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. 2001 Jun;158(2):549–562. doi: 10.1093/genetics/158.2.549

A role for the Swe1 checkpoint kinase during filamentous growth of Saccharomyces cerevisiae.

R La Valle 1, C Wittenberg 1
PMCID: PMC1461683  PMID: 11404321

Abstract

In this study we show that inactivation of Hsl1 or Hsl7, negative regulators of the Swe1 kinase, enhances the invasive behavior of haploid and diploid cells. The enhancement of filamentous growth caused by inactivation of both genes is mediated via the Swe1 protein kinase. Whereas Swe1 contributes noticeably to the effectiveness of haploid invasive growth under all conditions tested, its contribution to pseudohyphal growth is limited to the morphological response under standard assay conditions. However, Swe1 is essential for pseudohyphal differentiation under a number of nonstandard assay conditions including altered temperature and increased nitrogen. Swe1 is also required for pseudohyphal growth in the absence of Tec1 and for the induction of filamentation by butanol, a related phenomenon. Although inactivation of Hsl1 is sufficient to suppress the defect in filamentous growth caused by inactivation of Tec1 or Flo8, it is insufficient to promote filamentous growth in the absence of both factors. Moreover, inactivation of Hsl1 will not bypass the requirement for nitrogen starvation or growth on solid medium for pseudohyphal differentiation. We conclude that the Swe1 kinase modulates filamentous development under a broad spectrum of conditions and that its role is partially redundant with the Tec1 and Flo8 transcription factors.

