Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Dec 6;91(25):12105–12109. doi: 10.1073/pnas.91.25.12105

AFC1, a LAMMER kinase from Arabidopsis thaliana, activates STE12-dependent processes in yeast.

J Bender 1, G R Fink 1
PMCID: PMC45385  PMID: 7991592

Abstract

In the yeast Saccharomyces cerevisiae a kinase cascade activates the transcription factor STE12 leading to mating in haploid cells and pseudohyphal growth in diploid cells. To investigate related signal transduction pathways in higher plants, we have isolated a putative protein kinase gene from Arabidopsis thaliana that restores STE12-dependent functions to yeast with mutations in this signal transduction pathway. This Arabidopsis gene, AFC1, induces three STE12-dependent processes even in signal transduction-defective yeast strains: mating-specific gene expression in haploid yeast, mating of haploid yeast to yield diploids, and pseudohyphal growth in diploid yeast. AFC1 has no effect on transcription of the STE12 gene and, instead, is likely to activate the STE12 protein. However, AFC1 has only limited homology to FUS3 and KSS1, the endogenous yeast kinase regulators of STE12. AFC1 is a member of a recently described CDC2-related kinase subfamily, the LAMMER kinases. A close AFC1 homolog, AFC2, lacks STE12 activation phenotypes, indicating the specificity of AFC1. The phenotypes of AFC1 in yeast provide us with tools to elucidate the role of this kinase in Arabidopsis.

Full text

PDF
12105

Images in this article

Selected References

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

  1. Ben-David Y., Letwin K., Tannock L., Bernstein A., Pawson T. A mammalian protein kinase with potential for serine/threonine and tyrosine phosphorylation is related to cell cycle regulators. EMBO J. 1991 Feb;10(2):317–325. doi: 10.1002/j.1460-2075.1991.tb07952.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brill J. A., Elion E. A., Fink G. R. A role for autophosphorylation revealed by activated alleles of FUS3, the yeast MAP kinase homolog. Mol Biol Cell. 1994 Mar;5(3):297–312. doi: 10.1091/mbc.5.3.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chang F., Herskowitz I. Identification of a gene necessary for cell cycle arrest by a negative growth factor of yeast: FAR1 is an inhibitor of a G1 cyclin, CLN2. Cell. 1990 Nov 30;63(5):999–1011. doi: 10.1016/0092-8674(90)90503-7. [DOI] [PubMed] [Google Scholar]
  4. Courchesne W. E., Kunisawa R., Thorner J. A putative protein kinase overcomes pheromone-induced arrest of cell cycling in S. cerevisiae. Cell. 1989 Sep 22;58(6):1107–1119. doi: 10.1016/0092-8674(89)90509-6. [DOI] [PubMed] [Google Scholar]
  5. Dolan J. W., Fields S. Overproduction of the yeast STE12 protein leads to constitutive transcriptional induction. Genes Dev. 1990 Apr;4(4):492–502. doi: 10.1101/gad.4.4.492. [DOI] [PubMed] [Google Scholar]
  6. Elion E. A., Brill J. A., Fink G. R. FUS3 represses CLN1 and CLN2 and in concert with KSS1 promotes signal transduction. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9392–9396. doi: 10.1073/pnas.88.21.9392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Elion E. A., Grisafi P. L., Fink G. R. FUS3 encodes a cdc2+/CDC28-related kinase required for the transition from mitosis into conjugation. Cell. 1990 Feb 23;60(4):649–664. doi: 10.1016/0092-8674(90)90668-5. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Elledge S. J., Mulligan J. T., Ramer S. W., Spottswood M., Davis R. W. Lambda YES: a multifunctional cDNA expression vector for the isolation of genes by complementation of yeast and Escherichia coli mutations. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1731–1735. doi: 10.1073/pnas.88.5.1731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Errede B., Levin D. E. A conserved kinase cascade for MAP kinase activation in yeast. Curr Opin Cell Biol. 1993 Apr;5(2):254–260. doi: 10.1016/0955-0674(93)90112-4. [DOI] [PubMed] [Google Scholar]
  11. Gietz D., St Jean A., Woods R. A., Schiestl R. H. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 1992 Mar 25;20(6):1425–1425. doi: 10.1093/nar/20.6.1425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. Higgins D. G., Sharp P. M. Fast and sensitive multiple sequence alignments on a microcomputer. Comput Appl Biosci. 1989 Apr;5(2):151–153. doi: 10.1093/bioinformatics/5.2.151. [DOI] [PubMed] [Google Scholar]
  15. Howell B. W., Afar D. E., Lew J., Douville E. M., Icely P. L., Gray D. A., Bell J. C. STY, a tyrosine-phosphorylating enzyme with sequence homology to serine/threonine kinases. Mol Cell Biol. 1991 Jan;11(1):568–572. doi: 10.1128/mcb.11.1.568. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Johnson K. W., Smith K. A. Molecular cloning of a novel human cdc2/CDC28-like protein kinase. J Biol Chem. 1991 Feb 25;266(6):3402–3407. [PubMed] [Google Scholar]
  17. Liu H., Krizek J., Bretscher A. Construction of a GAL1-regulated yeast cDNA expression library and its application to the identification of genes whose overexpression causes lethality in yeast. Genetics. 1992 Nov;132(3):665–673. doi: 10.1093/genetics/132.3.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Liu H., Styles C. A., Fink G. R. Elements of the yeast pheromone response pathway required for filamentous growth of diploids. Science. 1993 Dec 10;262(5140):1741–1744. doi: 10.1126/science.8259520. [DOI] [PubMed] [Google Scholar]
  19. Minet M., Dufour M. E., Lacroute F. Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J. 1992 May;2(3):417–422. doi: 10.1111/j.1365-313x.1992.00417.x. [DOI] [PubMed] [Google Scholar]
  20. Ninomiya-Tsuji J., Nomoto S., Yasuda H., Reed S. I., Matsumoto K. Cloning of a human cDNA encoding a CDC2-related kinase by complementation of a budding yeast cdc28 mutation. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9006–9010. doi: 10.1073/pnas.88.20.9006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Padmanabha R., Gehrung S., Snyder M. The KNS1 gene of Saccharomyces cerevisiae encodes a nonessential protein kinase homologue that is distantly related to members of the CDC28/cdc2 gene family. Mol Gen Genet. 1991 Sep;229(1):1–9. doi: 10.1007/BF00264206. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Rabinow L., Birchler J. A. A dosage-sensitive modifier of retrotransposon-induced alleles of the Drosophila white locus. EMBO J. 1989 Mar;8(3):879–889. doi: 10.1002/j.1460-2075.1989.tb03449.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rabinow L., Chiang S. L., Birchler J. A. Mutations at the Darkener of apricot locus modulate transcript levels of copia and copia-induced mutations in Drosophila melanogaster. Genetics. 1993 Aug;134(4):1175–1185. doi: 10.1093/genetics/134.4.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rothstein R. J. One-step gene disruption in yeast. Methods Enzymol. 1983;101:202–211. doi: 10.1016/0076-6879(83)01015-0. [DOI] [PubMed] [Google Scholar]
  26. Song D., Dolan J. W., Yuan Y. L., Fields S. Pheromone-dependent phosphorylation of the yeast STE12 protein correlates with transcriptional activation. Genes Dev. 1991 May;5(5):741–750. doi: 10.1101/gad.5.5.741. [DOI] [PubMed] [Google Scholar]
  27. Trueheart J., Boeke J. D., Fink G. R. Two genes required for cell fusion during yeast conjugation: evidence for a pheromone-induced surface protein. Mol Cell Biol. 1987 Jul;7(7):2316–2328. doi: 10.1128/mcb.7.7.2316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Yun B., Farkas R., Lee K., Rabinow L. The Doa locus encodes a member of a new protein kinase family and is essential for eye and embryonic development in Drosophila melanogaster. Genes Dev. 1994 May 15;8(10):1160–1173. doi: 10.1101/gad.8.10.1160. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES