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Phosphorylation of two Thr residues in the C-terminal auto-inhibitory domain of plasma membrane H+-ATPase is crucial for light-induced stomatal opening

ABSTRACT: Plasma membrane H+-ATPase provides the driving force for light-induced stomatal opening. However, the mechanisms underlying the regulation of its activity remain unclear. Here, we showed that the phosphorylation of two Thr residues in the C-terminal autoinhibitory domain is crucial for H+-ATPase activation and stomatal opening. Our phosphoproteome analysis revealed that blue light induces the phosphorylation of Thr-881 within the C-terminal region I domain and penultimate Thr-948 in AUTOINHIBITED H+-ATPASE 1 (AHA1). The site-directed mutagenesis showed that both Thr phosphorylations are essential for H+ pumping and stomatal opening in response to blue light. The phosphorylation of Thr-948 is a prerequisite for the phosphorylation of Thr-881 by blue light. Furthermore, red-light-driven guard cell photosynthesis also caused Thr-881 phosphorylation, possibly contributing to red-light-dependent stomatal opening. Taken together, our findings provide mechanistic insights into H+-ATPase activation that exploits the ion transport across the plasma membrane and light signalling network in guard cells.

ORGANISM(S): Arabidopsis Thaliana (mouse-ear Cress)

SUBMITTER: Atsushi Takemiya

PROVIDER: PXD039740 | JPOST Repository | Mon Dec 25 00:00:00 GMT 2023

REPOSITORIES: jPOST

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Phosphorylation of two Thr residues in the C-terminal auto-inhibitory domain of plasma membrane H+-ATPase is crucial for light-induced stomatal opening-2

Project description:	Plasma membrane H+-ATPase provides the driving force for light-induced stomatal opening. However, the mechanisms underlying the regulation of its activity remain unclear. Here, we showed that the phosphorylation of two Thr residues in the C-terminal autoinhibitory domain is crucial for H+-ATPase activation and stomatal opening. Our phosphoproteome analysis revealed that blue light induces the phosphorylation of Thr-881 within the C-terminal region I domain and penultimate Thr-948 in AUTOINHIBITED H+-ATPASE 1 (AHA1). The site-directed mutagenesis showed that both Thr phosphorylations are essential for H+ pumping and stomatal opening in response to blue light. The phosphorylation of Thr-948 is a prerequisite for the phosphorylation of Thr-881 by blue light. Furthermore, red-light-driven guard cell photosynthesis also caused Thr-881 phosphorylation, possibly contributing to red-light-dependent stomatal opening. Taken together, our findings provide mechanistic insights into H+-ATPase activation that exploits the ion transport across the plasma membrane and light signalling network in guard cells.

2023-12-25 | PXD044476 | JPOST Repository

Metabolomics of red-light-induced stomatal opening in Arabidopsis thaliana: Coupling with abscisic acid and jasmonic acid metabolism

Project description:Environmental stimuli-triggered stomatal movement is a key physiological process that regulates CO2 uptake and water loss in plants. Stomata are defined by pairs of guard cells that perceive and transduce external signals, leading to cellular volume changes and consequent stomatal aperture change. Within the visible light spectrum, red light induces stomatal opening in intact leaves. However, there has been debate regarding the extent to which red-light-induced stomatal opening arises from direct guard cell sensing of red light versus indirect responses as a result of red light influences on mesophyll photosynthesis. Here we identify conditions that result in red-light-stimulated stomatal opening in isolated epidermal peels and enlargement of protoplasts, firmly establishing a direct guard cell response to red light. We then employ metabolomics workflows utilizing gas chromatography mass spectrometry and liquid chromatography mass spectrometry for metabolite profiling and identification of Arabidopsis guard cell metabolic signatures in response to red light in the absence of the mesophyll. We quantified 223 metabolites in Arabidopsis guard cells, with 104 found to be red light responsive. These red-light-modulated metabolites participate in the tricarboxylic acid cycle, carbon balance, phytohormone biosynthesis and redox homeostasis. We next analyzed selected Arabidopsis mutants, and discovered that stomatal opening response to red light is correlated with a decrease in guard cell abscisic acid content and an increase in jasmonic acid content. The red-light-modulated guard cell metabolome reported here provides fundamental information concerning autonomous red light signaling pathways in guard cells.

