Deciphering the functions of Y chromosome in mammals has been slow owing to the presence of repeats. Some of these repeats transcribe coding RNAs, the roles of which have been studied. Functions of the noncoding transcripts from Y chromosomal repeats however, remain unclear. While a majority of the genes expressed during spermatogenesis are autosomal, mice with different deletions of the long arm of the Y chromosome (Yq) were previously also shown to be characterized by subfertility, sterility and sperm abnormalities, suggesting the presence of effectors of spermatogenesis at this location. Here we report a set of novel noncoding RNAs from mouse Yq and explore their connection to some of the autosomal genes expressed in testis. We describe a set of novel mouse male-specific Y long arm (MSYq)-derived long noncoding (lnc) transcripts, named Pirmy and Pirmy-like RNAs. Pirmy shows a large number of splice variants in testis. We also identified Pirmy-like RNAs present in multiple copies at different loci on mouse Y chromosome. Further, we identified eight differentially expressed autosome-encoded sperm proteins in a mutant mouse strain, XYRIIIqdel (2/3 Yq-deleted). Pirmy and Pirmy-like RNAs have homology to 5'/3'UTRs of these deregulated autosomal genes. Several lines of experiments show that these short homologous stretches correspond to piRNAs. Thus, Pirmy and Pirmy-like RNAs act as templates for several piRNAs. In vitro functional assays reveal putative roles for these piRNAs in regulating autosomal genes. Our study elucidates a set of autosomal genes that are potentially regulated by MSYq-derived piRNAs in mouse testis. Sperm phenotypes from the Yq-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 MSYq-derived ncRNAs in male sterility and speciation.
The study was funded by Department of Science and Technology, India (SP/SO/B70/2001) and Department of Biotechnology, India (BT/PR 10707/AGR/36/596/2008, BT/PR6123/BRB/10/1185/2013), intramural funding from Council of Scientific and Industrial Research (CSIR), India to RAJ and research fellowships by CSIR, India to HMR, RB.
We would like to dedicate this manuscript to Prof. Lalji Singh and Prof. Paul S Burgoyne both of whom have left us for their heavenly abode and whom we miss greatly at this point of time. We gratefully acknowledge the gift of the XY RIII and XY RIII qdel mice by Prof. Paul S Burgoyne, MRC, Edinburgh, UK. This study could not have been done without the gift of these mice. We are grateful to Dr. Lekha D. Kumar for sharing the small RNA isolation protocol with us.?We thank Prof. Yukiko Yamashita for her inputs. We are grateful to Dr. Dinesh Kumar and Professor B. K. Thelma for reading and editing the manuscript and Mr. Sivarajan Karunanithi for help with partial in silico analysis.
© 2021, The Author(s).
- Alternative splicing
- Autosomal gene regulation
- Comparative sperm proteomics
- Long noncoding RNA
- Male sterility
- Mouse Y chromosome
- Pirmy-like RNAs
- Structural Biology
- Ecology, Evolution, Behavior and Systematics
- Biochemistry, Genetics and Molecular Biology(all)
- Agricultural and Biological Sciences(all)
- Plant Science
- Developmental Biology
- Cell Biology