Foliar stomatal movements are critical for regulating plant water loss and gas exchange. Elevated carbon dioxide (
Respiration in leaves and the continued elevation in the atmospheric
- NSF-PAR ID:
- 10077707
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- The Plant Journal
- Volume:
- 96
- Issue:
- 5
- ISSN:
- 0960-7412
- Page Range / eLocation ID:
- p. 1018-1035
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Summary CO 2) levels are known to induce stomatal closure. However, the current knowledge onCO 2signal transduction in stomatal guard cells is limited. Here we report metabolomic responses ofBrassica napus guard cells to elevatedCO 2using three hyphenated metabolomics platforms: gas chromatography‐mass spectrometry (MS ); liquid chromatography (LC )‐multiple reaction monitoring‐MS ; and ultra‐high‐performanceLC ‐quadrupole time‐of‐flight‐MS . A total of 358 metabolites from guard cells were quantified in a time‐course response to elevatedCO 2level. Most metabolites increased under elevatedCO 2, showing the most significant differences at 10 min. In addition, reactive oxygen species production increased and stomatal aperture decreased with time. Major alterations in flavonoid, organic acid, sugar, fatty acid, phenylpropanoid and amino acid metabolic pathways indicated changes in both primary and specialized metabolic pathways in guard cells. Most interestingly, the jasmonic acid (JA ) biosynthesis pathway was significantly altered in the course of elevatedCO 2treatment. Together with results obtained fromJA biosynthesis and signaling mutants as well asCO 2signaling mutants, we discovered thatCO 2‐induced stomatal closure is mediated byJA signaling. -
Summary Cytosolic calcium concentration ([Ca2+]cyt) and heterotrimeric G‐proteins are universal eukaryotic signaling elements. In plant guard cells, extracellular calcium (Cao) is as strong a stimulus for stomatal closure as the phytohormone abscisic acid (
ABA ), but underlying mechanisms remain elusive. Here, we report that the sole Arabidopsis heterotrimeric Gβ subunit,AGB 1, is required for four guard cell Caoresponses: induction of stomatal closure; inhibition of stomatal opening; [Ca2+]cytoscillation; and inositol 1,4,5‐trisphosphate (InsP3) production. Stomata in wild‐type Arabidopsis (Col) and in mutants of the canonical Gα subunit, , showed inhibition of stomatal opening and promotion of stomatal closure by Cao. By contrast, stomatal movements ofGPA 1agb1 mutants andagb1 /gpa1 double‐mutants, as well as those of theagg1agg2 Gγ double‐mutant, were insensitive to Cao. These behaviors contrast withABA ‐regulated stomatal movements, which involveGPA 1 andAGB 1/AGG 3 dimers, illustrating differential partitioning of G‐protein subunits among stimuli with similar ultimate impacts, which may facilitate stimulus‐specific encoding. knockouts retained reactive oxygen species andAGB 1NO production, but lostYC 3.6‐detected [Ca2+]cytoscillations in response to Cao, initiating only a single [Ca2+]cytspike. Experimentally imposed [Ca2+]cytoscillations restored stomatal closure inagb1 . Yeast two‐hybrid and bimolecular complementation fluorescence experiments revealed thatAGB 1 interacts with phospholipase Cs (PLCs), and Caoinduced InsP3 production in Col but not inagb1 . In sum, G‐protein signaling viaAGB 1/AGG 1/AGG 2 is essential for Cao‐regulation of stomatal apertures, and stomatal movements in response to Caoapparently require Ca2+‐induced Ca2+release that is likely dependent on Gβγ interaction withPLC s leading to InsP3 production. -
Increases in CO2concentration 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 CO2control 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 withslac1 -transformed plants expressing mutated SLAC1 proteins revealed that the SLAC1 residue R256 is required for CO2regulation 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 CO2signal transduction. Together, these analyses suggest that the SLAC1 anion channel is one of the physiologically relevant CO2/HCO3−sensors in guard cells. -
Stomatal pore apertures are narrowing globally due to the continuing rise in atmospheric [CO2]. CO2elevation 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 ) CO2elevation enhances ABA concentrations and/or early ABA signaling in guard cells to induce stomatal closure and (ii ) CO2signaling 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 mutantsnced3/nced5 andaba2-1 remain responsive to CO2elevation. 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 CO2elevation does not trigger [ABA] increases in guard cells, in contrast to control ABA exposures. Moreover, CO2activates guard cell S-type anion channels innced3/nced5 and ABA receptor hextuple mutants. Unexpectedly, in-gel protein kinase assays show that unlike ABA, elevated CO2does not activate OST1/SnRK2 kinases in guard cells. The present study points to a model in which rapid CO2signal 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]. -
Summary Little is known about long‐distance mesophyll‐driven signals that regulate stomatal conductance. Soluble and/or vapor‐phase molecules have been proposed. In this study, the involvement of the gaseous signal ethylene in the modulation of stomatal conductance in
Arabidopsis thaliana by CO2/abscisic acid (ABA) was examined.We present a diffusion model which indicates that gaseous signaling molecule/s with a shorter/direct diffusion pathway to guard cells are more probable for rapid mesophyll‐dependent stomatal conductance changes. We, therefore, analyzed different Arabidopsis ethylene‐signaling and biosynthesis mutants for their ethylene production and kinetics of stomatal responses to ABA/[CO2]‐shifts.
According to our research, higher [CO2] causes Arabidopsis rosettes to produce more ethylene. An ACC‐synthase octuple mutant with reduced ethylene biosynthesis exhibits dysfunctional CO2‐induced stomatal movements. Ethylene‐insensitive receptor (gain‐of‐function),
etr1‐1 andetr2‐1 , and signaling,ein2‐5 andein2‐1 , mutants showed intact stomatal responses to [CO2]‐shifts, whereas loss‐of‐function ethylene receptor mutants, includingetr2‐3;ein4‐4;ers2‐3 ,etr1‐6;etr2‐3 andetr1‐6 , showed markedly accelerated stomatal responses to [CO2]‐shifts. Further investigation revealed a significantly impaired stomatal closure to ABA in the ACC‐synthase octuple mutant and accelerated stomatal responses in theetr1‐6;etr2‐3 , andetr1‐6 , but not in theetr2‐3;ein4‐4;ers2‐3 mutants.These findings suggest essential functions of ethylene biosynthesis and signaling components in tuning/accelerating stomatal conductance responses to CO2and ABA.