Hydrostatic and osmotic pressure activated channel in plant vacuole

Alexandre, Joël; Lassalles, Jean-Paul

doi:10.1016/s0006-3495(91)82170-1

Cited by 59 publications

(23 citation statements)

References 17 publications

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“…The difference from our case may stem from a difference in the direction of the osmotic challenge or from a difference in the experimental system (vesicles from wheat roots in their case versus protoplasts from maize-originated undifferentiated cells in suspension in our case). Very likely, the changes in osmolarities were transduced onto the regulation of the dynamically changing P f via an osmolarity-sensing mechanism (the existence of which has been suggested already by Alexandre and Lassalles, 1991;Ramahaleo et al, 1996). Among the hypotonicity-mediating signals could be a varying level of cytosolic free [Ca 21 ], as in animal cells (e.g.…”

Section: The Effect Of Osmolaritymentioning

confidence: 89%

Dynamic Changes in the Osmotic Water Permeability of Protoplast Plasma Membrane

2004

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The osmotic water permeability coefficient (P f ) of plasma membrane of maize (Zea mays) Black Mexican Sweet protoplasts changed dynamically during a hypoosmotic challenge, as revealed using a model-based computational approach. The bestfitting model had three free parameters: initial P f , P f rate-of-change (slope Pf ), and a delay, which were hypothesized to reflect changes in the number and/or activity of aquaporins in the plasma membrane. Remarkably, the swelling response was delayed 2 to 11 s after start of the noninstantaneous (but accounted for) bath flush. The P f during the delay was #1 mm s 21 . During the swelling period following the delay, P f changed dynamically: within the first 15 s P f either (1) increased gradually to approximately 8 mm s 21 (in the majority population of low-initial-P f cells) or (2) increased abruptly to 10 to 20 mm s 21 and then decreased gradually to 3 to 6 mm s 21 (in the minority population of high-initial-P f cells). We affirmed the validity of our computational approach by the ability to reproduce previously reported initial P f values (including the absence of delay) in control experiments on Xenopus oocytes expressing the maize aquaporin ZmPIP2;5. Although mercury did not affect the P f in swelling Black Mexican Sweet cells, phloretin, another aquaporin inhibitor, inhibited swelling in a predicted manner, prolonging the delay and slowing P f increase, thereby confirming the hypothesis that P f dynamics, delay included, reflected the varying activity of aquaporins.The regulation of plant aquaporins is becoming a focus of research in an increasing number of laboratories Tyerman et al., 2002). However, the reports on the regulation of the water permeability of plant cells are still relatively few, very likely reflecting the technical difficulties inherent in such measurements.In order to quantify the permeability of a plant cell to water, one of the approaches consists of isolating protoplasts and monitoring the initial rate of change of their volume upon an osmotic challenge. If the osmotic potential of the external solution is changed instantaneously, the osmotic water permeability (termed P f or P os ) can be deduced from the initial rate of volume relaxation (e.g. Zhang et al., 1990;Verkman, 2000). There are at least two problems with this approach: (1) even when an instantaneous change of solution is possible, a systematic error is introduced, causing an underestimate of P f because, already during the initial phase of protoplast swelling, the volume, the surface area, and the internal concentration of solutes do not remain constant; and (2) instantaneous bath perfusion has technical-and physiological-limitations: unlike animal cells, isolated plant cell protoplasts (the terms protoplast and cell will be used here interchangeably) do not stick well to the chamber floor and defeat attempts of rapid (let alone, instantaneous) solution flushes. Very fast external solution exchange has been achieved by immobilizing the protoplast with a suction micropipette (e.g. Ramah...

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Section: The Effect Of Osmolaritymentioning

confidence: 89%

Dynamic Changes in the Osmotic Water Permeability of Protoplast Plasma Membrane

2004

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“…Apparently, pressure-sensitive regulation of symplastic solute transport through plasmodesmata (Robards and Lucas, 1990) may not explain completely the observed high ERs of roots (Bret-Harte and Silk, 1994). Alternatively, pressure-sensitive transport proteins (Kirst, 1990;Alexandre and Lassalles, 1991) could have mediated some of the radial solute transport. This alternative, however, would involve the apoplast as a pathway for solute transport, which has yet received only little attention.…”

Section: Discussionmentioning

confidence: 99%

Rapid Response of the Yield Threshold and Turgor Regulation during Adjustment of Root Growth to Water Stress in Zea mays

Frensch

Hsiao

1995

Plant Physiol.

