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Guard cell photosynthesis is crucial in abscisic acid-induced stomatal closure.

ABSTRACT: Reactive oxygen species (ROS) are ubiquitous signaling molecules involved in diverse physiological processes, including stomatal closure. Photosynthetic electron transport (PET) is the main source of ROS generation in plants, but whether it functions in guard cell signaling remains unclear. Here, we assessed whether PET functions in abscisic acid (ABA) signaling in guard cells. ABA-elicited ROS were localized to guard cell chloroplasts in Arabidopsis thaliana, Commelina benghalensis, and Vicia faba in the light and abolished by the PET inhibitors 3-(3, 4-dichlorophenyl)-1, 1-dimethylurea and 2, 5-dibromo-3-methyl-6-isopropyl-p-benzoquinone. These inhibitors reduced ABA-induced stomatal closure in all three species, as well as in the NADPH oxidase-lacking mutant atrboh D/F. However, an NADPH oxidase inhibitor did not fully eliminate ABA-induced ROS in the chloroplasts, and ABA-induced ROS were still observed in the guard cell chloroplasts of atrboh D/F. This study demonstrates that ROS generated through PET act as signaling molecules in ABA-induced stomatal closure and that this occurs in concert with ROS derived through NADPH oxidase.

SUBMITTER: Iwai S

PROVIDER: S-EPMC6589527 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Guard cell photosynthesis is crucial in abscisic acid-induced stomatal closure.

Iwai Sumio S Ogata Sho S Yamada Naotaka N Onjo Michio M Sonoike Kintake K Shimazaki Ken-Ichiro KI

Plant direct 20190530 5

Reactive oxygen species (ROS) are ubiquitous signaling molecules involved in diverse physiological processes, including stomatal closure. Photosynthetic electron transport (PET) is the main source of ROS generation in plants, but whether it functions in guard cell signaling remains unclear. Here, we assessed whether PET functions in abscisic acid (ABA) signaling in guard cells. ABA-elicited ROS were localized to guard cell chloroplasts in <i>Arabidopsis thaliana</i>, <i>Commelina benghalensis</i ...[more]

PMID: 31245777

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Project description:Stomatal pores play a central role in the control of carbon assimilation and plant water status. The guard cell pair that borders each pore integrates information from environmental and endogenous signals and accordingly swells or deflates, thereby increasing or decreasing the stomatal aperture. Prior research shows that there is a complex cellular network underlying this process. We have previously constructed a signal transduction network and a Boolean dynamic model describing stomatal closure in response to signals including the plant hormone abscisic acid (ABA), calcium or reactive oxygen species (ROS). Here, we improve the Boolean network model such that it captures the biologically expected response of the guard cell in the absence or following the removal of a closure-inducing signal such as ABA or external Ca2+. The expectation from the biological system is reversibility, i.e., the stomata should reopen after the closing signal is removed. We find that the model's reversibility is obstructed by the previously assumed persistent activity of four nodes. By introducing time-dependent Boolean functions for these nodes, the model recapitulates stomatal reopening following the removal of a signal. The previous version of the model predicts ∼20% closure in the absence of any signal due to uncertainty regarding the initial conditions of multiple network nodes. We systematically test and adjust these initial conditions to find the minimally restrictive combinations that appropriately result in open stomata in the absence of a closure signal. We support these results by an analysis of the successive stabilization of feedback motifs in the network, illuminating the system's dynamic progression toward the open or closed stomata state. This analysis particularly highlights the role of cytosolic calcium oscillations in causing and maintaining stomatal closure. Overall, we illustrate the strength of the Boolean network modeling framework to efficiently capture cellular phenotypes as emergent outcomes of intracellular biological processes.

Dataset Information

Guard cell photosynthesis is crucial in abscisic acid-induced stomatal closure.

Publications

Guard cell photosynthesis is crucial in abscisic acid-induced stomatal closure.

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