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White cells facilitate opposite- and same-sex mating of opaque cells in Candida albicans.

Tao L, Cao C, Liang W, Guan G, Zhang Q, Nobile CJ, Huang G - PLoS Genet. (2014)

Bottom Line: Modes of sexual reproduction in eukaryotic organisms are extremely diverse.Deletion of genes encoding the pheromone precursor proteins and inactivation of the pheromone response signaling pathway (Ste2-MAPK-Cph1) impair the promoting role of white cells (MTLa) in the sexual mating of opaque cells.This coordination between the two different cell types may be a trade-off strategy between sexual and asexual lifestyles in C. albicans.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China.

ABSTRACT
Modes of sexual reproduction in eukaryotic organisms are extremely diverse. The human fungal pathogen Candida albicans undergoes a phenotypic switch from the white to the opaque phase in order to become mating-competent. In this study, we report that functionally- and morphologically-differentiated white and opaque cells show a coordinated behavior during mating. Although white cells are mating-incompetent, they can produce sexual pheromones when treated with pheromones of the opposite mating type or by physically interacting with opaque cells of the opposite mating type. In a co-culture system, pheromones released by white cells induce opaque cells to form mating projections, and facilitate both opposite- and same-sex mating of opaque cells. Deletion of genes encoding the pheromone precursor proteins and inactivation of the pheromone response signaling pathway (Ste2-MAPK-Cph1) impair the promoting role of white cells (MTLa) in the sexual mating of opaque cells. White and opaque cells communicate via a paracrine pheromone signaling system, creating an environment conducive to sexual mating. This coordination between the two different cell types may be a trade-off strategy between sexual and asexual lifestyles in C. albicans.

No MeSH data available.


Related in: MedlinePlus

Schematic models for the role of white cells in opposite- and same-sex mating of opaque cells.(A) The majority of white cells (a) secrete pheromone to facilitate opposite- and same-sex mating of the minority opaque cells. (i) When the majority are a/α cells, sexual mating between the minority of opaque a and α cells is rare. Opaque α cells secrete α-pheromone constitutively, while opaque a cells do not secrete a-pheromone without exposure to a certain level of α-pheromone. When both opaque a and α cells are rare, the threshold for pheromone and mating responses is typically not reached. (ii) When the majority are white a cells, sexual mating between the minority opaque a and α cells can occur. Opaque α cells secrete α-pheromone and induce the majority of white a cells to secrete a-pheromone. Thus, a-pheromone in turn induces opaque α cells to form long mating projections, which facilitate them to reach opaque a mating partners. (iii) White a/α cells do not induce mating projections and do not facilitate same-sex mating of opaque α cells. (iv) White a cells facilitate same-sex mating of opaque α cells. Opaque α cells secrete α-pheromone and induce white a cells to secrete a-pheromone. In turn, a-pheromone induces opaque α cells to form mating projections and undergo same-sex mating. (B) Schematic model depicting the crosstalk between white and opaque pheromone response pathways. First, opaque α cells constitutively secrete α-pheromone and activate the white pheromone response pathway to induce a-pheromone secretion in a cells. Then, a-pheromone secreted by white a cells activates the opaque pheromone response pathway to promote mating projection formation in opaque α cells.
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pgen-1004737-g006: Schematic models for the role of white cells in opposite- and same-sex mating of opaque cells.(A) The majority of white cells (a) secrete pheromone to facilitate opposite- and same-sex mating of the minority opaque cells. (i) When the majority are a/α cells, sexual mating between the minority of opaque a and α cells is rare. Opaque α cells secrete α-pheromone constitutively, while opaque a cells do not secrete a-pheromone without exposure to a certain level of α-pheromone. When both opaque a and α cells are rare, the threshold for pheromone and mating responses is typically not reached. (ii) When the majority are white a cells, sexual mating between the minority opaque a and α cells can occur. Opaque α cells secrete α-pheromone and induce the majority of white a cells to secrete a-pheromone. Thus, a-pheromone in turn induces opaque α cells to form long mating projections, which facilitate them to reach opaque a mating partners. (iii) White a/α cells do not induce mating projections and do not facilitate same-sex mating of opaque α cells. (iv) White a cells facilitate same-sex mating of opaque α cells. Opaque α cells secrete α-pheromone and induce white a cells to secrete a-pheromone. In turn, a-pheromone induces opaque α cells to form mating projections and undergo same-sex mating. (B) Schematic model depicting the crosstalk between white and opaque pheromone response pathways. First, opaque α cells constitutively secrete α-pheromone and activate the white pheromone response pathway to induce a-pheromone secretion in a cells. Then, a-pheromone secreted by white a cells activates the opaque pheromone response pathway to promote mating projection formation in opaque α cells.

