The osmotic motor that drives stomatal movement

Exploring biophysical and biochemical components of the osmotic motor that drives stomatal movement

by Raschke K., Hedrich R., Reckmann U., Schroeder J. I. (1988)

In Botanica Acta 101: 283-294 – https://doi.org/10.1111/j.1438-8677.1988.tb00046.x

https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1438-8677.1988.tb00046.x

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Ca2+ signals are likely to activate CPKs, which enhance the activity of S‐type anion channels and boost stomatal closure

Ca2+ signals in guard cells enhance the efficiency by which ABA triggers stomatal closure

by Huang S., Waadt R., Nuhkat M., Kollist H., Hedrich R., Roelfsema M. R. G. (2019)

Shouguang Huang, Rainer Waadt, Maris Nuhkat, Hannes Kollist,Rainer Hedrich, M. Rob G. Roelfsema,

Molecular Plant Physiology and Biophysics Julius‐von‐Sachs Institute for Biosciences Biocenter, Würzburg University, Julius‐von‐Sachs‐Platz 2, D‐97082 Würzburg, Germany

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In New Phytologist https://doi.org/10.1111/nph.15985

https://nph.onlinelibrary.wiley.com/doi/abs/10.1111/nph.15985?af=R

Summary

During drought, abscisic acid (ABA) induces closure of stomata via a signaling pathway that involves the Ca2+‐independent protein kinase OST1, as well as Ca2+‐dependent protein kinases (CPKs). However, the interconnection between OST1 and Ca2+ signaling in ABA‐induced stomatal closure has not been fully resolved.

ABA‐induced Ca2+ signals were monitored in intact Arabidopsis leaves, which express the ratiometric Ca2+ reporter R‐GECO1‐mTurquoise and the Ca2+‐dependent activation of S‐type anion channels was recorded with intracellular double‐barreled microelectrodes.

ABA triggered Ca2+ signals that occurred during the initiation period, as well as the acceleration phase of stomatal closure. However, a subset of stomata closed in the absence of Ca2+ signals. On average, stomata closed faster if Ca2+ signals were elicited during the ABA response. Loss of OST1 prevented ABA‐induced stomatal closure and repressed Ca2+ signals, while elevation of the cytosolic Ca2+concentration caused a rapid activation of SLAC1 and SLAH3 anion channels.

Our data show that the majority of Ca2+ signals are evoked during the acceleration phase of stomatal closure, which is initiated by OST1. These Ca2+ signals are likely to activate CPKs, which enhance the activity of S‐type anion channels and boost stomatal closure.

Optimization of photosynthesis and stomatal conductance during acclimation to heat and drought

Optimization of photosynthesis and stomatal conductance in the date palm Phoenix dactylifera during acclimation to heat and drought

by Kruse J., Adams M., Winkler B., Ghirardo A., Alfarraj S., Kreuzwieser J., Hedrich R., Schnitzler J.-P., Rennenberg H. (2019)

Jörg Kruse, Mark Adams, Barbro Winkler, Andrea Ghirardo, Saleh Alfarraj, Jürgen Kreuzwieser, Rainer Hedrich, Jörg‐Peter Schnitzler, Heinz Rennenberg,

Institute of Forest Sciences, Chair of Tree Physiology, University of Freiburg, Georges‐Köhler‐Allee 53/54, 79110 Freiburg, Germany

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In New Phytologist https://doi.org/10.1111/nph.15923

https://nph.onlinelibrary.wiley.com/doi/abs/10.1111/nph.15923?af=R

Abstract

We studied acclimation of leaf gas exchange to differing seasonal climate and soil water availability in slow‐ growing date palm seedlings (Phoenix dactylifera). We used an extended Arrhenius‐equation to describe instantaneous temperature responses of leaf net photosynthesis (A) and stomatal conductance (G), and derived physiological parameters suitable for characterization of acclimation (Topt, Aopt and Tequ).

Optimum temperature of A (Topt) ranged between 20 ‐33°C in winter and 28 ‐45°C in summer. Growth temperature (Tgrowth) explained ~50% of the variation in Topt, which additionally depended on leaf water status at the time‐ of‐ measurement. During water‐stress, light ‐ saturated rates of A at Topt (i.e, Aopt) were reduced to 30‐80% of control levels, albeit not limited by CO2‐ supply per se.

Equilibrium temperature (Tequ), around which A/G and substomatal [CO2] are constant, remained tightly coupled with Topt. Our results suggest that acclimatory shifts in Topt and Aopt reflect a balance between maximization of photosynthesis whilst minimizing the risk of metabolic perturbations caused by imbalances in cellular [CO2].

This novel perspective on acclimation of leaf gas exchange is compatible with optimization theory, and might help elucidating other acclimation and growth strategies in species adapted to differing climates.

