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.

  • Review Article
  • Published:

A regulatory hierarchy for cell specialization in yeast

Nature volume 342, pages 749–757 (1989)Cite this article

Abstract

The specialized sets of genes that determine different cell types in yeast are controlled by combinations of DNA-binding proteins some of which are present only in certain cell types whereas others are present in all cell types. Final differentiation requires an inductive signal that triggers both gene transcription and cell-cycle arrest. Synthesis of the proteins coded by the 'master regulatory' mating-type locus is regulated so as to generate a heterogeneous mitotic cell population containing a stem-cell lineage.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Herskowitz, I. Microbiol. Rev. 52, 536–553 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Cross, F., Hartwell, L. H., Jackson, C. & Konopka, J. B. A. Rev. Cell Biol. 4, 429–57 (1988).

    CAS  Google Scholar 

  3. Nasmyth, K. & Shore, D. Science 237, 1162–1170 (1987).

    ADS  CAS  PubMed  Google Scholar 

  4. Strathern, J., Hicks, J. & Herskowitz, I. J. molec. Biol. 147, 357–372 (1981).

    CAS  PubMed  Google Scholar 

  5. Astell, C. R. et al. Cell 27, 15–23 (1981).

    CAS  PubMed  Google Scholar 

  6. Goutte, C. & Johnson, A. D. Cell 52, 875–882 (1988).

    CAS  PubMed  Google Scholar 

  7. Klar, A. J. S., Strathern, J. N., Broach, J. R. & Hicks, J. B. Nature 289, 239–244 (1981).

    ADS  CAS  PubMed  Google Scholar 

  8. Nasmyth, K. A., Tatchell, K., Hall, B. D., Astell, C. & Smith, M. Nature 289, 244–250 (1981).

    ADS  CAS  PubMed  Google Scholar 

  9. Sprague, G. F. Jr., Jensen, R. & Herskowitz, I. Cell 32, 409–415 (1983).

    CAS  PubMed  Google Scholar 

  10. Wilson, K. L. & Herskowitz, I. Molec. cell. Biol. 4, 2420–2427 (1984).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Jensen, R., Sprague, G. F. Jr. & Herskowitz, I. Proc. natn. Acad. Sci. U.S.A. 80, 3035–3039 (1983).

    ADS  CAS  Google Scholar 

  12. Mitchell, A. P. & Herskowitz, I. Nature 319, 738–742 (1986).

    ADS  CAS  PubMed  Google Scholar 

  13. Jarvis, E. E., Hagen, D. C. & G. F. Sprague, Jr. Molec. cell. Biol. 8, 309–320 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Inokuchi, K., Nakayama, A. & Hishinuma, F. Molec. cell. Biol. 7, 3185–3193 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Johnson, A. D. & Herskowitz, I. Cell 42, 237–247 (1985).

    CAS  PubMed  Google Scholar 

  16. Miller, A. M., MacKay, V. L. & Nasmyth, K. A. Nature 314, 598–603 (1985).

    ADS  CAS  PubMed  Google Scholar 

  17. Keleher, C. A., Goutte, C. & Johnson, A. D. Cell 53, 927–936 (1988).

    CAS  PubMed  Google Scholar 

  18. Bender, A. & Sprague, G. F. Jr Cell 50, 681–691 (1987).

    CAS  PubMed  Google Scholar 

  19. Tan, S., Ammerer, G. & Richmond, T. J. EMBO J. 7, 4255–4264 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Kassir, Y. & Simchen, G. Genetics 82, 187–206 (1976).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Kassir, Y., Granot, D. & Simchen, G. Cell 52, 853–862 (1988).

    CAS  PubMed  Google Scholar 

  22. Keleher, C. A., Passmore, S. & Johnson, A. D. Molec. cell. Biol. 9, 5228–5230 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Passmore, S., Elble, R. & Tye, B.-K. Genes Dev. 3, 921–935 (1989).