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Selected References

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  1. Ahn S. H., Acurio A., Kron S. J. Regulation of G2/M progression by the STE mitogen-activated protein kinase pathway in budding yeast filamentous growth. Mol Biol Cell. 1999 Oct;10(10):3301–3316. doi: 10.1091/mbc.10.10.3301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alspaugh J. A., Perfect J. R., Heitman J. Cryptococcus neoformans mating and virulence are regulated by the G-protein alpha subunit GPA1 and cAMP. Genes Dev. 1997 Dec 1;11(23):3206–3217. doi: 10.1101/gad.11.23.3206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Banuett F., Herskowitz I. Identification of fuz7, a Ustilago maydis MEK/MAPKK homolog required for a-locus-dependent and -independent steps in the fungal life cycle. Genes Dev. 1994 Jun 15;8(12):1367–1378. doi: 10.1101/gad.8.12.1367. [DOI] [PubMed] [Google Scholar]
  4. Barral Y., Parra M., Bidlingmaier S., Snyder M. Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast. Genes Dev. 1999 Jan 15;13(2):176–187. doi: 10.1101/gad.13.2.176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Berning C. K., Griffith J. F., Wild J. E. Research on the effectiveness of denatonium benzoate as a deterrent to liquid detergent ingestion by children. Fundam Appl Toxicol. 1982 Jan-Feb;2(1):44–48. doi: 10.1016/s0272-0590(82)80063-8. [DOI] [PubMed] [Google Scholar]
  6. Blacketer M. J., Madaule P., Myers A. M. Mutational analysis of morphologic differentiation in Saccharomyces cerevisiae. Genetics. 1995 Aug;140(4):1259–1275. doi: 10.1093/genetics/140.4.1259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Booher R. N., Deshaies R. J., Kirschner M. W. Properties of Saccharomyces cerevisiae wee1 and its differential regulation of p34CDC28 in response to G1 and G2 cyclins. EMBO J. 1993 Sep;12(9):3417–3426. doi: 10.1002/j.1460-2075.1993.tb06016.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Borges-Walmsley M. I., Walmsley A. R. cAMP signalling in pathogenic fungi: control of dimorphic switching and pathogenicity. Trends Microbiol. 2000 Mar;8(3):133–141. doi: 10.1016/s0966-842x(00)01698-x. [DOI] [PubMed] [Google Scholar]
  9. Dickinson J. R. 'Fusel' alcohols induce hyphal-like extensions and pseudohyphal formation in yeasts. Microbiology. 1996 Jun;142(Pt 6):1391–1397. doi: 10.1099/13500872-142-6-1391. [DOI] [PubMed] [Google Scholar]
  10. Edgington N. P., Blacketer M. J., Bierwagen T. A., Myers A. M. Control of Saccharomyces cerevisiae filamentous growth by cyclin-dependent kinase Cdc28. Mol Cell Biol. 1999 Feb;19(2):1369–1380. doi: 10.1128/mcb.19.2.1369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fujita A., Tonouchi A., Hiroko T., Inose F., Nagashima T., Satoh R., Tanaka S. Hsl7p, a negative regulator of Ste20p protein kinase in the Saccharomyces cerevisiae filamentous growth-signaling pathway. Proc Natl Acad Sci U S A. 1999 Jul 20;96(15):8522–8527. doi: 10.1073/pnas.96.15.8522. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gavrias V., Andrianopoulos A., Gimeno C. J., Timberlake W. E. Saccharomyces cerevisiae TEC1 is required for pseudohyphal growth. Mol Microbiol. 1996 Mar;19(6):1255–1263. doi: 10.1111/j.1365-2958.1996.tb02470.x. [DOI] [PubMed] [Google Scholar]
  13. Gietz R. D., Sugino A. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene. 1988 Dec 30;74(2):527–534. doi: 10.1016/0378-1119(88)90185-0. [DOI] [PubMed] [Google Scholar]
  14. Gimeno C. J., Fink G. R. Induction of pseudohyphal growth by overexpression of PHD1, a Saccharomyces cerevisiae gene related to transcriptional regulators of fungal development. Mol Cell Biol. 1994 Mar;14(3):2100–2112. doi: 10.1128/mcb.14.3.2100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gimeno C. J., Ljungdahl P. O., Styles C. A., Fink G. R. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell. 1992 Mar 20;68(6):1077–1090. doi: 10.1016/0092-8674(92)90079-r. [DOI] [PubMed] [Google Scholar]
  16. Gold S. E., Brogdon S. M., Mayorga M. E., Kronstad J. W. The Ustilago maydis regulatory subunit of a cAMP-dependent protein kinase is required for gall formation in maize. Plant Cell. 1997 Sep;9(9):1585–1594. doi: 10.1105/tpc.9.9.1585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gold S., Duncan G., Barrett K., Kronstad J. cAMP regulates morphogenesis in the fungal pathogen Ustilago maydis. Genes Dev. 1994 Dec 1;8(23):2805–2816. doi: 10.1101/gad.8.23.2805. [DOI] [PubMed] [Google Scholar]
  18. Grenson M., Mousset M., Wiame J. M., Bechet J. Multiplicity of the amino acid permeases in Saccharomyces cerevisiae. I. Evidence for a specific arginine-transporting system. Biochim Biophys Acta. 1966 Oct 31;127(2):325–338. doi: 10.1016/0304-4165(66)90387-4. [DOI] [PubMed] [Google Scholar]
  19. Imam N., Carpenter C. C., Mayer K. H., Fisher A., Stein M., Danforth S. B. Hierarchical pattern of mucosal candida infections in HIV-seropositive women. Am J Med. 1990 Aug;89(2):142–146. doi: 10.1016/0002-9343(90)90291-k. [DOI] [PubMed] [Google Scholar]
  20. Kaiser P., Moncollin V., Clarke D. J., Watson M. H., Bertolaet B. L., Reed S. I., Bailly E. Cyclin-dependent kinase and Cks/Suc1 interact with the proteasome in yeast to control proteolysis of M-phase targets. Genes Dev. 1999 May 1;13(9):1190–1202. doi: 10.1101/gad.13.9.1190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kron S. J., Styles C. A., Fink G. R. Symmetric cell division in pseudohyphae of the yeast Saccharomyces cerevisiae. Mol Biol Cell. 1994 Sep;5(9):1003–1022. doi: 10.1091/mbc.5.9.1003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Köhler J. R., Fink G. R. Candida albicans strains heterozygous and homozygous for mutations in mitogen-activated protein kinase signaling components have defects in hyphal development. Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13223–13228. doi: 10.1073/pnas.93.23.13223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Leberer E., Harcus D., Broadbent I. D., Clark K. L., Dignard D., Ziegelbauer K., Schmidt A., Gow N. A., Brown A. J., Thomas D. Y. Signal transduction through homologs of the Ste20p and Ste7p protein kinases can trigger hyphal formation in the pathogenic fungus Candida albicans. Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13217–13222. doi: 10.1073/pnas.93.23.13217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Leberer E., Ziegelbauer K., Schmidt A., Harcus D., Dignard D., Ash J., Johnson L., Thomas D. Y. Virulence and hyphal formation of Candida albicans require the Ste20p-like protein kinase CaCla4p. Curr Biol. 1997 Aug 1;7(8):539–546. doi: 10.1016/s0960-9822(06)00252-1. [DOI] [PubMed] [Google Scholar]
