scholarly journals Unisexual reproduction promotes competition for mating partners in the global human fungal pathogenCryptococcus deneoformans

2019 ◽  
Author(s):  
Ci Fu ◽  
Torin P. Thielhelm ◽  
Joseph Heitman

AbstractCourtship is pivotal for successful mating. However, courtship is challenging for theCryptococcus neoformansspecies complex, comprised of opportunistic fungal pathogens, as the majority of isolates are α mating type. In the absence of mating partners of the opposite mating type,C. deneoformanscan undergo unisexual reproduction, during which a yeast-to-hyphal morphological transition occurs. Hyphal growth during unisexual reproduction is a quantitative trait, which reflects a strain’s ability to undergo unisexual reproduction. In this study, we determined whether unisexual reproduction confers an ecological benefit by promoting foraging for mating partners. Through competitive mating assays using strains with different abilities to produce hyphae, we showed that unisexual reproduction potential did not enhance competition for mating partners of the same mating type, but when cells of the opposite mating type were present, cells with enhanced hyphal growth were more competitive for mating partners of either the same or opposite mating type. Enhanced mating competition was also observed in a strain with increased hyphal production that lacks the mating repressor geneGPA3, which contributes to the pheromone response. Hyphal growth in unisexual strains also enables contact between adjacent colonies and enhances mating efficiency during mating confrontation assays. The pheromone response pathway activation positively correlated with unisexual reproduction hyphal growth during bisexual mating and exogenous pheromone promoted bisexual cell fusion. Despite the benefit in competing for mating partners, unisexual reproduction conferred a fitness cost. Taken together, these findings suggestC. deneoformansemploys hyphal growth to facilitate contact between colonies at long distances and utilizes pheromone sensing to enhance mating competition.Author SummarySexual reproduction plays a pivotal role in shaping fungal population structure and diversity in nature. The global human fungal pathogenCryptococcus neoformansspecies complex evolved distinct sexual cycles: bisexual reproduction between mating partners of the opposite mating types, and unisexual reproduction with only one mating type. During both sexual cycles, cells undergo a yeast-to-hyphal morphological transition and nuclei diploidize through either cell-cell fusion followed by nuclear fusion during bisexual reproduction or endoreplication during unisexual reproduction. Despite the complex sexual life cycle, the majority of Cryptococcal isolates are α mating type. Albeit the scarcity ofMATacells in the environment, meiotic recombination is prevalent. To decipher this conundrum, we ask whether there is an underlying mechanism in whichCryptococcusspecies increase their mating opportunities. In this study, we showed that the undirected hyphal growth during unisexual reproduction enablesMATα cells to forage for mating partners over a larger surface area, and whenMATα hyphae come into close proximity of rareMATacells, pheromone response pathway activation in bothMATα andMATacells can further enhance mating. This mating enhancement could promote outcrossing and facilitate genome reshuffling via meiotic recombination.

2013 ◽  
Vol 12 (8) ◽  
pp. 1155-1159 ◽  
Author(s):  
Sujal S. Phadke ◽  
Marianna Feretzaki ◽  
Joseph Heitman

ABSTRACT Unisexual reproduction is a novel homothallic sexual cycle recently discovered in both ascomycetous and basidiomycetous pathogenic fungi. It is a form of selfing that induces the yeast-to-hyphal dimorphic transition in isolates of the α mating type of the human fungal pathogen Cryptococcus neoformans . Unisexual reproduction may benefit the pathogen by facilitating sexual reproduction in the absence of the opposite a mating type and by generating infectious propagules called basidiospores. Here, we report an independent potential selective advantage of unisexual reproduction beyond genetic exchange and recombination. We competed a wild-type strain capable of undergoing unisexual reproduction with mutants defective in this developmental pathway and found that unisexual reproduction provides a considerable dispersal advantage through hyphal growth and sporulation. Our results show that unisexual reproduction may serve to facilitate access to both nutrients and potential mating partners and may provide a means to maintain the capacity for dimorphic transitions in the environment.


