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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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Screening of an overexpression library of 107 putative transcription factor genes of Candida albicans.This screening process revealed that overexpression of only one gene, TEC1, in the absence of α-pheromone, induced more than a 100-fold increase in adhesion. (A) Number of adherent cells per well bottom for the 107 strains in the presence of doxycycline and the absence of α-pheromone. For comparison, the levels in the control strain P37005 are also presented both in the absence (−) and presence (+) of α-pheromone. (B) Examples of adhesion of P37005 and the overexpression P37005-TETp-TEC1 in the absence (−) and presence (+) of α-pheromone (α-ph) or doxycycline (Dox). (C) A comparison of WPRE and TCS, the putative cis-acting sequences interacting with Tec1 in C. albicans and S. cerevisiae, respectively, and OPRE and PRE, interacting with Cph1 and the homolog Ste12 in C. albicans and S. cerevisiae, respectively. (D) Comparison of the Tec1 DNA-binding domains of C. albicans (Ca) and S. cerevisiae (Sc).
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pbio-1000363-g001: Screening of an overexpression library of 107 putative transcription factor genes of Candida albicans.This screening process revealed that overexpression of only one gene, TEC1, in the absence of α-pheromone, induced more than a 100-fold increase in adhesion. (A) Number of adherent cells per well bottom for the 107 strains in the presence of doxycycline and the absence of α-pheromone. For comparison, the levels in the control strain P37005 are also presented both in the absence (−) and presence (+) of α-pheromone. (B) Examples of adhesion of P37005 and the overexpression P37005-TETp-TEC1 in the absence (−) and presence (+) of α-pheromone (α-ph) or doxycycline (Dox). (C) A comparison of WPRE and TCS, the putative cis-acting sequences interacting with Tec1 in C. albicans and S. cerevisiae, respectively, and OPRE and PRE, interacting with Cph1 and the homolog Ste12 in C. albicans and S. cerevisiae, respectively. (D) Comparison of the Tec1 DNA-binding domains of C. albicans (Ca) and S. cerevisiae (Sc).

Mentions: Each of the 107 overexpression strains was tested in the absence of pheromone for increased adhesion to a plastic surface in the absence or presence of 100 µg per ml of doxycycline. To obtain a measure of maximum pheromone induction, white cells of the parental control strain P37005 were first analyzed in the absence and presence of α-pheromone. Adhesion was negligible (<106 cells per well bottom) in the absence and maximal (>108 cells per well bottom) in the presence of α-pheromone (Figure 1A). In the absence of α-pheromone, doxycycline induced adhesion in only one of the 107 overexpression strains, and did so to the same extent as α-pheromone induction in control cells (Figure 1A). That single strain overexpressed the gene TEC1. In Figure 1B, induction in the TEC1 overexpression strain is obvious in images of the well bottoms after rinsing. TEC1 has been shown to be involved in the induction of filamentation in both S. cerevisiae [32],[35] and C. albicans [34], as well as during biofilm formation in C. albicans a/α strains [36]. It should be noted that overexpression of CPH1, the transcription factor mediating the opaque pheromone response [10],[26],[27], had no effect on adhesion (Figure 1A).


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)

Screening of an overexpression library of 107 putative transcription factor genes of Candida albicans.This screening process revealed that overexpression of only one gene, TEC1, in the absence of α-pheromone, induced more than a 100-fold increase in adhesion. (A) Number of adherent cells per well bottom for the 107 strains in the presence of doxycycline and the absence of α-pheromone. For comparison, the levels in the control strain P37005 are also presented both in the absence (−) and presence (+) of α-pheromone. (B) Examples of adhesion of P37005 and the overexpression P37005-TETp-TEC1 in the absence (−) and presence (+) of α-pheromone (α-ph) or doxycycline (Dox). (C) A comparison of WPRE and TCS, the putative cis-acting sequences interacting with Tec1 in C. albicans and S. cerevisiae, respectively, and OPRE and PRE, interacting with Cph1 and the homolog Ste12 in C. albicans and S. cerevisiae, respectively. (D) Comparison of the Tec1 DNA-binding domains of C. albicans (Ca) and S. cerevisiae (Sc).
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2864266&req=5

pbio-1000363-g001: Screening of an overexpression library of 107 putative transcription factor genes of Candida albicans.This screening process revealed that overexpression of only one gene, TEC1, in the absence of α-pheromone, induced more than a 100-fold increase in adhesion. (A) Number of adherent cells per well bottom for the 107 strains in the presence of doxycycline and the absence of α-pheromone. For comparison, the levels in the control strain P37005 are also presented both in the absence (−) and presence (+) of α-pheromone. (B) Examples of adhesion of P37005 and the overexpression P37005-TETp-TEC1 in the absence (−) and presence (+) of α-pheromone (α-ph) or doxycycline (Dox). (C) A comparison of WPRE and TCS, the putative cis-acting sequences interacting with Tec1 in C. albicans and S. cerevisiae, respectively, and OPRE and PRE, interacting with Cph1 and the homolog Ste12 in C. albicans and S. cerevisiae, respectively. (D) Comparison of the Tec1 DNA-binding domains of C. albicans (Ca) and S. cerevisiae (Sc).
Mentions: Each of the 107 overexpression strains was tested in the absence of pheromone for increased adhesion to a plastic surface in the absence or presence of 100 µg per ml of doxycycline. To obtain a measure of maximum pheromone induction, white cells of the parental control strain P37005 were first analyzed in the absence and presence of α-pheromone. Adhesion was negligible (<106 cells per well bottom) in the absence and maximal (>108 cells per well bottom) in the presence of α-pheromone (Figure 1A). In the absence of α-pheromone, doxycycline induced adhesion in only one of the 107 overexpression strains, and did so to the same extent as α-pheromone induction in control cells (Figure 1A). That single strain overexpressed the gene TEC1. In Figure 1B, induction in the TEC1 overexpression strain is obvious in images of the well bottoms after rinsing. TEC1 has been shown to be involved in the induction of filamentation in both S. cerevisiae [32],[35] and C. albicans [34], as well as during biofilm formation in C. albicans a/α strains [36]. It should be noted that overexpression of CPH1, the transcription factor mediating the opaque pheromone response [10],[26],[27], had no effect on adhesion (Figure 1A).

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
Related in: MedlinePlus