Y chromosomal noncoding RNA regulates autosomal gene expression via piRNAs in mouse testis

Repeats from the male-specific long arm of mouse Y-chromosome (MSYq) transcribe protein coding and noncoding RNAs. Majority of genes expressed during spermatogenesis are autosomal. Mice with different deletions of Yq show sub-fertility and sterility, depending on the length of deletion. The connection between Yq deletion and autosomal gene regulation was not well studied before. We describe a novel multi-copy mouse Yq-derived long noncoding RNA, Pirmy (piRNA from mouse Y chromosome), which shows unprecedented alternative splicing in testis. Further, Pirmy acts as a template for several piRNAs in mouse testis. Mice with deletions of Yq including the region of Pirmy exhibit differential male fertility, aberrant sperm morphology, motility and sex ratio skewed towards females. We identified deregulation of ten autosome-encoded sperm proteins in a Y-deleted strain of mouse. Pirmy splice variants have homology to 5′/3′ UTRs of these deregulated autosomal genes. Thus, subfertility in Y-deleted mice appears to be a polygenic phenomenon that is partially regulated epistatically by the Y-encoded Pirmy . Our study provides novel and interesting insights into possible role of MSY-derived noncoding RNAs in male fertility and reproduction. Finally, sperm phenotypes from Y-deleted mice seem to be similar to that reported in inter-specific male-sterile hybrids. Taken together, this study provides novel insights into possible role of Y-derived noncoding RNAs in male sterility and speciation.