A unified framework for hydromechanical signaling can explain transmission of local and long-distance signals in plants

Abstract

Local wounding in plants triggers signals that travel locally within the wounded leaf or systemically through the vasculature to distant leaves. Our understanding of the mechanisms of initiation and propagation of this ubiquitous class of signals remains incomplete. 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 nonvascular tissue drives swelling and mass flow that can transport chemical elicitors to distant leaves. We confront predictions from our model with measurements of signaling dynamics in several species to show that i) the poroelastic model can capture the observed dynamics of purely mechanical changes (swelling of distant leaves) induced by wounding; ii) advection and diffusion of hypothetical elicitors with mass flows induced by poroelastic relaxations can explain distant cellular responses observed with gene-encoded reporters of cytosolic calcium concentration and electrical signals; and iii) poroelastic diffusion of pressure changes around local wounds in nonvascular tissue matches the observed cytosolic calcium signals and represents an alternative hypothesis relative to molecular diffusion of chemical elicitors. 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.