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Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast

Nature volume 389, pages 90–93 (1997)Cite this article

The cytoplasmic localization of messenger RNA creates an asymmetric distribution of proteins that specify cell fate during development in multicellular eukaryotes1,2. The protein Ash1 is a cell-fate determinant in budding yeast which localizes preferentially to the presumptive daughter nucleus, where it inhibits mating-type switching3,4. Here we show that Ash1 mRNA is localized to the distal tip of daughter buds in post-anaphase cells. Three-dimensional imaging reveals that Ash1 mRNA is assembled into particles that associate with the cell cortex. To achieve this localization, Ash1 mRNA must have its 3′ untranslated region and the actin cytoskeleton must be intact. Ash1 mRNA is not localized correctly in the absence of a myosin (Myo4) and is mislocalized to the mother-bud neck in the absence of a regulator of the actin cytoskeleton known as Bni1. We propose that Ash1 mRNA particles are transported into the daughter bud along actin filaments and are anchored at the distal tip. Thus, as in higher eukaryotes, Saccharomyces cerevisiae employs RNA localization to generate an asymmetric distribution of proteins and hence to determine cell fate.

Transcription of the ASH1 gene and translation of its RNA occur in large-budded cells that have undergone nuclear division but not cytokinesis3,4. In these post-anaphase cells, Ash1 protein localizes preferentially to the nucleus in the bud (incipient daughter cell). In principle, asymmetric localization of Ash1 protein could result from restriction of ASH1 transcription to the incipient daughter nucleus, accumulation of Ash1 mRNA in the incipient daughter cell, or accumulation of Ash1 protein in the incipient daughter as a result of a localization determinant on the protein itself.

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Figure 1: Ash1 mRNA is localized to the distal tip of the presumptive daughter cell.
Figure 2: Three-dimensional reconstruction of Ash1 mRNA-containing particles.
Figure 3: Ash1 mRNA localization requires its 3′UTR and the cytoskeletal proteins, Bni1 and Myo4.
Figure 4: The actin cytoskeleton is required for Ash1 mRNA localization.
Figure 5: The ASH1 3′UTR is sufficient for asymmetric RNA localization to the bud.

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Acknowledgements

We thank J. Sedat and D. Agard for use of their CCD-based optical sectioning microscope and image processing facilities; R. P. Jansen and K. Nasmyth for strains; E. O'Shea for plasmids; and D. Drubin for latrunculin A. This work was supported by grants from the NIH (R.D.V. and I.H.) and a grant from the Cancer Research Fund of the Damon Runyon–Walter Winchell Foundation Fellowship (J.R.S.).

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Authors and Affiliations

  1. Howard Hughes Medical Institute and Departments of,

    Peter A. Takizawa

  2. Cellular Molecular Pharmacology,

    Peter A. Takizawa & Jason R. Swedlow

  3. Biochemistry and Biophysics, University of California, SanFrancisco, 94143-0450, California, USA

    Anita Sil & Ira Herskowitz

Author notes

  1. Ronald D. Vale: Correspondence and requests for materials should be addressed to R.D.V.

    • Ronald D. Vale
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Takizawa, P., Sil, A., Swedlow, J. et al. Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast. Nature 389, 90–93 (1997). https://doi.org/10.1038/38015

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