Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Yeasts make their mark

Abstract

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 options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Intrinsic spatial cues establish sites of polarized cell growth and division.
Figure 2: Polarity pathways in S. cerevisiae during budding and mating.
Figure 3: Model for microtubule regulation of cell polarity in fission yeast.

References

  1. 1

    Bähler J. & Peter, M. in Frontiers in Molecular Biology, Vol. Cell polarity, 21–77 (Oxford Univ. Press, Oxford, 2000).

    Google Scholar 

  2. 2

    Pruyne, D. & Bretscher, A. Polarization of cell growth in yeast. J. Cell Sci. 113, 571–585 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. 3

    Pruyne, D. & Bretscher, A. Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J. Cell Sci. 113, 365–375 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. 4

    Chang, F. Establishment of a cellular axis in fission yeast. Trends Genet. 17, 273–278 (2001).

    CAS  Google Scholar 

  5. 5

    Schott, D., Huffaker, T. & Bretscher, A. Microfilaments and microtubules: the news from yeast. Curr. Opin Microbiol. 5, 564–574 (2002).

    CAS  PubMed  Google Scholar 

  6. 6

    Lew, D.J. & Reed, S.I. Morphogenesis in the yeast cell cycle: Regulation by Cdc28 and cyclins. J. Cell Biol. 120, 1305–1320 (1993).

    CAS  PubMed  Google Scholar 

  7. 7

    Mitchison, J.M. & Nurse, P. Growth in cell length in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 75, 357–376 (1985).

    CAS  Google Scholar 

  8. 8

    Drubin, D.G. Development of cell polarity in budding yeast. Cell 65, 1093–1096 (1991).

    CAS  PubMed  Google Scholar 

  9. 9

    Pringle, J.R. et al. Establishment of cell polarity in yeast. Cold Spring Harb. Symp. Quant. Biol. 60, 729–744 (1995).

    CAS  PubMed  Google Scholar 

  10. 10

    Chant, J. Cell polarity in yeast. Annu. Rev. Cell Dev. Biol. 15, 365–391 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. 11

    Madden, K. & Snyder, M. Cell polarity and morphogenesis in budding yeast. Annu. Rev. Microbiol. 52, 687–744 (1998).

    CAS  PubMed  Google Scholar 

  12. 12

    Longtine, M.S. et al. The septins: roles in cytokinesis and other processes. Curr. Opin. Cell Biol. 8, 106–119 (1996).

    CAS  PubMed  Google Scholar 

  13. 13

    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).

    CAS  PubMed  Google Scholar 

  14. 14

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 15

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. 16

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. 17

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. 18

    Chen, T. et al. Multigenerational cortical inheritance of the Rax2 protein in orienting polarity and division in yeast. Science 290, 1975–1978 (2000).

    CAS  PubMed  Google Scholar 

  19. 19

    Ni, L. & Snyder, M. A genomic study of the bipolar bud site selection pattern in Saccharomyces cerevisiae. Mol. Biol. Cell 12, 2147–2170 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 20

    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).

    CAS  PubMed  Google Scholar 

  21. 21

    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).

    CAS  PubMed  Google Scholar 

  22. 22

    Drummond, D.R. & Cross, R.A. Dynamics of interphase microtubules in Schizosaccharomyces pombe. Curr. Biol. 10, 766–775 (2000).

    CAS  PubMed  Google Scholar 

  23. 23

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. 24

    Brunner, D. & Nurse, P. CLIP170-like tip1p spatially organizes microtubular dynamics in fission yeast. Cell 102, 695–704 (2000).

    CAS  Google Scholar 

  25. 25

    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).

    CAS  Google Scholar 

  26. 26

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. 28

    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).

    CAS  Google Scholar 

  29. 29

    Arellano, M., Niccoli, T. & Nurse, P. Tea3p is a cell end marker activating polarized growth in Schizosaccharomyces pombe. Curr. Biol. 12, 751–756 (2002).

    CAS  PubMed  Google Scholar 

  30. 30

    Sawin, K.E. & Nurse, P. Regulation of cell polarity by microtubules in fission yeast. J. Cell Biol. 142, 457–471 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. 31

    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).

    CAS  PubMed  Google Scholar 

  32. 32

    Chant, J. Cell polarity in yeast. Trends Genet. 10, 328–333 (1994).

    CAS  PubMed  Google Scholar 

  33. 33

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. 34

    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).

    CAS  PubMed  Google Scholar 

  35. 35

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. 36

    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).

    CAS  PubMed  Google Scholar 

  37. 37

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. 38

    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).

    CAS  PubMed  Google Scholar 

  39. 39

    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).

    CAS  PubMed  Google Scholar 

  40. 40

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. 41

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. 42

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. 43

    Segall, J.E. Polarization of yeast cells in spatial gradients of alpha mating factor. Proc. Natl Acad. Sci. USA 90, 8332–8336 (1993).

