Utilizing systems biology to unravel stomatal function and the hierarchies underpinning its control

Stomata control the concomitant exchange of CO2 and transpiration in land plants. While a constant supply of CO2 is need to maintain the rate of photosynthesis, the accompanying water losses must be tightly regulated to prevent dehydration and undesired metabolic changes. The factors affecting stomatal movement are directly coupled with the cellular networks of guard cells. Although the guard cell has been used as a model for characterization of signaling pathways, several important questions about its functioning remain elusive. Current modeling approaches describe the stomatal conductance in terms of relatively few easy-to-measure variables being unsuitable for in silico design of genetic manipulation strategies. Here, we argue that a system biology approach, combining modeling and high-throughput experiments, may be used to elucidate the mechanisms underlying stomata control and to determine targets for modulation of stomatal responses to environment. In support of our opinion, we review studies demonstrating how high-throughput approaches have provided a systems-view of guard cells. Finally, we emphasize the opportunities and challenges of genome-scale modeling and large-scale data integration for in silico manipulation of guard cell functions to improve crop yields, particularly under stress conditions which are of pertinence both to climate change and water use efficiency. In this opinion we discuss how the main factors affecting stomatal movement are directly coupled with the cellular networks of guard cells. Recent advances in high-throughput technologies have facilitated system-based dissection of the molecular components and mechanisms underlying the behavior of guard cells and their influence on other cell types and ultimately the entire plant. We suggest alternative approaches to those commonly used to illuminate stomatal behavior and in doing so hope to bridge the gap between ecophysiological and molecular views of this important cell-to-environment interaction.