Mate and fuse: how yeast cells do it

Merlini, Laura; Dudin, Omaya; Martin, Sophie G.

doi:10.1098/rsob.130008

Cited by 217 publications

(227 citation statements)

References 148 publications

Supporting

Mentioning

203

Contrasting

Unclassified

Order By: Relevance

“…In S. cerevisiae, in contrast, each offspring is immediately diploid and each has a different combination of parental alleles, having inherited only one of two homologous parental chromosomes, with parental alleles on these partially unlinked by chiasma formation (Carlile et al 2001). S. cerevisiae's sexual cycle further increases efficacy of selection of the best allele combinations by allowing frequent return to the mating-competent state, not by spontaneous LOH but in response to environmental cues (Merlini et al 2013), increasing the likelihood that mating-competent cells will quickly find a compatible partner and reducing the cost of the slower growth of mating competent cells.…”

Section: Discussionmentioning

confidence: 99%

Selective Advantages of a Parasexual Cycle for the YeastCandida albicans

Zhang

Magee

et al. 2015

Genetics

View full text Add to dashboard Cite

The yeast Candida albicans can mate. However, in the natural environment mating may generate progeny (fusants) fitter than clonal lineages too rarely to render mating biologically significant: C. albicans has never been observed to mate in its natural environment, the human host, and the population structure of the species is largely clonal. It seems incapable of meiosis, and most isolates are diploid and carry both mating-type-like (MTL) locus alleles, preventing mating. Only chromosome loss or localized loss of heterozygosity can generate mating-competent cells, and recombination of parental alleles is limited. To determine if mating is a biologically significant process, we investigated if mating is under selection. The ratio of nonsynonymous to synonymous mutations in mating genes and the frequency of mutations abolishing mating indicated that mating is under selection. The MTL locus is located on chromosome 5, and when we induced chromosome 5 loss in 10 clinical isolates, most of the resulting MTL-homozygotes could mate with each other, producing fusants. In laboratory culture, a novel environment favoring novel genotypes, some fusants grew faster than their parents, in which loss of heterozygosity had reduced growth rates, and also faster than their MTL-heterozygous ancestors-albeit often only after serial propagation. In a small number of experiments in which co-inoculation of an oral colonization model with MTL-homozygotes yielded small numbers of fusants, their numbers declined over time relative to those of the parents. Overall, our results indicate that mating generates genotypes superior to existing MTL-heterozygotes often enough to be under selection.KEYWORDS Candida albicans; mating; parasexual cycle; cryptic sexual cycle S EX is costly and disrupts well-adapted allele combinations. It can also be advantageous by speeding up adaptation or by purging deleterious mutations. It has been difficult to establish how, precisely, these and other benefits outweigh the cost of sex. Indeed, abandoning sex in favor of clonal reproduction can be advantageousasexual species arise frequently. Their life spans are short, however, indicating that sex may be essential for the long-term survival of species (Otto and Lenormand 2002;Rice 2002).Sexual cycles have not been observed for 20% of fungal species (Carlile et al. 2001). Whether these species are truly asexual or merely restrict the frequency of sex-a strategy believed to maximize its benefits (Heitman 2006)-is difficult to determine. Genetic marker distributions in such species often suggest limited recombination (Carlile et al. 2001). However, clonal reproduction will initially copy the genetic marker distributions that were generated by sex, and new mutations and genetic drift will only slowly erase evidence of past recombination (Schmid et al. 2004;Cox et al. 2013). With rare exceptions, fungi without observable sexual cycles are derived from recent sexual ancestors (Carlile et al. 2001;Schmid et al. 2004;Butler 2007). Thus genetic marker distributi...

show abstract

Section: Discussionmentioning

confidence: 99%

Selective Advantages of a Parasexual Cycle for the YeastCandida albicans

Zhang

Magee

et al. 2015

Genetics

View full text Add to dashboard Cite

show abstract

“…cerevisiae and S. pombe are distantly related yeasts (Sipiczki 2000) and hence studies addressing mating in both organisms might help to understand the conserved and divergent functions of proteins involved in this developmental process (Merlini et al 2013). In this work we have analyzed the role of S. pombe prm1 + in mating and its relationship with other genes involved in cell fusion.…”

mentioning

confidence: 99%

Membrane Organization and Cell Fusion During Mating in Fission Yeast Requires Multipass Membrane Protein Prm1