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Responses of cortical cell turgor ( P ) following rapid changes in osmotic pressure (m,,,) were measured throughout the elongation zone of maize (Zea mays 1.) roots using a cell pressure probe and compared with simultaneously measured root elongation to evaluate: yield threshold ( Y ) (minimum P for growth), wall extensibility, growth-zone radial hydraulic conductivity (K), and turgor recovery rate. Small increases in rr,,, (0.1 MPa) temporarily decreased P and growth,;which recovered fully in 5 to 10 min. Under stronger rr,,, Roots adjust their growth rate when subjected to water stress. The phenomenon is commonly studied using Lockhart's concept of growth, which relates growth to cell wall mechanics and hydraulic and osmotic properties of the growing tissue (Lockhart, 1965;Hsiao et al., 1976;Boyer, 1985;Cosgrove, 1986). Of the parameters in the Lockhart equations, the yield threshold Y and wall extensibility m are often evaluated from plots (usually linear) of growth rates versus P, with Y representing the intercept on the P axis and m representing the slope for roots (Pritchard et al., 1990b) as well as leaves (Bunce, 1977;Hsiao and Jing, 1987 , 1990a, 1991, 1993Spollen and Sharp, 1991). Indeed, early work on algae (Green et al., 1971) and more recently on roots (Hsiao and Jing, 1987;Frensch and Hsiao, 1994) showed rapid changes of Y with water stress. Measurements of P and root growth during osmotic transitions revealed values of Y much closer to P (Frensch and Hsiao, 1994). This indicates that m is large and factors different from changes in m could be equally or more important in determining rates of elongation. The rate of cell expansion along the elongation zone is not uniform. For maize (Zea mays L.) roots, local relative Abbreviations: A, surface area (m'); AT,,,, change of osmotic pressure in the medium (MPa); E, volumetric elastic coefficient (MPa); ER, elongation rate (mm h-'); k, rate constant of water exchange (s-'); K, tissue hydraulic conductivity coefficient (m2 s-' MPa-I); LRER, local relative elongation rate (h-'); LVDT, linear variable differential transducer; m, cell wall extensibility (MPa-' h-'); P, cell turgor (MPa); Pmin (P,,,), minimum (maximum) turgor measured during the response of P to a decrease (increase) in V of the medium; ( P -Y), growth-effective turgor; T, osmotic pressure (MPa); V, water potential (MPa); r, radius (mm); t,,2, half-time of water exchange (s); V, volume (m3); Y, yield threshold (MPa); Ytrans,', Y evaluated from the turgor decline phase during the biphasic pressure-response curve; Ytrans,2, similar to Ytrans,' but evaluated from the turgor recovery instead of the decline phase; z, length of the root elongation zone; subscript "c" associates a parameter with a cell; subscript "m" associates a parameter with the medium; subscript "r" associates a parameter with the root; subscript "t" indicates the dependency of a parameter on time; subscript "z" associates a parameter with respect to its position along the elongation zone.www.plantphysiol.org on May 12, 2018 -P...

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“…In summary, MSL10 forms a channel with a moderate preference for anions, passing ∼6 chloride ions for every sodium ion. Gadolinium ions are commonly used to inhibit K + , Ca 2+ , and metazoan MS channels (27) and have also been demonstrated to inhibit the activity of MS channels in plants (28)(29)(30) and bacteria (31). Inhibition of MSL10 activity was observed after excised inside-out patches were perfused in a bath containing 100 μM GdCl 3 (Fig.…”

Section: Msl10 Exhibits a Moderate Preference For Anionsmentioning

confidence: 97%

MscS-Like10 is a stretch-activated ion channel from Arabidopsis thaliana with a preference for anions

Maksaev

Haswell

2012

Proc. Natl. Acad. Sci. U.S.A.

132

156

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Like many other organisms, plants are capable of sensing and responding to mechanical stimuli such as touch, osmotic pressure, and gravity. One mechanism for the perception of force is the activation of mechanosensitive (or stretch-activated) ion channels, and a number of mechanosensitive channel activities have been described in plant membranes. Based on their homology to the bacterial mechanosensitive channel MscS, the 10 MscS-Like (MSL) proteins of Arabidopsis thaliana have been hypothesized to form mechanosensitive channels in plant cell and organelle membranes. However, definitive proof that MSLs form mechanosensitive channels has been lacking. Here we used single-channel patch clamp electrophysiology to show that MSL10 is capable of providing a MS channel activity when heterologously expressed in Xenopus laevis oocytes. This channel had a conductance of ∼100 pS, consistent with the hypothesis that it underlies an activity previously observed in the plasma membrane of plant root cells. We found that MSL10 formed a channel with a moderate preference for anions, which was modulated by strongly positive and negative membrane potentials, and was reversibly inhibited by gadolinium, a known inhibitor of mechanosensitive channels. MSL10 demonstrated asymmetric activation/ inactivation kinetics, with the channel closing at substantially lower tensions than channel opening. The electrophysiological characterization of MSL10 reported here provides insight into the evolution of structure and function of this important family of proteins.T he perception of mechanical stimuli like gravity, touch, or osmotic pressure is essential to normal plant growth and development and is further implicated in biotic and abiotic stress responses (1). One of the best-studied strategies for perceiving force involves membrane-embedded channels that are gated by tension, known as mechanosensitive (MS) channels (2). Numerous MS channel activities (>17 to date) have been described in the membranes of diverse tissues from a variety of plant species (summarized in ref. 3, also refs. 4 and 5). Many of these observed MS channel activities differ in their conductance, ion selectivity, and/or sensitivity to the direction of activation pressure, suggesting that multiple classes of mechanosensitive channels are present in plant cells.No mechanosensitive ion channel activity discovered in plant membranes has yet been definitively identified at the molecular level, but two families of proteins serve as strong candidates. The first is the Mid1-Complementing Activity (MCA) family, members of which are required for root response to touch in the model plant Arabidopsis thaliana, induce Ca 2+ uptake in rice and Arabidopsis cells (6, 7), and are associated with increased current in response to hypotonic stimulation of Xenopus oocytes (8). The second family of candidates for plant MS channels is the MscS-Like (MSL) family, first identified based on modest homology to the wellcharacterized bacterial MS channel MscS from Escherichia coli (3, 9). MscS is a lar...

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Hydrostatic and osmotic pressure activated channel in plant vacuole

Cited by 59 publications

References 17 publications

Dynamic Changes in the Osmotic Water Permeability of Protoplast Plasma Membrane

Dynamic Changes in the Osmotic Water Permeability of Protoplast Plasma Membrane

Rapid Response of the Yield Threshold and Turgor Regulation during Adjustment of Root Growth to Water Stress in Zea mays

MscS-Like10 is a stretch-activated ion channel from Arabidopsis thaliana with a preference for anions

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