Mmi1 RNA surveillance machinery directs RNAi complex RITS to specific meiotic genes in fission yeast

• Published in: The EMBO journal 2012-05, Vol.31 (10), p.2296-2308
• Main Authors: Hiriart, Edwige, Vavasseur, Aurélia, Touat-Todeschini, Leila, Yamashita, Akira, Gilquin, Benoit, Lambert, Emeline, Perot, Jonathan, Shichino, Yuichi, Nazaret, Nicolas, Boyault, Cyril, Lachuer, Joel, Perazza, Daniel, Yamamoto, Masayuki, Verdel, André
• Format: Article
• Language: English
• Subjects: Cell cycle; Deoxyribonucleic acid; DNA; EMBO06; EMBO36; Gene expression; Gene Expression Regulation, Fungal; Genes, Fungal; Genetics; Life Sciences; Mmi1; Models, Biological; Molecular biology; mRNA Cleavage and Polyadenylation Factors - metabolism; Protein Binding; Ribonucleic acid; RITS; RNA; RNA, Fungal - metabolism; RNA-Induced Silencing Complex - metabolism; RNAi; S. pombe; Schizosaccharomyces - genetics; Schizosaccharomyces - metabolism; Schizosaccharomyces pombe; Schizosaccharomyces pombe Proteins - metabolism; sexual differentiation; Yeast; Yeasts
• ISSN: 0261-4189; 1460-2075
• DOI: 10.1038/emboj.2012.105

RNA interference (RNAi) silences gene expression by acting both at the transcriptional and post‐transcriptional levels in a broad range of eukaryotes. In the fission yeast Schizosaccharomyces pombe the RNA‐Induced Transcriptional Silencing (RITS) RNAi complex mediates heterochromatin formation at non‐coding and repetitive DNA. However, the targeting and role of RITS at other genomic regions, including protein‐coding genes, remain unknown. Here we show that RITS localizes to specific meiotic genes and mRNAs. Remarkably, RITS is guided to these meiotic targets by the RNA‐binding protein Mmi1 and its associated RNA surveillance machinery that together degrade selective meiotic mRNAs during vegetative growth. Upon sexual differentiation, RITS localization to the meiotic genes and mRNAs is lost. Large‐scale identification of Mmi1 RNA targets reveals that RITS subunit Chp1 associates with the vast majority of them. In addition, loss of RNAi affects the effective repression of sexual differentiation mediated by the Mmi1 RNA surveillance machinery. These findings uncover a new mechanism for recruiting RNAi to specific meiotic genes and suggest that RNAi participates in the control of sexual differentiation in fission yeast. The Mmi1 RNA surveillance machinery degrades meiotic mRNAs during vegetative growth in fission yeast. This study reveals an additional function in recruiting the RNA‐Induced Transcriptional Silencing (RITS) RNAi complex to these meiotic targets to induce heterochromatin formation.