2022-01-21 | MTBLS1326 | MetaboLights

bHLH transcription factors facilitating K+ uptake during stomatal opening are repressed by abscisic acid through phosphorylation

Project description:Stomata open in response to light and close following exposure to abscisic acid (ABA). They regulate gas exchange between plants and atmosphere, allowing plants to adapt to changing environmental conditions. ABA binding to receptors initiates a signaling cascade that involves protein phosphorylation. Here we show that ABA induced phosphorylation of three basic helix-loop-helix (bHLH) transcription factors, called AKSs (ABA-RESPONSIVE KINASE SUBSTRATES; AKS1, AKS2, AKS3), in Arabidopsis guard cells, and that they facilitated stomatal opening through the transcription of genes encoding inwardly-rectifying K+ channels. aks1aks2-1 double mutant plants showed decreases in light-induced stomatal opening, K+ accumulation in response to light, activity of inwardly-rectifying K+ channels, and transcription of genes encoding major inwardly-rectifying K+ channels. Overexpression of POTASSIUM CHANNEL IN ARABIDOPSIS THALIANA 1 (KAT1), which encodes a major inwardly-rectifying K+ channel in guard cells, rescued the phenotype of aks1aks2-1 plants. AKS1 bound directly to the promoter of KAT1, an interaction that was attenuated after ABA-induced phosphorylation. The ABA agonist pyrabactin induced phosphorylation of AKSs. Our results demonstrate that the AKS family of bHLH transcription factors facilitates stomatal opening through transcription of genes encoding inwardly-rectifying K+ channels, and that ABA suppresses the activity of inwardly-rectifying K+ channel activity by triggering the phosphorylation of these transcription factors. To find the affect of AKS1 and AKS2 transcription factors on gene expression, Arabidopsis guard cell protoplasts from wild type and aks1aks2-1 mutant were compared. Three independent experiments were performed.

2013-06-17 | E-GEOD-46574 | biostudies-arrayexpress

bHLH transcription factors facilitating K+ uptake during stomatal opening are repressed by abscisic acid through phosphorylation

2013-06-17 | GSE46574 | GEO

Microarray analysis of scap1 mutant and wild type in Arabidopsis thaliana guard cell protoplast

Project description:Stomata are highly specialized organs which consist of pairs of guard cells and regulate gas and water vapor exchange in plants. While early stages of guard cell differentiation have been described and were interpreted in analogy to processes of cell type differentiation in animals, the downstream development of functional stomatal guard cells remains poorly understood. We have isolated an Arabidopsis mutant, scap1 (stomatal carpenter 1), that develops irregularly shaped guard cells and lacks the ability to control stomatal aperture, including CO2-induced stomatal closing and light-induced stomatal opening. SCAP1 was identified as a plant-specific Dof-type transcription factor expressed in maturing guard cells but not in guard mother cells. SCAP1 regulates the expression of genes encoding key elements of stomatal functioning and morphogenesis, such as a K+ channel protein, MYB60 transcription factor, and pectin methyl esterase. Consequently, ion homeostasis was disturbed in scap1 guard cells, and esterification of extracellular pectins was impaired so that the cell walls lining the pores did not mature normally. We conclude that SCAP1 regulates essential processes of stomatal guard cell maturation and functions as a key transcription factor regulating the final stages of guard cell differentiation. We isolated guard cell protoplasts from 4-week-old WT(Col-0) and scap1 mutant plants and extracted RNA independently. Four biological replicates were performed for each experiment.

