The Mating-specific Gα Interacts with a Kinesin-14 and Regulates Pheromone-induced Nuclear Migration in Budding Yeast

Zaichick, Sofia; Metodiev, Metodi V.; Nelson, Scott A.; Durbrovskyi, Oleksii; Draper, Edward; Cooper, John A.; Stone, David E.

doi:10.1091/mbc.e09-01-0069

Cited by 18 publications

(17 citation statements)

References 42 publications

(59 reference statements)

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“…The use of Gpa1 mutants indicated that Gpa1 affects positively the association of Kar3 to the shmoo tip as well as the dynamics and orientation of microtubules. These results suggest that Gpa1 serves as an externally regulated position determinant anchoring Kar3, a role not previously known for G␣ proteins (125). VOL.…”

Section: Pheromone Response and Nuclear Migrationmentioning

confidence: 60%

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Basidiomycete Mating Type Genes and Pheromone Signaling

2010

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2The genome sequences of the basidiomycete Agaricomycetes species Coprinopsis cinerea, Laccaria bicolor, Schizophyllum commune, Phanerochaete chrysosporium, and Postia placenta, as well as of Cryptococcus neoformans and Ustilago maydis, are now publicly available. Out of these fungi, C. cinerea, S. commune, and U. maydis, together with the budding yeast Saccharomyces cerevisiae, have been investigated for years genetically and molecularly for signaling in sexual reproduction. The comparison of the structure and organization of mating type genes in fungal genomes reveals an amazing conservation of genes regulating the sexual reproduction throughout the fungal kingdom. In agaricomycetes, two mating type loci, A, coding for homeodomain type transcription factors, and B, encoding a pheromone/receptor system, regulate the four typical mating interactions of tetrapolar species. Evidence for both A and B mating type genes can also be identified in basidiomycetes with bipolar systems, where only two mating interactions are seen. In some of these fungi, the B locus has lost its self/nonself discrimination ability and thus its specificity while retaining the other regulatory functions in development. In silico analyses now also permit the identification of putative components of the pheromone-dependent signaling pathways. Induction of these signaling cascades leads to development of dikaryotic mycelia, fruiting body formation, and meiotic spore production. In pheromone-dependent signaling, the role of heterotrimeric G proteins, components of a mitogen-activated protein kinase (MAPK) cascade, and cyclic AMP-dependent pathways can now be defined. Additionally, the pheromone-dependent signaling through monomeric, small GTPases potentially involved in creating the polarized cytoskeleton for reciprocal nuclear exchange and migration during mating is predicted. THE MATING SYSTEMS IN BASIDIOMYCETESThe typical life cycle of the higher basidiomycetes, presently classified as Agaricomycetes (Table 1) (34), consists of haploid, monokaryotic as well as dikaryotic stages, the latter of which prevails in nature. The monokaryotic mycelium contains nuclei of only one genetic type and is thus termed homokaryon. This mycelium, grown from haploid spores, in general contains one nucleus per cell (Fig. 1). The dikaryon is formed when genetically different homokaryons mate. In the saprotrophic agaricomycetes, the mushroom-forming species Schizophyllum commune and Coprinopsis cinerea (Table 1), mating is regulated by a tetrapolar system consisting of two unlinked genetic complexes, named A and B. The term tetrapolar reflects the fact that there are four possible mating interactions scored in matings between haploid strains derived from spores formed on the fruiting bodies of same parent dikaryon: a fully compatible interaction occurs when both A and B between the mates are of different specificities (Fig. 1), an incompatible interaction occurs when allelic specificities are all the same, and two semicompatible interactions occur when either A-o...

