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Tec1 mediates the pheromone response of the white phenotype of Candida albicans: insights into the evolution of new signal transduction pathways.

Sahni N, Yi S, Daniels KJ, Huang G, Srikantha T, Soll DR - PLoS Biol. (2010)

Bottom Line: The three portions of this new regulatory pathway appear to have been derived from three different ancestral programs still functional in C. albicans.The upstream portion, including signals, receptors, the trimeric G protein complex, and the MAP kinase cascade, was derived intact from the upstream portion of the opaque pheromone response pathway of the mating process; Tec1, the transcription factor targeted by the MAP kinase pathway, was derived from a filamentation pathway; and the white-specific downstream target genes were derived from an ancestral biofilm process.The evolution of this pheromone response pathway provides a possible paradigm for how such signal transduction pathways evolve.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, The University of Iowa, Iowa City, Iowa, United States of America.

ABSTRACT
The way in which signal transduction pathways evolve remains a mystery, primarily because we have few examples of ones that have newly evolved. There are numerous examples of how signal transduction pathways in the same organism selectively share components, most notably between the signal transduction pathways in Saccharomyces cerevisiae for the mating process, the filamentation process, cell wall integrity, ascospore formation, and osmoregulation. These examples, however, have not provided insights into how such pathways evolve. Here, through construction of an overexpression library for 107 transcription factors, and through mutational analyses, we have identified the transcription factor Tec1 as the last component of the newly evolved signal transduction pathway that regulates the pheromone response of the white cell phenotype in Candida albicans. The elucidation of this last component, Tec1, establishes a comprehensive description of the pheromone response pathway in the white cell phenotype of C. albicans, providing a unique perspective on how new signal transduction pathways may evolve. The three portions of this new regulatory pathway appear to have been derived from three different ancestral programs still functional in C. albicans. The upstream portion, including signals, receptors, the trimeric G protein complex, and the MAP kinase cascade, was derived intact from the upstream portion of the opaque pheromone response pathway of the mating process; Tec1, the transcription factor targeted by the MAP kinase pathway, was derived from a filamentation pathway; and the white-specific downstream target genes were derived from an ancestral biofilm process. The evolution of this pheromone response pathway provides a possible paradigm for how such signal transduction pathways evolve.

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Evolution of the white cell pheromone response pathway.(A) A comparison of common components in the S. cerevisiae filamentation pathway, pheromone response pathway, and osmolarity pathway. pm, plasma membrane. (B) A comparison of common components of the S. cerevisiae pheromone response pathway, the C. albicans opaque cell pheromone response pathway, and the C. albicans white cell pheromone response pathway. pher., pheromone. (C) Derivation of the three major portions of the white cell pheromone response pathway.
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pbio-1000363-g006: Evolution of the white cell pheromone response pathway.(A) A comparison of common components in the S. cerevisiae filamentation pathway, pheromone response pathway, and osmolarity pathway. pm, plasma membrane. (B) A comparison of common components of the S. cerevisiae pheromone response pathway, the C. albicans opaque cell pheromone response pathway, and the C. albicans white cell pheromone response pathway. pher., pheromone. (C) Derivation of the three major portions of the white cell pheromone response pathway.

Mentions: In S. cerevisiae, MAP kinase signaling pathways have been compared for common components between the best understood one, the pheromone response pathway, and a number of others, including those for filamentation, high osmolarity, cell wall integrity, and cell wall assembly [58]. Remarkably, except for the mating pathway, the signal–receptor interactions for the rest are poorly understood. The sharing of common components between these pathways is limited, except for the pheromone response pathway and the filamentation pathway. For these pathways, the GTPase Cdc42 and the kinase Ste20 immediately upstream of the MAP kinase pathway, as with the downstream components of the MAP kinase pathway, Ste11, Ste7, and Kss1, are shared (Figure 6A).


Tec1 mediates the pheromone response of the white phenotype of Candida albicans: insights into the evolution of new signal transduction pathways.

Sahni N, Yi S, Daniels KJ, Huang G, Srikantha T, Soll DR - PLoS Biol. (2010)

Evolution of the white cell pheromone response pathway.(A) A comparison of common components in the S. cerevisiae filamentation pathway, pheromone response pathway, and osmolarity pathway. pm, plasma membrane. (B) A comparison of common components of the S. cerevisiae pheromone response pathway, the C. albicans opaque cell pheromone response pathway, and the C. albicans white cell pheromone response pathway. pher., pheromone. (C) Derivation of the three major portions of the white cell pheromone response pathway.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2864266&req=5

pbio-1000363-g006: Evolution of the white cell pheromone response pathway.(A) A comparison of common components in the S. cerevisiae filamentation pathway, pheromone response pathway, and osmolarity pathway. pm, plasma membrane. (B) A comparison of common components of the S. cerevisiae pheromone response pathway, the C. albicans opaque cell pheromone response pathway, and the C. albicans white cell pheromone response pathway. pher., pheromone. (C) Derivation of the three major portions of the white cell pheromone response pathway.
Mentions: In S. cerevisiae, MAP kinase signaling pathways have been compared for common components between the best understood one, the pheromone response pathway, and a number of others, including those for filamentation, high osmolarity, cell wall integrity, and cell wall assembly [58]. Remarkably, except for the mating pathway, the signal–receptor interactions for the rest are poorly understood. The sharing of common components between these pathways is limited, except for the pheromone response pathway and the filamentation pathway. For these pathways, the GTPase Cdc42 and the kinase Ste20 immediately upstream of the MAP kinase pathway, as with the downstream components of the MAP kinase pathway, Ste11, Ste7, and Kss1, are shared (Figure 6A).

Bottom Line: The three portions of this new regulatory pathway appear to have been derived from three different ancestral programs still functional in C. albicans.The upstream portion, including signals, receptors, the trimeric G protein complex, and the MAP kinase cascade, was derived intact from the upstream portion of the opaque pheromone response pathway of the mating process; Tec1, the transcription factor targeted by the MAP kinase pathway, was derived from a filamentation pathway; and the white-specific downstream target genes were derived from an ancestral biofilm process.The evolution of this pheromone response pathway provides a possible paradigm for how such signal transduction pathways evolve.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, The University of Iowa, Iowa City, Iowa, United States of America.

ABSTRACT
The way in which signal transduction pathways evolve remains a mystery, primarily because we have few examples of ones that have newly evolved. There are numerous examples of how signal transduction pathways in the same organism selectively share components, most notably between the signal transduction pathways in Saccharomyces cerevisiae for the mating process, the filamentation process, cell wall integrity, ascospore formation, and osmoregulation. These examples, however, have not provided insights into how such pathways evolve. Here, through construction of an overexpression library for 107 transcription factors, and through mutational analyses, we have identified the transcription factor Tec1 as the last component of the newly evolved signal transduction pathway that regulates the pheromone response of the white cell phenotype in Candida albicans. The elucidation of this last component, Tec1, establishes a comprehensive description of the pheromone response pathway in the white cell phenotype of C. albicans, providing a unique perspective on how new signal transduction pathways may evolve. The three portions of this new regulatory pathway appear to have been derived from three different ancestral programs still functional in C. albicans. The upstream portion, including signals, receptors, the trimeric G protein complex, and the MAP kinase cascade, was derived intact from the upstream portion of the opaque pheromone response pathway of the mating process; Tec1, the transcription factor targeted by the MAP kinase pathway, was derived from a filamentation pathway; and the white-specific downstream target genes were derived from an ancestral biofilm process. The evolution of this pheromone response pathway provides a possible paradigm for how such signal transduction pathways evolve.

Show MeSH