    CAS  PubMed  Google Scholar 

  24. Jarvis, E. E., Clark, K. L. & Sprague, G. F. Jr Genes Dev. 3, 936–945 (1989).

    CAS  PubMed  Google Scholar 

  25. Kronstad, J. W., Holly, J. A. & MacKay, V. L. Cell 50, 369–377 (1987).

    CAS  PubMed  Google Scholar 

  26. Passmore, S., Maine, G. T., Elble, R., Christ, C. & Tye, B.-K. J. molec. Biol. 204, 593–606 (1988).

    CAS  PubMed  Google Scholar 

  27. Berry, M., Nunez, A. - M. & Chambon, P. Proc. natn. Acad. Sci. U.S.A. 86, 1218–1222 (1989).

    ADS  CAS  Google Scholar 

  28. Ptashne, M. Nature 335, 683–689 (1988).

    ADS  CAS  PubMed  Google Scholar 

  29. Norman, C., Runswick, M., Pollock, R. & Treisman, R. Cell 55, 989–1003 (1988).

    CAS  PubMed  Google Scholar 

  30. Hayes, T. E., Sengupta, P. & Cochran, B. H. Genes Dev. 2, 1713–1722 (1988).

    CAS  PubMed  Google Scholar 

  31. Johnston, M. A. Microbiol. Rev. 51, 458–476 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Shepard, J. C. W., McGinnis, W., Carrasco, A. E., De Robertis, E. M. & Gehring, W. J. Nature 310, 70–71 (1984).

    ADS  Google Scholar 

  33. Laughon, A. & Scott, M. P. Nature 310, 25–31 (1984).

    Article  ADS  CAS  PubMed  Google Scholar 

  34. He, X. et al. Nature 340, 35–42 (1989).

    ADS  CAS  PubMed  Google Scholar 

  35. Siliciano, P. G. & Tatchell, K. Proc. natn. Acad. Sci. U.S.A. 83, 2320–2324 (1986).

    ADS  CAS  Google Scholar 

  36. Errede, B., Company, M. & Hutchison, C. A. III Molec. cell. Biol. 7, 258–265 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Winston, F., et al. Genetics 115, 649–656 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Stern, M., Jensen, R. E. & Herskowitz, I. J. molec. Biol. 178, 853–868 (1984).

    CAS  PubMed  Google Scholar 

  39. Trueheart, J., Boeke, J. D. & Fink, G. R. Molec. cell. Biol. 7, 2316–2328 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. McCaffrey, G., Clay, F. J., Kelsay, K. & Sprague, G. F. Jr Molec. cell. Biol. 7, 2680–2690 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Hagen, D. C. & Sprague, G. F. Jr J. molec. Biol. 178, 835–852 (1984).

    CAS  PubMed  Google Scholar 

  42. Hartig, A., Holly, J., Saari, G. & MacKay, V. L. Molec. cell. Biol. 6, 2106–2114 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Anderegg, R. J., Betz, R., Carr, S. A., Crabb, J. W. & Duntze, W. J. biol. Chem. 263, 18236–18240 (1988).

    CAS  PubMed  Google Scholar 

  44. Wilkinson, L. W. & Pringle, J. R. Expl Cell Res. 89, 175–189 (1974).

    CAS  Google Scholar 

  45. Bücking-Throm, E., Duntze, W., Hartwell, L. H. & Manney, T. R. Expl Cell Res. 76, 99–110 (1973).

    Google Scholar 

  46. Reed, S. I., Hadwiger, J. A. & Lorincz, A. T. Proc. natn. Acad. Sci. U.S.A. 82, 4055–4059 (1985).

    ADS  CAS  Google Scholar 

  47. Mendenhall, M. D., Jones, C. A. & Reed, S. I. Cell 50, 927–935 (1987).

    CAS  PubMed  Google Scholar 

  48. Pringle, J. R. & Hartwell, L. H. In The Molecular Biology of the Yeast Saccharomyces (eds Strathern, J. N., Jones, E. W. & Brach, J. R.) 97–142 (Cold Spring Harbor Press, New York, 1981).

    Google Scholar 

  49. Marsh, L. & Herskowitz, I. Cold Spring Harb. Symp. quant. Biol. 53, 557–565 (1988).

    CAS  PubMed  Google Scholar 

  50. Dietzel, C. & Kurjan, J. Cell 50, 1001–1010 (1987).

    CAS  PubMed  Google Scholar 

  51. Van Arsdell, S. W., Stetler, G. L. & Thorner, J. Molec. cell. Biol. 7, 749–759 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Teague, M. A., Chaleff, D. T. & Errede, B. Proc. natn. Acad. Sci. U.S.A. 83, 7371–7375 (1986).

    ADS  CAS  Google Scholar 

  53. Dolan, J. W., Kirkman, C. & Fields, S. Proc. natn. Acad. Sci. U.S.A. 86, 5703–5707 (1989).

    ADS  CAS  Google Scholar 

  54. Errede, B. & Ammerer, G. Genes Dev. 3, 1349–1361 (1989).

    CAS  PubMed  Google Scholar 

  55. Sorger, P. K. & Pelham, H. R. B. Cell 54, 855–864 (1988).

    CAS  PubMed  Google Scholar 

  56. Mylin, L. M., Bhat, J. P. & Hopper, J. E. Genes Dev. 3, 1157–1165 (1989).

    CAS  PubMed  Google Scholar 

  57. Fields, S. & Herskowitz, I. Cell 42, 923–930 (1985).

    CAS  PubMed  Google Scholar 

  58. Fields, S., Chaleff, D. T. & Sprague, G. F. Jr Molec. cell. Biol. 8, 551–556 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Weeks, D. L. & Melton, D. A. Cell 51, 861–867 (1987).

