LncRNA transcription induces meiotic recombination through chromatin remodelling in fission yeast

Satoshi Senmatsu,Ryuta Asada,Charles S Hoffman,Kunihiro Ohta,Arisa Oda,Kouji Hirota

doi:10.1038/s42003-021-01798-8

Abstract

Noncoding RNAs (ncRNAs) are involved in various biological processes, including gene expression, development, and disease. Here, we identify a novel consensus sequence of a cis-element involved in long ncRNA (lncRNA) transcription and demonstrate that lncRNA transcription from this cis-element activates meiotic recombination via chromatin remodeling. In the fission yeast fbp1 gene, glucose starvation induces a series of promoter-associated lncRNAs, referred to as metabolic-stress-induced lncRNAs (mlonRNAs), which contribute to chromatin remodeling and fbp1 activation. Translocation of the cis-element required for mlonRNA into a well-characterized meiotic recombination hotspot, ade6-M26, further stimulates transcription and meiotic recombination via local chromatin remodeling. The consensus sequence of this cis-element (mlon-box) overlaps with meiotic recombination sites in the fission yeast genome. At one such site, the SPBC24C6.09c upstream region, meiotic double-strand break (DSB) formation is induced in an mlon-box-dependent manner. Therefore, mlonRNA transcription plays a universal role in chromatin remodeling and the regulation of transcription and recombination.

Highlights

Noncoding RNAs are involved in various biological processes, including gene expression, development, and disease
We investigated whether mlonRNA transcription plays a universal role in chromatin remodeling in the fission yeast genome, leading to the discovery that this long noncoding RNAs (ncRNAs) (lncRNA) transcription induces meiotic recombination through inducing chromatin remodeling
To investigate the generality of the role of mlonRNA transcription in chromatin modulation and to further assess the role of this lncRNA transcription in other aspects of chromosomal regulation, we inserted this cis-element into the ade6-M26 meiotic recombination hotspot (Fig. 1c)[27,28]

Summary

Introduction

Noncoding RNAs (ncRNAs) are involved in various biological processes, including gene expression, development, and disease. Atf1-Pcr[1] binding induces M26 transcription from the M26-mutation site in the ade[6] ORF, followed by histone acetylation and chromatin remodeling around the M26 site, thereby inducing meiotic recombination[31,32,33] Taken together, these observations suggest that local chromatin configuration, histone modifications and transcriptional activity play key roles in the location of meiotic DSB sites in budding yeast and fission yeast[13,32,33,34,35,36]. Stepwise mlonRNA transcription (mlonRNA-a, mlonRNA-b, and mlonRNA-c initiating progressively closer to the fbp[1] transcription start site [TSS]) induces chromatin remodeling at the fbp[1] promoter (Fig. 1a), and subsequently facilitates transcription factor binding to activate fbp[1] expression[37] These observations indicate that mlonRNA transcription mediates chromatin remodeling and thereby contribute to the robust induction of fbp[1] transcription upon glucose starvation. We investigated whether mlonRNA transcription plays a universal role in chromatin remodeling in the fission yeast genome, leading to the discovery that this lncRNA transcription induces meiotic recombination through inducing chromatin remodeling

Methods

Results

Conclusion