scholarly journals Gaining or cutting SLAC: the evolution of plant guard cell signalling pathways

2021 ◽  
Author(s):  
Frances C Sussmilch ◽  
Tobias Maierhofer ◽  
Johannes Herrmann ◽  
Lena J Voss ◽  
Christof Lind ◽  
...  
Keyword(s):  
Guard Cell ◽  
Stomatal Closure ◽  
Cell Signalling ◽  
Guard Cells ◽  
Land Plant ◽  
Signalling Pathways ◽  
Anion Channels ◽  
Plant Groups ◽  
Activation Mechanisms ◽  
Stomatal Movements

The evolution of adjustable plant pores (stomata), enabling CO2 acquisition in cuticle wax-sealed tissues was one of the most significant events in the development of life on land. But how did the guard cell signalling pathways that regulate stomatal movements evolve? We investigate this through comparison of fern and angiosperm guard cell transcriptomes. We find that these divergent plant groups share expression of similar genes in guard cells including biosynthesis and signalling genes for the drought stress hormone abscisic acid (ABA). However, despite conserved expression in guard cells, S-type anion channels from the SLAC/SLAH family — known for ABA-mediated stomatal closure in angiosperms — are not activated by the same pathways in ferns, highlighting likely differences in functionality. Examination of other land plant channels revealed a complex evolutionary history, featuring multiple gains or losses of SLAC activation mechanisms, as these channels were recruited to a role in stomatal closure. Taken together, the guard cells of flowering and non-flowering plants share similar core features, but also show lineage-specific and ecological niche-related adaptations, likely underlying differences in behaviour.

scholarly journals Optogenetic control of the guard cell membrane potential and stomatal movement by the light-gated anion channel GtACR1

2021 ◽  
Vol 7 (28) ◽  
pp. eabg4619
Author(s):  
Shouguang Huang ◽  
Meiqi Ding ◽  
M. Rob G. Roelfsema ◽  
Ingo Dreyer ◽  
Sönke Scherzer ◽  
...  
Keyword(s):  
Guard Cell ◽  
Stomatal Closure ◽  
Green Light ◽  
Anion Channel ◽  
Guard Cells ◽  
Wild Type ◽  
Anion Channels ◽  
Light Pulses ◽  
Cell Turgor ◽  
Open Question

Guard cells control the aperture of plant stomata, which are crucial for global fluxes of CO2 and water. In turn, guard cell anion channels are seen as key players for stomatal closure, but is activation of these channels sufficient to limit plant water loss? To answer this open question, we used an optogenetic approach based on the light-gated anion channelrhodopsin 1 (GtACR1). In tobacco guard cells that express GtACR1, blue- and green-light pulses elicit Cl− and NO3− currents of −1 to −2 nA. The anion currents depolarize the plasma membrane by 60 to 80 mV, which causes opening of voltage-gated K+ channels and the extrusion of K+. As a result, continuous stimulation with green light leads to loss of guard cell turgor and closure of stomata at conditions that provoke stomatal opening in wild type. GtACR1 optogenetics thus provides unequivocal evidence that opening of anion channels is sufficient to close stomata.

scholarly journals Identification of SLAC1 anion channel residues required for CO2/bicarbonate sensing and regulation of stomatal movements

2018 ◽  
Vol 115 (44) ◽  
pp. 11129-11137 ◽  
Author(s):  
Jingbo Zhang ◽  
Nuo Wang ◽  
Yinglong Miao ◽  
Felix Hauser ◽  
J. Andrew McCammon ◽  
...  
Keyword(s):  
Stomatal Closure ◽  
Anion Channel ◽  
Guard Cells ◽  
Channel Activity ◽  
Plant Leaves ◽  
In Planta ◽  
Anion Channels ◽  
Accelerated Molecular Dynamics ◽  
Bicarbonate Ions ◽  
Stomatal Movements

