Integration of electric, calcium, reactive oxygen species and hydraulic signals during rapid systemic signaling in plants

Abstract

The sensing of abiotic stress, mechanical injury, or pathogen attack by a single plant tissue results in the activation of systemic signals that travel from the affected tissue to the entire plant, alerting it of an impending stress or pathogen attack. This process is essential for plant survival during stress and is termed systemic signaling. Among the different signals triggered during this process are calcium, electric, reactive oxygen species (ROS) and hydraulic signals. These are thought to propagate at rapid rates through the plant vascular bundles and to regulate many of the systemic processes essential for plant survival. Although the different signals activated during systemic signaling are thought to be interlinked, their coordination and hierarchy remain to be determined. Here, using a combination of advanced whole-plant imaging and hydraulic pressure measurements, we studied the activation of all four systemic signals in wild type and different Arabidopsis thaliana mutants subjected to a local high light (HL) stress or wounding. Our findings reveal that in response to wounding systemic changes in membrane potential, calcium, ROS, and hydraulic pressure are coordinated by glutamate receptor-like (GLR) proteins 3.3 and 3.6, while in response to HL the respiratory burst oxidase homolog D-driven systemic ROS signal could be separated from systemic changes in membrane potential and calcium levels. We further determine that plasmodesmata functions are required for systemic changes in membrane potential, calcium, and ROS during systemic signaling. Our findings shed new light on the different mechanisms that integrate different systemic signals in plants during stress. Significance statementThe ability of plants to transmit a signal from a stressed or wounded tissue to the entire plant, termed systemic signaling, is key to plant survival during conditions of environmental stress. At least four different systemic signals are thought to be involved in this process: electric, calcium, reactive oxygen and hydraulic. However, how are they coordinated and whether they can be stress-specific is mostly unknown. Here we report that different types of stimuli can induce different types of systemic signals that may or may not be linked with each other. We further reveal that hydraulic waves can be actively regulated in plants in response to wounding, and that proteins that regulate plasmodesmata pores play a key role in systemic signaling.