    CAS  PubMed  Google Scholar 

  60. Tomlinson, A. & Ready, D. F. Devl Biol. 120, 366–376 (1987).

    CAS  Google Scholar 

  61. Zipursky, S. L. Trends Neurosci. 12, 183–189 (1989).

    CAS  PubMed  Google Scholar 

  62. Sternberg, P. W. & Horvitz, H. R. Cell 58, 679–693 (1989).

    CAS  PubMed  Google Scholar 

  63. Strazdis, J. R. & MacKay, V. L. Nature 305, 543–545 (1983).

    ADS  CAS  PubMed  Google Scholar 

  64. Ingham, P. W. Nature 335, 25–34 (1988).

    ADS  CAS  PubMed  Google Scholar 

  65. Lewis, E. B. Nature 276, 565–570 (1978).

    ADS  CAS  PubMed  Google Scholar 

  66. Hicks, J. B., Strathern, J. N. & Herskowitz, I. in DNA Insertion Elements, Plasmids and Episomes (eds Bukhari, A., Shapiro, J. & Adhya, S.) 457–462 (Cold Spring Harbor Press, New York, 1977).

    Google Scholar 

  67. Herskowitz, I. & Oshima, Y. in The Molecular Biology of the Yeast Saccharomyces cerevisiae: Life Cycle and Inheritance (eds Strathern, J. N., Jones, E. W., & Broach, J. R.) 181–209 (Cold Spring Harbor Press, New York, 1981).

    Google Scholar 

  68. Kostriken, R. & Heffron, F. Cold Spring Harb. Symp. quant. Biol. 49, 89–96 (1984).

    CAS  PubMed  Google Scholar 

  69. Nasmyth, K. Cell 42, 225–235 (1985).

    CAS  PubMed  Google Scholar 

  70. Nasmyth, K. Nature 302, 670–676 (1983).

    ADS  CAS  PubMed  Google Scholar 

  71. Strathern, J. N. & Herskowitz, I. Cell 17, 371–381 (1979).

    CAS  PubMed  Google Scholar 

  72. Nasmyth, K. Cell 42, 213–223 (1985).

    CAS  PubMed  Google Scholar 

  73. Breeden, L. & Nasmyth, K. Cell 48, 389–397 (1987).

    CAS  PubMed  Google Scholar 

  74. Sternberg, P. W., Stern, M. J., Clark, I. & Herskowitz, I. Cell 48, 567–577 (1987).

    CAS  PubMed  Google Scholar 

  75. Nasmyth, K., Stillman, D. & Kipling, D. Cell 48, 579–587 (1987).

    CAS  PubMed  Google Scholar 

  76. Andrews, B. J. & Herskowitz, I. Cell 57, 21–29 (1989).

    CAS  PubMed  Google Scholar 

  77. Cisek, L. J. & Corden, J. L. Nature 339, 679–684 (1989).

    ADS  CAS  PubMed  Google Scholar 

  78. Stillman, D. J., Bankier, A. T., Seddon, A., Groenhout, E. G. & Nasmyth, K. A. EMBO J. 7, 485–494 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Nagai, K., Nakesoko, Y., Nasmyth, K. & Rhodes, D. Nature 332, 284–286 (1988).

    ADS  CAS  PubMed  Google Scholar 

  80. Nasmyth, K., Seddon, A. & Ammerer, G. Cell 49, 549–558 (1987).

    CAS  PubMed  Google Scholar 

  81. Guarente, L., Lalonde, B., Gifford, P. & Alani, E. Cell 36, 503–511 (1983).

    Google Scholar 

  82. Beach, D., Durkacz, B. & Nurse, P. Nature 300, 706–709 (1982).

    ADS  CAS  PubMed  Google Scholar 

  83. Gautier, J., Norbury, C., Lohka, M., Nurse, P. & Maller, J. Cell 54, 433–439 (1988).

    CAS  PubMed  Google Scholar 

  84. Breeden, L. & Nasmyth, K. Nature 329, 651–654 (1987).

    ADS  CAS  PubMed  Google Scholar 

  85. Yochem, J. & Greenwald, I. Cell 58, 553–563 (1989).

    CAS  PubMed  Google Scholar 

  86. Biggin, M. D. & Tjian, R. Cell 58, 433–440 (1989).

    CAS  PubMed  Google Scholar 

  87. Herskowitz, I. Cold Spring Harb. Symp. quant. Biol. 50, 565–574 (1985).

    CAS  PubMed  Google Scholar 

  88. Lindegren, C. C. & Lindegren, G. Ann. Mo. bot. Gdn 30, 453–469 (1943).

    Google Scholar 

  89. MacKay, V. L. & Manney, T. R. Genetics 76, 273–288 (1974).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Blau, H. M. Cell 53, 673–674 (1988).

