Symmetry Breaking in Spore Germination Relies on an Interplay between Polar Cap Stability and Spore Wall Mechanics

Bonazzi, Daria; Julien, Jean-Daniel; Romao, Maryse; Seddiki, Rima; Piel, Matthieu; Boudaoud, Arezki; Minc, Nicolas

doi:10.1016/j.devcel.2018.07.018

Cited by 24 publications

(54 citation statements)

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“…As for other walled cells, their shape is defined by their CW encasing the plasma membrane (5). Building on previous methodologies to map CW thickness and compute its surface stiffness (10,11,15,16), we sought to develop a systematic approach to map those key mechanical parameters in large populations of cycling cells and mutants with medium-throughput ( Fig. 1A).…”

Section: A Medium-throughput Methods To Map Subcellular Mechanical Promentioning

confidence: 99%

“…1B). After imaging a cell to compute wall thickness, we immediately deflated it by piercing the wall with a UV laser focused at a small diffraction-limited point on the surface (11,15,24). Cells deflated with a marked and homogenous reduction in the lateral radius, as well as changes in curvature at cell tips.…”

Section: A Medium-throughput Methods To Map Subcellular Mechanical Promentioning

confidence: 99%

“…Measuring the mechanical properties of the cell wall is a long-term endeavor in plant and microbial sciences. Methods to measure wall stiffness include Atomic Force Microscopy (AFM) (13), active cell bending or compression (7,8,14), and strain-stress assays through the modulation of turgor pressure (10,11,(15)(16)(17)(18). Those allow to extract a surface elasticity but are in general low-throughput, and importantly do not take into account putative global or local variations in wall thickness, thereby preventing to discern contributions from bulk material properties vs thickness to cell wall elasticity.…”

Section: Introductionmentioning

confidence: 99%

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Systematic Mapping of cell Wall Mechanics in the Regulation of Cell Morphogenesis

Davì

Guo

Tanimoto

et al. 2018

Preprint

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Walled cells of plants, fungi and bacteria, come with a large range of shapes and sizes, which are ultimately dictated by the mechanics of their cell wall. This stiff and thin polymeric layer encases the plasma membrane and protects the cells mechanically by opposing large turgor pressure derived stresses. To date, however, we still lack a quantitative understanding for how local and/or global mechanical properties of the wall support cell morphogenesis. Here, we combine super-resolution imaging, and laser-mediated wall relaxation, to quantitate subcellular values of wall thickness (h) and bulk elastic moduli (Y) in large populations of live mutant cells and conditions affecting cell diameter in the rod-shaped model fission yeast.We find that lateral wall stiffness, defined by the surface modulus, σ=hY, robustly scales with cell diameters. This scaling is valid in tens of mutants covering various functions, within the population of individual isogenic strains, along single misshaped cells, and even across the fission yeasts clade. Dynamic modulations of cell diameter by chemical and/or mechanical means suggest that the cell wall can rapidly adapt its surface mechanics, rendering stretched wall portions stiffer than unstretched ones. Size-dependent wall stiffening constrains diameter definition and limits size variations, and may also provide and efficient mean to keep elastic strains in the wall below failure strains potentially promoting cell survival. This quantitative set of data impacts our current understanding of the mechanics of cell walls, and its contribution to morphogenesis.

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Section: A Medium-throughput Methods To Map Subcellular Mechanical Promentioning

confidence: 99%

Section: A Medium-throughput Methods To Map Subcellular Mechanical Promentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Systematic Mapping of cell Wall Mechanics in the Regulation of Cell Morphogenesis

Davì

Guo

Tanimoto

et al. 2018

Preprint

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“…However, the formation of a Cdc42 activity zone is also thought to rely on positive feedback mechanisms that locally amplify Cdc42 activation. Positive feedbacks are thought to be important for spontaneous symmetry breaking, when cells establish polarity in the absence of internal or external landmarks, for instance during spore germination or upon exposure to homogeneous pheromone signals (Bendezu and Martin, 2013;Bonazzi et al, 2014;Goryachev and Leda, 2017;Johnson et al, 2011;Martin, 2015;Wedlich-Soldner and Li, 2003). Furthermore, the dynamic oscillatory patterns of Cdc42 activity, during vegetative growth (Das et al, 2012;Howell et al, 2012) and sexual reproduction (Bendezu and Martin, 2013;Khalili et al, 2018), are indicative of negative in addition to positive feedback regulations.…”

