Dynamics of stomatal regulation: A systems-scale model for understanding coupling between active and passive mechanisms

Climate change, with heightened stresses like water scarcity and atmospheric dryness poses challenges to crop productivity and food security. Stomata, the pores defined by guard cells on leaf surfaces, play a vital role in controlling carbon and water vapor exchange. Stomatal regulation involves water movement in or out of guard cells, influenced by leaf tissue biomechanics and hydraulics. This movement occurs through two mechanisms: hydropassive (HP), driven by changes in guard cell turgor pressure, and hydroactive (HA), initiated by biochemical osmotic adjustments in guard cells. Current mechanistic models for stomatal regulation lack coupling between the HA and HP mechanisms.



We introduce a framework coupling HP, poroelastic transport at the tissue scale, and HA, biochemical regulation in individual guard cells. First, we confront of our model by with experimental data. We proceed to use the model to elucidate the following: 1) the hydraulic architecture and constitutive properties of cellular structures govern the dynamics of HP stomatal regulation, and 2) the dynamics of the intracellular signaling in the HA mechanism control the rates of the plant’s overall stomatal response to water stress. We conclude with a discussion of the implications of these coupled, multiscale mechanisms for the management of water stress in leaves and of future experiments for genetic, molecular, and biophysical interventions to enhance water and carbon gas exchange for improved crop efficiency.