Pressure Regulation of the Electrical Properties of Growing Arabidopsis thaliana L. Root Hairs

Lew, Roger R.

doi:10.1104/pp.112.3.1089

Cited by 96 publications

(61 citation statements)

References 28 publications

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“…However, it can be argued that these changes did not reflect the occurrence of streaming potentials, but rather changes in the membrane potentials of root cells generated by osmotically induced changes of the turgor pressure of these cells. Turgor pressure-dependent transport processes in the plasmalemma membrane of algae and higher plants are well known (Zimmermann & Steudle 1974;Zimmermann & Beckers 1977;Wendler, Zimmermann & Bentrup 1983;Stahlberg & Cosgrove 1997;Lew 1996).…”

Section: Discussionmentioning

confidence: 99%

Simultaneous recording of xylem pressure and trans‐root potential in roots of intact glycophytes using a novel xylem pressure probe technique

Wegner

Zimmermann

1998

Plant Cell & Environment

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The radial electrical potential difference between the root xylem and the bathing solution, i.e. the so-called trans-root potential, was measured in intact maize and wheat plants using a xylem pressure probe into which an Ag/AgCl electrode was incorporated. Besides other advantages (e.g. detection and removal of tip clogging; determination of the radial root resistance), the novel probe allowed placement of the electrode precisely in a single xylem vessel as indicated by the reading of sub-atmospheric or negative pressure values upon penetration. The trans-root potentials were of the order of 0 to -70 mV and + 40 to -20 mV for 2-to 3-week-old maize and wheat plants, respectively. Osmotic experiments performed on maize demonstrated that addition of 100 mM mannitol to the solution resulted in a decrease of xylem pressure associated with a slow, but continuous depolarization. The depolarization was reversible upon removal of the mannitol. For wheat plants it could be shown that the oscillations of the xylem pressure described recently by Schneider et al. (1997, Plant, Cell and Environment 20, 221-229) were accompanied by (rectangular, saw-tooth and/or U-shaped) oscillations in the trans-root potential (but not by corresponding changes of the membrane potential of the cortical cells measured simultaneously with conventional microelectrodes). Increase of the light intensity (up to 550 µmol m -2 s -1 ) resulted in a drop of the xylem pressure in wheat, whereas the trans-root potential showed a biphasic response: first hyperpolarization (by about 10 mV) was observed, followed by depolarization (by up to about + 40 mV). Similar light-induced biphasic (but often less pronounced) changes in the trans-root potential were also recorded for maize plants. Most interestingly, the response of the trans-root potential was always faster (by about 1-3 min) than the response of the xylem pressure upon illumination, suggesting that changes in the transpiration rate are reflected very quickly in the electrical properties of the root tissue. The impact of this and other findings on long-distance transport of solutes and water as well as on long-distance signalling is discussed. Key-words:Poaceae; Triticum aestivum L. cv. Alexandria; wheat; Zea mays L. cv. Zelltic; maize; electrokinetic effects, pressure-potential probe; trans-root potential (TRP); xylem pressure. INTRODUCTIONMeasurements of the electrical potential difference between the solution bathing the root and the xylem, i.e. the so-called trans-root potential, provide a way to elucidate the contribution of electrical forces to solute and water transport through the root (Etherton & Higinbotham 1960;Bowling & Spanswick 1964;Shone 1969;Davis & Higinbotham 1969;Läuchli, Spurr & Epstein 1971;Cortes 1992;Rygol et al. 1993;Clarkson 1993;Marschner 1995). Reliable data on these forces and their coupling to transpiration-induced changes in xylem pressure, and to turgor pressure of the hydraulically coupled root cells (Andrews 1976;Stahlberg & Cosgrove 1995;Schneider, Zhu & Zimm...

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Section: Discussionmentioning

confidence: 99%

Simultaneous recording of xylem pressure and trans‐root potential in roots of intact glycophytes using a novel xylem pressure probe technique

Wegner

Zimmermann

1998

Plant Cell & Environment

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“…In either case, the rapid electrical responses occurred with similar timing and magnitude. The electrophysiological techniques have been described in detail elsewhere (Lew, 1996(Lew, , 2007. Voltage clamping was performed using double-barrel micropipettes and a bipolar staircase of clamped voltages.…”

Section: Methodsmentioning

confidence: 99%

Transient responses during hyperosmotic shock in the filamentous fungus Neurospora crassa

Lew

Nasserifar

2009

Microbiology

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Fungal cells maintain an internal hydrostatic pressure (turgor) of about 400-500 kPa. In the filamentous fungus Neurospora crassa, the initial cellular responses to hyperosmotic treatment are loss of turgor, a decrease in relative hyphal volume per unit length (within 1 min) and cell growth arrest; all recover over a period of 10-60 min due to increased net ion uptake and glycerol production. The electrical responses to hyperosmotic treatment are a transient depolarization of the potential (within 1 min), followed by a sustained hyperpolarization (after 4 min) to a potential more negative than the initial potential (a driving force for ion uptake). The nature of the transient depolarization was explored in the context of other transient responses to hyperosmotic shock, to determine whether activation of a specific ion permeability or some other rapid change in electrogenic transport was responsible. Changing the ionic composition of the extracellular medium revealed that K + permeability increases and H + permeability declines during the transient depolarization. We suggest that these changes are due to concerted inhibition of the electrogenic H + -ATPase, and an increase in a K + conductance. Knockout mutants of known K + (tok, trk, trm-8, hak-1) and Cl " (a clc-3 homologue) channels and transporters had no effect on the transient depolarization, but trk and hak-1 do play a role in osmoadaptation, as does a homologue of a serine kinase regulator of H + -ATPase in yeast, Ptk2.

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“…The results at negative membrane potentials are most likely to represent the behavior of the MSL10 in planta, because the transmembrane potential of Arabidopsis root cells has been measured at approximately −180 mV (for example, see ref. 22). MSL10 singlechannel openings were readily detected in response to membrane stretch generated by both negative (Fig.…”

Section: Msl10 Forms a ∼100-ps Mechanosensitive Channel In The Plasmamentioning

confidence: 99%

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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Pressure Regulation of the Electrical Properties of Growing Arabidopsis thaliana L. Root Hairs

Cited by 96 publications

References 28 publications

Simultaneous recording of xylem pressure and trans‐root potential in roots of intact glycophytes using a novel xylem pressure probe technique

Simultaneous recording of xylem pressure and trans‐root potential in roots of intact glycophytes using a novel xylem pressure probe technique

Transient responses during hyperosmotic shock in the filamentous fungus Neurospora crassa

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

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