Abstract
Stomata, microscopic pores in leaf surfaces through which water loss and carbon dioxide uptake occur, are closed in response to drought by the phytohormone abscisic acid (ABA). This process is vital for drought tolerance and has been the topic of extensive experimental investigation in the last decades. Although a core signaling chain has been elucidated consisting of ABA binding to receptors, which alleviates negative regulation by protein phosphatases 2C (PP2Cs) of the protein kinase OPEN STOMATA 1 (OST1) and ultimately results in activation of anion channels, osmotic water loss, and stomatal closure, over 70 additional components have been identified, yet their relationships with each other and the core components are poorly elucidated. We integrated and processed hundreds of disparate observations regarding ABA signal transduction responses underlying stomatal closure into a network of 84 nodes and 156 edges and, as a result, established those relationships, including identification of a 36-node, strongly connected (feedback-rich) component as well as its in- and out-components. The network’s domination by a feedback-rich component may reflect a general feature of rapid signaling events. We developed a discrete dynamic model of this network and elucidated the effects of ABA plus knockout or constitutive activity of 79 nodes on both the outcome of the system (closure) and the status of all internal nodes. The model, with more than 1024 system states, is far from fully determined by the available data, yet model results agree with existing experiments in 82 cases and disagree in only 17 cases, a validation rate of 75%. Our results reveal nodes that could be engineered to impact stomatal closure in a controlled fashion and also provide over 140 novel predictions for which experimental data are currently lacking. Noting the paucity of wet-bench data regarding combinatorial effects of ABA and internal node activation, we experimentally confirmed several predictions of the model with regard to reactive oxygen species, cytosolic Ca2+ (Ca2+c), and heterotrimeric G-protein signaling. We analyzed dynamics-determining positive and negative feedback loops, thereby elucidating the attractor (dynamic behavior) repertoire of the system and the groups of nodes that determine each attractor. Based on this analysis, we predict the likely presence of a previously unrecognized feedback mechanism dependent on Ca2+c. This mechanism would provide model agreement with 10 additional experimental observations, for a validation rate of 85%. Our research underscores the importance of feedback regulation in generating robust and adaptable biological responses. The high validation rate of our model illustrates the advantages of discrete dynamic modeling for complex, nonlinear systems common in biology.
Highlights
The epidermes of leaves and other aerial plant parts have natural openings known as stomata
Guard cells, located in pairs on the surface of plant leaves, circumscribe microscopic pores called stomata, through which plants take up gaseous carbon dioxide that will be fixed by photosynthesis into sugars
The plant hormone abscisic acid (ABA) causes volume changes in guard cells that result in stomatal closure, thereby restricting water loss
Summary
The epidermes of leaves and other aerial plant parts have natural openings known as stomata. Each stomate is surrounded by a pair of guard cells that modulate stomatal apertures in response to endogenous water status, to multiple phytohormones, and to many environmental signals such as light and CO2 [1,2,3,4]. Abscisic acid (ABA) is a key phytohormone that functions as an essential signal in plant responses to abiotic and biotic stress [5, 6]. ABA activates complex intracellular signaling cascades that open anion channels at the guard cell membrane [9], leading to anion efflux and cellular depolarization, which in turn drives K+ efflux through depolarization-activated outward K+ channels [10, 11]. Solute loss drives the osmotic efflux of water through aquaporins [12], resulting in guard cell deflation and stomatal closure [13]
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