Nuclear envelope: a new frontier in plant mechanosensing?

Biophysical Reviews, Aug 2017

In animals, it is now well established that forces applied at the cell surface are propagated through the cytoskeleton to the nucleus, leading to deformations of the nuclear structure and, potentially, to modification of gene expression. Consistently, altered nuclear mechanics has been related to many genetic disorders, such as muscular dystrophy, cardiomyopathy and progeria. In plants, the integration of mechanical signals in cell and developmental biology has also made great progress. Yet, while the link between cell wall stresses and cytoskeleton is consolidated, such cortical mechanical cues have not been integrated with the nucleoskeleton. Here, we propose to take inspiration from studies on animal nuclei to identify relevant methods amenable to probing nucleus mechanics and deformation in plant cells, with a focus on microrheology. To identify potential molecular targets, we also compare the players at the nuclear envelope, namely lamina and LINC complex, in both plant and animal nuclei. Understanding how mechanical signals are transduced to the nucleus across kingdoms will likely have essential implications in development (e.g. how mechanical cues add robustness to gene expression patterns), in the nucleoskeleton–cytoskeleton nexus (e.g. how stress is propagated in turgid/walled cells), as well as in transcriptional control, chromatin biology and epigenetics.

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Nuclear envelope: a new frontier in plant mechanosensing?

Nuclear envelope: a new frontier in plant mechanosensing? Kateryna Fal 0 1 2 Atef Asnacios 0 1 2 Marie-Edith Chabouté 0 1 2 Olivier Hamant 0 1 2 0 Institut de Biologie Moléculaire des Plantes, CNRS, Université de Strasbourg , 67000 Strasbourg , France 1 Laboratoire Matières et Systèmes Complexes, Université Paris-Diderot and CNRS, UMR 7057, Sorbonne Paris Cité , Paris , France 2 Laboratoire Reproduction et Développement des Plantes, Université de Lyon, ENS de Lyon , UCB Lyon 1, CNRS, INRA, 69342 Lyon , France In animals, it is now well established that forces applied at the cell surface are propagated through the cytoskeleton to the nucleus, leading to deformations of the nuclear structure and, potentially, to modification of gene expression. Consistently, altered nuclear mechanics has been related to many genetic disorders, such as muscular dystrophy, cardiomyopathy and progeria. In plants, the integration of mechanical signals in cell and developmental biology has also made great progress. Yet, while the link between cell wall stresses and cytoskeleton is consolidated, such cortical mechanical cues have not been integrated with the nucleoskeleton. Here, we propose to take inspiration from studies on animal nuclei to identify relevant methods amenable to probing nucleus mechanics and deformation in plant cells, with a focus on microrheology. To identify potential molecular targets, we also compare the players at the nuclear envelope, namely lamina and LINC complex, in both plant and animal nuclei. Understanding how mechanical signals are transduced to the nucleus across kingdoms will likely have essential implications in development (e.g. how mechanical cues add robustness to gene expression patterns), in the nucleoskeletoncytoskeleton nexus (e.g. how stress is propagated in turgid/ walled cells), as well as in transcriptional control, chromatin biology and epigenetics. Nuclear envelope; Lamina; LINC complex; Cytoskeleton; Chromatin; Mechanical force; Microrheology; Plants Introduction Plants, like animals, respond to mechanical stimuli. This is probably most obvious when looking at a section of a tree branch: its anatomical asymmetry reveals the existence of so-called Breaction wood^, the product of an active mechanical reinforcement that matches the asymmetric load caused by gravity. In recent years, plant mechanosensing research is turning more and more towards cell and molecular aspects, from cytoskeleton behaviour to the regulation of gene expression following mechanical perturbations (Braam 2005; Hamant 2013; Monshausen and Haswell 2013; Coutand et al. 2009; Geitmann 2010) . Although plants exhibit specific cell features, like a stiff cell wall (in the MPa range) and high hydrostatic pressure (turgor pressure, also in the MPa range), both kingdoms display a number of comparable responses to mechanical cues. Animal cells respond to their mechanical environment, notably through interactions with their extracellular matrix (see e.g. Vogel and Sheetz 2006, 2009; Discher et al. 2005, 2009) . Plant and animal extracellular matrices are structurally and chemically very different. From the signalling point of view, the quasi absence of true integrins in plant genomes (for an exception, see Knepper et al. 2011) needs to be put in context against the high number of receptor-like kinase in plants. Several of these proteins can interact with wall components (e.g. the WAK receptor with the backbone of pectins; Anderson et al. 2001; Wolf et al. 2012) , a bit like integrin with fibronectin, arguably. Interestingly, one such receptor-like kinase, FERONIA, contributes to mechanoperception in Arabidopsis roots (Shih et al. 2014) . At the plasma membrane, a role of tension in cell polarity has been shown in both kingdoms, notably through the inhibitory role of membrane tension on endocytosis, that can trap transporters (e.g. Heisler et al. 2010; Nakayama et al. 2012) or receptors (e.g. Pouille et al. 2009) in polar domains (for a comparative review between plants and animals, see Asnacios and Hamant 2012) . Similarly, in both kingdoms, membrane tension should lead to membrane thinning, which, in turn, changes the conformation of mechanosensitive channels, leading to their opening (Haswell et al. 2011) . Inside the cell, the cortical cytoskeleton is a focus of mechanotransduction research in both plants and animals. However, one must highlight here that most animal cells exhibit an actomyosin-rich cortex, consistent with their contractility, whereas plant cells have a microtubule-rich cortex: cortical microtubules (CMTs) guide the cellulose synthase complex at the plasma membrane, thus channelling the production of cellulose microfibrils in the wall (Green 1962; Paredez et al. 2006) . Both actomyosin and microtubules respond to mechanical cues. In animal cells for instance, myosin is preferentially recruited on tensed membrane, providing a positive feedback loop for cell contraction, (...truncated)


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Kateryna Fal, Atef Asnacios, Marie-Edith Chabouté, Olivier Hamant. Nuclear envelope: a new frontier in plant mechanosensing?, Biophysical Reviews, 2017, pp. 1-15, DOI: 10.1007/s12551-017-0302-6