Abscisic acid-mediated water stress regulation can mechanistically explain oscillations and water stress memory in stomatal conductance

Abstract

Stomatal pores, formed by guard cells, govern the critical trade-off between carbon assimilation and water loss in plants. Their dynamic responses to environmental stresses, such as stomatal oscillations and drought "stress memory" (hysteresis), have lacked a unified mechanistic explanation. While abscisic acid (ABA) is believed to play key roles in water stress responses, no model has linked its core regulatory kinetics to these complex stomatal behaviors. Here, we introduce a coupled hydropassive-hydroactive (HP-HA) model that integrates leaf hydraulics with the biokinetics of guard cell-autonomous ABA regulation and plasma membrane-mediated osmoregulation. We demonstrate that this framework predicts accurate, genotype-specific stomatal regulation across wildtype, ABA-insensitive mutant (ost1-3), and ABA-synthesis mutant (aao3-2) in Arabidopsis thaliana (At) and that non-linear feedbacks in ABA autoregulation can drive both stomatal oscillations and hysteresis. This work unifies genetic, signaling, and membrane processes with leaf-scale physiological dynamics, providing a new predictive foundation for understanding and modulating plant management of water use and water stress.