Role of the α‐glucanase Agn2p in ascus‐wall endolysis following sporulation in fission yeast

Dekker, Natashe Lemos; Rijssel, Jos van; Distel, Ben; Hochstenbach, Frans

doi:10.1002/yea.1464

Cited by 28 publications

(36 citation statements)

References 34 publications

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“…In addition, we noted that significant numbers of asci from dma1-D homozygous meiosis failed to release spores in the first 24 hours after placement on yeast extract (YE) plates (Table 1B). The reason for the delayed germination of dma1-D spores is unclear, but might reflect alterations in the composition of the spore wall or alterations in the expression of agn2, which is required for the release of spores from the ascus (Dekker et al, 2007).…”

Section: Meiosis In the Absence Of Dma1 Function Produces Asci With Lmentioning

confidence: 99%

The role ofSchizosaccharomyces pombe dma1in spore formation during meiosis

Krapp

Rosario

2010

Journal of Cell Science

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SummaryMeiosis is a specialised form of the cell cycle that gives rise to haploid gametes. In Schizosaccharomyces pombe, the products of meiosis are four spores, which are formed by encapsulation of the four meiosis II nuclei within the cytoplasm of the zygote produced by fusion of the mating cells. The S. pombe spindle pole body is remodelled during meiosis II and membrane vesicles are then recruited there to form the forespore membrane, which encapsulates the haploid nucleus to form a prespore. Spore wall material is then deposited, giving rise to the mature spore. The septation initiation network is required to coordinate cytokinesis and mitosis in the vegetative cycle and for spore formation in the meiotic cycle. We have investigated the role of the SIN regulator dma1p in meiosis; we find that although both meiotic divisions occur in the absence of dma1p, asci frequently contain fewer than four spores, which are larger than in wild-type meiosis. Our data indicate that dma1p acts in parallel to the leading-edge proteins and septins to assure proper formation for the forespore membrane. Dma1p also contributes to the temporal regulation of the abundance of the meiosis-specific SIN component mug27p.

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Section: Meiosis In the Absence Of Dma1 Function Produces Asci With Lmentioning

confidence: 99%

The role ofSchizosaccharomyces pombe dma1in spore formation during meiosis

Krapp

Rosario

2010

Journal of Cell Science

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“…When the spore cell wall is synthesized, the inner layer of the forespore membrane becomes the spore plasma membrane, whereas the outer layer autolyzes. It is possible that a similar degradation occurs with the plasma membrane of the ascus, allowing Eng2 and Agn2 to access their substrates, as has been previously proposed (7). Interestingly, the genomes of other yeasts, such as S. cerevisiae and Candida albicans, contain a pair of endo-␤-1,3-glucanases, one of which lacks a signal peptide (4,9).…”

mentioning

confidence: 56%

“…For conjugation and sporulation assays, haploid cells of opposite mating types were induced to conjugate and sporulate on EMM-N solid medium (EMM without the nitrogen source). The regulated expression of eng2 ϩ during sporulation was achieved as previously described (7). Diploid cells first were grown to the exponential phase in EMM containing 1% ammonium chloride (EMM-AC).…”

Section: Methodsmentioning

confidence: 99%

“…The ascus wall is the cell wall of vegetative cells that fuse to form a diploid and is thus mainly composed of ␣-and ␤-glucans (17,21). Recently, it has been shown that the ␣-1,3-glucanase Agn2 functions late in sporulation and that it is necessary for the hydrolysis of the ␣-1,3-glucan of the ascus wall for release of the ascospores (6,7). Agn2 lacks a signal sequence for secretion, and the protein localizes to the epiplasm, the material surrounding the ascospores inside the ascus wall (6).…”

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confidence: 99%

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β-Glucanase Eng2 Is Required for Ascus Wall Endolysis after Sporulation in the Fission Yeast Schizosaccharomyces pombe

