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A Guard Cell Abscisic Acid (ABA) Network Model That Captures the Stomatal Resting State

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. Pri...

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Autores principales: Maheshwari, Parul, Assmann, Sarah M., Albert, Reka
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7438572/
https://www.ncbi.nlm.nih.gov/pubmed/32903539
http://dx.doi.org/10.3389/fphys.2020.00927
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author Maheshwari, Parul
Assmann, Sarah M.
Albert, Reka
author_facet Maheshwari, Parul
Assmann, Sarah M.
Albert, Reka
author_sort Maheshwari, Parul
collection PubMed
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 Ca(2+). 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.
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spelling pubmed-74385722020-09-03 A Guard Cell Abscisic Acid (ABA) Network Model That Captures the Stomatal Resting State Maheshwari, Parul Assmann, Sarah M. Albert, Reka Front Physiol Physiology 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 Ca(2+). 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. Frontiers Media S.A. 2020-08-13 /pmc/articles/PMC7438572/ /pubmed/32903539 http://dx.doi.org/10.3389/fphys.2020.00927 Text en Copyright © 2020 Maheshwari, Assmann and Albert. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Maheshwari, Parul
Assmann, Sarah M.
Albert, Reka
A Guard Cell Abscisic Acid (ABA) Network Model That Captures the Stomatal Resting State
title A Guard Cell Abscisic Acid (ABA) Network Model That Captures the Stomatal Resting State
title_full A Guard Cell Abscisic Acid (ABA) Network Model That Captures the Stomatal Resting State
title_fullStr A Guard Cell Abscisic Acid (ABA) Network Model That Captures the Stomatal Resting State
title_full_unstemmed A Guard Cell Abscisic Acid (ABA) Network Model That Captures the Stomatal Resting State
title_short A Guard Cell Abscisic Acid (ABA) Network Model That Captures the Stomatal Resting State
title_sort guard cell abscisic acid (aba) network model that captures the stomatal resting state
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7438572/
https://www.ncbi.nlm.nih.gov/pubmed/32903539
http://dx.doi.org/10.3389/fphys.2020.00927
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