Coordinating cell polarization and morphogenesis through mechanical feedback

Abstract

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.

Three-dimensional stochastic simulation of chemoattractant-mediated excitability in cells

“…Moreover, our solution domain is fixed and of regular geometry; we leave these research avenues for the future study. We note that the URDME approach was recently combined with a moving boundary framework to describe yeast polarization [ 105 ].…”

Unravelling cell migration: defining movement from the cell surface

“…They included the chemo-mechanics of the stress fibers and focal adhesions, as well as the contractile forces pulling the nucleus of tumor cells against the elastic resistance of the endothelial cells. Banavar and colleagues [ 337 ] focused their attention on the role of genetically encoded mechanical feedback as a coordinator of cell morphogenesis and polarity. Also, Bennett and colleagues [ 338 ] developed a continuum model to explain the DNA damage occurring during constricted migration.…”

Expression Levels of Genes Encoding Proteins Involved in the Cell Wall–Plasma Membrane–Cytoskeleton Continuum Are Associated With the Maturation-Related Adventitious Rooting Competence of Pine Stem Cuttings

“…Although the initial response to IBA was similar for specific genes between rooting-competent and non-competent cuttings, the distance of the responses between rooting-competent and non-competent cuttings, and in their responses to auxin exposure, indicated that these genes may be involved in the maturation-related decline of adventitious root formation. Overall, these results suggested that most RLKs and specific mechanosensitive channels should be downregulated during adventitious root formation for root induction, perhaps to avoid specific functional redundancies and compensation involved in the maintenance of tissue and organ integrity (Banavar et al, 2021). An L-type LecRLK, LecRK-I.9, mediates cell wall-plasma membrane contacts through protein-protein interactions using arginine-glycine-aspartic acid (RGD)containing proteins as the potential ligands (Bouwmeester et al, 2011).…”