1971 ◽  
Vol 18 (3) ◽  
pp. 255-264 ◽  
Author(s):  
B. C. Lamb

SUMMARYRecombination data from crosses made at a single constant temperature of incubation were compared with those from crosses transferred to a different temperature at either the time of conidiation of protoperithecia by the strain of opposite mating-type, or after fertilization when crozier stages were first visible. Results were also compared from reciprocal crosses, from crosses made in different ways and from crosses in which protoperithecia were conidiated at different stages of maturity.Different temperature regimes during vegetative growth and proto-perithecial development had highly significant effects on subsequent meiotic recombination, while temperature differences during later premeiotic stages (between conidiation of protoperithecia and the crozier stage) had no or little effect. It was found that premeiotic controls could have as great, or greater, effects on meiotic recombination than those operating directly during meiosis. The possible adaptive significance of this is discussed.Recombination frequencies were affected by the method of making a cross (joint-inoculation of strains of opposite mating-type, or conidiation of protoperithecia), and by protoperithecial age at the time of conidiation by the opposite mating-type. Differences in recombination between reciprocal crosses were obtained and were dependent on temperature of incubation and age of protoperithecia at the time of conidiation. Recombination was not affected by different lysine concentrations in the medium. Genetic differences in premeiotic effector-production between the strains used were inferred.


Genetics ◽  
2000 ◽  
Vol 155 (3) ◽  
pp. 1005-1018 ◽  
Author(s):  
Paul J Cullen ◽  
Janet Schultz ◽  
Joe Horecka ◽  
Brian J Stevenson ◽  
Yoshifumi Jigami ◽  
...  

Abstract In haploid Saccharomyces cerevisiae, mating occurs by activation of the pheromone response pathway. A genetic selection for mutants that activate this pathway uncovered a class of mutants defective in cell wall integrity. Partial loss-of-function alleles of PGI1, PMI40, PSA1, DPM1, ALG1, MNN10, SPT14, and OCH1, genes required for mannose utilization and protein glycosylation, activated a pheromone-response-pathway-dependent reporter (FUS1) in cells lacking a basal signal (ste4). Pathway activation was suppressed by the addition of mannose to hexose isomerase mutants pgi1-101 and pmi40-101, which bypassed the requirement for mannose biosynthesis in these mutants. Pathway activation was also suppressed in dpm1-101 mutants by plasmids that contained RER2 or PSA1, which produce the substrates for Dpm1. Activation of FUS1 transcription in the mannose utilization/protein glycosylation mutants required some but not all proteins from three different signaling pathways: the pheromone response, invasive growth, and HOG pathways. We specifically suggest that a Sho1 → Ste20/Ste50 → Ste11 → Ste7 → Kss1 → Ste12 pathway is responsible for activation of FUS1 transcription in these mutants. Because loss of pheromone response pathway components leads to a synthetic growth defect in mannose utilization/protein glycosylation mutants, we suggest that the Sho1 → Ste12 pathway contributes to maintenance of cell wall integrity in vegetative cells.


2020 ◽  
Author(s):  
Vikas Yadav ◽  
Sheng Sun ◽  
Joseph Heitman

AbstractSome animal species require an opposite-sex partner for their sexual development but discard the partner’s genome before gamete formation, generating hemi-clonal progeny in a process called hybridogenesis. In this study, we discovered hybridogenesis-like reproduction in a basidiomycete fungus, Cryptococcus neoformans. C. neoformans has two mating types, MATa and MATα, which fuse to produce a dikaryotic zygote that completes a sexual cycle producing recombinant meiotic progeny. Here, we discovered exclusive uniparental inheritance of nuclear genetic material in a fraction of the F1 progeny produced during bisexual reproduction of two opposite mating-type partners. By analyzing strains expressing fluorescent reporter proteins, we observed that dikaryotic hyphae were produced, but only one parental nuclei was found in the terminal basidium where sporulation occurs. Whole-genome sequencing revealed the nuclear genome of the progeny was identical with one or the other parental genome, whereas the mitochondrial genome was always inherited from the MATa parent. Uniparental sporulation was also observed in natural isolate crosses occurring in concert with biparental sporulation. The meiotic recombinase Dmc1 was found to be critical for uniparental reproduction. These findings reveal an unusual mode of eukaryotic microbial unisexual reproduction that shares features with hybridogenesis in animals.


