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The Role of the Cell Integrity Pathway in Septum Assembly in Yeast

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The Role of the Cell Integrity Pathway in Septum Assembly in Yeast Journal of Fungi Review The Role of the Cell Integrity Pathway in Septum Assembly in Yeast Cesar Roncero *, Rubén Celador , Noelia Sánchez, Patricia García and Yolanda Sánchez * Departamento de Microbiología y Genética, Instituto de Biología Funcional y Genómica, CSIC/Universidad de Salamanca, C/Zacarías González, s/n, 37007 Salamanca, Spain; [email protected] (R.C.); [email protected] (N.S.); [email protected] (P.G.) * Correspondence: [email protected] (C.R.); [email protected] (Y.S.) Abstract: Cytokinesis divides a mother cell into two daughter cells at the end of each cell cycle and proceeds via the assembly and constriction of a contractile actomyosin ring (CAR). Ring constriction promotes division furrow ingression, after sister chromatids are segregated to opposing sides of the cleavage plane. Cytokinesis contributes to genome integrity because the cells that fail to complete cytokinesis often reduplicate their chromosomes. While in animal cells, the last steps of cytokinesis involve extracellular matrix remodelling and mid-body abscission, in yeast, CAR constriction is coupled to the synthesis of a polysaccharide septum. To preserve cell integrity during cytokinesis, fungal cells remodel their cell wall through signalling pathways that connect receptors to downstream effectors, initiating a cascade of biological signals. One of the best-studied signalling pathways is the cell wall integrity pathway (CWI) of the budding yeast Saccharomyces cerevisiae and its counterpart in the fission yeast Schizosaccharomyces pombe, the cell integrity pathway (CIP). Both are signal transduction pathways relying upon a cascade of MAP kinases. However, despite strong similarities in the assembly of the septa in both yeasts, there are significant mechanistic differences, including Citation: Roncero, C.; Celador, R.; the relationship of this process with the cell integrity signalling pathways. Sánchez, N.; García, P.; Sánchez, Y. The Role of the Cell Integrity Keywords: yeast; cytokinesis; actomyosin ring; septum; cell integrity Pathway in Septum Assembly in Yeast. J. Fungi 2021, 7, 729. https:// doi.org/10.3390/jof7090729 1. Maintaining the Shape: The Cell Integrity Signaling Pathways Academic Editors: María Molina and The cell integrity signalling pathways are usually described as fairly linear, they chan- Humberto Martín nel the signal from the cell surface to the nucleus without significant branching (Figure1) . Cell wall stress is detected by two conserved families of single-pass transmembrane cell Received: 30 July 2021 wall sensors of the WSC and MID types. Their role is well documented in S. cerevisiae, Accepted: 31 August 2021 where these sensors can detect the mechanical tension between the cell wall (CW) and Published: 6 September 2021 the plasma membrane (PM) [1,2]. They function as upstream triggers of the cell integrity pathway and activate membrane-associated RhoA type GTPases through specific GEFs, Publisher’s Note: MDPI stays neutral the ScRom2p and SpRgf1p [3,4]. In S. cerevisiae, signalling is also associated with Tus1p, with regard to jurisdictional claims in another Rho1p-GEF and a functional homologue of SpRgf3p, whose relevance in CIP published maps and institutional affil- activation is unknown. Signalling in S. cerevisiae is directly translated to the MAP kinase iations. cascade through the GTPase Rho1p and its effector the Pkc1p kinase (Figure1B). In S. pombe, the situation is a bit more complex (Figure1A), there are two different Rho A homologues (Rho1p and Rho2p) and two Pkc kinases (Pck1p and Pck2p), participating in signalling. The major signal input is channelled through Pkc2p, which receives different inputs, the Copyright: © 2021 by the authors. main one through the Rho2p GTPase and a minor one through Rho1p, which also transmits Licensee MDPI, Basel, Switzerland. a minor signal through the Pkc1p branch [5,6]. In both yeasts, the signal from the PKC This article is an open access article kinase is transmitted to a MAP kinase cascade that ends with the MAP kinases ScSlt2p distributed under the terms and and SpPmk1p. These kinases participate in phosphorylation events of specific nuclear conditions of the Creative Commons transcription factors. The S. pombe Pmk1p phosphorylates Atf1p and Mbx2p transcription Attribution (CC BY) license (https:// factors, but to date, only a few downstream targets have been characterised. In S. cerevisiae, creativecommons.org/licenses/by/ the MAP kinase Slt2p phosphorylates the Rlm1p transcription factor that mediates a strong 4.0/). J. Fungi 2021, 7, 729. https://doi.org/10.3390/jof7090729 https://www.mdpi.com/journal/jof J. Fungi 2021, 7, x FOR PEER REVIEW 2 of 17 J. Fungi 2021, 7, 729 