Budding and fission yeast serve as genetic model organisms for the study of the molecular mechanisms of cell polarity in single cells. Similar to other polarized eukaryotic cells, yeast cells have polarity programmes that regulate where they grow and divide. Here, we describe recent advances in defining the proteins that establish cell polarity and the numerous molecular interactions that may link these factors to the actin cytoskeleton. As many of these components are identified, a comprehensive understanding of complex pathways is beginning to emerge.
Access optionsAccess options
Subscribe to Journal
Get full journal access for 1 year
only $18.75 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Bähler J. & Peter, M. in Frontiers in Molecular Biology, Vol. Cell polarity, 21–77 (Oxford Univ. Press, Oxford, 2000).
Pruyne, D. & Bretscher, A. Polarization of cell growth in yeast. J. Cell Sci. 113, 571–585 (2000).
Pruyne, D. & Bretscher, A. Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J. Cell Sci. 113, 365–375 (2000).
Chang, F. Establishment of a cellular axis in fission yeast. Trends Genet. 17, 273–278 (2001).
Schott, D., Huffaker, T. & Bretscher, A. Microfilaments and microtubules: the news from yeast. Curr. Opin Microbiol. 5, 564–574 (2002).
Lew, D.J. & Reed, S.I. Morphogenesis in the yeast cell cycle: Regulation by Cdc28 and cyclins. J. Cell Biol. 120, 1305–1320 (1993).
Mitchison, J.M. & Nurse, P. Growth in cell length in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 75, 357–376 (1985).
Drubin, D.G. Development of cell polarity in budding yeast. Cell 65, 1093–1096 (1991).
Pringle, J.R. et al. Establishment of cell polarity in yeast. Cold Spring Harb. Symp. Quant. Biol. 60, 729–744 (1995).
Chant, J. Cell polarity in yeast. Annu. Rev. Cell Dev. Biol. 15, 365–391 (1999).
Madden, K. & Snyder, M. Cell polarity and morphogenesis in budding yeast. Annu. Rev. Microbiol. 52, 687–744 (1998).
Longtine, M.S. et al. The septins: roles in cytokinesis and other processes. Curr. Opin. Cell Biol. 8, 106–119 (1996).
Kinoshita, M., Field, C.M., Coughlin, M.L., Straight, A.F. & Mitchison, T.J. Self- and actin-templated assembly of mammalian septins. Dev. Cell 3, 791–802 (2002).
Taheri, N., Kohler, T., Braus, G.H. & Mosch, H.U. Asymmetrically localized Bud8p and Bud9p proteins control yeast cell polarity and development. EMBO J. 19, 6686–6696 (2000).
Zahner, J.E., Harkins, H.A. & Pringle, J.R. Genetic analysis of the bipolar pattern of bud site selection in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 1857–1870 (1996).
Harkins, H.A. et al. Bud8p and Bud9p, proteins that may mark the sites for bipolar budding in yeast. Mol. Biol. Cell 12, 2497–2518 (2001).
Schenkman, L.R., Caruso, C., Page, N. & Pringle, J.R. The role of cell cycle-regulated expression in the localization of spatial landmark proteins in yeast. J. Cell Biol. 156, 829–841 (2002).
Chen, T. et al. Multigenerational cortical inheritance of the Rax2 protein in orienting polarity and division in yeast. Science 290, 1975–1978 (2000).
Ni, L. & Snyder, M. A genomic study of the bipolar bud site selection pattern in Saccharomyces cerevisiae. Mol. Biol. Cell 12, 2147–2170 (2001).
Toda, T., Umesono, K., Hirata, A. & Yanagida, M. Cold-sensitive nuclear division arrest mutants of the fission yeast Schizosaccharomyces pombe. J. Mol. Biol. 168, 251–270 (1983).
Verde, F., Mata, J. & Nurse, P. Fission yeast cell morphogenesis: Identification of new genes and analysis of their role during the cell cycle. J. Cell Biol. 131, 1529–1538 (1995).
Drummond, D.R. & Cross, R.A. Dynamics of interphase microtubules in Schizosaccharomyces pombe. Curr. Biol. 10, 766–775 (2000).
