Academic journal article Genetics

Genetic Evidence for a SPO1-Dependent Signaling Pathway Controlling Meiotic Progression in Yeast

Academic journal article Genetics

Genetic Evidence for a SPO1-Dependent Signaling Pathway Controlling Meiotic Progression in Yeast

Article excerpt

ABSTRACT

The yeast spindle pole body (SPB) plays a unique role in meiosis, initiating both spindle assembly and prospore membrane synthesis. SPO1, induced early in development, encodes a meiosis-specific phospholipase B (PLB) homolog required at three stages of SPB morphogenesis: MI, MII, and spore formation. Here we report in-depth analysis of the SPO1 gene including its transcriptional control by regulators of early gene expression, protein localization to the ER lumen and periplasmic space, and molecular genetic studies of its role in meiosis. Evidence is presented that multiple arrest points in spo1Δ occur independently, demonstrating that Spo1 acts at distinct steps. Loss of Spo1 is suppressed by high-copy glycosylphosphatidylinositol (GPI) proteins, dependent on sequence, timing, and strength of induction in meiosis. Since phosphatidylinositol (PI) serves as both an anchor component and a lipase substrate, we hypothesized that GPI-protein expression might substitute for Spo1 by decreasing levels of its potential substrates, PI and phosphatidylinositol phosphates (PIPs). Partial spo1Δ complementation by PLB3 (encoding a unique PLB capable of cleaving PI) and relatively strong Spo1 binding to PI(4)P derivatives (via a novel N-terminal lysine-rich fragment essential for Spo1 function) are consistent with this view. Epistasis of SPO1 mutations to those in SPO14 (encoding a PLD involved in signaling) and physical interaction of Spo1 with Spo23, a protein regulating PI synthesis required for wild-type sporulation, further support this notion. Taken together these findings implicate PI and/or PIPs in Spo1 function and suggest the existence of a novel Spo1-dependent meiosis-specific signaling pathway required for progression of MI, MII, and spore formation via regulation of the SPB.

THE unicellular eukaryote Saccharomyces cerevisiae undergoes gametogenesis in response to both cell type and environmental signals (for recent reviews see NASMYTH 2003; ESPOSITO 2006). A number of genes are specifically required for this process that are not expressed during vegetative growth (CHU et al. 1998; PRIMIG et al. 2000). Premeiotic DNA synthesis, followed by genetic recombination and two successive nuclear divisions (MI and MII), results in the formation of asci containing four haploidmeiotic products encapsulated in spores. The process of spore wall development is highly coordinated with progression of the meiotic divisions beginning at approximately the same time as MII. The yeast spindle pole body (SPB) plays a unique role in meiosis, initiating both spindle assembly and prosporemembrane synthesis. The SPB is a tripartite structure embedded in the nuclear membrane (reviewed in JASPERSEN and WINEY 2004). During early MII, SPBs undergo a modification enlarging their outer plaques, making them distinct from both mitotic and MI SPBs (MOENS 1974). Several meiosis-specific proteins localize to the modified outer plaques (MOPs) and promote recruitment of lipid vesicles that fuse to form an expanding prospore membrane (KNOP and STRASSER 2000; MORENO-BORCHART et al. 2001; NEIMAN 2005). This process is controlled by a specialized branch of the secretory pathway (NEIMAN 1998). Prospores then mature by the ordered assembly of mannan, glucan, chitosan, and dityrosine layers, respectively (SMITS et al. 2001; COLUCCIO et al. 2004). Since SPBs nucleate both spindle formation (at MI and MII) and prospore membrane synthesis, regulation of its morphogenesis is a likely target of processes ensuring coordination of the nuclear divisions with gamete differentiation. At present, little is known about the mechanism( s) coordinating meiosis with gamete development in any organism. This study aims at understanding this process, using budding yeast as a model system.

We previously provided evidence that SPO1, a gene implicated in meiotic SPB morphogenesis, potentially functions in coordinating the divisions with gamete development (TEVZADZE et al. …

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