Differential expression of K+ channels between stomatal guard cells and subsidiary cells

Differential expression of K+ channels between guard cells and subsidiary cells within the maize stomatal complex

Büchsenschütz K., Marten I., Becker D., Philippar K. (2), Ache P., Hedrich R. (2005)

  • Kai Büchsenschütz, Irene Marten, Dirk Becker, Katrin Philippar, Peter Ache, Rainer Hedrich,
  1. Molecular Plant Physiology and Biophysics, Julius-von-Sachs Institute for Bioscience, University of Wuerzburg, Wuerzburg, Germany
  2. Department of Biology I, Botany III, Ludwig-Maximilians-University Muenchen, Muenchen, Germany

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In Planta 222: 968– 976 – https://doi.org/10.1007/s00425-005-0038-6

https://link.springer.com/article/10.1007%2Fs00425-005-0038-6

Abstract

Grass stomata are characterized by dumbbell-shaped guard cells forming a complex with a pair of specialized epidermal cells, the subsidiary cells. Stomatal movement is accomplished by a reversible exchange of potassium and chloride between these two cell types.

To gain insight into the molecular machinery involved in K+ transport within the stomatal complex of Zea mays, we determined the spatial and temporal expression pattern of potassium channels in the maize leaf. 

KZM2 and ZORK were isolated and identified as new members of the plant Shaker K+ channel family. Northern blot analysis identified fully developed leaves as the predominant site of KZM2 expression.

Following enzymatic digestion and separation of leaf tissue into epidermal, mesophyll, and vascular fractions, KZM2 and ZORK transcripts were localized in the epidermis.

Identification, characterization, and regulation of a stomatal guard cell anion channel

Voltage‐dependent chloride channels in plant cells: identification, characterization, and regulation of a guard cell anion channel

by Hedrich R. (1994)

Rainer Hedrich

Institut für Biophysik, Universität Hannover, D-30419 Hannover 21, Germany

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In Current Topics in Membranes 4 : 1 33 – https://doi.org/10.1016/S0070-2161(08)60816-3 –

https://www.sciencedirect.com/science/article/pii/S0070216108608163

Publisher Summary

The early voltage-clamp experiments from Cole and Curtis on giant algal cells, excitability has been recognized in the membranes of animals and plants. The action potential in the plasma membrane of these algal cells, which were often called “green muscles,” is generated by conductance changes with respect to calcium, chloride, and potassium ions.

In contrast to the giant algal cells that allow the application of conventional voltage-clamp and internal perfusion techniques, the elucidation of ion channels in smaller plant cells awaits the development of the patch-clamp technique.

As in animal cells the major biophysical advances of the past decade depends heavily on the ability to isolate single sensory cells-often by using enzymes and to patch clamp them. The combined use of the patch-clamp technique and the development of new methods to isolate wall-free cells (protoplasts), which essentially were based on the availability of improved enzyme preparations, enabled direct studies on ion channels embedded in the plasma membrane, the vacuolar membrane, and the photosynthetic membrane.

Evolution of stomatal signalling pathways

Two open stomatal pores on the surface of a fern leaf, each surrounded by two kidney-shaped guard cells. Right panel: important moments during the evolution of stomata. Stomata probably evolved in an early land plant, from which all today’s species descend, but were likely lost in liverworts. Some genes that control stomatal movement in flowering plants likely arose recently, in seed plants, from within ancient gene families that were present in algae. Signalling genes with specific roles in guard cells likely arose after mosses diverged from a common ancestor.
Credit: Stephan Liebig

Acquiring Control: The Evolution of Stomatal Signalling Pathways

by Sussmilch F. C., Schulz J., Hedrich R., Roelfsema M. R. G. (2019)

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In Trends in Plant Science – DOI:https://doi.org/10.1016/j.tplants.2019.01.002 – 

https://www.sciencedaily.com/releases/2019/02/190221111659.htm

https://www.cell.com/trends/plant-science/fulltext/S1360-1385(19)30014-7?_returnURL=https%3A%2F%2Flinkinghub.elsevier.com%2Fretrieve%2Fpii%2FS1360138519300147%3Fshowall%3Dtrue

Highlights

Recent findings reveal that stomata function differently in mosses and hornworts than in vascular plants, with bryophyte stomata promoting rather than preventing water loss.

Important signalling genes that control stomatal opening and closure in response to changes in a plant’s environment have been characterised in angiosperms.

Less is known about the evolutionary origins of these signalling pathways, and whether or not they are also present in bryophytes.

Here, we review recent findings in this field, and further examine the evolutionary origins and expression patterns of key signalling genes, using newly available plant genomic and transcriptomic resources.

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In vascular plants, stomata balance two opposing functions: they open to facilitate CO 2uptake and close to prevent excessive water loss.

