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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 depicting that white cells facilitate same-sex mating of opaque cells.(A) When the majority are white a and/or α cells, same-sex mating between the minority opaque α and α cells can occur. (1) Opaque α cells secrete α-pheromone and (2) induce the majority white a cells to secrete a-pheromone. (3) a-Pheromone in turn induces opaque α cells to form long mating projections and undergo same-sex mating. (4) a-Pheromone induces white α cells to secrete α-pheromone. (5) α-Pheromone further activates white a cells to secrete a-pheromone. (B) When the majority are a/α cells, the minority of opaque α cells cannot form mating projections and cannot undergo same-sex mating. Opaque α cells secrete α-pheromone constitutively, while a/α cells do not secrete pheromone. (C) In the absence of white a cells, opaque α cells cannot form mating projections and cannot undergo same-sex mating.
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pgen-1004737-g007: Schematic models depicting that white cells facilitate same-sex mating of opaque cells.(A) When the majority are white a and/or α cells, same-sex mating between the minority opaque α and α cells can occur. (1) Opaque α cells secrete α-pheromone and (2) induce the majority white a cells to secrete a-pheromone. (3) a-Pheromone in turn induces opaque α cells to form long mating projections and undergo same-sex mating. (4) a-Pheromone induces white α cells to secrete α-pheromone. (5) α-Pheromone further activates white a cells to secrete a-pheromone. (B) When the majority are a/α cells, the minority of opaque α cells cannot form mating projections and cannot undergo same-sex mating. Opaque α cells secrete α-pheromone constitutively, while a/α cells do not secrete pheromone. (C) In the absence of white a cells, opaque α cells cannot form mating projections and cannot undergo same-sex mating.

Mentions: Since sexual mating in C. albicans is directed by the pheromone-mediated signaling pathway, it is perhaps not surprising that pheromone released by white cells is able to facilitate opaque cell mating by increasing the levels of extracellular pheromone. This is the case for both opposite- and same-sex mating of opaque cells (Tables 1 and 2). Given that the white phase is the default state, opaque cells are likely to be the minority in a natural population. In such a situation, mating between opaque cells would be rare because the concentration of pheromone produced by opaque cells would not reach the threshold required for activating the mating signaling process. Moreover, low pheromone levels do not arrest opaque cells in the G1 phase of the cell cycle [21], [47], which is a prerequisite for mating in C. albicans. In the presence of pheromone-secreting white a or α cells, the general pheromone level of the population may be increased and thus opaque cell mating could become possible. In the absence of opposite MTL type cells, same-sex mating is unable to occur due to the absence of the opposite mating type pheromone. In Figure 7, we propose a model depicting how white cells could facilitate same-sex mating of opaque cells under natural conditions. In response to α-pheromone released by opaque α cells, white a cells secrete a-pheromone and thus promote same-sex mating of opaque α cells (Figure 7A). In the absence of white a cells, same-sex mating of opaque cells could not occur (Figure 7B and 7C). Our experiments were performed on colonies on plates and on planktonic liquid cultures. We believe that both of these culture conditions are relevant for commensal and pathogenic lifestyles in C. albicans. Colonies represent an architecturally structured community, where cells exist in close proximity to one another, while the planktonic state is the state that cells exist in during a disseminated bloodstream infection. It was suggested that C. albicans can use different strategies to increase mating efficiency [20]. Alby and Bennett (2011) recently reported that interspecies pheromone signaling can promote same-sex mating in C. albicans[48]. This is interesting because C. albicans is often present with other microbiome members within the host, including other fungal, bacterial, and archaeal species. Therefore, to mate efficiently, opaque cells likely take advantage of a number of different strategies and may utilize a multitude of environmental signals to communicate in natural environments.


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 depicting that white cells facilitate same-sex mating of opaque cells.(A) When the majority are white a and/or α cells, same-sex mating between the minority opaque α and α cells can occur. (1) Opaque α cells secrete α-pheromone and (2) induce the majority white a cells to secrete a-pheromone. (3) a-Pheromone in turn induces opaque α cells to form long mating projections and undergo same-sex mating. (4) a-Pheromone induces white α cells to secrete α-pheromone. (5) α-Pheromone further activates white a cells to secrete a-pheromone. (B) When the majority are a/α cells, the minority of opaque α cells cannot form mating projections and cannot undergo same-sex mating. Opaque α cells secrete α-pheromone constitutively, while a/α cells do not secrete pheromone. (C) In the absence of white a cells, opaque α cells cannot form mating projections and cannot undergo same-sex mating.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4199524&req=5

pgen-1004737-g007: Schematic models depicting that white cells facilitate same-sex mating of opaque cells.(A) When the majority are white a and/or α cells, same-sex mating between the minority opaque α and α cells can occur. (1) Opaque α cells secrete α-pheromone and (2) induce the majority white a cells to secrete a-pheromone. (3) a-Pheromone in turn induces opaque α cells to form long mating projections and undergo same-sex mating. (4) a-Pheromone induces white α cells to secrete α-pheromone. (5) α-Pheromone further activates white a cells to secrete a-pheromone. (B) When the majority are a/α cells, the minority of opaque α cells cannot form mating projections and cannot undergo same-sex mating. Opaque α cells secrete α-pheromone constitutively, while a/α cells do not secrete pheromone. (C) In the absence of white a cells, opaque α cells cannot form mating projections and cannot undergo same-sex mating.
Mentions: Since sexual mating in C. albicans is directed by the pheromone-mediated signaling pathway, it is perhaps not surprising that pheromone released by white cells is able to facilitate opaque cell mating by increasing the levels of extracellular pheromone. This is the case for both opposite- and same-sex mating of opaque cells (Tables 1 and 2). Given that the white phase is the default state, opaque cells are likely to be the minority in a natural population. In such a situation, mating between opaque cells would be rare because the concentration of pheromone produced by opaque cells would not reach the threshold required for activating the mating signaling process. Moreover, low pheromone levels do not arrest opaque cells in the G1 phase of the cell cycle [21], [47], which is a prerequisite for mating in C. albicans. In the presence of pheromone-secreting white a or α cells, the general pheromone level of the population may be increased and thus opaque cell mating could become possible. In the absence of opposite MTL type cells, same-sex mating is unable to occur due to the absence of the opposite mating type pheromone. In Figure 7, we propose a model depicting how white cells could facilitate same-sex mating of opaque cells under natural conditions. In response to α-pheromone released by opaque α cells, white a cells secrete a-pheromone and thus promote same-sex mating of opaque α cells (Figure 7A). In the absence of white a cells, same-sex mating of opaque cells could not occur (Figure 7B and 7C). Our experiments were performed on colonies on plates and on planktonic liquid cultures. We believe that both of these culture conditions are relevant for commensal and pathogenic lifestyles in C. albicans. Colonies represent an architecturally structured community, where cells exist in close proximity to one another, while the planktonic state is the state that cells exist in during a disseminated bloodstream infection. It was suggested that C. albicans can use different strategies to increase mating efficiency [20]. Alby and Bennett (2011) recently reported that interspecies pheromone signaling can promote same-sex mating in C. albicans[48]. This is interesting because C. albicans is often present with other microbiome members within the host, including other fungal, bacterial, and archaeal species. Therefore, to mate efficiently, opaque cells likely take advantage of a number of different strategies and may utilize a multitude of environmental signals to communicate in natural environments.

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