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. 1999 Apr;151(4):1327–1340. doi: 10.1093/genetics/151.4.1327

Distinct steps in yeast spore morphogenesis require distinct SMK1 MAP kinase thresholds.

M Wagner 1, P Briza 1, M Pierce 1, E Winter 1
PMCID: PMC1460549  PMID: 10101160

Abstract

The SMK1 mitogen-activated protein kinase is required for spore morphogenesis in Saccharomyces cerevisiae. In contrast to the multiple aberrant spore wall assembly patterns seen even within a single smk1 null ascus, different smk1 missense mutants block in a coordinated fashion at intermediate stages. One smk1 mutant forms asci in which the four spores are surrounded only by prospore wall-like structures, while another smk1 mutant forms asci in which the spores are surrounded by inner but not outer spore wall layers. Stepwise increases in gene dosage of a hypomorphic smk1 allele allow for the completion of progressively later morphological and biochemical events and for the acquisition of distinct spore-resistance phenotypes. Furthermore, smk1 allelic spore phenotypes can be recapitulated by reducing wild-type SMK1 expression. The data demonstrate that SMK1 is required for the execution of multiple steps in spore morphogenesis that require increasing thresholds of SMK1 activity. These results suggest that quantitative changes in mitogen-activated protein kinase signaling play a role in coordinating multiple events of a single cellular differentiation program.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alani E., Padmore R., Kleckner N. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell. 1990 May 4;61(3):419–436. doi: 10.1016/0092-8674(90)90524-i. [DOI] [PubMed] [Google Scholar]
  2. Blenis J. Signal transduction via the MAP kinases: proceed at your own RSK. Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):5889–5892. doi: 10.1073/pnas.90.13.5889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blumer K. J., Johnson G. L. Diversity in function and regulation of MAP kinase pathways. Trends Biochem Sci. 1994 Jun;19(6):236–240. doi: 10.1016/0968-0004(94)90147-3. [DOI] [PubMed] [Google Scholar]
  4. Briza P., Breitenbach M., Ellinger A., Segall J. Isolation of two developmentally regulated genes involved in spore wall maturation in Saccharomyces cerevisiae. Genes Dev. 1990 Oct;4(10):1775–1789. doi: 10.1101/gad.4.10.1775. [DOI] [PubMed] [Google Scholar]
  5. Briza P., Eckerstorfer M., Breitenbach M. The sporulation-specific enzymes encoded by the DIT1 and DIT2 genes catalyze a two-step reaction leading to a soluble LL-dityrosine-containing precursor of the yeast spore wall. Proc Natl Acad Sci U S A. 1994 May 10;91(10):4524–4528. doi: 10.1073/pnas.91.10.4524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Briza P., Ellinger A., Winkler G., Breitenbach M. Characterization of a DL-dityrosine-containing macromolecule from yeast ascospore walls. J Biol Chem. 1990 Sep 5;265(25):15118–15123. [PubMed] [Google Scholar]
  7. Briza P., Ellinger A., Winkler G., Breitenbach M. Chemical composition of the yeast ascospore wall. The second outer layer consists of chitosan. J Biol Chem. 1988 Aug 15;263(23):11569–11574. [PubMed] [Google Scholar]
  8. Briza P., Winkler G., Kalchhauser H., Breitenbach M. Dityrosine is a prominent component of the yeast ascospore wall. A proof of its structure. J Biol Chem. 1986 Mar 25;261(9):4288–4294. [PubMed] [Google Scholar]
  9. Carr A. M., MacNeill S. A., Hayles J., Nurse P. Molecular cloning and sequence analysis of mutant alleles of the fission yeast cdc2 protein kinase gene: implications for cdc2+ protein structure and function. Mol Gen Genet. 1989 Jul;218(1):41–49. doi: 10.1007/BF00330563. [DOI] [PubMed] [Google Scholar]
  10. Christodoulidou A., Bouriotis V., Thireos G. Two sporulation-specific chitin deacetylase-encoding genes are required for the ascospore wall rigidity of Saccharomyces cerevisiae. J Biol Chem. 1996 Dec 6;271(49):31420–31425. doi: 10.1074/jbc.271.49.31420. [DOI] [PubMed] [Google Scholar]
  11. Dawes I. W., Hardie I. D. Selective killing of vegetative cells in sporulated yeast cultures by exposure to diethyl ether. Mol Gen Genet. 1974;131(4):281–289. doi: 10.1007/BF00264859. [DOI] [PubMed] [Google Scholar]
  12. Eisenmann D. M., Kim S. K. Signal transduction and cell fate specification during Caenorhabditis elegans vulval development. Curr Opin Genet Dev. 1994 Aug;4(4):508–516. doi: 10.1016/0959-437x(94)90065-b. [DOI] [PubMed] [Google Scholar]
  13. Elion E. A., Satterberg B., Kranz J. E. FUS3 phosphorylates multiple components of the mating signal transduction cascade: evidence for STE12 and FAR1. Mol Biol Cell. 1993 May;4(5):495–510. doi: 10.1091/mbc.4.5.495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Espinoza F. H., Farrell A., Erdjument-Bromage H., Tempst P., Morgan D. O. A cyclin-dependent kinase-activating kinase (CAK) in budding yeast unrelated to vertebrate CAK. Science. 1996 Sep 20;273(5282):1714–1717. doi: 10.1126/science.273.5282.1714. [DOI] [PubMed] [Google Scholar]
