Halophytic guard cells are less sensitive than glycophytic guard cells, providing opportunities to manipulate stomatal behavior and improve plant productivity

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盐生植物的保卫细胞比糖生植物的保卫细胞不太敏感，这提供了操纵气孔行为和提高植物产量的机会。

As células-guarda halofíticas são menos sensíveis do que as células-guarda glicofíticas, proporcionando oportunidades para manipular o comportamento estomático e melhorar a produtividade das plantas.

Las células guardas halofíticas son menos sensibles que las células guardas glicofíticas, lo que proporciona oportunidades para manipular el comportamiento estomático y mejorar la productividad de las plantas.

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Under salt stress guard cells rewire ion transport and abscisic acid signaling

Karimi S. M., Freund M., Wager B. M., Knoblauch M., Fromm J., Mueller H.M., Ache P., Krischke M., Mueller M. J., Müller T., Dittrich M., Geilfus C.-M., Alfarhan A. H., Hedrich R., Deeken R. (2021)

Sohail M. Karimi, Matthias Freund, Brittney M. Wager, Michael Knoblauch, Jörg Fromm, Heike M. Mueller, Peter Ache, Markus Krischke, Martin J. Mueller, Tobias Müller, Marcus Dittrich, Christoph-Martin Geilfus, Ahmed H. Alfarhan, Rainer Hedrich, Rosalia Deeken,

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New Phytologist 231(3) : 1040-1055 – https://doi.org/10.1111/nph.17376 –

https://nph.onlinelibrary.wiley.com/doi/10.1111/nph.17376

Summary

• Soil salinity is an increasingly global problem which hampers plant growth and crop yield. Plant productivity depends on optimal water-use efficiency and photosynthetic capacity balanced by stomatal conductance. Whether and how stomatal behavior contributes to salt sensitivity or tolerance is currently unknown. This work identifies guard cell-specific signaling networks exerted by a salt-sensitive and salt-tolerant plant under ionic and osmotic stress conditions accompanied by increasing NaCl loads.
• We challenged soil-grown Arabidopsis thaliana and Thellungiella salsuginea plants with short- and long-term salinity stress and monitored genome-wide gene expression and signals of guard cells that determine their function.
• Arabidopsis plants suffered from both salt regimes and showed reduced stomatal conductance while Thellungiella displayed no obvious stress symptoms. The salt-dependent gene expression changes of guard cells supported the ability of the halophyte to maintain high potassium to sodium ratios and to attenuate the abscisic acid (ABA) signaling pathway which the glycophyte kept activated despite fading ABA concentrations.
• Our study shows that salinity stress and even the different tolerances are manifested on a single cell level. Halophytic guard cells are less sensitive than glycophytic guard cells, providing opportunities to manipulate stomatal behavior and improve plant productivity.

Stomatal closure was found to be accompanied by an initial hyperpolarization and cytosolic acidification of subsidiary cells

Cell type-specific regulation of ion channels within the maize stomatal complex

Mumm P., Wolf T., Fromm J., Roelfsema M. R. G., Marten I. (2011)

Patrick Mumm, Thomas Wolf, Jörg Fromm, M Rob G Roelfsema, Irene Marten,

Plant Cell Physiol 52: 1365–1375 – doi: 10.1093/pcp/pcr082 – Epub 2011 Jun 20 –

https://pubmed.ncbi.nlm.nih.gov/21690176/

Abstract

The stomatal complex of Zea mays is composed of two pore-forming guard cells and two adjacent subsidiary cells. For stomatal movement, potassium ions and anions are thought to shuttle between these two cell types. As potential cation transport pathways, K(+)-selective channels have already been identified and characterized in subsidiary cells and guard cells. However, so far the nature and regulation of anion channels in these cell types have remained unclear. In order to bridge this gap, we performed patch-clamp experiments with subsidiary cell and guard cell protoplasts. Voltage-independent anion channels were identified in both cell types which, surprisingly, exhibited different, cell-type specific dependencies on cytosolic Ca(2+) and pH. After impaling subsidiary cells of intact maize plants with microelectrodes and loading with BCECF [(2′,7′-bis-(2-carboxyethyl)-5(and6)carboxyflurescein] as a fluorescent pH indicator, the regulation of ion channels by the cytosolic pH and the membrane voltage was further examined. Stomatal closure was found to be accompanied by an initial hyperpolarization and cytosolic acidification of subsidiary cells, while opposite responses were observed during stomatal opening. Our findings suggest that specific changes in membrane potential and cytosolic pH are likely to play a role in determining the direction and capacity of ion transport in subsidiary cells.