2013-02-28 | E-GEOD-43964 | biostudies-arrayexpress

Microarray analysis of scap1 mutant and wild type in Arabidopsis thaliana guard cell protoplast

2013-02-28 | GSE43964 | GEO

bHLH Transcription Factors that Facilitate K+ Uptake During Stomatal Opening are Repressed by Abscisic Acid through Phosphorylation

Project description:Stomata open in response to light and close following exposure to abscisic acid (ABA). They regulate gas exchange between plants and atmosphere, allowing plants to adapt to changing environmental conditions. ABA binding to receptors initiates a signaling cascade that involves protein phosphorylation. Here we show that ABA induced phosphorylation of three basic helix-loop-helix (bHLH) transcription factors, called AKSs (ABA-RESPONSIVE KINASE SUBSTRATES; AKS1, AKS2, AKS3), in Arabidopsis guard cells, and that they facilitated stomatal opening through the transcription of genes encoding inwardly-rectifying K+ channels. aks1aks2-1 double mutant plants showed decreases in light-induced stomatal opening, K+ accumulation in response to light, activity of inwardly-rectifying K+ channels, and transcription of genes encoding major inwardly-rectifying K+ channels without affecting ABA-mediated stomatal closure. Overexpression of POTASSIUM CHANNEL IN ARABIDOPSIS THALIANA 1 (KAT1), which encodes a major inwardly-rectifying K+ channel in guard cells, rescued the phenotype of aks1aks2-1 plants. AKS1 bound directly to the promoter of KAT1, an interaction that was attenuated after ABA-induced phosphorylation. The ABA agonist pyrabactin induced phosphorylation of AKSs. Our results demonstrate that the AKS family of bHLH transcription factors facilitates stomatal opening through transcription of genes encoding inwardly-rectifying K+ channels, and that ABA suppresses the activity of inwardly-rectifying K+ channel activity by triggering the phosphorylation of these transcription factors. Microarray data have been deposited in the Gene Expression Omnibus with accession number: GSE46574.

2013-06-28 | PXD000235 | Pride

Blue light and CO2 signals converge to regulate light-induced stomatal opening

Project description:Stomata regulate gas exchange between plants and the atmosphere by integrating opening and closing signals. Stomata open in response to low CO2 concentrations to maximize photosynthesis in the light; however, the mechanisms that coordinate photosynthesis and stomatal conductance have yet to be identified. Here, we characterize CBC1/2 [CONVERGENCE of BLUE LIGHT (BL) and CO2 1/2], two kinases that link BL, a major component of photosynthetically active radiation (PAR), and the signals from low concentrations of CO2 in guard cells. CBC1/CBC2 redundantly stimulate stomatal opening by negatively regulating S-type anion channels in response to both BL and low concentrations of CO2. CBC1/CBC2 function in the signaling pathways of phototropins and HT1 (HIGH LEAF TEMPERATURE 1). CBC1/CBC2 interacted with and were phosphorylated by HT1. We propose that CBCs regulate stomatal aperture by integrating signals from BL and CO2 and act as the convergence site for signals from PAR and low CO2.

2017-05-24 | MSV000081109 | MassIVE

AtMYB60

Project description:Stomatal guard-cells modulate gas exchange between the plant and the atmosphere. Regulation of transcription is emerging as an important mechanism in controlling guard cells activity. The Arabidopsis transcription factor AtMYB60, is specifically expressed in guard cells and controls stomatal movements. Opening of stomatal pores is constitutively reduced in the atmyb60-1 null allele, and water loss during drought is diminished in the mutant compared to wild type. To address the effect of the AtMYB60 disruption on global gene expression, total mRNAs, derived from atmyb60-1 and WT rosette leaves, grown in standard conditions, were hybridized to a cDNA microarray.

2005-01-10 | E-MEXP-225 | biostudies-arrayexpress

Guard cell proteome - Dawn regulates guard cell proteins in Arabidopsis thaliana that function in ATP production from fatty acid beta-oxidation

Project description:Proteome changes that happen in the guard cells during dawn were up till now poorly described. Bad accessibility to pure and intact guard cell samples can be considered as the primary reason behind this lack of knowledge. By elucidating the identities of enzymes that change in abundance by the transition from dark to light, we corroborate the hypothesis that respiratory ATP production for stomatal opening results from fatty acid beta-oxidation.

2018-11-07 | PXD009918 | Pride

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