A unified framework for hydromechanical signaling: Do plant signals go with the flow?

Abstract

Local wounding in plants triggers signals that travel locally within the wounded leaf or systemically through the vasculature to distal leaves. The transmission mechanisms of this ubiquitous class of signals remain poorly understood. Here, we develop a unifying framework based on poroelastic dynamics to study two coupled biophysical processes - propagation of pressure changes and transmission of chemical elicitors via mass flows driven by these pressure changes - as potential mechanisms for the initiation and propagation of wound-induced signals. We show that rapid pressure changes in the xylem can transmit mechanical information across the plant, while their coupling with neighboring non-vascular tissue drives swelling and mass flow that can transport chemical elicitors to distal leaves. We confront our model predictions with signaling dynamics measurements in several species, and show that the poroelastic model captures observed mechanical, biochemical, and electrophysiological signals. This framework provides a valuable foundation for assessing mechanisms of signal transmission and for designing future experiments to elucidate factors involved in signal initiation, propagation, and target elicitation.