  15. Esposito R. E., Dresser M., Breitenbach M. Identifying sporulation genes, visualizing synaptonemal complexes, and large-scale spore and spore wall purification. Methods Enzymol. 1991;194:110–131. doi: 10.1016/0076-6879(91)94010-a. [DOI] [PubMed] [Google Scholar]
  16. Firtel R. A. Integration of signaling information in controlling cell-fate decisions in Dictyostelium. Genes Dev. 1995 Jun 15;9(12):1427–1444. doi: 10.1101/gad.9.12.1427. [DOI] [PubMed] [Google Scholar]
  17. Friesen H., Lunz R., Doyle S., Segall J. Mutation of the SPS1-encoded protein kinase of Saccharomyces cerevisiae leads to defects in transcription and morphology during spore formation. Genes Dev. 1994 Sep 15;8(18):2162–2175. doi: 10.1101/gad.8.18.2162. [DOI] [PubMed] [Google Scholar]
  18. Gaskins C., Clark A. M., Aubry L., Segall J. E., Firtel R. A. The Dictyostelium MAP kinase ERK2 regulates multiple, independent developmental pathways. Genes Dev. 1996 Jan 1;10(1):118–128. doi: 10.1101/gad.10.1.118. [DOI] [PubMed] [Google Scholar]
  19. Glise B., Noselli S. Coupling of Jun amino-terminal kinase and Decapentaplegic signaling pathways in Drosophila morphogenesis. Genes Dev. 1997 Jul 1;11(13):1738–1747. doi: 10.1101/gad.11.13.1738. [DOI] [PubMed] [Google Scholar]
  20. Gotoh Y., Masuyama N., Suzuki A., Ueno N., Nishida E. Involvement of the MAP kinase cascade in Xenopus mesoderm induction. EMBO J. 1995 Jun 1;14(11):2491–2498. doi: 10.1002/j.1460-2075.1995.tb07246.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Guan K. L. The mitogen activated protein kinase signal transduction pathway: from the cell surface to the nucleus. Cell Signal. 1994 Aug;6(6):581–589. doi: 10.1016/0898-6568(94)90041-8. [DOI] [PubMed] [Google Scholar]
  22. Hanks S. K., Quinn A. M., Hunter T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science. 1988 Jul 1;241(4861):42–52. doi: 10.1126/science.3291115. [DOI] [PubMed] [Google Scholar]
  23. Hsu J. C., Perrimon N. A temperature-sensitive MEK mutation demonstrates the conservation of the signaling pathways activated by receptor tyrosine kinases. Genes Dev. 1994 Sep 15;8(18):2176–2187. doi: 10.1101/gad.8.18.2176. [DOI] [PubMed] [Google Scholar]
  24. Kaldis P., Sutton A., Solomon M. J. The Cdk-activating kinase (CAK) from budding yeast. Cell. 1996 Aug 23;86(4):553–564. doi: 10.1016/s0092-8674(00)80129-4. [DOI] [PubMed] [Google Scholar]
  25. Krisak L., Strich R., Winters R. S., Hall J. P., Mallory M. J., Kreitzer D., Tuan R. S., Winter E. SMK1, a developmentally regulated MAP kinase, is required for spore wall assembly in Saccharomyces cerevisiae. Genes Dev. 1994 Sep 15;8(18):2151–2161. doi: 10.1101/gad.8.18.2151. [DOI] [PubMed] [Google Scholar]
  26. LaBonne C., Burke B., Whitman M. Role of MAP kinase in mesoderm induction and axial patterning during Xenopus development. Development. 1995 May;121(5):1475–1486. doi: 10.1242/dev.121.5.1475. [DOI] [PubMed] [Google Scholar]
  27. Marshall C. J. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell. 1995 Jan 27;80(2):179–185. doi: 10.1016/0092-8674(95)90401-8. [DOI] [PubMed] [Google Scholar]
  28. Peter M., Gartner A., Horecka J., Ammerer G., Herskowitz I. FAR1 links the signal transduction pathway to the cell cycle machinery in yeast. Cell. 1993 May 21;73(4):747–760. doi: 10.1016/0092-8674(93)90254-n. [DOI] [PubMed] [Google Scholar]
  29. Rothstein R. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 1991;194:281–301. doi: 10.1016/0076-6879(91)94022-5. [DOI] [PubMed] [Google Scholar]
  30. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Thuret J. Y., Valay J. G., Faye G., Mann C. Civ1 (CAK in vivo), a novel Cdk-activating kinase. Cell. 1996 Aug 23;86(4):565–576. doi: 10.1016/s0092-8674(00)80130-0. [DOI] [PubMed] [Google Scholar]
  32. Umbhauer M., Marshall C. J., Mason C. S., Old R. W., Smith J. C. Mesoderm induction in Xenopus caused by activation of MAP kinase. Nature. 1995 Jul 6;376(6535):58–62. doi: 10.1038/376058a0. [DOI] [PubMed] [Google Scholar]
  33. Wagner M., Pierce M., Winter E. The CDK-activating kinase CAK1 can dosage suppress sporulation defects of smk1 MAP kinase mutants and is required for spore wall morphogenesis in Saccharomyces cerevisiae. EMBO J. 1997 Mar 17;16(6):1305–1317. doi: 10.1093/emboj/16.6.1305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Waskiewicz A. J., Cooper J. A. Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast. Curr Opin Cell Biol. 1995 Dec;7(6):798–805. doi: 10.1016/0955-0674(95)80063-8. [DOI] [PubMed] [Google Scholar]

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