2 of 17 Mbx2p transcription factors, but to date, only a few downstream targets have been char- acterised. In S. cerevisiae, the MAP kinase Slt2p phosphorylates the Rlm1p transcription factortranscriptional that mediates response. a strong This transcriptiona response encompassesl response. genes This involvedresponse inencompasses chitin and glucan genes involvedsynthesis in as chitin well asand genes glucan encoding synthesis cell as wall well remodelling as genes encoding activities, cell among wall remodelling others [7,8]. activities,ScSlt2p also among phosphorylates others [7,8]. the ScSlt2p heterodimeric also phosphorylates SBF transcription the heterodimeric factor that promotes SBF tran- the scriptionG1/S transition factor that [9]. promotes the G1/S transition [9]. Figure 1. TheThe cell cell integrity integrity cascade cascade in in yeast. yeast. (A (A) )The The cell cell integrity integrity pathway pathway (CIP) (CIP) in inSchizosaccharo-Schizosaccha- mycesromyces pombe pombe. (.(B)B The) The cell cell wall wall integrity integrity pathway pathway (CWI) (CWI) in in Saccharomyces cerevisiae .. Both cascadescascades signal from the mechanosensors in the PM (Mid/Wsc) to to the the transcrip transcriptiontion factor factor in in the the nucleus nucleus (N). (N). Red boxed proteins are those for which expression is transcriptionally regulatedregulated by the cascade and are involved in the cell wall and/or septum assembly. Black boxed proteins represent cytosolic tar- are involved in the cell wall and/or septum assembly. Black boxed proteins represent cytosolic targets gets of the cascade at different levels that are related to septum assembly. For additional description of the cascade at different levels that are related to septum assembly. For additional description of of the cascade, see text. the cascade, see text. In addition to their signalling through tr transcriptionalanscriptional regulation, these pathways act through cytosolic cytosolic targets. targets. The The Rho1/2p Rho1/2p GTPases GTPases are are directly directly involved involved in the in thebiological biological cy- clescycles of actin, of actin, regulating regulating patches patches and andfilament filamentss turnover turnover that affect that affectendocytosis, endocytosis, cell polar- cell isationpolarisation and therefore and therefore the assembly the assembly of the ofyeast the yeastcell wall. cell Additional wall. Additional targets targets of the signal of the transductionsignal transduction in S. pombe in S. have pombe beenhave elusive, been elusive,but are numerous but are numerous in S. cerevisiae in S.. cerevisiae The potential. The effectpotential of such effect targets of such will targets be described will be described later in the later context in the of context septum of assembly. septum assembly. 22.. S. pombe, pombe, the the Fission Fission Yeast In S. pombe, pombe, the cells cells are are cylindrical and grow by elongation at their tips. Cell division is accomplishedaccomplished by by medial medial fission fission using using a contractile a contractile actomyosin actomyosin ring (CAR), ring (CAR), which guideswhich guidesthe formation the formation of the cell of the wall cell septum. wall septum. Cell separation Cell separation also involves also involves cell wall cell degradation wall deg- radationbetween between the two halvesthe two of halves the division of the division septum septum that will that constitute will constitute the new the ends new of ends the ofdaughter the daughter cells. The cells. overall The overall process process has been has deeply been deeply studied, studied, and there and are there excellent are excellent reviews reviewson cytokinesis on cytokinesis [10–13], septation [10–13], septation [14,15] and [14,15] cell separation and cell separation [16]. In this [16]. review, In this we willreview, first wesummarise will first key summarise steps of fission key steps yeast of cytokinesis, fission yeast including cytokinesis, ring assembly,including constriction ring assembly, and constrictionseptum formation, and septum before formation, discussing before emerging discussing mechanisms emerging that mechanisms involve the cellthat integrity involve thepathway cell integrity (CIP) in pathway the regulation (CIP) in of the cytokinesis regulation and of theircytokinesis biological and implications. their biological impli- cations. 2.1. Before Septum Assembly: Actomyosin Ring Positioning and Assembly The CAR in S. pombe is composed of short actin filaments assembled by formins and myosin motors (actomyosin) that produce the force to arrange the actin filaments (revised J. Fungi 2021, 7, x FOR PEER REVIEW 3 of 17 J. Fungi 2021, 7, 729 3 of 17 2.1. Before Septum Assembly: Actomyosin Ring Positioning and Assembly The CAR in S. pombe is composed of short actin filaments assembled by formins and myosin motors
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