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

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. 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 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 still need 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 treatment of high-light (HL) stress or wounding. Our findings reveal that activation of systemic membrane potential, calcium, reactive oxygen species and hydraulic pressure signals, in response to wounding, is dependent on glutamate receptor-like proteins 3.3 and 3.6. In contrast, in response to HL stress, systemic changes in calcium and membrane potential depended on glutamate receptor-like 3.3 and 3.6, while systemic hydraulic signals did not. We further show that plasmodesmata functions are required for systemic changes in membrane potential and calcium during responses to HL stress or wounding. Our findings shed new light on the different mechanisms that integrate different systemic signals in plants during stress.