Section: Introductionmentioning

confidence: 99%

Optogenetics reveals Cdc42 local activation by scaffold-mediated positive feedback and Ras GTPase

Lamas

Merlini

Vještica

et al. 2019

Preprint

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The small GTPase Cdc42 is critical for cell polarization. Scaffold-mediated positive feedback regulation was proposed to mediate symmetry-breaking to a single active zone in budding yeast cells. In rod-shaped fission yeast S. pombe cells, active Cdc42-GTP localizes to both cell poles, where it promotes bipolar growth. Here, we implement the CRY2-CIBN optogenetic system for acute light-dependent protein recruitment to the plasma membrane, which allowed to directly demonstrate positive feedback. Indeed, optogenetic recruitment of constitutively active Cdc42 leads to co-recruitment of the GEF Scd1, in a manner dependent on the scaffold protein Scd2. We show that Scd2 function is completely bypassed and positive feedback restored by an engineered interaction between the GEF and a Cdc42 effector, the Pak1 kinase. Remarkably, such re-wired cells are viable and grow in a bipolar manner even when lacking otherwise essential Cdc42 activators.Interestingly, these cells reveal that Ras1 GTPase plays a dual role in localizing and activating the GEF, thus potentiating the feedback. We conclude that scaffoldmediated positive feedback, gated by Ras activity, is minimally required for rodshape formation.

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“…There, it oscillates in an anti-correlated manner (Das et al, 2012) to drive the bipolar growth patterns of these cells and defines cellular dimensions during mitotic growth Kelly and Nurse, 2011). Upon spore germination, Cdc42-GTP polarizes spontaneously, forming dynamic zones that stabilize upon spore outgrowth (Bonazzi et al, 2014). During sexual differentiation, Cdc42-GTP also forms unstable zones that explore the cell periphery upon pheromone exposure and become stabilized upon increased pheromone concentrations (Bendezu and Martin, 2013).…”

Section: Introductionmentioning

confidence: 99%

Differential GAP requirement for Cdc42-GTP polarization during proliferation and sexual reproduction

Castro

Martin

2018

Preprint

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The formation of a local zone of Cdc42 GTPase activity, which governs cell polarization in many cell types, requires not only local activation but also switch-off mechanisms. Here we identify Rga3, a paralog of Rga4, as a novel Cdc42 GTPase activating protein (GAP) in the fission yeast S. pombe. Contrary to Rga4, Rga3 localizes with Cdc42-GTP to sites of polarity. Rga3 is dispensable for cell polarization during mitotic growth, but limits the lifetime of unstable Cdc42-GTP patches that underlie cell pairing during sexual reproduction, masking a partly compensatory patch wandering motion. In consequence, cells lacking rga3 hyperpolarize and loose out in mating competition. Rga3 synergizes with the Cdc42 GAPs Rga4 and Rga6 to restrict Cdc42-GTP zone sizes during mitotic growth. Surprisingly, triple mutant cells, which are almost fully round, retain pheromone-dependent dynamic polarization of Cdc42-GTP, extend a polarized projection and mate. Thus, the requirement for Cdc42-GTP hydrolysis by GTPase activating proteins is distinct during polarization by intrinsic or extrinsic cues.

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Symmetry Breaking in Spore Germination Relies on an Interplay between Polar Cap Stability and Spore Wall Mechanics

Cited by 24 publications

References 0 publications

Systematic Mapping of cell Wall Mechanics in the Regulation of Cell Morphogenesis

Systematic Mapping of cell Wall Mechanics in the Regulation of Cell Morphogenesis

Optogenetics reveals Cdc42 local activation by scaffold-mediated positive feedback and Ras GTPase

Differential GAP requirement for Cdc42-GTP polarization during proliferation and sexual reproduction

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