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The Novel Fission Yeast (1,3)Β-D-Glucan Synthase Catalytic

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The Novel Fission Yeast (1,3)Β-D-Glucan Synthase Catalytic Research Article 157 The novel fission yeast (1,3)β-D-glucan synthase catalytic subunit Bgs4p is essential during both cytokinesis and polarized growth Juan Carlos G. Cortés1, Elena Carnero1, Junpei Ishiguro2, Yolanda Sánchez1, Angel Durán1 and Juan Carlos Ribas1,* 1Instituto de Microbiología Bioquímica and Departamento de Microbiología y Genética, Consejo Superior de Investigaciones Científicas (CSIC) / Universidad de Salamanca, 37007 Salamanca, Spain 2Department of Biology, Faculty of Science and Engineering, Konan University, Okamoto 8-9-1, Kobe 658-8501, Japan *Author for correspondence (e-mail: [email protected]) Accepted 7 October 2004 Journal of Cell Science 118, 157-174 Published by The Company of Biologists 2005 doi:10.1242/jcs.01585 Summary Schizosaccharomyces pombe contains four putative (1,3)β- germination. Bgs4p timing and requirements for proper D-glucan synthase (GS) catalytic subunits, Bgs1p-4p. In positioning during cytokinesis and its localization pattern this work, we cloned bgs4+ and show that Bgs4p is the only during spore maturation differ from those of Bgs1p. Bgs4p subunit found to be a part of the GS enzyme and essential localizes overlapping the contractile ring once Bgs1p is for maintaining cell integrity during cytokinesis and present and a Calcofluor white-stained septum material is polarized growth. Here we show that bgs4+, cwg1+ (cwg1-1 detected, suggesting that Bgs4p is involved in a late process shows reduced cell-wall β-glucan and GS catalytic activity) of secondary or general septum synthesis. Unlike Bgs1p, and orb11+ (orb11-59 is defective in cell morphogenesis) are Bgs4p needs the medial ring but not the septation initiation the same gene. bgs4+ is essential for spore germination and network proteins to localize with the other septation bgs4+ shut-off produces cell lysis at growing poles and components. Furthermore, Bgs4p localization depends on mainly at the septum prior to cytokinesis, suggesting that the polarity establishment proteins. Finally, F-actin is Bgs4p is essential for cell wall growth and to compensate necessary for Bgs4p delocalization from and relocalization for an excess of cell wall degradation during cytokinesis. to the growing regions, but it is not needed for the stable Shut-off and overexpression analysis suggest that Bgs4p maintenance of Bgs4p at the growing sites, poles and forms part of a GS catalytic multiprotein complex and that septum. All these data show for the first time an essential Journal of Cell Science Bgs4p-promoted cell-wall β-glucan alterations induce role for a Bgs subunit in the synthesis of a (1,3)β-D-glucan compensatory mechanisms from other Bgs subunits necessary to preserve cell integrity when cell wall synthesis and (1,3)α-D-glucan synthase. Physiological localization or repair are needed. studies showed that Bgs4p localizes to the growing ends, the medial ring and septum, and at each stage of wall synthesis or remodeling that occurs during sexual differentiation: Key words: Cell integrity, Cell wall, Cytokinesis, Fission yeast, mating, zygote and spore formation, and spore Glucan, (1,3)-β-D-Glucan Synthase Introduction (Schmidt et al., 2002), and flanked at both sides by the The fission yeast Schizosaccharomyces pombe provides an secondary septum. Once the septum has formed, cell division ideal model to study cell morphogenesis (Brunner and Nurse, proceeds by dissolution of the primary septum (Martin- 2000). The cells are cylindrical and grow from their ends in a Cuadrado et al., 2003). polarized fashion (Chang and Peter, 2003; Hayles and Nurse, The S. pombe cell wall is a well-organized structure 2001). Genetic studies have identified many genes important consisting of an outer layer enriched in glycoproteins and an for the different steps of cytokinesis, a process similar to that inner layer of carbohydrates, including (1,3)β-D-, (1,6)β-D- in animal cells, such as the positioning and assembly of the and (1,3)α-D-glucans (for a review, see Duran and Perez, actomyosin ring, the recruitment of actin patches to the medial 2004; Perez and Ribas, 2004). (1,3)β-D-glucan is the major ring and the activation of ring contraction by a network of contributor to the cell wall framework. In situ localization regulatory proteins referred to as the septation initiation studies (Humbel et al., 2001) have indicated that (1,6)β-D- network (SIN) (Balasubramanian et al., 2004; Guertin et al., branched (1,3)β-D-glucan is localized, forming filamentous 2002; Krapp et al., 2004). Centripetal ring contraction and structures all over the cell wall non-dense layer and throughout septum synthesis are perfectly coordinated, resulting in a three- the septum; (1,6)β-D-glucan appears in the same cell wall non- layered septum structure between the membranes of both dense layer