Increases in CO2 concentration in plant leaves due to respiration in the dark and the continuing atmospheric [CO2] rise cause closing of stomatal pores, thus affecting plant–water relations globally. However, the underlying CO2/bicarbonate (CO2/HCO3−) sensing mechanisms remain unknown. [CO2] elevation in leaves triggers stomatal closure by anion efflux mediated via the SLAC1 anion channel localized in the plasma membrane of guard cells. Previous reconstitution analysis has suggested that intracellular bicarbonate ions might directly up-regulate SLAC1 channel activity. However, whether such a CO2/HCO3− regulation of SLAC1 is relevant for CO2 control of stomatal movements in planta remains unknown. Here, we computationally probe for candidate bicarbonate-interacting sites within the SLAC1 anion channel via long-timescale Gaussian accelerated molecular dynamics (GaMD) simulations. Mutations of two putative bicarbonate-interacting residues, R256 and R321, impaired the enhancement of the SLAC1 anion channel activity by CO2/HCO3− in Xenopus oocytes. Mutations of the neighboring charged amino acid K255 and residue R432 and the predicted gate residue F450 did not affect HCO3− regulation of SLAC1. Notably, gas-exchange experiments with slac1-transformed plants expressing mutated SLAC1 proteins revealed that the SLAC1 residue R256 is required for CO2 regulation of stomatal movements in planta, but not for abscisic acid (ABA)-induced stomatal closing. Patch clamp analyses of guard cells show that activation of S-type anion channels by CO2/HCO3−, but not by ABA, was impaired, indicating the relevance of R256 for CO2 signal transduction. Together, these analyses suggest that the SLAC1 anion channel is one of the physiologically relevant CO2/HCO3− sensors in guard cells.

scholarly journals Eukaryotic lipid metabolic pathway is essential for functional chloroplasts and CO2 and light responses in Arabidopsis guard cells

2018 ◽  
Vol 115 (36) ◽  
pp. 9038-9043 ◽  
Author(s):  
Juntaro Negi ◽  
Shintaro Munemasa ◽  
Boseok Song ◽  
Ryosuke Tadakuma ◽  
Mayumi Fujita ◽  
...  
Keyword(s):  
Metabolic Pathway ◽  
Guard Cell ◽  
Membrane Lipids ◽  
Stomatal Closure ◽  
Guard Cells ◽  
Land Plant ◽  
In The Wild ◽  
Stomatal Guard Cells ◽  
Guard Cell Chloroplasts ◽  
And Function

Stomatal guard cells develop unique chloroplasts in land plant species. However, the developmental mechanisms and function of chloroplasts in guard cells remain unclear. In seed plants, chloroplast membrane lipids are synthesized via two pathways: the prokaryotic and eukaryotic pathways. Here we report the central contribution of endoplasmic reticulum (ER)-derived chloroplast lipids, which are synthesized through the eukaryotic lipid metabolic pathway, in the development of functional guard cell chloroplasts. We gained insight into this pathway by isolating and examining an Arabidopsis mutant, gles1 (green less stomata 1), which had achlorophyllous stomatal guard cells and impaired stomatal responses to CO2 and light. The GLES1 gene encodes a small glycine-rich protein, which is a putative regulatory component of the trigalactosyldiacylglycerol (TGD) protein complex that mediates ER-to-chloroplast lipid transport via the eukaryotic pathway. Lipidomic analysis revealed that in the wild type, the prokaryotic pathway is dysfunctional, specifically in guard cells, whereas in gles1 guard cells, the eukaryotic pathway is also abrogated. CO2-induced stomatal closing and activation of guard cell S-type anion channels that drive stomatal closure were disrupted in gles1 guard cells. In conclusion, the eukaryotic lipid pathway plays an essential role in the development of a sensing/signaling machinery for CO2 and light in guard cell chloroplasts.

scholarly journals Concentration matters: different stomatal CO2-responses at sub-ambient and above-ambient CO2 levels

2021 ◽  
Author(s):  
Hanna Hõrak ◽  
Kaspar Koolmeister ◽  
Ebe Merilo ◽  
Hannes Kollist
Keyword(s):  
Guard Cell ◽  
Stomatal Closure ◽  
Cell Signalling ◽  
Anion Channel ◽  
Leaf Temperature ◽  
Signalling Pathways ◽  
Stomatal Responses ◽  
Slow Type ◽  
Ambient Concentrations ◽  
Ambient Co2

Stomatal pores, formed of paired guard cells, mediate CO2 uptake for photosynthesis and water loss via transpiration in plants. Globally rising atmospheric CO2 concentration triggers stomatal closure, contributing to increased leaf temperature and reduced nutrient uptake due to lower transpiration rate. Hence, it is important to understand the signalling pathways that control elevated CO2-induced stomatal closure to identify targets for breeding climate-ready crops. CO2-induced stomatal closure can be studied by increasing CO2 concentration from ambient to above-ambient concentrations, or elevation of CO2 levels from sub-ambient to above-ambient. Previous experiments comparing ferns with angiosperms suggested that stomatal responses to CO2 may be different, when changing CO2 levels in the sub-ambient or above-ambient ranges. Here, we set out to test this by comparing CO2-induced stomatal closure in key guard cell signalling mutants in response to CO2 elevation from 100 to 400 ppm or 400 to 800 ppm. We show that signalling components that contribute to CO2-induced stomatal closure are different in the sub-ambient and above-ambient CO2 levels, with guard cell slow-type anion channel SLAC1 involved mainly in above-ambient CO2-induced stomatal closure.

