Stomatal action directly feeds back on leaf turgor: New insights into the regulation of the plant water status from non-invasive pressure probe measurements

Universität Würzburg, Biozentrum, Julius-von-Sachs-Institut für Biowissenschaften, Julius-von-Sachs-Platz 2, 97082 Würzburg, Germany.
The Plant Journal (Impact Factor: 5.97). 03/2010; 62(6):1072-82. DOI: 10.1111/j.1365-313X.2010.04213.x
Source: PubMed


Uptake of CO(2) by the leaf is associated with loss of water. Control of stomatal aperture by volume changes of guard cell pairs optimizes the efficiency of water use. Under water stress, the protein kinase OPEN STOMATA 1 (OST1) activates the guard-cell anion release channel SLOW ANION CHANNEL-ASSOCIATED 1 (SLAC1), and thereby triggers stomatal closure. Plants with mutated OST1 and SLAC1 are defective in guard-cell turgor regulation. To study the effect of stomatal movement on leaf turgor using intact leaves of Arabidopsis, we used a new pressure probe to monitor transpiration and turgor pressure simultaneously and non-invasively. This probe permits routine easy access to parameters related to water status and stomatal conductance under physiological conditions using the model plant Arabidopsis thaliana. Long-term leaf turgor pressure recordings over several weeks showed a drop in turgor during the day and recovery at night. Thus pressure changes directly correlated with the degree of plant transpiration. Leaf turgor of wild-type plants responded to CO(2), light, humidity, ozone and abscisic acid (ABA) in a guard cell-specific manner. Pressure probe measurements of mutants lacking OST1 and SLAC1 function indicated impairment in stomatal responses to light and humidity. In contrast to wild-type plants, leaves from well-watered ost1 plants exposed to a dry atmosphere wilted after light-induced stomatal opening. Experiments with open stomata mutants indicated that the hydraulic conductance of leaf stomata is higher than that of the root-shoot continuum. Thus leaf turgor appears to rely to a large extent on the anion channel activity of autonomously regulated stomatal guard cells.