Here, we discuss the evolution of three major signalling pathways that are known to control stomatal movements in angiosperms in response to light, CO 2, and abscisic acid (ABA).

We examine the evolutionary origins of key signalling genes involved in these pathways, and compare their expression patterns between an angiosperm and moss.

We propose that variation in stomatal sensitivity to stimuli between plant groups are rooted in differences in:

(i) gene presence/absence,

(ii) specificity of gene spatial expression pattern, and

(iii) protein characteristics and functional interactions.

Sulfate is Incorporated into Cysteine to Trigger ABA Production and Stomatal Closure

Figure 9.Model for the Function of Sulfate in ABA Biosynthesis and Stomatal Closure.
Enzymes catalyzing reactions (black arrows) in the biosynthesis pathways of Cys and ABA as well as the sensing of ABA for stomatal closure are shown in yellow boxes. Red box indicates the nonactive apoenzyme, which requires the cofactor for activation. Asterisks indicate enzymes that have been shown by this study to be essential for sulfate/Cys-induced stomatal closure. The stimulating effects of metabolites or enzymes on downstream reactions are depicted as blue arrows or green open arrows, respectively. Numbers in gray circles indicate references for known regulations/processes not experimentally addressed:
1: Synthesis of Cys is limited by provision of O-actylserine and sulfide (Takahashi et al., 2011).
2: Cys is the substrate of the MoCo-sulfurylase ABA3 required for activation of AAO3 (Bittner et al., 2001).
3: Cys level affects AAO activity in vivo (Cao et al., 2014).
4: PYR/PYL acts as an ABA receptor and controls PP2C activity (e.g. ABI1; Park et al., 2009).
5: PP2C activity regulates activation of OST1 in response to ABA (Vlad et al., 2009).
6: OST1 activates SLAC1 by phosphorylation at multiple residues (Geiger et al., 2009Lee et al., 2009).
7: OST1 phosphorylates RBOHF (NADPH oxidase; Sirichandra et al., 2009).
8: ROS induce stomatal closure in an ABA2-dependent manner (Sierla et al., 2016).
9: SLAC1 is essential for ABA-induced stomatal closure (Vahisalu et al., 2008).

Sulfate is Incorporated into Cysteine to Trigger ABA Production and Stomatal Closure

by Batool S. , Uslu V. V., Rajab H., Ahmad N., Waadt R., Geiger D., Maalgoli M., Xiang C.-B., Hedrich R., Rennenberg H., Herschbach C;, Hell R., Wirtz M. (2018)

Sundas Batool, Veli Vural Uslu, Hala Rajab, Nisar Ahmad, Rainer Waadt, Dietmar Geiger, Mario Malagoli, Cheng-Bin Xiang, Rainer Hedrich, Heinz Rennenberg, Cornelia Herschbach, Ruediger Hell, Markus Wirtz,

In Plant Cell – DOI: https://doi.org/10.1105/tpc.18.00612

http://www.plantcell.org/content/30/12/2973

Abstract

Plants close stomata when root water availability becomes limiting.

Recent studies have demonstrated that soil-drying induces root-to-shoot sulfate transport via the xylem and that sulfate closes stomata.

Here we provide evidence for a physiologically relevant signaling pathway that underlies sulfate-induced stomatal closure in Arabidopsis (Arabidopsis thaliana). We uncovered that, in the guard cells, sulfate activates NADPH oxidases to produce reactive oxygen species (ROS) and that this ROS induction is essential for sulfate-induced stomata closure. In line with the function of ROS as the second-messenger of abscisic acid (ABA) signaling, sulfate does not induce ROS in the ABA-synthesis mutant, aba31, and sulfate-induced ROS were ineffective at closing stomata in the ABA-insensitive mutant abi21 and a SLOW ANION CHANNEL1 loss-of-function mutant.

We provided direct evidence for sulfate-induced accumulation of ABA in the cytosol of guard cells by application of the ABAleon2.1 ABA sensor, the ABA signaling reporter ProRAB18:GFP, and quantification of endogenous ABA marker genes.

In concordance with previous studies, showing that ABA DEFICIENT3 uses Cys as the substrate for activation of the ABSCISIC ALDEHYDE OXIDASE3 (AAO3) enzyme catalyzing the last step of ABA production, we demonstrated that assimilation of sulfate into Cys is necessary for sulfate-induced stomatal closure and that sulfate-feeding or Cys-feeding induces transcription of NINE-CIS-EPOXYCAROTENOID DIOXYGENASE3, limiting the synthesis of the AAO3 substrate.

Consequently, Cys synthesis-depleted mutants are sensitive to soil-drying due to enhanced water loss. Our data demonstrate that sulfate is incorporated into Cys and tunes ABA biosynthesis in leaves, promoting stomatal closure, and that this mechanism contributes to the physiological water limitation response.