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Genetics, Vol. 165, 997-1015, November 2003, Copyright © 2003

Phenotypic and Transcriptional Plasticity Directed by a Yeast Mitogen-Activated Protein Kinase Network

Ashton Breitkreutza, Lorrie Bouchera,b, Bobby-Joe Breitkreutza, Mujahid Sultanc,d, Igor Jurisicac,d, and Mike Tyersa,b
a Samuel Lunenfeld Research Institute, Mount Sinai Hospital, Toronto, Ontario M5G 1X5, Canada,
b Department of Medical Genetics and Microbiology, University of Toronto, Toronto, Ontario M4G 1A8, Canada,
c Ontario Cancer Institute, Princess Margaret Hospital, University Health Network, Division of Cancer Informatics, Toronto, Ontario M5G 2M9, Canada
d Department of Computer Science and Medical Biophysics, University of Toronto, Toronto, Ontario M4G 1A8, Canada

Corresponding author: Mike Tyers, Room 1080, Mount Sinai Hospital, 600 University Ave., Toronto, ON M5G 1X5, Canada., tyers{at}mshri.on.ca (E-mail)

Communicating editor: M. JOHNSTON

The yeast pheromone/filamentous growth MAPK pathway mediates both mating and invasive-growth responses. The interface between this MAPK module and the transcriptional machinery consists of a network of two MAPKs, Fus3 and Kss1; two regulators, Rst1 and Rst2 (a.k.a. Dig1 and Dig2); and two transcription factors, Ste12 and Tec1. Of 16 possible combinations of gene deletions in FUS3, KSS1, RST1, and RST2 in the {sum}1278 background, 10 display constitutive invasive growth. Rst1 was the primary negative regulator of invasive growth, while other components either attenuated or enhanced invasive growth, depending on the genetic context. Despite activation of the invasive response by lesions at the same level in the MAPK pathway, transcriptional profiles of different invasive mutant combinations did not exhibit a unified program of gene expression. The distal MAPK regulatory network is thus capable of generating phenotypically similar invasive-growth states (an attractor) from different molecular architectures (trajectories) that can functionally compensate for one another. This systems-level robustness may also account for the observed diversity of signals that trigger invasive growth.




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