Mesophyll cells mediate systemic reactive oxygen signaling during wounding or heat stress

Abstract

Sensing of heat, high light (HL), or mechanical injury by a single leaf of a plant results in the activation of different systemic signals that reach systemic tissues within minutes and trigger systemic acquired acclimation (SAA) or systemic wound responses (SWRs), resulting in a heightened state of stress readiness of the entire plant. Among the different signals associated with rapid systemic responses to stress in plants are electric, calcium and reactive oxygen species (ROS) waves. These signals propagate from the stressed or injured leaf to the rest of the plant through the plant vascular bundles, and trigger SWRs and SAA in systemic tissues. However, whether they can propagate through other cell types, and whether or not they are interlinked, remain open questions. Here we report that in response to wounding or heat stress (HS), but not HL stress, the ROS wave can propagate through mesophyll cells of Arabidopsis thaliana. Moreover, we show that propagation of the ROS wave through mesophyll cells during these stresses is sufficient to restore SWR and SAA transcript accumulation in systemic leaves, as well as SAA to HS (but not HL). We further show that propagation of the ROS wave through mesophyll cells could contribute to systemic signal integration during HL&HS stress combination. Our findings reveal that the ROS wave can propagate through tissues other than the vascular bundles of plants, and that different stresses can trigger different types of systemic signals that propagate through different cell layers and induce stress-specific systemic responses.

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

“…This finding suggests that different stresses could trigger different types of systemic signals that might or might not be co-regulated. This possibility is further supported by our recent findings that during wounding, but not HL stress, the systemic ROS signal can propagate through mesophyll cells (28,42). Different types of stress could therefore trigger different types of systemic signals that could propagate through different cell layers.…”

“…To follow changes in local and systemic ROS levels in response to a local treatment of HL stress or wounding in wild type plants and the different mutants, we used the whole-plant live ROS imaging method we developed and used to study systemic ROS signals (26). Using this method, we were able to determine that the systemic ROS signal propagates through the vascular bundles in response to HL or wounding, and through the vascular bundles and/or mesophyll cells in response to wounding or heat stress (28,42), that in response to HL the systemic ROS signal requires the function of RBOHD, PDLP5, CNGC2, plasma membrane intrinsic protein (PIP) 2;1, MSL2 and other proteins (44), and that during a combination of two different stresses applied to two different leaves, the systemic ROS signal is involved in integrating the two different systemic signals generated by the two different stresses (27). In agreement with our previous studies (44), in response to a local application of HL stress, the systemic ROS signal was blocked in the rbohD and pdlp5 mutants, but only suppressed in the glr3.3;glr3.6 double mutant (Fig.…”