Y chromosomal noncoding RNAs regulate autosomal gene expression via piRNAs in mouse testis.

Hemakumar M. Reddy, Rupa Bhattacharya, Shrish Tiwari, Kankadeb Mishra, Pranatharthi Annapurna, Zeenath Jehan, Nissankararao Mary Praveena, Jomini Liza Alex, Vishnu M. Dhople, Lalji Singh, Mahadevan Sivaramakrishnan, Anurag Chaturvedi, Nandini Rangaraj, Thomas Michael Shiju, Badanapuram Sreedevi, Sachin Kumar, Ram Reddy Dereddi, Sunayana M. Rayabandla, Rachel A. Jesudasan

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Abstract

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.
Original languageEnglish
Article number198
JournalBMC Biology
Volume19
Issue number1
DOIs
Publication statusPublished - 9 Sep 2021

Keywords

  • Alternative splicing
  • Autosomal gene regulation
  • Comparative sperm proteomics
  • Long noncoding RNA
  • Male sterility
  • Mouse Y chromosome
  • Pirmy
  • Pirmy-like RNAs
  • piRNA

ASJC Scopus subject areas

  • Biotechnology
  • Structural Biology
  • Ecology, Evolution, Behavior and Systematics
  • Physiology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • Plant Science
  • Developmental Biology
  • Cell Biology

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