scholarly journals Ethylene Inhibits Methyl Jasmonate-Induced Stomatal Closure by Modulating Guard Cell Slow-Type Anion Channel Activity via the OPEN STOMATA 1/SnRK2.6 Kinase-Independent Pathway in Arabidopsis

2019 ◽  
Vol 60 (10) ◽  
pp. 2263-2271 ◽  
Author(s):  
Shintaro Munemasa ◽  
Yukari Hirao ◽  
Kasumi Tanami ◽  
Yoshiharu Mimata ◽  
Yoshimasa Nakamura ◽  
...  
Keyword(s):  
Methyl Jasmonate ◽  
Guard Cell ◽  
Stomatal Closure ◽  
Guard Cells ◽  
Defense Responses ◽  
Ros Production ◽  
Ethylene Signaling ◽  
Aba Signaling ◽  
Anion Channels ◽  
Signal Crosstalk

Abstract Signal crosstalk between jasmonate and ethylene is crucial for a proper maintenance of defense responses and development. Although previous studies reported that both jasmonate and ethylene also function as modulators of stomatal movements, the signal crosstalk mechanism in stomatal guard cells remains unclear. Here, we show that the ethylene signaling inhibits jasmonate signaling as well as abscisic acid (ABA) signaling in guard cells of Arabidopsis thaliana and reveal the signaling crosstalk mechanism. Both an ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) and an ethylene-releasing compound ethephon induced transient stomatal closure, and also inhibited methyl jasmonate (MeJA)-induced stomatal closure as well as ABA-induced stomatal closure. The ethylene inhibition of MeJA-induced stomatal closure was abolished in the ethylene-insensitive mutant etr1–1, whereas MeJA-induced stomatal closure was impaired in the ethylene-overproducing mutant eto1–1. Pretreatment with ACC inhibited MeJA-induced reactive oxygen species (ROS) production as well as ABA-induced ROS production in guard cells but did not suppress ABA activation of OPEN STOMATA 1 (OST1) kinase in guard cell-enriched epidermal peels. The whole-cell patch-clamp analysis revealed that ACC attenuated MeJA and ABA activation of S-type anion channels in guard cell protoplasts. However, MeJA and ABA inhibitions of Kin channels were not affected by ACC pretreatment. These results suggest that ethylene signaling inhibits MeJA signaling and ABA signaling by targeting S-type anion channels and ROS but not OST1 kinase and K+ channels in Arabidopsis guard cells.

scholarly journals The role of strigolactones in regulation of stomatal conductance and plant-pathogen interactions inArabidopsis thaliana

2019 ◽  
Author(s):  
Maria Kalliola ◽  
Liina Jakobson ◽  
Pär Davidsson ◽  
Ville Pennanen ◽  
Cezary Waszczak ◽  
...  
Keyword(s):  
Gene Expression ◽  
Stomatal Conductance ◽  
Pseudomonas Syringae ◽  
Guard Cell ◽  
Stomatal Closure ◽  
Cell Signalling ◽  
Guard Cells ◽  
Signalling Pathway ◽  
Ozone Sensitivity

AbstractStrigolactones are a group of phytohormones that control shoot branching inArabidopsis thaliana. However, in recent years they have been shown to affect many other plant processes. We previously showed that the strigolactone perception mutantmore axillary branches 2 (max2)has increased susceptibility to plant pathogenic bacteria as a result of more open stomata as well as alterations in hormonal signalling. Here we show that both, strigolactone biosynthesis- (max3andmax4), and perception mutants (max2anddwarf14) are significantly more sensitive toPseudomonas syringaeDC3000. Moreover, in response toP. syringaeinfection, high levels of SA accumulated inmax2and this mutant was ozone sensitive. To search for the mechanisms that could explain pathogen- and ozone sensitivity we performed gene expression analysis and several different assays that explore the function of guard cells and regulation of guard cell signalling.Treatments with GR24 (a strigolactone analogue) resulted in very modest changes in defence-related gene expression. In contrast, guard cell function was clearly impaired inmax2and depending on the assay used, also inmax3, max4andd14mutants. Moreover, stomatal responses to stimuli that cause stomatal closure in wild-type plants (darkness, high CO2and ABA) were analysed in the strigolactone mutants. In darkness both strigolactone biosynthesis and perception mutants showed reduced stomatal closure, whereas the response to high CO2was impaired only inmax2andd14. The response to ABA was not impaired in any of the mutants. To position the role of MAX2 in the guard cell signalling network,max2was crossed with mutants defective in ABA biosynthesis (aba2), in guard cell ABA signalling (ost1) and a scaffold protein required for proper ion channel activity (ghr1). The stomatal conductance of double mutants was consistently higher than the corresponding single mutants, suggesting that MAX2 acts in a signalling pathway that functions in parallel to the well characterized guard cell ABA signalling pathway. We propose that the impaired defence responses ofmax2is related to more open stomata that allows increased entry of bacteria or air pollutants like ozone. Furthermore, as MAX2 appears to act in a specific branch of guard cell signalling (related to CO2signalling), this protein could be one of the elusive components that allow guard cells to distinguish between different environmental conditions.

