Mechanosensitive channels: feeling tension in a world under pressure

Abstract

Plants, like other organisms, are facing multiple mechanical constraints generated both in their tissues and by the surrounding environments. They need to sense and adapt to these forces throughout their lifetimes. To do so, different mechanisms devoted to force transduction have emerged. Here we focus on fascinating proteins: the mechanosensitive (MS) channels. Mechanosensing in plants has been described for centuries but the molecular identification of MS channels occurred only recently. This review is aimed at plant biologists and plant biomechanists who want to be introduced to MS channel identity, how they work and what they might do in planta? In this review, electrophysiological properties, regulations, and functions of well-characterized MS channels belonging to bacteria and animals are compared with those of plants. Common and specific properties are discussed. We deduce which tools and concepts from animal and bacterial fields could be helpful for improving our understanding of plant mechanotransduction. MS channels embedded in their plasma membrane are sandwiched between the cell wall and the cytoskeleton. The consequences of this peculiar situation are analyzed and discussed. We also stress how important it is to probe mechanical forces at cellular and subcellular levels in planta in order to reveal the intimate relationship linking the membrane with MS channel activity. Finally we will propose new tracks to help to reveal their physiological functions at tissue and plant levels.

Keywords: MSL; MscS; cytoskeleton; mechanobiology; mechanotransduction; membrane tension; plant; stretch-activated channels.

FIGURE 1

Mechanical feedback affects the whole plant physiology acting on both gene and proteins and plays major role especially in development, growth and tropisms.

FIGURE 2

Patch clamp combined with fast speed pressure stimulation allows to study kinetic properties of mechanosensitive (MS) channels. (A) The four patch clamp configuration allowing to record either single channel current (Cell attached, Inside-out, and Outside-out) or a population channel current (Whole cell) are represented. Channels are stimulated by applying a pulse of pressure against the membrane. (B) Recording of the Arabidopsis MSL10 channel activity in outside-out configuration. The activity of the channel is elicited by pulses of increasing pressure. The open probability (P_open)-pressure relationship of the channel fit a Boltzmann function on which are mentioned: the activation threshold, the half pressure activation (P_1/2), the pressure of maximum activation. (C) MS channel reconstituted in a spherical proteoliposome. (D) Poking and carbon fiber techniques allow to apply membrane stretch while recording the cell (arrows show forces applied to the system).

FIGURE 3

Most MS channels exhibit fast activation followed by a slower inactivation or desensitization kinetics in response to pressure stimulation. Schematic representations showing that activation inactivation and desensitization kinetics occurred in the time range of ms to s depending on the channel (A) Escherichia coli MscS [inspired from Boer et al. (2011)], (B) Piezo mouse channels [inspired from Coste et al. (2012)], and (C) Arabidopsis MscS-like 10 channel [inspired from Maksaev and Haswell (2012)]. For MscS-like 10, the presence or absence of inactivation not being definitively settled, the two possibilities are mentioned. Channels are elicited by a step of sub-saturating pressure applied to the membrane.

FIGURE 4

Membrane tension and pressure within cells: milestones and experimental data. References; a: Wolfe et al. (1985), b: Gustin et al. (1988), c: Sachs and Morris (1998), d: Boer et al. (2011), e: Nichol and Hutter (1996), f: Dai et al. (1998), g: Evans and Ludwig (2000), h: Solsona et al. (1998), i: Kwok and Evans (1981), j: Meckel et al. (2004), k: Cosgrove (1996), l: Franks et al. (2001), m: Pritchard et al. (1990), n: Shabala and Lew (2002), o: Haswell et al. (2008), p: Sukharev and Sachs (2012), q: ( Wood, 1999), r: Petrov et al. (2013), s: Morris and Homann (2001). In green: characteristics related to plant, WC, whole-cell configuration; PC, phosphatidylcholine.