Predicting Essential Components of Signal Transduction Networks: A Dynamic Model of Guard Cell Abscisic Acid Signaling

Abstract

Plants both lose water and take in carbon dioxide through microscopic stomatal pores, each of which is regulated by a surrounding pair of guard cells. During drought, the plant hormone abscisic acid (ABA) inhibits stomatal opening and promotes stomatal closure, thereby promoting water conservation. Dozens of cellular components have been identified to function in ABA regulation of guard cell volume and thus of stomatal aperture, but a dynamic description is still not available for this complex process. Here we synthesize experimental results into a consistent guard cell signal transduction network for ABA-induced stomatal closure, and develop a dynamic model of this process. Our model captures the regulation of more than 40 identified network components, and accords well with previous experimental results at both the pathway and whole-cell physiological level. By simulating gene disruptions and pharmacological interventions we find that the network is robust against a significant fraction of possible perturbations. Our analysis reveals the novel predictions that the disruption of membrane depolarizability, anion efflux, actin cytoskeleton reorganization, cytosolic pH increase, the phosphatidic acid pathway, or K+ efflux through slowly activating K+ channels at the plasma membrane lead to the strongest reduction in ABA responsiveness. Initial experimental analysis assessing ABA-induced stomatal closure in the presence of cytosolic pH clamp imposed by the weak acid butyrate is consistent with model prediction. Simulations of stomatal response as derived from our model provide an efficient tool for the identification of candidate manipulations that have the best chance of conferring increased drought stress tolerance and for the prioritization of future wet bench analyses. Our method can be readily applied to other biological signaling networks to identify key regulatory components in systems where quantitative information is limited.

Oxidative Stress: Antagonistic Signaling for Acclimation or Cell Death?

“…However, it is known to also involve GPA1-mediated negative control of H 2 O 2 production, which is most likely from a plasma membrane-derived source (Galvez-Valdivieso et al, 2009;Galvez-Valdivieso and Mullineaux, 2010). This agrees with a link between NADPH oxidase and GPA1 postulated in the ABA network model for guard cell signaling (Li et al, 2006).…”

Roles of ion channels and transporters in guard cell signal transduction

“…Only regulators that have been demonstrated to participate in modulation of transport functions are shown, so the models show only a subset of the current information on guard cell signal transduction (cf. [57] for more information) and are depicted in a simplified, largely linear fashion. (A) Model depicting ion channels and transporters that are active during stomatal opening, and the regulatory proteins and secondary messengers which regulate them.…”

“…Modeling approaches such as those developed by Li et al [57] can help to organize this information and infer a hierarchy of signaling events.…”

“…3). However, there is also evidence that ROS regulate ABI1 activity (discussed in [57]). Additionally abi1-1, but not abi2-1, inhibits ABA activation of OST1 protein kinase [125], so the relative positions of these components in the signaling cascade remain uncertain.…”

An Integrated Hydraulic-Hormonal Model of Conifer Stomata Predicts Water Stress Dynamics

“…A complete description in terms of ion channels is difficult (Hills et al, 2012), even without considering the complex signaling pathways involved (Li et al, 2006). Instead, a simplified approach was taken, with steady-state guard cell osmotic pressure governed by the balance between inward and outward fluxes of solutes.…”