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Selective elimination of messenger RNA prevents an incidence of untimely meiosis

Abstract

Much remains unknown about the molecular regulation of meiosis. Here we show that meiosis-specific transcripts are selectively removed if expressed during vegetative growth in fission yeast. These messenger RNAs contain a cis-acting region—which we call the DSR—that confers this removal via binding to a YTH-family protein Mmi1. Loss of Mmi1 function severely impairs cell growth owing to the untimely expression of meiotic transcripts. Microarray analysis reveals that at least a dozen such meiosis-specific transcripts are eliminated by the DSR–Mmi1 system. Mmi1 remains in the form of multiple nuclear foci during vegetative growth. At meiotic prophase these foci precipitate to a single focus, which coincides with the dot formed by the master meiosis-regulator Mei2. A meiotic arrest due to the loss of the Mei2 dot is released by a reduction in Mmi1 activity. We propose that Mei2 turns off the DSR–Mmi1 system by sequestering Mmi1 to the dot and thereby secures stable expression of meiosis-specific transcripts.

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Figure 1: Selective removal of mei4 mRNA in mitotic cells.
Figure 2: DSRs found on meiosis-specific mRNAs.
Figure 3: The mmi1 gene and expression of meiotic mRNAs in the absence of mmi1 function.
Figure 4: The Mei2 dot anchors Mmi1.

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Acknowledgements

We thank A. M. Carr for providing the chromosomal N-terminal tagging system, G. R. Smith for fission yeast strains, and M. Sato for help in strain construction. This work was supported by a Grant-in-Aid for Specially Promoted Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (to M.Y.) and a Grant from the Japan Science and Technology Agency (to Y. Hiraoka). Y. Harigaya was a recipient of a JSPS Research Fellowship for Young Scientists (DC) associating with a 21st Century COE Program led by M.Y.

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Correspondence to Masayuki Yamamoto.

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The entire microarray data obtained in this study has been deposited in the Gene Expression Omnibus (GEO), under the accession number GSE3314. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

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Harigaya, Y., Tanaka, H., Yamanaka, S. et al. Selective elimination of messenger RNA prevents an incidence of untimely meiosis. Nature 442, 45–50 (2006). https://doi.org/10.1038/nature04881

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