Skip to main content
SpringerLink
Log in

Specificity of MAPK signaling towards FLO11 expression is established by crosstalk from cAMP pathway

  • Research Article
  • Published:
Systems and Synthetic Biology

Abstract

In budding yeast, elements of a single MAP Kinase cascade are shared to regulate a wide range of functions such as mating, differentiation and osmotic stress. However, cells have programmed to execute correct event in response to a given input signal without cross activating other responses. Studies have observed that magnitude and duration of MAPK activation encodes specificity. Similarly, the differential regulation of Tec1p, a transcriptional activator of invasive growth gene, FLO11 by MAP kinases has been observed to bring specificity in mating and invasive growth signaling. However, the understanding of interactions between the shared components and other signaling pathways related to the phenotypic response in contributing towards specificity remains unclear. We specifically address the crosstalk of cAMP pathway with MAPK pathway in haploid invasive growth and show the contribution and importance of cAMP pathway towards invasive growth irrespective of the activation status of MAPK pathway. Our analysis shows that crosstalk from cAMP pathway in haploids might offer an advantage in terms of amplifying the observed weak signaling through MAPK pathway. Further, we show that such a crosstalk in haploids leads to higher FLO11 expression than diploids. We also demonstrate the positive and negative role of Tpk1 and Tpk3 in haploid invasive growth. Finally, we observe that a cross-inhibition at gene level brought about by cAMP pathway controlled inhibitor, Sfl1, perhaps help in deamplifying the MAPK signal and also in preventing FLO11 expression in the absence of cAMP pathway activation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Arkinstall SJ, Papasavvas SG, Payton MA (1991) Yeast alpha-mating factor receptor-linked G-protein signal transduction suppresses Ras-dependent activity. FEBS Lett 284:123–128

    Article  PubMed  CAS  Google Scholar 

  • Bao MZ, Schwartz MA, Cantin GT, Yates JR, Madhani HD (2004) Pheromone-dependent destruction of the Tec1 transcription factor is required for MAP kinase signaling specificity in yeast. Cell 119:991–1000

    Article  PubMed  CAS  Google Scholar 

  • Bardwell L, Cook JG, Inouye CJ, Thorner J (1994) Signal propagation and regulation in the mating pheromone response pathway of the yeast Saccharomyces cerevisiae. Dev Biol 166:363–379

    Article  PubMed  CAS  Google Scholar 

  • Bardwell L (2005) A walk-through of the yeast mating pheromone response pathway. Peptides 26:337–350

    Article  CAS  Google Scholar 

  • Braus GH, Grundmann O, Bruckner S, Mosch HU (2003) Amino acid starvation and Gcn4p regulate adhesive growth and FLO11 gene expression in Saccharomyces cerevisiae. Mol Biol Cell 14:4272–4284

    Article  PubMed  CAS  Google Scholar 

  • Bruckner S, Kohler T, Braus GH, Heise B, Bolte M, Mesch HU (2004) Differential regulation of Tec1 by Fus3 and Kss1 confers signaling specificity in yeast development. Curr Genet 46:331–342

    Article  PubMed  Google Scholar 

  • Conlan RS, Tzamarias D (2001) Sfl1 functions via the co-repressor Ssn6-Tup1 and the cAMP-dependent protein kinase Tpk2. J Mol Biol 309:1007–1015

    Article  PubMed  CAS  Google Scholar 

  • Cullen PJ, Sprague GF (2000) Glucose depletion causes haploid invasive growth in yeast. Proc Natl Acad Sci USA 97:13619–13624

    Article  PubMed  CAS  Google Scholar 

  • Elion EA, Qi MS, Chen WD (2005) Signaling specificity in yeast. Science 307:687–688

    Article  PubMed  CAS  Google Scholar 

  • Erdman S, Snyder M (2001) A filamentous growth response mediated by the yeast mating pathway. Genetics 159:919–928

    PubMed  CAS  Google Scholar 

  • Fields S, Herskowitz I (1987) Regulation by the Yeast Mating-Type Locus of Ste12, a Gene Required for Cell-Type-Specific Expression. Mol Cell Biol 7:3818–3821

    PubMed  CAS  Google Scholar 

  • Fischer G (2005) Regulation of Flo11p-dependent adhesion in Saccharomyces cerevisiae, dissertation. Institute of Microbiology and Genetics, Georg-August-Universität, 37077 Göttingen, Germany

  • Flatauer LJ, Zadeh SF, Bardwell L (2005) Mitogen-activated protein kinases with distinct requirements for Ste5 scaffolding influence signaling specificity in Saccharomyces cerevisiae. Mol Cell Biol 25:1793–1803

    Article  PubMed  CAS  Google Scholar 

  • Fleming AB, Pennings S (2001) Antagonistic remodelling by Swi-Snf and Tup1-Ssn6 of an extensive chromatin region forms the background for FLO1 gene regulation. EMBO J 20:5219–5231

    Article  PubMed  CAS  Google Scholar 

  • Gagiano M, Bauer FF, Pretorius IS (2002) The sensing of nutritional status and the relationship to filamentous growth in Saccharomyces cerevisiae. FEMS Yeast Res 2:433–470

    PubMed  CAS  Google Scholar 

  • Gimeno CJ, Ljungdahl PO, Styles CA, Fink GR (1992) Unipolar Cell Divisions in the Yeast Saccharomyces cerevisiae lead to Filamentous Growth - Regulation by Starvation and Ras. Cell 68:1077–1090

    Article  PubMed  CAS  Google Scholar 

  • Koshland Jr DE, Goldbeter A, Stock JB (1982) Amplification and adaptation in regulatory and sensory systems. Science 217:220–225