    CAS  PubMed  Google Scholar 

  44. 44

    Nielsen, O. & Davey, J. Pheromone communication in the fission yeast Schizosaccharomyces pombe. Semin. Cell Biol. 6, 95–104 (1995).

    CAS  PubMed  Google Scholar 

  45. 45

    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).

    CAS  PubMed  Google Scholar 

  46. 46

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. 47

    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).

    CAS  PubMed  Google Scholar 

  48. 48

    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).

    CAS  Google Scholar 

  49. 49

    Nern, A. & Arkowitz, R.A. Nucleocytoplasmic shuttling of the Cdc42p exchange factor Cdc24p. J. Cell Biol. 148, 1115–1122 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. 50

    Niccoli, T. & Nurse, P. Different mechanisms of cell polarisation in vegetative and shmooing growth in fission yeast. J. Cell Sci. 115, 1651–1662 (2002).

    CAS  PubMed  Google Scholar 

  51. 51

    Johnson, D.I. Cdc42: An essential Rho-type GTPase controlling eukaryotic cell polarity. Microbiol. Mol. Biol. Rev. 63, 54–105 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. 52

    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).

    CAS  Google Scholar 

  53. 53

    Drees, B.L. et al. A protein interaction map for cell polarity development. J. Cell Biol. 154, 549–571 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54

    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).

    CAS  PubMed  Google Scholar 

  55. 55

    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).

    CAS  PubMed  Google Scholar 

  56. 56

    Yang, H.C. & Pon, L.A. Actin cable dynamics in budding yeast. Proc. Natl Acad. Sci. USA 99, 751–756 (2002).

    CAS  PubMed  Google Scholar 

  57. 57

    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).

    CAS  PubMed  Google Scholar 

  58. 58

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. 59

    Evangelista, M. et al. Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276, 118–122 (1997).

    CAS  PubMed  Google Scholar 

  60. 60

    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).

    CAS  Google Scholar 

  61. 61

    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).

    CAS  PubMed  Google Scholar 

  62. 62

    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).

    CAS  Google Scholar 

  63. 63

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. 64

    Sawin, K.E. Cell polarity: following formin function. Curr. Biol. 12, R6–R8 (2002).

    CAS  PubMed  Google Scholar 

  65. 65

    Pruyne, D. et al. Role of formins in actin assembly: nucleation and barbed-end association. Science 297, 612–615 (2002).

    CAS  PubMed  Google Scholar 

  66. 66

    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).

    CAS  PubMed  Google Scholar 

  67. 67

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. 68

    Finger, F.P. & Novick, P. Spatial regulation of exocytosis: lessons from yeast. J. Cell Biol. 142, 609–612 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. 69

    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).

    CAS  PubMed  Google Scholar 

  70. 70

    Zhang, X. et al. Cdc42 interacts with the exocyst and regulates polarized secretion. J. Biol Chem. 276, 46745–46750 (2001).

    CAS  PubMed  Google Scholar 

  71. 71

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. 72

    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).

    CAS  PubMed  Google Scholar 

  73. 73

    Bagnat, M. & Simons, K. Lipid rafts in protein sorting and cell polarity in budding yeast Saccharomyces cerevisiae. Biol. Chem. 383, 1475–1480 (2002).

    CAS  PubMed  Google Scholar 

  74. 74

    Bagnat, M. & Simons, K. Cell surface polarization during yeast mating. Proc. Natl Acad. Sci. USA 99, 14183–14188 (2002).

    CAS  PubMed  Google Scholar 

  75. 75

    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).

    CAS  PubMed  Google Scholar 

  76. 76

    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).

    CAS  PubMed  Google Scholar 

  77. 77

    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).

    CAS  PubMed  Google Scholar 

  78. 78

    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).

    CAS  PubMed  Google Scholar 

  79. 79

    Chang, F. & Nurse, P. How fission yeast fission in the middle. Cell 84, 191–194 (1996).

    CAS  PubMed  Google Scholar 

  80. 80

    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).

    CAS  PubMed  Google Scholar 

  81. 81

    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).

    CAS  PubMed  Google Scholar 

  82. 82

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. 83

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. 84

    Feierbach, B. & Chang, F. Cytokinesis and the contractile ring in fission yeast. Curr. Opin Microbiol. 4, 713–719 (2001).

    CAS  PubMed  Google Scholar 

  85. 85

    Weiner, O.D. Regulation of cell polarity during eukaryotic chemotaxis: the chemotactic compass. Curr. Opin. Cell Biol. 14, 196–202 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. 86

    Jin, H. & Amberg, D.C. The secretory pathway mediates localization of the cell polarity regulator Aip3p/Bud6p. Mol. Biol. Cell. 11, 647–661 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

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.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Fred Chang.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Chang, F., Peter, M. Yeasts make their mark. Nat Cell Biol 5, 294–299 (2003). https://doi.org/10.1038/ncb0403-294

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing