y and mitochondrial genome. An excess of differentially regulated non-coding RNAs was found on Chromosome 2 including the intronic antisense RNAs, intergenic RNAs and premature forms of Piwi-interacting RNAs (piRNAs). Moreover, striking difference was found in the expression of X-linked G6pdx gene, the parental gene of the autosomal retrogene G6pd2.Conclusions/SignificanceThe prevalence of non-coding RNAs among differentially expressed transcripts indicates their role in species-specific regulation of spermatogenesis. The postmeiotic expression of G6pdx in Mus spretus points towards the continuous evolution of X-chromosome silencing and provides an example of expression change accompanying the out-of-the X-chromosomal retroposition.
Highlights
Spermatogenesis is a tightly regulated process of germ cell mitotic proliferation, differentiation, and two consecutive meiotic divisions forming spermatozoa
Differential levels of testicular transcripts between Mus spretus and Mus musculus As we wanted to determine how testicular transcriptomes differ between two mouse species by an unbiased experimental method we used mouse tiling arrays
From the group of downregulated clusters in Mus spretus we focused only on two clusters of Chromosome 2 (Figure 2), since they are abundant in Piwi-interacting RNAs with an obvious role in spermatogenesis [5,6,27]
Summary
Spermatogenesis is a tightly regulated process of germ cell mitotic proliferation, differentiation, and two consecutive meiotic divisions forming spermatozoa. Beside the protein-coding genes, the testicular transcriptome is abundant in antisense transcripts [1], transcribed pseudogenes [2], retrogenes, and various types of non-coding RNAs including microRNAs (miRNAs) [3], and Piwi-interacting RNAs (piRNAs) [4,5]. Several forms of these transcripts were shown to play a crucial role in spermatogenesis. Comparison of testicular transcriptomes between closely related species can reveal unique regulatory patterns and shed light on evolutionary constraints separating the species
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