    Article  PubMed  CAS  Google Scholar 

  • Liu HP, Styles CA, Fink GR (1993) Elements of the Yeast Pheromone Response Pathway Required for Filamentous Growth of Diploids. Science 262:1741–1744

    Article  PubMed  CAS  Google Scholar 

  • Liu HP, Styles CA, Fink GR (1996) Saccharomyces cerevisiae S288C has a mutation in FLO8 a gene required for filamentous growth. Genetics 144:967–978

    PubMed  CAS  Google Scholar 

  • Lo WS, Dranginis AM (1998) The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. Mol Biol Cell 9:161–171

    PubMed  CAS  Google Scholar 

  • Lorenz M C, Heitman J (1997) Yeast pseudohyphal growth is regulated by GPA2, a G protein a homolog. EMBO J 16:7008–7018

    Article  PubMed  CAS  Google Scholar 

  • Madhani HD, Fink GR (1997) Combinatorial control required for the specificity of yeast MAPK signaling. Science 275:1314–1317

    Article  PubMed  CAS  Google Scholar 

  • Mosch HU, Roberts RL, Fink GR (1996) Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. Proc Natl Acad Sci USA. 93:5352–5356

    Article  PubMed  CAS  Google Scholar 

  • Mosch HU, Kubler E, Krappmann S, Fink GR., Braus GH (1999) Crosstalk between the Ras2p-controlled mitogen-activated protein kinase and cAMP pathways during invasive growth of Saccharomyces cerevisiae. Mol Biol Cell 10:1325–1335

    PubMed  CAS  Google Scholar 

  • Neelajan S, Vinod PK, Venkatesh KV (2007) Crosstalk between cAMP-PKA and MAP kinase pathways is a key regulatory design necessary to regulate FLO11 expression. Biophys Chem 125:59–71

    Article  Google Scholar 

  • Nelson C, Goto S, Lund K, Hung W, Sadowski I (2003) Srb10/Cdk8 regulates yeast filamentous growth by phosphorylating the transcription factor Ste12. Nature 421:187–190

    Article  PubMed  CAS  Google Scholar 

  • Palecek SP, Parikh AS, Kron SJ (2002) Sensing, signalling and integrating physical processes during Saccharomyces cerevisiae invasive and filamentous growth. Microbiology 148:893–907

    PubMed  CAS  Google Scholar 

  • Pan XW, Heitman J (1999) Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol Cell Biol 19:4874–4887

    PubMed  CAS  Google Scholar 

  • Pan X, Heitman J (2002) Protein Kinase A operates a molecular switch that governs yeast Pseudohyphal differentiation. Mol Cell Biol 22:3981–3993

    Article  PubMed  CAS  Google Scholar 

  • Papasavvas S, Arkinstall S, Reid J, Payton M (1992) Yeast Alpha-Mating Factor Receptor and G-Protein-Linked Adenylyl Cyclase Inhibition Requires Ras2 and Gpa2 Activities. Biochem Biophys Res Commun 184:1378–1385

    Article  PubMed  CAS  Google Scholar 

  • Pingsheng M, Stefan W, Patrick VD, Thevelein JM (1999) The PDE1-encoded low-affinity phosphodiesterase in the yeast Saccharomyces cerevisiae has a specific function in controlling agonist-induced cAMP signaling. Mol Biol Cell 10:91–104

    Google Scholar 

  • Roberts RL, Fink GR (1994) Elements of a Single Map Kinase Cascade in Saccharomyces-Cerevisiae Mediate 2 Developmental Programs in the Same Cell-Type - Mating and Invasive Growth. Genes Dev 8:2974–2985

    Article  PubMed  CAS  Google Scholar 

  • Robertson LS, Fink GR (1998) The three yeast A kinases have specific signaling functions in pseudohyphal growth. Proc Natl Acad Sci USA 95:13783– 13787

    Article  PubMed  CAS  Google Scholar 

  • Rupp S, Summers E, Lo HJ, Madhani H, Fink G (1999) MAP kinase and cAMP filamentation signaling pathways converge on the unusually large promoter of the yeast FLO11 gene. EMBO J 18:1257–1269

    Article  PubMed  CAS  Google Scholar 

  • Sabbagh W, Flatauer LJ, Bardwell AJ, Bardwell L (2001) Specificity of MAP kinase signaling in yeast differentiation involves transient versus sustained MAPK activation. Mol Cell 8:683–691

    Article  PubMed  CAS  Google Scholar 

  • Schwartz MA, Madhani HD (2004) Principles of MAP kinase signaling specificity in Saccharomyces cerevisiae. Ann Rev Genet 38:725–748

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

K.V.Venkatesh acknowledges financial support from the Swarnajayanti fellowship, Department of Science and Technology, India.

Author information

Authors and Affiliations

  1. School of Biosciences and Bioengineering, Indian Institute of Technology, Bombay, Powai, Mumbai, 400 076, India

    P. K. Vinod & K. V. Venkatesh

  2. Biosystems Engineering Lab, Department of Chemical Engineering, IIT Bombay, Powai, Mumbai, 400076, India

    K. V. Venkatesh

Authors
  1. P. K. Vinod
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. V. Venkatesh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. V. Venkatesh.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(DOC 75 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vinod, P.K., Venkatesh, K.V. Specificity of MAPK signaling towards FLO11 expression is established by crosstalk from cAMP pathway. Syst Synth Biol 1, 99–108 (2007). https://doi.org/10.1007/s11693-007-9007-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11693-007-9007-7

Keywords

Search

Navigation