The guard cell osmotic motor driving stomatal closure uses nitrate as the signal to open the major anion channel SLAC1

Date palm (Phoenix dactylifera) stomata characteristics. (a) Two‐year‐old date palms grow three to five pinnate leaves. (b) Electron micrograph of the upper leaf surface. Stomata are arranged in rows, as in grasses. The epidermis is covered with epicuticular waxes. (c, d) Laser scanning images of the date palm leaf surface stained with propidium iodide (excitation at 458 nm, fluorescence recorded at wavelengths of 490–550 nm). (d) Stomata are surrounded by lateral and polar subsidiary cells (highlighted in green in the right image, guard cells are coloured yellow). These two pairs of cells very probably produce the waxy stomatal chimney.

The desert plant Phoenix dactylifera closes stomata via nitrate‐regulated SLAC1 anion channel

by Müller H. M., Schäfer N., Bauer H., Geiger D., Lautner S., Fromm J., Riederer M., Bueno A., Nussbaumer T., Mayer K., Alquraishi S. A., Alfarhan A. H., Neher E., Al‐Rasheid K. A. S., Ache P., Hedrich R. (2017)

Heike M. Müller, Nadine Schäfer, Hubert Bauer, Dietmar Geiger, Silke Lautner, Jörg Fromm, Markus Riederer, Amauri Bueno, Thomas Nussbaumer, Klaus Mayer, Saleh A. Alquraishi, Ahmed H. Alfarhan, Erwin Neher, Khaled A. S. Al‐Rasheid, Peter Ache, Rainer Hedrich,

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In New Phytol. 216(1): 150-162 – https://doi.org/10.1111/nph.14672 –

https://nph.onlinelibrary.wiley.com/doi/full/10.1111/nph.14672

Date palm (Phoenix dactylifera) stomata morphology. (a, b) Raster electron micrograph from a stoma on the lower leaf surface. Stomata are surrounded by a huge epicuticular wax chimney, thereby increasing the thickness of the boundary layer above the stomatal pore and, consequently, the total resistance to stomatal transpiration. The wax seems to emerge from the cells neighbouring the guard cells. (b, lower image) Magnification of a stomatal wax chimney.

Summary

Subcellular components of date palm (Phoenix dactylifera) stomata, transmission electron microscopy (TEM) cross‐sections. (a) Overview of a stomatal complex with guard cells (gc), subsidiary cells (sc) and neighbouring epidermal cell. The pair of guard cells is clearly separated from epidermal cells by subsidiary cells. Subsidiary cells possess large central vacuoles (v) and mitochondria (m). Guard cells contain a large nucleus (n). (b) Detailed view of the guard cell pair. The guard cells do not share plasmodesmatal connections with the subsidiary cells, and so are symplastically isolated. Guard cells exhibit large vacuoles (v), numerous mitochondria (m) and few chloroplasts (chl). (c) Detailed view of a guard cell chloroplast containing massive starch grains (black spots). (d) Mesophyll cell showing large chloroplasts (chl) with stroma and grana thylakoids in close contact with numerous mitochondria (m), indicating high photosynthetic activity.