  25. Lew D. J., Reed S. I. A cell cycle checkpoint monitors cell morphogenesis in budding yeast. J Cell Biol. 1995 May;129(3):739–749. doi: 10.1083/jcb.129.3.739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Liu H., Köhler J., Fink G. R. Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science. 1994 Dec 9;266(5191):1723–1726. doi: 10.1126/science.7992058. [DOI] [PubMed] [Google Scholar]
  27. Liu H., Styles C. A., Fink G. R. Saccharomyces cerevisiae S288C has a mutation in FLO8, a gene required for filamentous growth. Genetics. 1996 Nov;144(3):967–978. doi: 10.1093/genetics/144.3.967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lo W. S., Dranginis A. M. The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. Mol Biol Cell. 1998 Jan;9(1):161–171. doi: 10.1091/mbc.9.1.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Loeb J. D., Kerentseva T. A., Pan T., Sepulveda-Becerra M., Liu H. Saccharomyces cerevisiae G1 cyclins are differentially involved in invasive and pseudohyphal growth independent of the filamentation mitogen-activated protein kinase pathway. Genetics. 1999 Dec;153(4):1535–1546. doi: 10.1093/genetics/153.4.1535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Loeb J. D., Sepulveda-Becerra M., Hazan I., Liu H. A G1 cyclin is necessary for maintenance of filamentous growth in Candida albicans. Mol Cell Biol. 1999 Jun;19(6):4019–4027. doi: 10.1128/mcb.19.6.4019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lorenz M. C., Cutler N. S., Heitman J. Characterization of alcohol-induced filamentous growth in Saccharomyces cerevisiae. Mol Biol Cell. 2000 Jan;11(1):183–199. doi: 10.1091/mbc.11.1.183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lorenz M. C., Heitman J. Regulators of pseudohyphal differentiation in Saccharomyces cerevisiae identified through multicopy suppressor analysis in ammonium permease mutant strains. Genetics. 1998 Dec;150(4):1443–1457. doi: 10.1093/genetics/150.4.1443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Madhani H. D., Galitski T., Lander E. S., Fink G. R. Effectors of a developmental mitogen-activated protein kinase cascade revealed by expression signatures of signaling mutants. Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12530–12535. doi: 10.1073/pnas.96.22.12530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. McMillan J. N., Longtine M. S., Sia R. A., Theesfeld C. L., Bardes E. S., Pringle J. R., Lew D. J. The morphogenesis checkpoint in Saccharomyces cerevisiae: cell cycle control of Swe1p degradation by Hsl1p and Hsl7p. Mol Cell Biol. 1999 Oct;19(10):6929–6939. doi: 10.1128/mcb.19.10.6929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Mösch H. U., Fink G. R. Dissection of filamentous growth by transposon mutagenesis in Saccharomyces cerevisiae. Genetics. 1997 Mar;145(3):671–684. doi: 10.1093/genetics/145.3.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Oehlen L. J., Cross F. R. Potential regulation of Ste20 function by the Cln1-Cdc28 and Cln2-Cdc28 cyclin-dependent protein kinases. J Biol Chem. 1998 Sep 25;273(39):25089–25097. doi: 10.1074/jbc.273.39.25089. [DOI] [PubMed] [Google Scholar]
  37. Pan X., Heitman J. Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol Cell Biol. 1999 Jul;19(7):4874–4887. doi: 10.1128/mcb.19.7.4874. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Plate K., Hellwig D., Rossberg C., Mennel H. D. Spinale angiomatöse Fehlbildung: Klinischer Verlauf und Grenzen der apparativen Diagnostik. Zentralbl Neurochir. 1990;51(1):49–52. [PubMed] [Google Scholar]
  39. Rupp S., Summers E., Lo H. J., Madhani H., Fink G. MAP kinase and cAMP filamentation signaling pathways converge on the unusually large promoter of the yeast FLO11 gene. EMBO J. 1999 Mar 1;18(5):1257–1269. doi: 10.1093/emboj/18.5.1257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Shulewitz M. J., Inouye C. J., Thorner J. Hsl7 localizes to a septin ring and serves as an adapter in a regulatory pathway that relieves tyrosine phosphorylation of Cdc28 protein kinase in Saccharomyces cerevisiae. Mol Cell Biol. 1999 Oct;19(10):7123–7137. doi: 10.1128/mcb.19.10.7123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sia R. A., Herald H. A., Lew D. J. Cdc28 tyrosine phosphorylation and the morphogenesis checkpoint in budding yeast. Mol Biol Cell. 1996 Nov;7(11):1657–1666. doi: 10.1091/mbc.7.11.1657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. 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]
  43. Singh P., Ganesan K., Malathi K., Ghosh D., Datta A. ACPR, a STE12 homologue from Candida albicans, is a strong inducer of pseudohyphae in Saccharomyces cerevisiae haploids and diploids. Biochem Biophys Res Commun. 1994 Dec 15;205(2):1079–1085. doi: 10.1006/bbrc.1994.2776. [DOI] [PubMed] [Google Scholar]
  44. Wach A., Brachat A., Pöhlmann R., Philippsen P. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast. 1994 Dec;10(13):1793–1808. doi: 10.1002/yea.320101310. [DOI] [PubMed] [Google Scholar]
  45. Xu J. R., Hamer J. E. MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev. 1996 Nov 1;10(21):2696–2706. doi: 10.1101/gad.10.21.2696. [DOI] [PubMed] [Google Scholar]
  46. Ye X. S., Lee S. L., Wolkow T. D., McGuire S. L., Hamer J. E., Wood G. C., Osmani S. A. Interaction between developmental and cell cycle regulators is required for morphogenesis in Aspergillus nidulans. EMBO J. 1999 Dec 15;18(24):6994–7001. doi: 10.1093/emboj/18.24.6994. [DOI] [PMC free article] [PubMed] [Google Scholar]

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