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 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 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.

Reactive Carbonyl Species Mediate Methyl Jasmonate-Induced Stomatal Closure

2020 ◽  
Vol 61 (10) ◽  
pp. 1788-1797
Author(s):  
Md. Moshiul Islam ◽  
Wenxiu Ye ◽  
Fahmida Akter ◽  
Mohammad Saidur Rhaman ◽  
Daiki Matsushima ◽  
...  
Keyword(s):  
Methyl Jasmonate ◽  
Stomatal Closure ◽  
Guard Cells ◽  
H2o2 Production ◽  
Aba Signaling ◽  
Tobacco Plants ◽  
Reactive Carbonyl Species ◽  
In The Wild ◽  
Carbonyl Species ◽  
Reactive Carbonyl

Abstract Production of reactive oxygen species (ROS) is a key signal event for methyl jasmonate (MeJA)- and abscisic acid (ABA)-induced stomatal closure. We recently showed that reactive carbonyl species (RCS) stimulates stomatal closure as an intermediate downstream of hydrogen peroxide (H2O2) production in the ABA signaling pathway in guard cells of Nicotiana tabacum and Arabidopsis thaliana. In this study, we examined whether RCS functions as an intermediate downstream of H2O2 production in MeJA signaling in guard cells using transgenic tobacco plants overexpressing A. thaliana 2-alkenal reductase (n-alkanal + NAD(P)+ ⇌ 2-alkenal + NAD(P)H + H+) (AER-OE tobacco) and Arabidopsis plants. The stomatal closure induced by MeJA was impaired in the AER-OE tobacco and was inhibited by RCS scavengers, carnosine and pyridoxamine, in the wild-type (WT) tobacco plants and Arabidopsis plants. Application of MeJA significantly induced the accumulation of RCS, including acrolein and 4-hydroxy-(E)-2-nonenal, in the WT tobacco but not in the AER-OE plants. Application of MeJA induced H2O2 production in the WT tobacco and the AER-OE plants and the H2O2 production was not inhibited by the RCS scavengers. These results suggest that RCS functions as an intermediate downstream of ROS production in MeJA signaling and in ABA signaling in guard cells.

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 Molecular basis for the R-type anion channel QUAC1 activity in guard cells

2021 ◽  
Author(s):  
Li Qin ◽  
Ling-hui Tang ◽  
Jia-shu Xu ◽  
Xian-hui Zhang ◽  
Yun Zhu ◽  
...  
Keyword(s):  
Molecular Basis ◽  
Stomatal Closure ◽  
Anion Channel ◽  
Guard Cells ◽  
Channel Activity ◽  
Cytoplasmic Domains ◽  
Anion Channels ◽  
Channel Activation ◽  
Environmental Stimuli ◽  
Functional Analyses

SUMMARYThe rapid (R)-type anion channel plays a central role in controlling stomatal closure in plant guard cells, thus regulating the exchange of water and photosynthetic gas (CO2) in response to environmental stimuli. The activity of the R- type anion channel is regulated by malate. However, the molecular basis of the R-type anion channel activity remains elusive. Here, we describe the first cryo-EM structure of the R-type anion channel QUAC1 at 3.5 Å resolution in the presence of malate. The structure reveals that the QUAC1 is a symmetrical dimer, forming a single electropositive T-shaped pore for passing anions across the membrane. The transmembrane and cytoplasmic domains are assembled into a twisted bi-layer architecture, with the associated dimeric interfaces nearly perpendicular. Our structural and functional analyses reveal that QUAC1 functions as an inward rectifying anion channel and suggests a mechanism for malate-mediated channel activation. Altogether, our study uncovers the molecular basis for a novel class of anion channels and provides insights into the gating and modulation of the R-type anion channel.

scholarly journals Guard Cell Membrane Anion Transport Systems and Their Regulatory Components: An Elaborate Mechanism Controlling Stress-Induced Stomatal Closure

Plants ◽  
2019 ◽  
Vol 8 (1) ◽  
pp. 9 ◽  
Author(s):  
Shunya Saito ◽  
Nobuyuki Uozumi
Keyword(s):  
Guard Cell ◽  
Chloride Channels ◽  
Environmental Changes ◽  
Stomatal Closure ◽  
Ion Homeostasis ◽  
Transport Systems ◽  
Bacterial Invasion ◽  
Anion Channels ◽  
Regulation Network ◽  
Membrane Transport Systems