Author(s):  
Anna Carolina Borges Pereira Costa ◽  
Raha Parvizi Omran ◽  
Chris Law ◽  
Vanessa Dumeaux ◽  
Malcolm Whiteway

Abstract Candida albicans opaque cells release pheromones to stimulate cells of opposite mating type to activate their pheromone response pathway. Although this fungal pathogen shares orthologous proteins involved in the process with Saccharomyces cerevisiae, the pathway in each organism has unique characteristics. We have used GFP-tagged fusion proteins to investigate the localization of the scaffold protein Cst5, as well as the MAP kinases Cek1 and Cek2, during pheromone response in C. albicans. In wild-type cells, pheromone treatment directed Cst5-GFP to surface puncta concentrated at the tips of mating projections. These puncta failed to form in cells defective in either the Gα or β subunits. However, they still formed in response to pheromone in cells missing Ste11, but with the puncta distributed around the cell periphery in the absence of mating projections. These puncta were absent from hst7Δ/Δ cells, but could be detected in the ste11Δ/Δ hst7Δ/Δ double mutant. Cek2-GFP showed a strong nuclear localization late in the response, consistent with a role in adaptation, while Cek1-GFP showed a weaker, but early increase in nuclear localization after pheromone treatment. Activation loop phosphorylation of both Cek1 and Cek2 required the presence of Ste11. In contrast to Cek2-GFP, which showed no localization signal in ste11Δ/Δ cells, Cek1-GFP showed enhanced nuclear localization that was pheromone independent in the ste11Δ/Δ mutant. The results are consistent with CaSte11 facilitating Hst7-mediated MAP kinase phosphorylation and also playing a potentially critical role in both MAP kinase and Cst5 scaffold localization.


1975 ◽  
Vol 17 (3) ◽  
pp. 441-449 ◽  
Author(s):  
A. M. DeLange ◽  
A. J. F. Griffiths

In Neurospora crassa, strains of opposite mating type generally do not form stable heterokaryons because the mating type locus acts as a heterokaryon incompatibility locus. However, when one A and one a strain, having complementing auxotrophic mutants, are placed together on minimal medium, growth may occur, although the growth is generally slow. In this study, escape from such slow growth to that at a wild type or near-wild type rate was observed. The escaped cultures are stable heterokaryons, mostly having lost the mating type allele function from one component nucleus, so that the nuclear types are heterokaryon compatible. Either A or a mating type can be lost. This loss of function has been attributed to deletion since only one nuclear type could be recovered in all heterokaryons except one, but deletion spanning adjacent loci has been directly demonstrated in a minority of cases. Alternatively when one component strain is tol and the other tol+ (tol being a recessive mutant suppressing the heterokaryon incompatibility associated with mating type), escape may occur by the deletion or mutation of tol+, also resulting in heterokaryon compatibility. An induction mechanism for escape is speculated upon.


1993 ◽  
Vol 13 (5) ◽  
pp. 3067-3075 ◽  
Author(s):  
K S Lee ◽  
K Irie ◽  
Y Gotoh ◽  
Y Watanabe ◽  
H Araki ◽  
...  

Mitogen-activated protein (MAP) kinases are activated in response to a variety of stimuli through a protein kinase cascade that results in their phosphorylation on tyrosine and threonine residues. The molecular nature of this cascade is just beginning to emerge. Here we report the isolation of a Saccharomyces cerevisiae gene encoding a functional analog of mammalian MAP kinases, designated MPK1 (for MAP kinase). The MPK1 gene was isolated as a dosage-dependent suppressor of the cell lysis defect associated with deletion of the BCK1 gene. The BCK1 gene is also predicted to encode a protein kinase which has been proposed to function downstream of the protein kinase C isozyme encoded by PKC1. The MPK1 gene possesses a 1.5-kb uninterrupted open reading frame predicted to encode a 53-kDa protein. The predicted Mpk1 protein (Mpk1p) shares 48 to 50% sequence identity with Xenopus MAP kinase and with the yeast mating pheromone response pathway components, Fus3p and Kss1p. Deletion of MPK1 resulted in a temperature-dependent cell lysis defect that was virtually indistinguishable from that resulting from deletion of BCK1, suggesting that the protein kinases encoded by these genes function in a common pathway. Expression of Xenopus MAP kinase suppressed the defect associated with loss of MPK1 but not the mating-related defects associated with loss of FUS3 or KSS1, indicating functional conservation between the former two protein kinases. Mutation of the presumptive phosphorylated tyrosine and threonine residues of Mpk1p individually to phenylalanine and alanine, respectively, severely impaired Mpk1p function. Additional epistasis experiments, and the overall architectural similarity between the PKC1-mediated pathway and the pheromone response pathway, suggest that Pkc1p regulates a protein kinase cascade in which Bck1p activates a pair of protein kinases, designated Mkk1p and Mkk2p (for MAP kinase-kinase), which in turn activate Mpk1p.


Sign in / Sign up

Export Citation Format

Share Document