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Section: Pheromone Response and Nuclear Migrationmentioning

confidence: 60%

“…In S. cerevisiae, it is reported that a mating-specific G␣, Gpa1, interacts with kinesin-14 (Kar-3), a minus-end-directed microtubule-associated motor, in a pheromone-responsive way (125). The interaction regulates pheromone-induced nuclear migration to the shmoo tip.…”

Section: Pheromone Response and Nuclear Migrationmentioning

confidence: 99%

Basidiomycete Mating Type Genes and Pheromone Signaling

2010

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“…In shmooing cells, cytoplasmic Kar3/Cik1 has been proposed to maintain depolymerizing MT plus ends at the shmoo tip (Meluh and Rose 1990;Maddox et al 2003). This is likely due to an interaction of Kar3 with the mating-specific Ga subunit of a trimeric G protein involved in pheromone signaling (Zaichick et al 2009). Pheromone stimulation increases the expression of KAR3 and CIK1 via activation of the transcription factors Ste12 and Kar4 (Kurihara et al 1996;Gammie et al 1999;Lahav et al 2007) and underlies the expression of the shorter NLS-less cytoplasmic Cik1 variant (Manning et al 1999;Benanti et al 2009).…”

Section: Discussionmentioning

confidence: 99%

Spindle pole body-anchored Kar3 drives the nucleus along microtubules from another nucleus in preparation for nuclear fusion during yeast karyogamy

et al. 2013

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Nuclear migration during yeast karyogamy, termed nuclear congression, is required to initiate nuclear fusion. Congression involves a specific regulation of the microtubule minus end-directed kinesin-14 motor Kar3 and a rearrangement of the cytoplasmic microtubule attachment sites at the spindle pole bodies (SPBs). However, how these elements interact to produce the forces necessary for nuclear migration is less clear. We used electron tomography, molecular genetics, quantitative imaging, and first principles modeling to investigate how cytoplasmic microtubules are organized during nuclear congression. We found that Kar3, with the help of its light chain, Cik1, is anchored during mating to the SPB component Spc72 that also serves as a nucleator and anchor for microtubules via their minus ends. Moreover, we show that no direct microtubule-microtubule interactions are required for nuclear migration. Instead, SPB-anchored Kar3 exerts the necessary pulling forces laterally on microtubules emanating from the SPB of the mating partner nucleus. Therefore, a twofold symmetrical application of the core principle that drives nuclear migration in higher cells is used in yeast to drive nuclei toward each other before nuclear fusion.

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“…In the latter case, further increases in the ratio of G proteins to receptors would be expected to lead to more complete suppression of the dominant-negative phenotype. However, it would be difficult to achieve such high levels without altering the balance of subunit biosynthesis or inducing secondary effects on the overall responses of the pheromone pathway arising from the multiplicity of roles of subunits (35,48,57).…”

Section: Fig 1 Cellular Level Of Expression Of Chromosomally Encoded mentioning

confidence: 99%

Functional and Physical Interactions among Saccharomyces cerevisiae α-Factor Receptors

2012

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The ␣-factor receptor Ste2p is a G protein-coupled receptor (GPCR) expressed on the surface of MATa haploid cells of the yeast Saccharomyces cerevisiae. Binding of ␣-factor to Ste2p results in activation of a heterotrimeric G protein and of the pheromone response pathway. Functional interactions between ␣-factor receptors, such as dominant-negative effects and recessive behavior of constitutive and hypersensitive mutant receptors, have been reported previously. We show here that dominant-negative effects of mutant receptors persist over a wide range of ratios of the abundances of G protein to receptor and that such effects are not blocked by covalent fusion of G protein ␣ subunits to normal receptors. In addition, we detected dominant effects of mutant C-terminally truncated receptors, which had not been previously reported to act in a dominant manner. Furthermore, coexpression of C-terminally truncated receptors with constitutively active mutant receptors results in enhancement of constitutive signaling. Together with previous evidence for oligomerization of Ste2p receptors, these results are consistent with the idea that functional interactions between coexpressed receptors arise from physical interactions between them rather than from competition for limiting downstream components, such as G proteins.

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The Mating-specific Gα Interacts with a Kinesin-14 and Regulates Pheromone-induced Nuclear Migration in Budding Yeast

Cited by 18 publications

References 42 publications

Basidiomycete Mating Type Genes and Pheromone Signaling

Basidiomycete Mating Type Genes and Pheromone Signaling

Spindle pole body-anchored Kar3 drives the nucleus along microtubules from another nucleus in preparation for nuclear fusion during yeast karyogamy

Functional and Physical Interactions among Saccharomyces cerevisiae α-Factor Receptors

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