Dataset Information

Model-driven discovery of calcium-related protein-phosphatase inhibition in plant guard cell signaling.

ABSTRACT: The plant hormone abscisic acid (ABA) promotes stomatal closure via multifarious cellular signaling cascades. Our previous comprehensive reconstruction of the stomatal closure network resulted in an 81-node network with 153 edges. Discrete dynamic modeling utilizing this network reproduced over 75% of experimental observations but a few experimentally supported results were not recapitulated. Here we identify predictions that improve the agreement between model and experiment. We performed dynamics-preserving network reduction, resulting in a condensed 49 node and 113 edge stomatal closure network that preserved all dynamics-determining network motifs and reproduced the predictions of the original model. We then utilized the reduced network to explore cases in which experimental activation of internal nodes in the absence of ABA elicited stomatal closure in wet bench experiments, but not in our in silico model. Our simulations revealed that addition of a single edge, which allows indirect inhibition of any one of three PP2C protein phosphatases (ABI2, PP2CA, HAB1) by cytosolic Ca2+ elevation, resolves the majority of the discrepancies. Consistent with this hypothesis, we experimentally show that Ca2+ application to cellular lysates at physiological concentrations inhibits PP2C activity. The model augmented with this new edge provides new insights into the role of cytosolic Ca2+ oscillations in stomatal closure, revealing a mutual reinforcement between repeated increases in cytosolic Ca2+ concentration and a self-sustaining feedback circuit inside the signaling network. These results illustrate how iteration between model and experiment can improve predictions of highly complex cellular dynamics.

SUBMITTER: Maheshwari P

PROVIDER: S-EPMC6837631 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Model-driven discovery of calcium-related protein-phosphatase inhibition in plant guard cell signaling.

Maheshwari Parul P Du Hao H Sheen Jen J Assmann Sarah M SM Albert Reka R

PLoS computational biology 20191028 10

The plant hormone abscisic acid (ABA) promotes stomatal closure via multifarious cellular signaling cascades. Our previous comprehensive reconstruction of the stomatal closure network resulted in an 81-node network with 153 edges. Discrete dynamic modeling utilizing this network reproduced over 75% of experimental observations but a few experimentally supported results were not recapitulated. Here we identify predictions that improve the agreement between model and experiment. We performed dynam ...[more]

PMID: 31658257

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Project description:Background and aimsTurgor pressure within a plant cell represents the key to the mechanistical descriptiion of plant growth, combining the effects of both water and carbon availability. The high level of spatio-temporal variation and diurnal dynamics in turgor pressure within a single plant make it a challenge to model these on the fine spatial scale required for functional-structural plant models (FSPMs). A conceptual model for turgor-driven growth in FSPMs has been established previously, but its practical use has not yet been explored.MethodsA turgor-driven growth model was incorporated in a newly established FSPM for soybean. The FSPM simulates dynamics in photosynthesis, transpiration and turgor pressure in direct relation to plant growth. Comparisons of simulations with field data were used to evaluate the potential and shortcomings of the modelling approach.Key resultsModel simulations revealed the need to include an initial seed carbon contribution, a more realistic sink function, an estimation of respiration, and the distinction between osmotic and structural sugars, in order to achieve a realistic model of plant growth. However, differences between simulations and observations remained in individual organ growth patterns and under different environmental conditions. This exposed the need to further investigate the assumptions of developmental and environmental (in)sensitivity of the parameters, which represent physiological and biophysical organ properties in the model, in future research.ConclusionsThe model in its current form is primarily a diagnostic tool, to better understand and model the behaviour of water relations on the scale of individual plant organs throughout the plant life cycle. Potential future applications include its use as a phenotyping tool to capture differences in plant performance between genotypes and growing environments in terms of specific plant characteristics. Additionally, focused experiments can be used to further improve the model mechanisms to lead to better predictive FSPMs, including scenarios of water deficit.

Dataset Information

Model-driven discovery of calcium-related protein-phosphatase inhibition in plant guard cell signaling.

Publications

Model-driven discovery of calcium-related protein-phosphatase inhibition in plant guard cell signaling.

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