• Date palm Phoenix dactylifera is a desert crop well adapted to survive and produce fruits under extreme drought and heat. How are palms under such harsh environmental conditions able to limit transpirational water loss?
• Here, we analysed the cuticular waxes, stomata structure and function, and molecular biology of guard cells from P. dactylifera.
• To understand the stomatal response to the water stress phytohormone of the desert plant, we cloned the major elements necessary for guard cell fast abscisic acid (ABA) signalling and reconstituted this ABA signalosome in Xenopus oocytes. The PhoenixSLAC1‐type anion channel is regulated by ABA kinase PdOST1. Energy‐dispersive X‐ray analysis (EDXA) demonstrated that date palm guard cells release chloride during stomatal closure. However, in Cl⁻ medium, PdOST1 did not activate the desert plant anion channel PdSLAC1 per se. Only when nitrate was present at the extracellular face of the anion channel did the OST1‐gated PdSLAC1 open, thus enabling chloride release. In the presence of nitrate, ABA enhanced and accelerated stomatal closure.
• Our findings indicate that, in date palm, the guard cell osmotic motor driving stomatal closure uses nitrate as the signal to open the major anion channel SLAC1. This initiates guard cell depolarization and the release of anions together with potassium.

Stomatal specific calcium sensitivity of high density and activity SV/TPC1 channels

 

 

Guard cell-specific calcium sensitivity of high density and activity SV/TPC1 channels

by Rienmüller F., Beyhl D., Lautner S., Fromm J., Al-Rasheid K. A. S., Ache P., Farmer E. E., Marten I., Hedrich R. (2010)

Florian Rienmüller 1 , Diana Beyhl 1 , Silke Lautner 2 , Jörg Fromm 2 , Khaled A. S. Al-Rasheid 3 , Peter Ache 1 , Edward E. Farmer 4 , Irene Marten 1, Rainer Hedrich 1

1 University of Wuerzburg, Institute for Molecular Plant Physiology and Biophysics, Julius-von-Sachs Platz 2, D-97082 Wuerzburg, Germany

2 University of Hamburg, Institute for Wood Biology, Leuschnerstr. 91, 21031 Hamburg, Germany

3 King Saud University, College of Science, Zoology Department, PO Box 2455, Riyadh 11451, Saudi Arabia

4 Gene Expression Laboratory, Plant Molecular Biology, University of Lausanne, CH-1015 Lausanne, Switzerland

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in Plant Cell Physiol. 51: 1548–1554 – doi: 10.1093/pcp/pcq102 –

https://www.ncbi.nlm.nih.gov/pubmed/20630987

Abstract

The slow vacuolar (SV) channel, a Ca2+-regulated vacuolar cation conductance channel, in Arabidopsis thaliana is encoded by the single-copy gene AtTPC1.

Although loss-of-function tpc1 mutants were reported to exhibit a stoma phenotype, knowledge about the underlying guard cell-specific features of SV/TPC1 channels is still lacking.

Here we demonstrate that TPC1 transcripts and SV current density in guard cells were much more pronounced than in mesophyll cells. Furthermore, the SV channel in motor cells exhibited a higher cytosolic Ca2+ sensitivity than in mesophyll cells.

These distinct features of the guard cell SV channel therefore probably account for the published stomatal phenotype of tpc1-2.

A tandem amino acid residue motif that within the SLAC1 channels differs fundamentally between monocots and dicots

Processes in a leaf pore (stoma) of grasses. When the leaves open and close, a shuttle service takes ions to and fro between guard cells and subsidiary cells.

Credit: Dietmar Geiger (https://www.sciencedaily.com/releases/2018/04/180427113245.htm)

 

A tandem amino acid residue motif in guard cell SLAC1 anion channel of grasses allows for the control of stomatal aperture by nitrate

by Schäfer N., Maierhofer T., Herrmann J., Jørgensen M. E., Lind C., von Meyer K., Lautner S., Fromm J., Felder M., Hetherington A. M., Ache P., Geiger D., Hedrich R. (2018)

Nadine Schäfer, Tobias Maierhofer, Johannes Herrmann, Morten Egevang Jørgensen, Christof Lind, Katharina von Meyer, Silke Lautner, Jörg Fromm, Marius Felder, Alistair M. Hetherington, Peter Ache, Dietmar Geiger, Rainer Hedrich,

University of Würzburg, Germany

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in Current Biology,26 April 2018 DOI: 10.1016/j.cub.2018.03.027 –

https://www.scoop.it/t/plant-hormones-by-julio-retamales/p/4097207899/2018/04/26/a-tandem-amino-acid-residue-motif-in-guard-cell-slac1-anion-channel-of-grasses-allows-for-the-control-of-stomatal-aperture-by-nitrate

https://www.cell.com/current-biology/abstract/S0960-9822(18)30356-7

Highlights:  