Tran, P.T., Marsh, L., Doye, V., Inoue, S. & Chang, F. A mechanism for nuclear positioning in fission yeast based upon microtubule pushing. J. Cell Biol. 153, 397–411 (2001).
Brunner, D. & Nurse, P. CLIP170-like tip1p spatially organizes microtubular dynamics in fission yeast. Cell 102, 695–704 (2000).
Mata, J. & Nurse, P. tea1 and the microtubular cytoskeleton are important for generating global spatial order within the fission yeast cell. Cell 89, 939–949 (1997).
Behrens, R. & Nurse, P. Roles of fission yeast tea1p in the localization of polarity factors and in organizing the microtubular cytoskeleton. J. Cell Biol. 157, 783–793 (2002).
Browning, H. et al. Tea2p is a kinesin-like protein required to generate polarized growth in fission yeast. J. Cell Biol. 151, 15–28 (2000).
Glynn, J.M., Lustig, R.J., Berlin, A. & Chang, F. Role of bud6p and tea1p in the interaction between actin and microtubules for the establishment of cell polarity in fission yeast. Curr. Biol. 11, 836–845 (2001).
Arellano, M., Niccoli, T. & Nurse, P. Tea3p is a cell end marker activating polarized growth in Schizosaccharomyces pombe. Curr. Biol. 12, 751–756 (2002).
Sawin, K.E. & Nurse, P. Regulation of cell polarity by microtubules in fission yeast. J. Cell Biol. 142, 457–471 (1998).
Tran, P.T., Doye, V., Chang, F. & Inoue, S. Microtubule-dependent nuclear positioning and nuclear-dependent septum positioning in the fission yeast Schizosaccharomyces pombe. Biol. Bull. 199, 205–206 (2000).
Chant, J. Cell polarity in yeast. Trends Genet. 10, 328–333 (1994).
Kang, P.J., Sanson, A., Lee, B. & Park, H.O. A GDP/GTP exchange factor involved in linking a spatial landmark to cell polarity. Science 292, 1376–1378 (2001).
Zheng, Y., Bender, A. & Cerione, R.A. Interactions among proteins involved in bud-site selection and bud-site assembly in Saccharomyces cerevisiae. J. Biol. Chem. 270, 626–630 (1995).
Park, H.O., Kang, P.J. & Rachfal, A.W. Localization of the Rsr1/Bud1 GTPase involved in selection of a proper growth site in yeast. J. Biol. Chem. 277, 26721–26724 (2002).
Gulli, M. et al. Phosphorylation of the cdc42 exchange factor cdc24 by the PAK-like kinase cla4 may regulate polarized growth in yeast. Mol. Cell 6, 1155–1167 (2000).
Butty, A.C. et al. A positive feedback loop stabilizes the guanine-nucleotide exchange factor Cdc24 at sites of polarization. EMBO J. 21, 1565–1576 (2002).
Caviston, J.P., Tcheperegine, S.E. & Bi, E. Singularity in budding: a role for the evolutionarily conserved small GTPase Cdc42p. Proc. Natl Acad. Sci. USA 99, 12185–12190 (2002).
Fukui, Y., Kozasa, T., Kaziro, Y., Takeda, T. & Yamamoto, M. Role of a ras homolog in the life cycle of Schizosaccharomyces pombe. Cell 44, 329–336 (1986).
Papadaki, P., Pizon, V., Onken, B. & Chang, E.C. Two ras pathways in fission yeast are differentially regulated by two ras guanine nucleotide exchange factors. Mol. Cell Biol. 22, 4598–4606 (2002).
Li, Y.C., Chen, C.R. & Chang, E.C. Fission yeast Ras1 effector Scd1 interacts with the spindle and affects its proper formation. Genetics 156, 995–1004 (2000).
Miller, P.J. & Johnson, D.I. Cdc42p GTPase is involved in controlling polarized cell growth in Schizosaccharomyces pombe. Mol. Cell. Biol. 14, 1075–1083 (1994).
Segall, J.E. Polarization of yeast cells in spatial gradients of alpha mating factor. Proc. Natl Acad. Sci. USA 90, 8332–8336 (1993).
