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Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in Plants.

ABSTRACT: Mechanical signals have recently emerged as a major cue in plant morphogenesis, notably influencing cytoskeleton organization, gene expression, protein polarity, or cell division. Although many putative mechanosensing proteins have been identified, it is unclear what mechanical cue they might sense and how this would occur. Here we briefly explain the notions of mechanical stress and strain. We present the challenges to understand their sensing by plants, focusing on the cell wall and the plasma membrane, and we review putative mechanosensing structures. We propose minimal biophysical models of mechanosensing, revealing the modes of mechanosensing according to mechanosensor lifetime, threshold force for mechanosensor dissociation, and type of association between the mechanosensor and the cell wall, as the sensor may be associated to a major load-bearing structure such as cellulose or to a minor load-bearing structure such as pectins or the plasma membrane. Permanent strain, permanent expansion, and relatively slow variations thereof are sensed in all cases; variations of stress are sensed in all cases; permanent stress is sensed only in the following specific cases: sensors associated to minor load-bearing structures slowly relaxing in a growing wall, long-lived sensors with high dissociation force and associated to major-load-bearing structures, and sensors with low dissociation force associated to major-load-baring structures behaving elastically. We also find that all sensors respond to variations in the composition or the mechanical properties of the cell wall. The level of sensing is modulated by the properties of all of mechanosensor, cell wall components, and plasma membrane. Although our models are minimal and not fully realistic, our results yield a framework to start investigating the possible functions of putative mechanosensors.

SUBMITTER: Fruleux A

PROVIDER: S-EPMC6581727 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in Plants.

Fruleux Antoine A Verger Stéphane S Boudaoud Arezki A

Frontiers in plant science 20190612

Mechanical signals have recently emerged as a major cue in plant morphogenesis, notably influencing cytoskeleton organization, gene expression, protein polarity, or cell division. Although many putative mechanosensing proteins have been identified, it is unclear what mechanical cue they might sense and how this would occur. Here we briefly explain the notions of mechanical stress and strain. We present the challenges to understand their sensing by plants, focusing on the cell wall and the plasma ...[more]

PMID: 31244875

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Project description:In cell proliferation, stem cell differentiation, chemoresistance, and tissue organization, the ubiquitous role of YAP/TAZ continues to impact our fundamental understanding in numerous physiological and disease systems. YAP/TAZ is an important signaling nexus integrating diverse mechanical and biochemical signals, such as ECM stiffness, adhesion ligand density, or cell-cell contacts, and thus strongly influences cell fate. Recent studies show that YAP/TAZ mechanical sensing is dependent on RhoA-regulated stress fibers. However, current understanding of YAP/TAZ remains limited due to the unknown interaction between the canonical Hippo pathway and cell tension. Furthermore, the multiscale relationship connecting adhesion signaling to YAP/TAZ activity through cytoskeleton dynamics remains poorly understood. To identify the roles of key signaling molecules in mechanical signal sensing and transduction, we present a, to our knowledge, novel computational model of the YAP/TAZ signaling pathway. This model converts extracellular-matrix mechanical properties to biochemical signals via adhesion, and integrates intracellular signaling cascades associated with cytoskeleton dynamics. We perform perturbations of molecular levels and sensitivity analyses to predict how various signaling molecules affect YAP/TAZ activity. Adhesion molecules, such as FAK, are predicted to rescue YAP/TAZ activity in soft environments via the RhoA pathway. We also found that changes of molecule concentrations result in different patterns of YAP/TAZ stiffness response. We also investigate the sensitivity of YAP/TAZ activity to ECM stiffness, and compare with that of SRF/MAL, which is another important regulator of differentiation. In addition, the model shows that the unresolved synergistic effect of YAP/TAZ activity between the mechanosensing and the Hippo pathways can be explained by the interaction of LIM-kinase and LATS. Overall, our model provides a, to our knowledge, novel platform for studying YAP/TAZ activity in the context of integrating different signaling pathways. This platform can be used to gain, to our knowledge, new fundamental insights into roles of key molecular and mechanical regulators on development, tissue engineering, or tumor progression.

Dataset Information

Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in Plants.

Publications

Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in Plants.

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