•Barley guard cells require nitrate for ABA-triggered fast stomatal closure

•Guard-cell-expressed barley anion channel HvSLAC1 is gated by extracellular nitrate

•Two residues on TMD3 of HvSLAC1 play a crucial role in nitrate-dependent gating

•Monocot SLAC1s developed nitrate-dependent gating after the split from dicots

Abstract:

“The latest major group of plants to evolve were the grasses. These became important in the mid-Paleogene about 40 million years ago. During evolution, leaf CO2 uptake and transpirational water loss were optimized by the acquisition of grass-specific stomatal complexes.

In contrast to the kidney-shaped guard cells (GCs) typical of the dicots such as Arabidopsis, in the grasses and agronomically important cereals, the GCs are dumbbell shaped and are associated with morphologically distinct subsidiary cells (SCs). We studied the molecular basis of GC action in the major cereal crop barley.

Upon feeding ABA to xylem sap of an intact barley leaf, stomata closed in a nitrate-dependent manner. This process was initiated by activation of GC SLAC-type anion channel currents. HvSLAC1 expressed in Xenopus oocytes gave rise to S-type anion currents that increased several-fold upon stimulation with >3 mM nitrate.

We identified a tandem amino acid residue motif that within the SLAC1 channels differs fundamentally between monocots and dicots. When the motif of nitrate-insensitive dicot Arabidopsis SLAC1 was replaced by the monocot signature, AtSLAC1 converted into a grass-type like nitrate-sensitive channel. Our work reveals a fundamental difference between monocot and dicot GCs and prompts questions into the selective pressures during evolution that resulted in fundamental changes in the regulation of SLAC1 function.”

Stomatal closure via nitrate-regulated SLAC1 anion channel

 

Photo credit: Google

Date palm

The desert plant Phoenix dactylifera closes stomata via nitrate-regulated SLAC1 anion channel

Müller H. M., Schäfer N., Bauer H., Geiger D., Lautner S., Fromm J., Riederer M., Bueno A., Nussbaumer T., Mayer K., Alquraishi S. A., Alfarhan A. H., Neher E., Al-Rasheid K. A. S., Ache P., Hedrich R. (2017)

Heike M. Müller, Nadine Schäfer, Hubert Bauer, Dietmar Geiger, Silke Lautner, Jörg Fromm, Markus Riederer, Amauri Bueno, Thomas Nussbaumer, Klaus Mayer, Saleh A. Alquraishi, Ahmed H. Alfarhan, Erwin Neher, Khaled A. S. Al-Rasheid, Peter Ache, Rainer Hedrich

in New Phytol. – DOI: 10.1111/nph.14672 – 

http://onlinelibrary.wiley.com/doi/10.1111/nph.14672/abstract;jsessionid=BD1807D23AC06ED98EACF0EDC014E1DF.f03t03

Summary

• Date palm Phoenix dactylifera is a desert crop well adapted to survive and produce fruits under extreme drought and heat. How are palms under such harsh environmental conditions able to limit transpirational water loss?
• Here, we analysed the cuticular waxes, stomata structure and function, and molecular biology of guard cells from P. dactylifera.
• To understand the stomatal response to the water stress phytohormone of the desert plant, we cloned the major elements necessary for guard cell fast abscisic acid (ABA) signalling and reconstituted this ABA signalosome in Xenopus oocytes. The PhoenixSLAC1-type anion channel is regulated by ABA kinase PdOST1. Energy-dispersive X-ray analysis (EDXA) demonstrated that date palm guard cells release chloride during stomatal closure. However, in Cl⁻ medium, PdOST1 did not activate the desert plant anion channel PdSLAC1 per se. Only when nitrate was present at the extracellular face of the anion channel did the OST1-gated PdSLAC1 open, thus enabling chloride release. In the presence of nitrate, ABA enhanced and accelerated stomatal closure.
• Our findings indicate that, in date palm, the guard cell osmotic motor driving stomatal closure uses nitrate as the signal to open the major anion channel SLAC1. This initiates guard cell depolarization and the release of anions together with potassium.

