Academic journal article Genetics

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

Academic journal article Genetics

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

Article excerpt

MEMBRANE 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 fi ssion yeast Schizosaccharomyces pombe, heterothallic cells belong to one of two mating types, M (h2 cells) or P (h+ cells) while h90 strains are homothallic (Arcangioli and Thon 2004). In rich medium, h+ and h2 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, 1998a,b; Kurahashi 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, leadingtoanaccumulationofprezygotes (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 is a formin required for the organization of actin patches at the shmoo tip (Petersen et al. 1995, 1998b). S. pombe diploid nuclei are unstable, such that meiosis occurs immediately after karyogamy, and zygotes give rise to asci containing four ascospores (Nielsen 2004; Yamamoto 2004).

Genome-wide analyses performed using nitrogen starvation and pheromone treatments have been used to analyze gene expression under mating conditions (Mata et al. 2002; Mata and Bahler 2006). Study of some previously uncharacterized genes whose expression was induced in response to mating conditions led to the characterization of the h+specific agglutinin map4+ (Yamamoto et al. 1997; Mata and Bahler 2006; Sharifmoghadam et al. 2006), and dni1+ and dni2+, two members of the Fig1-related family of fungal claudin-like proteins (Clemente-Ramos et al. 2009). dni1D and dni2D mutants exhibit a temperature-sensitive cell fusion defect due to a lack of coordination between membrane organization and cell-wall remodeling at the cell-cell contact region (Clemente-Ramos et al. 2009). The SPAP7G5.03 gene, which codes for a protein with several potential transmembrane domains that is 22% identical to the S. cerevisiae Prm1 (Heiman and Walter 2000), was not identified as a mating-induced gene in the extensive analyses (Mata et al. 2002; Mata and Bahler 2006). In budding yeast, PRM1 is highly induced in response to pheromones and its absence leads to a ^50% reduction in the efficiency of cell fusion during mating. S. cerevisiae prm1D mating partners degrade the cross wall separating both cells and their plasma membranes remain apposed but not fused (Heiman and Walter 2000). In the prm1D zygotes, intercellular bubbles and fingers are produced when the cytoplasm of one of the cells invades part of the cytoplasm of the other mating partner because the apposed membranes cannot support turgor pressure in the absence of the cell wall (Heiman and Walter 2000; Jin et al. 2004). It has been proposed that Prm1p is a fusion facilitator that might help to form a pore at the contact area between mating partners (White and Rose 2001; Olmo and Grote 2010a). Neurospora crassa has a PRM1 ortholog whose deletion leads to a 50% reduction in cell fusion during vegetative and sexual cell fusion, the appearance of intercellular bubbles/fingers with apposed plasma membranes during vegetative cell fusion, and defects in postmeiotic events that lead to complete sterility (Fleissner et al. 2009). Intercellular bubbles/fingers have also been observed in S. …

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