and in the secondary septum, whereas linear daughter cells that is composed of a middle disk structure (1,3)β-D-glucan is only present at the primary septum. called the primary septum, analogous to that of budding yeast The enzyme complex involved in (1,3)β-D-glucan synthesis 158 Journal of Cell Science 118 (1) in yeast is (1,3)β-D-glucan synthase (GS). It is formed by at positioning during septum formation as well as the localization least two components: a regulatory and a catalytic subunit pattern during spore maturation differ from those of Bgs1p. All (Kang and Cabib, 1986; Ribas et al., 1991). The regulatory the above data suggest that Bgs4p plays a role in each cell wall subunit is the GTPase Rho1p, which not only activates the GS synthesis process of the S. pombe life cycle by synthesizing a (Arellano et al., 1996; Drgonova et al., 1996) but is also (1,3)β-D-glucan that is essential for preserving cell integrity involved in other morphogenetic processes, such as and reinforce its importance as an essential target for the design organization of the actin cytoskeleton and genesis of the of specific antifungal drugs. In addition, the lytic phenotype growing regions (Arellano et al., 1999a; Cabib et al., 2001; observed during bgs4+ shut-off may be biotechnologically Drgonova et al., 1999). useful as an efficient and controlled cell-free system for S. pombe contains four putative GS catalytic subunits named heterologous protein expression and purification (Priority Bgs1p-4p. bgs1+, bgs2+ and bgs3+ have been reported to be patent application ES200401042; April 30, 2004). essential genes, at least for ascospore revival (Cortes et al., 2002; Liu et al., 2000; Liu et al., 1999; Martin et al., 2003; Materials and Methods Martin et al., 2000), but nothing is known about bgs4+. The + Strains and culture conditions first gene to be identified was bgs1 and this was initially ∆ named cps1+. It was cloned by complementation of several The S. pombe strains used in this work are listed in Table 1. bgs4 strain 561 containing an integrated GFP-bgs4+ copy was made by mutants unable to assemble the division septum, and it was transforming strain 498 (bgs4∆ pJG33, his3+ selection) with StuI- suggested to be involved in cytokinesis, polarity and in a digested pJG53 (leu1+ selection, see below), which directs its septation checkpoint that coordinates cytokinesis and the cell integration at the StuI site adjacent to bgs4∆::ura4+, at position –1320 cycle (Ishiguro et al., 1997; Le Goff et al., 1999; Liu et al., of the bgs4+ promoter sequence. The GFP-bgs4+ and bgs4::ura4+ 1999). Recently, Bgs1p has been localized to the contractile sequences are separated by a pJK148 backbone. In order to eliminate ring and septum in a manner dependent on the actomyosin ring pJG33, to analyze GFP-Bgs4p functionality and to confirm that and SIN (Cortes et al., 2002; Liu et al., 2002), as well as to the integration was in the bgs4+ promoter sequence, this strain was – – – growing poles and to other regions of cell wall synthesis during crossed with strain 285 (Leu , Ura , His ) and tetrad analysis was + the sexual phase of the life cycle (Cortes et al., 2002). However, performed. Leu and Ura phenotypes always co-segregated 2 :2–. neither GS activity nor cell wall (1,3)β-D-glucan synthesis has pJG33 was lost in most of the clones as result of the sporulation process. The GFP-bgs4+ bgs4∆ strain obtained displayed a wild-type been shown to depend on Bgs1p function. Therefore, the β phenotype under all conditions tested and expressed GFP-Bgs4p at involvement of Bgs1p in (1,3) -D-glucan synthesis remains to physiological levels from a single integrated GFP-bgs4+ gene under + be clarified. bgs2 is not expressed in vegetative cells but is the control of its own promoter. essential for proper spore wall maturation (Liu et al., 2000; Standard complete yeast growth (YES), selective (EMM) Martin et al., 2000). bgs3+ is also essential for vegetative cells supplemented with the appropriate amino acids (Alfa et al., 1993) and and Bgs3p has also been shown to be localized to sites of cell sporulation media (SPA) (Egel, 1984) have been described elsewhere. + wall growth. Similarly, bgs3 shut-off does not produce any EMM-N is EMM (0.5% NH4Cl) from which NH4Cl has been omitted. β Stable sterile diploids for complementation analyses were obtained apparent decrease in GS activity or cell wall (1,3) -D-glucan, – although the overall cell wall structure is altered (Martin et al., by mating mat2P-B102 and h strains (Egel, 1984). The general Journal of Cell Science 2003). Saccharomyces cerevisiae contain two putative GS procedures for yeast culture and genetic manipulations were carried out as described (Moreno et al., 1991). Latrunculin A (Lat A) was catalytic subunits, Fks1p and Fks2p, whose sequences share a from Sigma and was used at 100 µM final concentration (from a stock high homology with Bgs proteins. FKS1 and FKS2 are solution of 10 mM in DMSO).
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