A Positive Feedback between Growth and Polarity Provides Directional Persistency and Flexibility to the Process of Tip Growth

Haupt, Armin; Ershov, Dmitry; Minc, Nicolas

doi:10.1016/j.cub.2018.09.022

Cited by 36 publications

(55 citation statements)

References 48 publications

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“…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%

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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%

“…The general design, fabrication and assembly of microchannels to confine fission yeast cells is described in (24). Homothallic rga4 spores were inserted into the PDMS microchannels, let to germinate for >20h at 25°C in YE5S + Gs-IB4 -Alexafluor647.…”

Section: Microfabricated Chambersmentioning

confidence: 99%

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

Davì

Guo

Tanimoto

et al. 2018

Preprint

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“…The finding that recovery of active Cdc42 at the cell tips after Sty1 inactivation is very rapid (Mutavchiev et al 2016) also suggests that the MAP kinase may negatively regulate the coupling of the Cdc42 module to cell-polarity landmarks like Tea1-Tea4 or to the formin For3. In this context, reducing the growth rate of fission yeast cells using chemical, genetic, and mechanical means has been shown to induce active Cdc42 domains to rapidly oscillate from cell tips around the cell surface, whereas an abrupt increase in growth rate improves polar domain stabilization (Haupt et al 2018). A candidate screen for suppressors of the detachment of active Cdc42 domains from cell tips in response to osmotic stress revealed that vesicular transport along actin cables mediated by For3 and the myosin type V Myo52 are important players in mediating this process (Haupt et al 2018).…”

Section: Crosstalk Between Cdc42 and The Sapk Pathway During Fission mentioning

confidence: 99%

“…In this context, reducing the growth rate of fission yeast cells using chemical, genetic, and mechanical means has been shown to induce active Cdc42 domains to rapidly oscillate from cell tips around the cell surface, whereas an abrupt increase in growth rate improves polar domain stabilization (Haupt et al 2018). A candidate screen for suppressors of the detachment of active Cdc42 domains from cell tips in response to osmotic stress revealed that vesicular transport along actin cables mediated by For3 and the myosin type V Myo52 are important players in mediating this process (Haupt et al 2018). Remarkably, Sty1-less cells exhibited a lower suppression of this phenotype, which might suggest a functional interaction between Sty1 and For3.…”

Section: Crosstalk Between Cdc42 and The Sapk Pathway During Fission mentioning

confidence: 99%

Functional interaction between Cdc42 and the stress MAPK signaling pathway during the regulation of fission yeast polarized growth

et al. 2019

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Cell polarization can be defined as the generation and maintenance of directional cellular organization. The spatial distribution and protein or lipid composition of the cell are not symmetric but organized in specialized domains which allow cells to grow and acquire a certain shape that is closely linked to their physiological function. The establishment and maintenance of polarized growth requires the coordination of diverse processes including cytoskeletal dynamics, membrane trafficking, and signaling cascade regulation. Some of the major players involved in the selection and maintenance of sites for polarized growth are Rho GTPases, which recognize the polarization site and transmit the signal to regulatory proteins of the cytoskeleton. Additionally, cytoskeletal organization, polarized secretion, and endocytosis are controlled by signaling pathways including those mediated by mitogen-activated protein kinases (MAPKs). Rho GTPases and the MAPK signaling pathways are strongly conserved from yeast to mammals, suggesting that the basic mechanisms of polarized growth have been maintained throughout evolution. For this reason, the study of how polarized growth is established and regulated in simple organisms such as the fission yeast Schizosaccharomyces pombe has contributed to broaden our knowledge about these processes in multicellular organisms. We review here the function of the Cdc42 GTPase and the stress activated MAPK (SAPK) signaling pathways during fission yeast polarized growth, and discuss the relevance of the crosstalk between both pathways.

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“…415 However, the mechanical feedback described herein for mating projection growth in 416 budding yeast may also be present in closely related species, especially fungi like fission 417 yeast [62,63]. Indeed, fission yeast exhibits polarized growth and it has been recently 418 shown that stable polarization caps are destabilized by the arrest of growth [12], Coordination of cell polarization and mating projection growth via mechanical feedback. a, Unpolarized, spherical budding yeast cells can spontaneously break the symmetry and establish a polarization cap that is randomly located on the cell's surface (all locations on the cell surface are equally probable) or even create multiple polarization caps.…”

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confidence: 94%

Coordinating cell polarization and morphogenesis through mechanical feedback

Banavar

Trogdon

Drawert

et al. 2020

Preprint

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Many cellular processes require cell polarization to be maintained as the cell changes shape, grows or moves. Without feedback mechanisms relaying information about cell shape to the polarity molecular machinery, the coordination between cell polarization and morphogenesis, movement or growth would not be possible. Here we theoretically and computationally study the role of a genetically-encoded mechanical feedback (in the Cell Wall Integrity Pathway) as a potential coordination mechanism between cell morphogenesis and polarity during budding yeast mating projection growth. We developed a coarse-grained continuum description of the coupled dynamics of cell polarization and morphogenesis as well as 3D stochastic simulations of the molecular polarization machinery in the evolving cell shape. Both theoretical approaches show that in the absence of mechanical feedback (or in the presence of weak feedback), cell polarity cannot be maintained at the projection tip during growth, with the polarization cap wandering off the projection tip, arresting morphogenesis. In contrast, for mechanical feedback strengths above a threshold, cells can robustly maintain cell polarization at the tip and simultaneously sustain mating projection growth. These results indicate that the mechanical feedback encoded in the Cell Wall Integrity pathway can provide important positional information to the molecular machinery in the cell, thereby enabling the coordination of cell polarization and morphogenesis.

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A Positive Feedback between Growth and Polarity Provides Directional Persistency and Flexibility to the Process of Tip Growth

Cited by 36 publications

References 48 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

Functional interaction between Cdc42 and the stress MAPK signaling pathway during the regulation of fission yeast polarized growth

Coordinating cell polarization and morphogenesis through mechanical feedback

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