Mentions: In this study, we provide additional evidence for the evolution of coordination between white and opaque cells during sexual mating in C. albicans. We demonstrate that opaque cells can induce mating-incompetent white cells to secrete pheromone (Figure 2 and S5). Consistent with our data, Lin et al. recently reported that the expression level of MFA1 in white a cells was increased ∼475 fold upon treatment with α-pheromone [42]. We note that the studies by Yi et al.[39] and Sanhi et al.[43] demonstrate that the expression of MFA1 in white a cells remains unchanged in response to α-pheromone. As discussed in a recent review article [44], this discrepancy may be due to differences in laboratory growth conditions. In a system where white and opaque cells co-exist, pheromone signaling leads to the formation of a positive feedback loop, promoting the occurrence of opposite- and same-sex mating. Example scenarios of white and opaque cells co-existing, and the functional consequences of these interactions are summarized in Figure 6A and 6B, respectively. As shown in Figure 6B, opaque α cells constitutively secrete α-pheromone, which activates the pheromone response signaling pathway (Ste2-MAPK-Cph1) of white a cells. “Activated” white a cells are then induced to produce a-pheromone, which in turn activates the pheromone response signaling pathway (Ste3-MAPK-Cph1) and induces mating projection formation of opaque α cells. Of note, the expression of MFA1 is extremely low, even in opaque a cells, although it can be enhanced by treatment of the opaque a cells with α-pheromone (Figure 2 and [22]). This positive feedback loop for pheromone response is widely conserved in other yeasts. It is known that α cells can induce a-pheromone secretion of a cells in Saccharomyces cerevisiae[45]. Nielsen and coworkers reported that mating pheromone also triggers a positive feedback response in the fission yeast Schizosaccharomyces pombe[46]. This positive feedback loop for pheromone response is, therefore, a general feature in yeast species.


White cells facilitate opposite- and same-sex mating of opaque cells in Candida albicans.

Tao L, Cao C, Liang W, Guan G, Zhang Q, Nobile CJ, Huang G - PLoS Genet. (2014)

Schematic models for the role of white cells in opposite- and same-sex mating of opaque cells.(A) The majority of white cells (a) secrete pheromone to facilitate opposite- and same-sex mating of the minority opaque cells. (i) When the majority are a/α cells, sexual mating between the minority of opaque a and α cells is rare. Opaque α cells secrete α-pheromone constitutively, while opaque a cells do not secrete a-pheromone without exposure to a certain level of α-pheromone. When both opaque a and α cells are rare, the threshold for pheromone and mating responses is typically not reached. (ii) When the majority are white a cells, sexual mating between the minority opaque a and α cells can occur. Opaque α cells secrete α-pheromone and induce the majority of white a cells to secrete a-pheromone. Thus, a-pheromone in turn induces opaque α cells to form long mating projections, which facilitate them to reach opaque a mating partners. (iii) White a/α cells do not induce mating projections and do not facilitate same-sex mating of opaque α cells. (iv) White a cells facilitate same-sex mating of opaque α cells. Opaque α cells secrete α-pheromone and induce white a cells to secrete a-pheromone. In turn, a-pheromone induces opaque α cells to form mating projections and undergo same-sex mating. (B) Schematic model depicting the crosstalk between white and opaque pheromone response pathways. First, opaque α cells constitutively secrete α-pheromone and activate the white pheromone response pathway to induce a-pheromone secretion in a cells. Then, a-pheromone secreted by white a cells activates the opaque pheromone response pathway to promote mating projection formation in opaque α cells.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4199524&req=5