When plants are exposed to drastic environmental changes such as drought, salt or bacterial invasion, rapid stomatal movement confers tolerance to these stresses. This process involves a variety of guard cell expressed ion channels and their complex regulation network. Inward K+ channels mainly function in stomatal opening. On the other hand, guard cell anion channels play a crucial role in the closing of stomata, which is vital in terms of preventing water loss and bacterial entrance. Massive progress has been made on the research of these anion channels in the last decade. In this review, we focus on the function and regulation of Arabidopsis guard cell anion channels. Starting from SLAC1, a main contributor of stomatal closure, members of SLAHs (SLAC1 homologues), AtNRTs (Nitrate transporters), AtALMTs (Aluminum-activated malate transporters), ABC transporters, AtCLCs (Chloride channels), DTXs (Detoxification efflux carriers), SULTRs (Sulfate transporters), and their regulator components are reviewed. These membrane transport systems are the keys to maintaining cellular ion homeostasis against fluctuating external circumstances.

scholarly journals Abscisic acid-independent stomatal CO2 signal transduction pathway and convergence of CO2 and ABA signaling downstream of OST1 kinase

2018 ◽  
Vol 115 (42) ◽  
pp. E9971-E9980 ◽  
Author(s):  
Po-Kai Hsu ◽  
Yohei Takahashi ◽  
Shintaro Munemasa ◽  
Ebe Merilo ◽  
Kristiina Laanemets ◽  
...  
Keyword(s):  
Signal Transduction ◽  
Abscisic Acid ◽  
Protein Kinase ◽  
Stomatal Closure ◽  
Signal Transduction Pathway ◽  
Guard Cells ◽  
Aba Signaling ◽  
Time Resolved ◽  
Aba Receptor ◽  
Biochemical Analyses

Stomatal pore apertures are narrowing globally due to the continuing rise in atmospheric [CO2]. CO2 elevation and the plant hormone abscisic acid (ABA) both induce rapid stomatal closure. However, the underlying signal transduction mechanisms for CO2/ABA interaction remain unclear. Two models have been considered: (i) CO2 elevation enhances ABA concentrations and/or early ABA signaling in guard cells to induce stomatal closure and (ii) CO2 signaling merges with ABA at OST1/SnRK2.6 protein kinase activation. Here we use genetics, ABA-reporter imaging, stomatal conductance, patch clamp, and biochemical analyses to investigate these models. The strong ABA biosynthesis mutants nced3/nced5 and aba2-1 remain responsive to CO2 elevation. Rapid CO2-triggered stomatal closure in PYR/RCAR ABA receptor quadruple and hextuple mutants is not disrupted but delayed. Time-resolved ABA concentration monitoring in guard cells using a FRET-based ABA-reporter, ABAleon2.15, and ABA reporter gene assays suggest that CO2 elevation does not trigger [ABA] increases in guard cells, in contrast to control ABA exposures. Moreover, CO2 activates guard cell S-type anion channels in nced3/nced5 and ABA receptor hextuple mutants. Unexpectedly, in-gel protein kinase assays show that unlike ABA, elevated CO2 does not activate OST1/SnRK2 kinases in guard cells. The present study points to a model in which rapid CO2 signal transduction leading to stomatal closure occurs via an ABA-independent pathway downstream of OST1/SnRK2.6. Basal ABA signaling and OST1/SnRK2 activity are required to facilitate the stomatal response to elevated CO2. These findings provide insights into the interaction between CO2/ABA signal transduction in light of the continuing rise in atmospheric [CO2].

scholarly journals Transcriptional Regulation of Protein Phosphatase 2C Genes to Modulate Abscisic Acid Signaling

2020 ◽  
Vol 21 (24) ◽  
pp. 9517
Author(s):  
Choonkyun Jung ◽  
Nguyen Hoai Nguyen ◽  
Jong-Joo Cheong
Keyword(s):  
Abscisic Acid ◽  
Osmotic Stress ◽  
Gene Transcription ◽  
Stomatal Closure ◽  
Guard Cells ◽  
Stress Conditions ◽  
Physical Interaction ◽  
Aba Signaling ◽  
Negative Feedback Regulation ◽  
Pp2c Gene

The plant hormone abscisic acid (ABA) triggers cellular tolerance responses to osmotic stress caused by drought and salinity. ABA controls the turgor pressure of guard cells in the plant epidermis, leading to stomatal closure to minimize water loss. However, stomatal apertures open to uptake CO2 for photosynthesis even under stress conditions. ABA modulates its signaling pathway via negative feedback regulation to maintain plant homeostasis. In the nuclei of guard cells, the clade A type 2C protein phosphatases (PP2Cs) counteract SnRK2 kinases by physical interaction, and thereby inhibit activation of the transcription factors that mediate ABA-responsive gene expression. Under osmotic stress conditions, PP2Cs bind to soluble ABA receptors to capture ABA and release active SnRK2s. Thus, PP2Cs function as a switch at the center of the ABA signaling network. ABA induces the expression of genes encoding repressors or activators of PP2C gene transcription. These regulators mediate the conversion of PP2C chromatins from a repressive to an active state for gene transcription. The stress-induced chromatin remodeling states of ABA-responsive genes could be memorized and transmitted to plant progeny; i.e., transgenerational epigenetic inheritance. This review focuses on the mechanism by which PP2C gene transcription modulates ABA signaling.

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