Modulation of frequency and height of cytosolic calcium spikes by plasma membrane anion channels in guard cells

2021 ◽  
Author(s):  
Md Tahjib-Ul-Arif ◽  
Shintaro Munemasa ◽  
Toshiyuki Nakamura ◽  
Yoshimasa Nakamura ◽  
Yoshiyuki Murata
Keyword(s):  
Plasma Membrane ◽  
Stomatal Closure ◽  
Anion Channel ◽  
Guard Cells ◽  
Cytosolic Calcium ◽  
Peak Height ◽  
Extracellular Calcium ◽  
Wild Type ◽  
Anion Channels ◽  
In The Wild

Abstract Cytosolic calcium ([Ca2+]cyt) elevation activates plasma membrane anion channels in guard cells, which is required for stomatal closure. However, involvement of the anion channels in the [Ca2+]cyt elevation remains unclear. We investigated the involvement using Arabidopsis thaliana anion channel mutants, slac1-4 slah3-3 and slac1-4 almt12-1. Extracellular calcium induced stomatal closure in the wild-type plants but not in the anion channel mutant plants whereas extracellular calcium induced [Ca2+]cyt elevation both in the wild-type guard cells and in the mutant guard cells. The peak height and the number of the [Ca2+]cyt spike were lower and larger in the slac1-4 slah3-3 than in the wild-type and the height and the number in the slac1-4 almt12-1 were much lower and much larger than in the wild-type. These results suggest that the anion channels are involved in the regulation of [Ca2+]cyt elevation in guard cells.

scholarly journals Secreted Peptide PIP1 Induces Stomatal Closure by Activation of Guard Cell Anion Channels in Arabidopsis

2020 ◽  
Vol 11 ◽  
Author(s):  
Jianlin Shen ◽  
Wenzhu Diao ◽  
Linfang Zhang ◽  
Biswa R. Acharya ◽  
Mei Wang ◽  
...  
Keyword(s):  
Guard Cell ◽  
Stomatal Closure ◽  
Anion Channels

scholarly journals Downregulating VAC14 in Guard Cells Causes Drought Hypersensitivity by Inhibiting Stomatal Closure

2020 ◽  
Vol 11 ◽  
Author(s):  
Zong-Qi Wang ◽  
Qi Liu ◽  
Ju-Hua Wu ◽  
Juan Li ◽  
Jun-Min He ◽  
...  
Keyword(s):  
Stomatal Closure ◽  
Guard Cells ◽  
Land Plant ◽  
Scaffolding Protein ◽  
Stomatal Movement ◽  
Wild Type ◽  
Physiological Factors ◽  
Surrounding Environment ◽  
Intracellular Activities

Stomata are a key land plant innovation that permit the regulation of gaseous exchanges between the plant interior and the surrounding environment. By opening or closing, stomata regulate transpiration of water though the plant; and these actions are coordinated with acquisition of CO2 for photosynthesis. Stomatal movement is controlled by various environmental and physiological factors and associates with multiple intracellular activities, among which the dynamic remodeling of vacuoles plays a crucial role. Phosphatidylinositol 3,5-bisphosphate [PI(3,5)P2] is critical for dynamic remodeling of vacuoles. Its production requires a PI(3,5)P2-metabolizing complex consisting of FAB1/PIKfyve kinases, SAC phosphatases, and the scaffolding protein VAC14. Although genetic or pharmacological downregulation of PI(3,5)P2 causes hyposensitivity to ABA-induced stomatal closure, whether the effect of PI(3,5)P2 on stomatal movement is cell-autonomous and the physiological consequences of its reduction were unclear. We report that downregulating Arabidopsis VAC14 specifically in guard cells by artificial microRNAs (amiR-VAC14) results in enlarged guard cells and hyposensitivity to ABA- and dark-induced stomatal closure. Vacuolar fission during stomatal closure is compromised by downregulating VAC14 in guard cells. Exogenous application of PI(3,5)P2 rescued the amiR-VAC14 phenotype whereas PI(3,5)P2 inhibitor YM201636 caused wild-type plants to have inhibited stomatal closure. We further show that downregulating VAC14 specifically in guard cells impairs drought tolerance, suggestive of a key role of guard cell-produced PI(3,5)P2 in plant fitness.

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