Nielsen, O. & Davey, J. Pheromone communication in the fission yeast Schizosaccharomyces pombe. Semin. Cell Biol. 6, 95–104 (1995).
Butty, A.C., Pryciak, P.M., Huang, L.S., Herskowitz, I. & Peter, M. The role of Far1p in linking the heterotrimeric G protein to polarity establishment proteins during yeast mating. Science 282, 1511–1516 (1998).
Nern, A. & Arkowitz, R.A. A Cdc24p-Far1p-G beta gamma protein complex required for yeast orientation during mating. J. Cell Biol. 144, 1187–1202 (1999).
Gulli, M.P. & Peter, M. Temporal and spatial regulation of Rho-type guanine-nucleotide exchange factors: the yeast perspective. Genes Dev. 15, 365–379 (2001).
Shimada, Y., Gulli, M.-P. & Peter, M. Nuclear sequestration of the exchange factor Cdc24 by Far1 regulates cell polarity during mating. Nature Cell Biol. 2, 117–124 (2000).
Nern, A. & Arkowitz, R.A. Nucleocytoplasmic shuttling of the Cdc42p exchange factor Cdc24p. J. Cell Biol. 148, 1115–1122 (2000).
Niccoli, T. & Nurse, P. Different mechanisms of cell polarisation in vegetative and shmooing growth in fission yeast. J. Cell Sci. 115, 1651–1662 (2002).
Johnson, D.I. Cdc42: An essential Rho-type GTPase controlling eukaryotic cell polarity. Microbiol. Mol. Biol. Rev. 63, 54–105 (1999).
Bi, E. et al. Identification of novel, evolutionarily conserved Cdc42p-interacting proteins and of redundant pathways linking Cdc24p and Cdc42p to actin polarization in yeast. Mol. Biol. Cell 11, 773–793 (2000).
Drees, B.L. et al. A protein interaction map for cell polarity development. J. Cell Biol. 154, 549–571 (2001).
Pelham, R.J. & Chang, F. Role of actin polymerization and actin cables in actin-patch movement in Schizosaccharomyces pombe. Nature Cell Biol. 3, 235–244 (2001).
Smith, M.G., Swamy, S.R. & Pon, L.A. The life cycle of actin patches in mating yeast. J. Cell Sci. 114, 1505–1513 (2001).
Yang, H.C. & Pon, L.A. Actin cable dynamics in budding yeast. Proc. Natl Acad. Sci. USA 99, 751–756 (2002).
Winter, D., Lechler, T. & Li, R. Activation of the yeast Arp2/3 complex by Bee1p, a WASP-family protein. Curr. Biol. 9, 501–504 (1999).
Lechler, T., Jonsdottir, G.A., Klee, S.K., Pellman, D. & Li, R. A two-tiered mechanism by which Cdc42 controls the localization and activation of an Arp2/3-activating motor complex in yeast. J. Cell Biol. 155, 261–270 (2001).
Evangelista, M. et al. Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276, 118–122 (1997).
Feierbach, B. & Chang, F. Roles of the fission yeast formin for3p in cell polarity, actin cable formation and symmetric cell division. Curr. Biol. 11, 1656–1665 (2001).
Nakano, K. et al. The small GTPase Rho3 and the diaphanous/formin For3 function in polarized cell growth in fission yeast. J. Cell Sci. 115, 4629–4639 (2002).
Evangelista, M., Pruyne, D., Amberg, D.C., Boone, C. & Bretscher, A. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nature Cell Biol. 4, 32–41 (2002).
Sagot, I., Klee, S.K. & Pellman, D. Yeast formins regulate cell polarity by controlling the assembly of actin cables. Nature Cell Biol. 4, 42–50 (2002).
Sawin, K.E. Cell polarity: following formin function. Curr. Biol. 12, R6–R8 (2002).
Pruyne, D. et al. Role of formins in actin assembly: nucleation and barbed-end association. Science 297, 612–615 (2002).
Sagot, I., Rodal, A.A., Moseley, J., Goode, B.L. & Pellman, D. An actin nucleation mechanism mediated by Bni1 and profilin. Nature Cell Biol. 4, 626–631 (2002).