pgen-1004737-g006: Schematic models for the role of white cells in opposite- and same-sex mating of opaque cells.(A) The majority of white cells (a) secrete pheromone to facilitate opposite- and same-sex mating of the minority opaque cells. (i) When the majority are a/α cells, sexual mating between the minority of opaque a and α cells is rare. Opaque α cells secrete α-pheromone constitutively, while opaque a cells do not secrete a-pheromone without exposure to a certain level of α-pheromone. When both opaque a and α cells are rare, the threshold for pheromone and mating responses is typically not reached. (ii) When the majority are white a cells, sexual mating between the minority opaque a and α cells can occur. Opaque α cells secrete α-pheromone and induce the majority of white a cells to secrete a-pheromone. Thus, a-pheromone in turn induces opaque α cells to form long mating projections, which facilitate them to reach opaque a mating partners. (iii) White a/α cells do not induce mating projections and do not facilitate same-sex mating of opaque α cells. (iv) White a cells facilitate same-sex mating of opaque α cells. Opaque α cells secrete α-pheromone and induce white a cells to secrete a-pheromone. In turn, a-pheromone induces opaque α cells to form mating projections and undergo same-sex mating. (B) Schematic model depicting the crosstalk between white and opaque pheromone response pathways. First, opaque α cells constitutively secrete α-pheromone and activate the white pheromone response pathway to induce a-pheromone secretion in a cells. Then, a-pheromone secreted by white a cells activates the opaque pheromone response pathway to promote mating projection formation in opaque α cells.
Mentions: In this study, we provide additional evidence for the evolution of coordination between white and opaque cells during sexual mating in C. albicans. We demonstrate that opaque cells can induce mating-incompetent white cells to secrete pheromone (Figure 2 and S5). Consistent with our data, Lin et al. recently reported that the expression level of MFA1 in white a cells was increased ∼475 fold upon treatment with α-pheromone [42]. We note that the studies by Yi et al.[39] and Sanhi et al.[43] demonstrate that the expression of MFA1 in white a cells remains unchanged in response to α-pheromone. As discussed in a recent review article [44], this discrepancy may be due to differences in laboratory growth conditions. In a system where white and opaque cells co-exist, pheromone signaling leads to the formation of a positive feedback loop, promoting the occurrence of opposite- and same-sex mating. Example scenarios of white and opaque cells co-existing, and the functional consequences of these interactions are summarized in Figure 6A and 6B, respectively. As shown in Figure 6B, opaque α cells constitutively secrete α-pheromone, which activates the pheromone response signaling pathway (Ste2-MAPK-Cph1) of white a cells. “Activated” white a cells are then induced to produce a-pheromone, which in turn activates the pheromone response signaling pathway (Ste3-MAPK-Cph1) and induces mating projection formation of opaque α cells. Of note, the expression of MFA1 is extremely low, even in opaque a cells, although it can be enhanced by treatment of the opaque a cells with α-pheromone (Figure 2 and [22]). This positive feedback loop for pheromone response is widely conserved in other yeasts. It is known that α cells can induce a-pheromone secretion of a cells in Saccharomyces cerevisiae[45]. Nielsen and coworkers reported that mating pheromone also triggers a positive feedback response in the fission yeast Schizosaccharomyces pombe[46]. This positive feedback loop for pheromone response is, therefore, a general feature in yeast species.

Bottom Line: Modes of sexual reproduction in eukaryotic organisms are extremely diverse.Deletion of genes encoding the pheromone precursor proteins and inactivation of the pheromone response signaling pathway (Ste2-MAPK-Cph1) impair the promoting role of white cells (MTLa) in the sexual mating of opaque cells.This coordination between the two different cell types may be a trade-off strategy between sexual and asexual lifestyles in C. albicans.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China.

ABSTRACT
Modes of sexual reproduction in eukaryotic organisms are extremely diverse. The human fungal pathogen Candida albicans undergoes a phenotypic switch from the white to the opaque phase in order to become mating-competent. In this study, we report that functionally- and morphologically-differentiated white and opaque cells show a coordinated behavior during mating. Although white cells are mating-incompetent, they can produce sexual pheromones when treated with pheromones of the opposite mating type or by physically interacting with opaque cells of the opposite mating type. In a co-culture system, pheromones released by white cells induce opaque cells to form mating projections, and facilitate both opposite- and same-sex mating of opaque cells. Deletion of genes encoding the pheromone precursor proteins and inactivation of the pheromone response signaling pathway (Ste2-MAPK-Cph1) impair the promoting role of white cells (MTLa) in the sexual mating of opaque cells. White and opaque cells communicate via a paracrine pheromone signaling system, creating an environment conducive to sexual mating. This coordination between the two different cell types may be a trade-off strategy between sexual and asexual lifestyles in C. albicans.

No MeSH data available.


Related in: MedlinePlus