et al. 2009

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Meiosis is the developmental program by which sexually reproducing diploid organisms generate haploid gametes. In yeast, meiosis is followed by spore morphogenesis. When Schizosaccharomyces pombe diploid cells undergo meiosis, they differentiate into asci containing four haploid ascospores that are highly resistant to environmental stress. The formation of the ascospore wall requires the activity of several enzymes involved in the biosynthesis and modification of its components, such as ␣-and ␤-glucan synthases. Once the spores are completely mature, the wall of the ascus undergoes an endolytic process that results in the release of ascospores from the ascus, allowing their dispersal into the environment. This process requires the activity of the endo-␣-1,3-glucanase Agn2. Here, we focus on the characterization of the endo-␤-1,3-glucanase Eng2, which is also required for ascospore release from the ascus. Although Eng2 is present during the mitotic cycle, the protein accumulates after meiosis II. The expression of eng2 ؉ is required for the efficient release of ascospores, as shown by placing eng2 ؉ under the control of a repressible promoter. Furthermore, a point mutation that destroys the catalytic activity of the protein results in a phenotype similar to that of the mutant strain. Finally, we demonstrate that exogenous addition of purified Eng2 releases the ascospores from asci generated by an eng2⌬ mutant. We propose that Eng2 would act together with Agn2 to completely hydrolyze the ascus wall, thereby assisting in the release of ascospores in S. pombe.Cells of the fission yeast Schizosaccharomyces pombe have a rod-like shape and grow at the poles. S. pombe cells are stable in the haploid state and proliferate asexually until there is a shortage of nutrients. When cells are starved, especially of nitrogen, a sexual development program is triggered, and hence, cells from the opposite mating types conjugate to form zygotes. These immediately undergo meiosis, giving rise to four haploid zygotic ascospores (34).Spore formation is a complex differentiation program in which two sequential processes, meiosis and ascospore formation, occur in a coordinate fashion. During meiosis, the recently formed diploid nucleus undergoes a round of DNA replication, followed by two successive nuclear divisions generating four haploid nuclei (34). The morphogenetic program that leads to the formation of ascospores starts during meiosis II, when the four spindle-pole bodies (SPBs) differentiate into a sporulation-specific shape and change into a multilayered structure (15). These modified SPBs serve as the nucleation points for the fusion of membrane vesicles, resulting in the formation of a double-membrane structure, known as the forespore membrane, which engulfs each nuclear lobe and isolates the four haploid nuclei (15,33,34). Following this, the cell wall of the ascospore is synthesized de novo within the lumen of the forespore membrane through the deposition of successive layers of cell wall material mediated by the action of s...

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“…As Schizosaccharomyces pombe cells do not contain any obvious homologues of known exoglucanases or produce any detectable exoglucanase activity (Molero et al, 1999), candidates for conjugation-specific myosin V cargoes include the endoglucanases Eng1 (an endo--1,3-glucanase), Agn1 and Agn2 (endo--1,3-glucanases), which are required for the hydrolysis of cell wall sugars within the primary septum during cytokinesis (Dekker et al, 2004;Martin-Cuadrado et al, 2003). Although a role for Agn2 has been uncovered during the later stages of meiosis (Dekker et al, 2007), the fact that combinations of agn1, eng1 and agn2 mutants are not sterile suggests that they are not required for cell fusion to occur. It has been shown that the fission yeast exocyst complex is involved in targeting enzymes, including endoglucanases required for septum cleavage (Martin-Cuadrado et al, 2005;Wang et al, 2002).…”

Section: Myosin V Function During Conjugationmentioning

confidence: 99%

Fission yeast Myo51 is a meiotic spindle pole body component with discrete roles during cell fusion and spore formation

Doyle

Martin-Garcia

Coulton

et al. 2009

Journal of Cell Science

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Class V myosins are dimeric actin-associated motor proteins that deliver cellular cargoes to discrete cellular locations. Fission yeast possess two class V myosins, Myo51 and Myo52. Although Myo52 has been shown to have roles in vacuole distribution, cytokinesis and cell growth, Myo51 has no as yet discernible function in the vegetative life cycle. Here, we uncover distinct functions for this motor protein during mating and meiosis. Not only does Myo51 transiently localise to a foci at the site of cell fusion upon conjugation, but overexpression of the Myo51 globular tail also leads to disruption of cell fusion. Upon completion of meiotic prophase Myo51 localises to the outside of the spindle pole bodies (SPBs), where it remains until completion of meiosis II. Association of Myo51 with SPBs is not dependent upon actin or the septation initiation network (SIN); however, it is dependent on a stable microtubule cytoskeleton and the presence of the Cdc2-CyclinB complex. We observe a rapid and dynamic exchange of Myo51 at the SPB during meiosis I but not meiosis II. Finally, we show that Myo51 has an important role in regulating spore formation upon completion of meiosis.

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Role of the α‐glucanase Agn2p in ascus‐wall endolysis following sporulation in fission yeast

Cited by 28 publications

References 34 publications

The role ofSchizosaccharomyces pombe dma1in spore formation during meiosis

The role ofSchizosaccharomyces pombe dma1in spore formation during meiosis

β-Glucanase Eng2 Is Required for Ascus Wall Endolysis after Sporulation in the Fission Yeast Schizosaccharomyces pombe

Fission yeast Myo51 is a meiotic spindle pole body component with discrete roles during cell fusion and spore formation

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