Bahler, J. & Pringle, J.R. Pom1p, a fission yeast protein kinase that provides positional information for both polarized growth and cytokinesis. Genes Dev. 12, 1356–1370 (1998).
Finger, F.P. & Novick, P. Spatial regulation of exocytosis: lessons from yeast. J. Cell Biol. 142, 609–612 (1998).
Pruyne, D.W., Schott, D.H. & Bretscher, A. Tropomyosin-containing actin cables direct the Myo2p-dependent polarized delivery of secretory vesicles in budding yeast. J. Cell Biol. 143, 1931–1945 (1998).
Zhang, X. et al. Cdc42 interacts with the exocyst and regulates polarized secretion. J. Biol Chem. 276, 46745–46750 (2001).
Adamo, J.E. et al. Yeast Cdc42 functions at a late step in exocytosis, specifically during polarized growth of the emerging bud. J. Cell Biol. 155, 581–592 (2001).
Albert, S. & Gallwitz, D. Msb4p, a protein involved in Cdc42p-dependent organization of the actin cytoskeleton, is a Ypt/Rab-specific GAP. Biol. Chem. 381, 453–456 (2000).
Bagnat, M. & Simons, K. Lipid rafts in protein sorting and cell polarity in budding yeast Saccharomyces cerevisiae. Biol. Chem. 383, 1475–1480 (2002).
Bagnat, M. & Simons, K. Cell surface polarization during yeast mating. Proc. Natl Acad. Sci. USA 99, 14183–14188 (2002).
Wachtler, V., Rajagopalan, S. & Balasubramanian, M.K. Sterol-rich plasma membrane domains in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 116, 867–874 (2003).
Audhya, A. & Emr, S.D. Stt4 PI 4-kinase localizes to the plasma membrane and functions in the Pkc1-mediated MAP kinase cascade. Dev. Cell 2, 593–605 (2002).
Barral, Y., Mermall, V., Mooseker, M.S. & Snyder, M. Compartmentalization of the cell cortex by septins is required for maintenance of cell polarity in yeast. Mol. Cell 5, 841–851 (2000).
Takizawa, P.A., DeRisi, J.L., Wilhelm, J.E. & Vale, R.D. Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier. Science 290, 341–344 (2000).
Chang, F. & Nurse, P. How fission yeast fission in the middle. Cell 84, 191–194 (1996).
Chang, F., Woollard, A. & Nurse, P. Isolation and characterization of fission yeast mutants defective in the assembly and placement of the contractile actin ring. J. Cell Sci. 109, 131–142 (1996).
Sohrmann, M., Fankhauser, C., Brodbeck, C. & Simanis, V. The dmf1/mid1 gene is essential for correct positioning of the division septum in fission yeast. Genes Dev. 10, 2707–2719 (1996).
Paoletti, A. & Chang, F. Analysis of mid1p, a protein required for placement of the cell division site, reveals a link between the nucleus and the cell surface in fission yeast. Mol. Biol Cell. 11, 2757–2773 (2000).
Bahler, J. et al. Role of polo kinase and Mid1p in determining the site of cell division in fission yeast. J. Cell Biol. 143, 1603–1616 (1998).
Feierbach, B. & Chang, F. Cytokinesis and the contractile ring in fission yeast. Curr. Opin Microbiol. 4, 713–719 (2001).
Weiner, O.D. Regulation of cell polarity during eukaryotic chemotaxis: the chemotactic compass. Curr. Opin. Cell Biol. 14, 196–202 (2002).
Jin, H. & Amberg, D.C. The secretory pathway mediates localization of the cell polarity regulator Aip3p/Bud6p. Mol. Biol. Cell. 11, 647–661 (2000).
We thank the many colleagues who contributed unpublished results and Y. Barral, M. Gotta. Work in the laboratory of M.P. is supported by the SNF and the ETHZ. F.C. is supported by grants from the National Institutes of Health, American Cancer Society, March of Dimes and the Hirschl Trust.
About this article
Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures
Microbiology and Molecular Biology Reviews (2018)
Genome Biology and Evolution (2018)
Biophysical Reviews (2017)
Bioscience, Biotechnology, and Biochemistry (2016)
Frontiers in Microbiology (2016)