et al. 2014

View full text Add to dashboard Cite

The involvement of Schizosaccharomyces pombe prm1 + in cell fusion during mating and its relationship with other genes required for this process have been addressed. S. pombe prm1D mutant exhibits an almost complete blockade in cell fusion and an abnormal distribution of the plasma membrane and cell wall in the area of cell-cell interaction. The distribution of cellular envelopes is similar to that described for mutants devoid of the Fig1-related claudin-like Dni proteins; however, prm1 + and the dni + genes act in different subpathways. Time-lapse analyses show that in the wild-type S. pombe strain, the distribution of phosphatidylserine in the cytoplasmic leaflet of the plasma membrane undergoes some modification before an opening is observed in the cross wall at the cellcell contact region. In the prm1D mutant, this membrane modification does not take place, and the cross wall between the mating partners is not extensively degraded; plasma membrane forms invaginations and fingers that sometimes collapse/retract and that are sometimes strengthened by the synthesis of cell-wall material. Neither prm1D nor prm1D dniD zygotes lyse after cell-cell contact in medium containing and lacking calcium. Response to drugs that inhibit lipid synthesis or interfere with lipids is different in wild-type, prm1D, and dni1D strains, suggesting that membrane structure/organization/dynamics is different in all these strains and that Prm1p and the Dni proteins exert some functions required to guarantee correct membrane organization that are critical for cell fusion. M EMBRANE fusion is essential for several developmental processes. The characterization of mating in yeasts represents a useful tool for understanding the mechanisms involved in intercellular membrane merger and their regulation. In the fission yeast Schizosaccharomyces pombe, heterothallic cells belong to one of two mating types, M (h 2 cells) or P (h + cells) while h 90 strains are homothallic (Arcangioli and Thon 2004). In rich medium, h + and h 2 cells can proliferate actively together without mating. When nitrogen becomes scarce the cAMP level decreases, which triggers the expression of genes required for sexual differentiation. Cells arrest in G1 and polarize, giving rise to specialized cells termed shmoos (Yamamoto et al. 1997;Davey 1998;Nielsen 2004;Yamamoto 2004). After agglutination, the cross wall separating both parental cells is degraded, allowing cell fusion. Efficient cell fusion requires the correct organization of the cytoskeleton (Petersen et al. 1995(Petersen et al. , 1998aKurahashi et al. 2002;Doyle et al. 2009). The S. cerevisiae FUS1 and the S. pombe fus1 + genes have the same name and both mutants exhibit cell fusion defects during mating, leading to an accumulation of prezygotes (mating intermediates in which the mating partners have established a stable contact but have not yet fused). However, the corresponding proteins are not related; while Saccharomyces cerevisiae Fus1p is a membrane protein (Trueheart et al. 1987), S. pombe Fus1p ...

show abstract

“…During mating of the budding yeast, Saccharomyces cerevisiae, two haploid cells of opposite mating types fuse to form a diploid zygote, making this organism an excellent model to study cell fusion Merlini et al 2013). The yeast mating pathway begins with pheromone recognition and subsequent activation of a wellcharacterized kinase cascade.…”

mentioning

confidence: 99%

Kel1p Mediates Yeast Cell Fusion Through a Fus2p- and Cdc42p-Dependent Mechanism

Smith¹,

Rose

2016

Genetics

View full text Add to dashboard Cite

Cell fusion is ubiquitous among eukaryotes. Although little is known about the molecular mechanism, several proteins required for cell fusion in the yeast Saccharomyces cerevisiae have been identified. Fus2p, a key regulator of cell fusion, localizes to the shmoo tip in a highly regulated manner. C-terminal truncations of Fus2p cause mislocalization and fusion defects, which are suppressed by overexpression of Kel1p, a kelch-domain protein of unknown function previously implicated in cell fusion. We hypothesize that Fus2p mislocalization is caused by auto-inhibition, which is alleviated by Kel1p overexpression. Previous work showed that Fus2p localization is mediated by both Fus1p-and actin-dependent pathways. We show that the C-terminal mutations mainly affect the actindependent pathway. Suppression of the Fus2p localization defect by Kel1p is dependent upon Fus1p, showing that suppression does not bypass the normal pathway. Kel1p and a homolog, Kel2p, are required for efficient Fus2p localization, acting through the actindependent pathway. Although Kel1p overexpression can weakly suppress the mating defect of a FUS2 deletion, the magnitude of suppression is allele specific. Therefore, Kel1p augments, but does not bypass, Fus2p function. Fus2p mediates cell fusion by binding activated Cdc42p. Although Kel1p overexpression suppresses a Cdc42p mutant that is defective for Fus2p binding, cell fusion remains dependent upon Fus2p. These data suggest that Fus2p, Cdc42p, and Kel1p form a ternary complex, which is stabilized by Kel1p. Supporting this hypothesis, Kel1p interacts with two domains of Fus2p, partially dependent on Cdc42p. We conclude that Kel1p enhances the activity of Fus2p/Cdc42p in cell fusion.

show abstract

Mate and fuse: how yeast cells do it

Cited by 217 publications

References 148 publications

Selective Advantages of a Parasexual Cycle for the YeastCandida albicans

Selective Advantages of a Parasexual Cycle for the YeastCandida albicans

Membrane Organization and Cell Fusion During Mating in Fission Yeast Requires Multipass Membrane Protein Prm1

Kel1p Mediates Yeast Cell Fusion Through a Fus2p- and Cdc42p-Dependent Mechanism

Contact Info

Product

Resources

About