Ion channels within the maize stomata

 

Cell type-specific regulation of ion channels within the maize stomatal complex.

by Mumm P., Wolf T., Fromm J., Roelfsema M. R. G., Marten I. (2011)

1. Patrick Mumm
2. Thomas Wolf
3. Jörg Fromm
4. M. Rob G. Roelfsema
5. Irene Marten

in Plant and Cell Physiology 52 : 1365–1375. – doi: 10.1093/pcp/pcr082 –

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

http://pcp.oxfordjournals.org/content/52/8/1365

Abstract

The stomatal complex of Zea mays is composed of two pore-forming guard cells and two adjacent subsidiary cells.

For stomatal movement, potassium ions and anions are thought to shuttle between these two cell types. As potential cation transport pathways, K⁺-selective channels have already been identified and characterized in subsidiary cells and guard cells. However, so far the nature and regulation of anion channels in these cell types have remained unclear.

In order to bridge this gap, we performed patch–clamp experiments with subsidiary cell and guard cell protoplasts. Voltage-independent anion channels were identified in both cell types which, surprisingly, exhibited different, cell-type specific dependencies on cytosolic Ca²⁺ and pH. After impaling subsidiary cells of intact maize plants with microelectrodes and loading with

BCECF [(2′,7′-bis-(2-carboxyethyl)-5(and6)carboxyflurescein] as a fluorescent pH indicator, the regulation of ion channels by the cytosolic pH and the membrane voltage was further examined.

Stomatal closure was found to be accompanied by an initial hyperpolarization and cytosolic acidification of subsidiary cells, while opposite responses were observed during stomatal opening.

Our findings suggest that specific changes in membrane potential and cytosolic pH are likely to play a role in determining the direction and capacity of ion transport in subsidiary cells.

A role for ABA in regulating stomatal development

Photo credit: Plant Physiology

Typical stomata in wild-type (wt), ABI1, and abi1 poplars (leaf tissue double stained with anilin blue and safranin; bar 10 μm)

Expression of the Arabidopsis Mutant abi1 Gene Alters Abscisic Acid Sensitivity, Stomatal Development, and Growth Morphology in Gray Poplars

by Arend M., Schnitzler J.-P., Ehlting B., Hänsch R., Lange T., Rennenberg H., Himmelbach A., Grill E., Fromm J. (2009)

Matthias Arend, Jörg-Peter Schnitzler, Barbara Ehlting, Robert Hänsch, Theo Lange, Heinz Rennenberg, Axel Himmelbach, Erwin Grill, Jörg Fromm

in Plant Physiology December 2009 vol. 151 no. 4 2110-2119

ABSTRACT

The consequences of altered abscisic acid (ABA) sensitivity in gray poplar (Populus x canescens [Ait.] Sm.) development were examined by ectopic expression of the Arabidopsis (Arabidopsis thaliana) mutant abi1 (for abscisic acid insensitive1) gene. The expression resulted in an ABA-insensitive phenotype revealed by a strong tendency of abi1 poplars to wilt, impaired responsiveness of their stomata to ABA, and an ABA-resistant bud outgrowth. These plants therefore required cultivation under very humid conditions to prevent drought stress symptoms. Morphological alterations became evident when comparing abi1 poplars with poplars expressing Arabidopsis nonmutant ABI1 or wild-type plants. abi1 poplars showed increased stomatal size, enhanced shoot growth, and retarded leaf and root development. The increased stomatal size and its reversion to the size of wild-type plants by exogenous ABA indicate a role for ABA in regulating stomatal development. Enhanced shoot growth and retarded leaf and root development support the hypothesis that ABA acts independently from drought stress as a negative regulator of growth in shoots and as a positive regulator of growth in leaves and roots. In shoots, we observed an interaction of ABA with ethylene: abi1 poplars exhibited elevated ethylene production, and the ethylene perception inhibitor Ag+ antagonized the enhanced shoot growth. Thus, we provide evidence that ABA acts as negative regulator of shoot growth in nonstressed poplars by restricting ethylene production. Furthermore, we show that ABA has a role in regulating shoot branching by inhibiting lateral bud outgrowth.