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Available from: Rainer Hedrich, Oct 08, 2015
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    • "s was not significantly modified in pip2 ; 1 plants ( Supplemental Figure 11 ) . This lack of transpiration phenotype should be interpreted with care as it may reflect the cumulative effects of PIP2 ; 1 in guard cells and other cell types / organs . In particular , leaf vein cells are crucial for transferring water from the xylem into the lamina ( Ache et al . , 2010 ; Prado et al . , 2013 ) . Thus , a lack of function of PIP2 ; 1 at this site may result in a hydraulic limitation in veins , a drop in leaf water potential , and induction of stomatal closure . Conversely , a lack of function of PIP2 ; 1 in guard cells may antagonize stomatal closure . Because of these confounding physiological effects"
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    ABSTRACT: Stomatal movements in response to environmental stimuli critically control the plant water status. Although these movements are governed by osmotically driven changes in guard cell volume, the role of membrane water channels (aquaporins) has remained hypothetical. Assays in epidermal peels showed that knockout Arabidopsis thaliana plants lacking the Plasma membrane Intrinsic Protein 2;1 (PIP2;1) aquaporin have a defect in stomatal closure, specifically in response to abscisic acid (ABA). ABA induced a 2-fold increase in osmotic water permeability (Pf) of guard cell protoplasts and an accumulation of reactive oxygen species in guard cells, which were both abrogated in pip2;1 plants. Open stomata 1 (OST1)/Snf1-related protein kinase 2.6 (SnRK2.6), a protein kinase involved in guard cell ABA signaling, was able to phosphorylate a cytosolic PIP2;1 peptide at Ser-121. OST1 enhanced PIP2;1 water transport activity when coexpressed in Xenopus laevis oocytes. Upon expression in pip2;1 plants, a phosphomimetic form (Ser121Asp) but not a phosphodeficient form (Ser121Ala) of PIP2;1 constitutively enhanced the Pf of guard cell protoplasts while suppressing its ABA-dependent activation and was able to restore ABA-dependent stomatal closure in pip2;1. This work supports a model whereby ABA-triggered stomatal closure requires an increase in guard cell permeability to water and possibly hydrogen peroxide, through OST1-dependent phosphorylation of PIP2;1 at Ser-121. © 2015 American Society of Plant Biologists. All rights reserved.
    The Plant Cell 07/2015; 27(7). DOI:10.1105/tpc.15.00421 · 9.34 Impact Factor
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    • "results provided in vivo evidences that OST1 kinase is involved in stomatal closure and activation of S-type anion channels induced by a biotic stimulus, YEL. Though it is well known that OST1 is essential for stomatal closure in response to a variety of stimuli (Melotto et al. 2006, Xie et al. 2006, Ache et al. 2010, Vahisalu et al. 2010, Xue et al. 2011, Merilo et al. 2013, Montillet et al. 2013), to our knowledge there is no evidence that kinase activity of OST1 is increased in guard cells in response to stimuli other than ABA. On the other hand, it has been reported that flg22 does not elicit activation Fig. 6 YEL-induced transient [Ca 2+ ] cyt elevations in Col-0 and ost1-3 guard cells expressing the Ca 2+ -sensing fluorescent protein YC 3.6. "
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    ABSTRACT: We recently demonstrated that yeast elicitor (YEL)-induced stomatal closure requires a Ca(2+)-dependent kinase, CPK6. A Ca(2+)-independent kinase, Open Stomata 1 (OST1), is involved in stomatal closure induced by various stimuli including abscisic acid (ABA). In the present study, we investigated the role of OST1 in YEL-induced stomatal closure in Arabidopsis using a knock-out mutant, ost1-3, and a kinase-deficient mutant, ost1-2. Yeast elicitor did not induce stomatal closure or activation of guard cell S-type anion channels in the ost1 mutants unlike in wild-type plants. However, YEL did not increase OST1 kinase activity in wild-type guard cells. The YEL-induced stomatal closure and activation of S-type anion channels were also impaired in a gain-of-function mutant of a clade A type 2C protein phosphatase (ABA INSENSITIVE 1), abi1-1C. In the ost1 mutants like in the wild type, YEL induced H2O2 accumulation, activation of nonselective Ca(2+)-permeable cation (ICa) channels and transient elevations in cytosolic free Ca(2+) concentration ([Ca(2+)]cyt) in guard cells. These results suggest that OST1 kinase is essential for stomatal closure and activation of S-type anion channels induced by YEL and that OST1 is not involved in H2O2 accumulation, ICa channel activation, or [Ca(2+)]cyt elevations in guard cells induced by YEL. © The Author 2015. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For Permissions, please e-mail:
    Plant and Cell Physiology 04/2015; 56(6). DOI:10.1093/pcp/pcv051 · 4.93 Impact Factor
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    • "Under water stress, local changes in C w are quickly relayed throughout the plant xylem, thanks to the cohesion and tension properties of water. A turgor decrease below the plant's specific threshold value in the leaf lamina leads to increased ABA production (Liu et al., 1978; Pierce and Raschke, 1981; Lee et al., 2006; Tuteja, 2007; Ache et al., 2010), probably at its synthesis sites in shoot vascular parenchyma tissues and guard cells (Boursiac et al., 2013). The increase in the concentration of ABA in the xylem leads to reduced C leaf and K leaf in the BS, possibly due to reduced AQP expression and/or activity (Martre et al., 2002; Table II. "
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    ABSTRACT: Our understanding of the cellular role of aquaporins (AQPs) in the regulation of whole-plant hydraulics, in general, and extravascular, radial hydraulic conductance in leaves (Kleaf), in particular, is still fairly limited. We hypothesized that the aquaporins of the vascular bundle sheath (BS) cells regulate Kleaf. To examine this hypothesis, AQP genes were silenced using artificial microRNAs (amiRNAs) that were expressed constitutively or specifically targeted to the BS. MicroRNA sequences were designed to target all five AQP genes from thePIP1 subfamily. Our results show that the constitutively silenced PIP1 (35S promoter) plants had decreased PIP1 transcript and protein levels and decreased mesophyll and BS osmotic water permeability (Pf), mesophyll conductance of CO2 (gm), photosynthesis (AN), Kleaf, transpiration and shoot biomass. Plants in which the PIP1 subfamily was silenced only in the BS (SCR:mir plants) exhibited decreased mesophyll and BS Pf and decreased Kleaf, but no decreases in the rest of the parameters listed above, with the net result of increased shoot biomass. We excluded the possibility of SCR promoter activity in the mesophyll. Hence, the fact that SCR:mir mesophyll exhibited reduced Pf, but not reduced gm suggests that the BS-mesophyll hydraulic continuum acts as a feed-forward control signal. The role of AQPs in the hierarchy of the hydraulic signal pathway controlling leaf water status under normal and limited-water conditions is discussed. Keywords: Plasma membrane intrinsic proteins (PIPs), Aquaporins (AQPs), Bundle sheath, Leaf hydraulic conductivity (Kleaf), Artificial microRNA (amiRNA).
    Plant physiology 09/2014; 166(3). DOI:10.1104/pp.114.248633 · 6.84 Impact Factor
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