Dataset Information

Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure.

ABSTRACT: Stomatal movements are crucial for the control of plant water status and protection against pathogens. Assays on epidermal peels revealed that, similar to abscisic acid (ABA), pathogen-associated molecular pattern (PAMP) flg22 requires the AtPIP2;1 aquaporin to induce stomatal closure. Flg22 also induced an increase in osmotic water permeability (Pf) of guard cell protoplasts through activation of AtPIP2;1. The use of HyPer, a genetic probe for intracellular hydrogen peroxide (H2O2), revealed that both ABA and flg22 triggered an accumulation of H2O2 in wild-type but not pip2;1 guard cells. Pretreatment of guard cells with flg22 or ABA facilitated the influx of exogenous H2O2 Brassinosteroid insensitive 1-associated receptor kinase 1 (BAK1) and open stomata 1 (OST1)/Snf1-related protein kinase 2.6 (SnRK2.6) were both necessary to flg22-induced Pf and both phosphorylated AtPIP2;1 on Ser121 in vitro. Accumulation of H2O2 and stomatal closure as induced by flg22 was restored in pip2;1 guard cells by a phosphomimetic form (Ser121Asp) but not by a phosphodeficient form (Ser121Ala) of AtPIP2;1. We propose a mechanism whereby phosphorylation of AtPIP2;1 Ser121 by BAK1 and/or OST1 is triggered in response to flg22 to activate its water and H2O2 transport activities. This work establishes a signaling role of plasma membrane aquaporins in guard cells and potentially in other cellular context involving H2O2 signaling.

SUBMITTER: Rodrigues O

PROVIDER: S-EPMC5576802 | biostudies-other | 2017 Aug

REPOSITORIES: biostudies-other

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Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure.

Rodrigues Olivier O Reshetnyak Ganna G Grondin Alexandre A Saijo Yusuke Y Leonhardt Nathalie N Maurel Christophe C Verdoucq Lionel L

Proceedings of the National Academy of Sciences of the United States of America 20170807 34

Stomatal movements are crucial for the control of plant water status and protection against pathogens. Assays on epidermal peels revealed that, similar to abscisic acid (ABA), pathogen-associated molecular pattern (PAMP) flg22 requires the AtPIP2;1 aquaporin to induce stomatal closure. Flg22 also induced an increase in osmotic water permeability (Pf) of guard cell protoplasts through activation of AtPIP2;1. The use of HyPer, a genetic probe for intracellular hydro ...[more]

PMID: 28784763

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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

Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure.

Publications

Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure.

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