    CAS  PubMed  Google Scholar 

  91. Moses, K., Ellis, M. C. & Rubin, G. M. Nature 340, 531–536 (1989).

    ADS  CAS  PubMed  Google Scholar 

  92. Bodner, M. et al. Cell 55, 505–518 (1988).

    CAS  PubMed  Google Scholar 

  93. Ingraham, H. A. et al. Cell 55, 519–529 (1988).

    CAS  PubMed  Google Scholar 

  94. Davis, R. L., Weintraub, H. & Lassar, A. B. Cell 51, 987–1000 (1987).

    CAS  PubMed  Google Scholar 

  95. Wright, W. E., Sassoon, D. A. & Lin, V. K. Cell 56, 607–617 (1989).

    CAS  PubMed  Google Scholar 

  96. Edmondson, D. G. & Olson, E. N. Genes Dev. 3, 628–640 (1989).

    CAS  PubMed  Google Scholar 

  97. Braun, T., Buschhausen-Denker, G., Bober, E., Tannich, E. & Arnold, H. H. EMBO J. 8, 701–709 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Weintraub, H. et al. Proc. natn. Acad. Sci. U.S.A. 86, 5434–5438 (1989).

    ADS  CAS  Google Scholar 

  99. Ammerer, G., Sprague, G. F. Jr & Bender, A. Proc. natn. Acad. Sci. U.S.A. 82, 5855–5859 (1985).

    ADS  CAS  Google Scholar 

  100. Fields, S. & Herskowitz, I. Molec. cell. Biol. 7, 3818–3821 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Flessel, M. C., Brake, A. J. & Thorner, J. Genetics 121, 223–236 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Herskowitz, I. Nature 329, 219–222 (1987).

    ADS  CAS  PubMed  Google Scholar 

  103. Driever, W. & Nüsslein-Volhard, C. Nature 337, 138–143 (1989).

    ADS  CAS  PubMed  Google Scholar 

  104. Baker, B. S. Nature 340, 521–524 (1989).

    ADS  CAS  PubMed  Google Scholar 

  105. McGrath, J. P. & Varshavsky, A. Nature 340, 400–404 (1989).

    ADS  CAS  PubMed  Google Scholar 

  106. Elder, R. T., St. John, T. P., Stinchcomb, D. T. & Davis, R. W. Cold Spring Harb. Symp. quant. Biol. 45, 581–584 (1981).

    CAS  PubMed  Google Scholar 

  107. Errede, B., Cardillo, T. S., Wever, G. & Sherman, F. Cold Spring Harb. Symp. quant. Biol. 45, 593–602 (1981).

    CAS  PubMed  Google Scholar 

  108. Whiteway, M. et al. Cell 56, 467–477 (1989).

    CAS  PubMed  Google Scholar 

  109. Dranginis, A. Molec. cell. Biol. 9, 3992–3998 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Miyajima, I. et al. Cell 50, 1011–1019 (1987).

    CAS  PubMed  Google Scholar 

  111. Jahng, K.-Y., Ferguson, J. & Reed, S. I. Molec. cell. Biol. 8, 1440–1448 (1988).

    Google Scholar 

  112. Ivy, J. M., Klar, A. J. S. & Hicks, J. B. Molec. cell. Biol. 6, 688–702 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Strathern, J. N. et al. Cell 31, 183–192 (1982).

    CAS  PubMed  Google Scholar 

  114. Sauer, R. T., Smith, D. L. & Johnson, A. D. Genes Dev. 2, 1713–1722 (1988).

    Google Scholar 

  115. Andrews, B. J. & Herskowitz, I. Nature (in the press).

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry and Biophysics, University of California, San Francisco, California, 94143, USA

    Ira Herskowitz

Authors
  1. Ira Herskowitz
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Herskowitz, I. A regulatory hierarchy for cell specialization in yeast. Nature 342, 749–757 (1989). https://doi.org/10.1038/342749a0

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/342749a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced 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