Aboveground plant-to-plant electrical signaling mediates network acquired acclimation

Abstract

Systemic acquired acclimation and wound signaling require the transmission of electrical, calcium, and reactive oxygen species (ROS) signals between local and systemic tissues of the same plant. However, whether such signals can be transmitted between two different plants is largely unknown. Here, we reveal a new type of plant-to-plant aboveground direct communication involving electrical signaling detected at the surface of leaves, ROS, and photosystem networks. A foliar electrical signal induced by wounding or high light stress applied to a single dandelion leaf can be transmitted to a neighboring plant that is in direct contact with the stimulated plant, resulting in systemic photosynthetic, oxidative, molecular, and physiological changes in both plants. Furthermore, similar aboveground changes can be induced in a network of plants serially connected via touch. Such signals can also induce responses even if the neighboring plant is from a different plant species. Our study demonstrates that electrical signals can function as a communication link between transmitter and receiver plants that are organized as a network (community) of plants. This process can be described as network-acquired acclimation.

Relationship among Electrical Signals, Chlorophyll Fluorescence, and Root Vitality of Strawberry Seedlings under Drought Stress

“…The electrical signal is the change in membrane potential generated by tissues and cells in plants in response to external environmental stress [38]. It plays an important role in plant system communication [39][40][41]. The comparison between the physiological parameters of the plants and the electrical signal measurements has highlighted the possibility of using such electrical signals to detect the plant water status.…”

ROS are evolutionary conserved cell-to-cell signals

“…We previously identified and studied the ROS wave in several different angiosperm species including Arabidopsis, rice, tomato, maize, dandelion, and wheat 20,22,24,33 . However, whether ROS can function as a rapid systemic signal in gymnosperms, as well as other plant lineages is unknown.…”

“…The findings that rapid systemic ROS signals are conserved among many land plants (Figures 1 and 2) 20,22,24,33 prompted us to test whether they can also be found in multicellular ( Chara vulgaris ) and unicellular ( Chlamydomonas reinhardtii ) algae. Multicellular and unicellular algae are known to use extracellular ROS as signals and contain NOX/RBOH enzymes 40,41 .…”

“…Since the redox state of other neighboring cells will also be altered in a similar manner during this process (like the redox changes that occur in cells along the path of the ROS wave in plants) 63 , and these cells will also start accumulating and secreting ROS, the entire colony, biofilm, or tissue would respond in unison to the stress perceived by the initiating cell (Figure 8), improving its chances of acclimation to the sensed stress, as well as overall survival. Such a mechanism could have coordinated the redox and ROS accumulation responses of a network of cells and give this cell population a better chance of survival in the early environment that was present on Earth; and may have been conserved in one form or another in different organisms to date (Figures 1-7) [19][20][21][22][23][24] . ROS such and H2O2 could have therefore served as one of the first 'stress hormones' on Earth; and to induce a response, the level of this stress hormone (i.e., H2O2) had to be increased (Figures 1-8).…”

“…All organisms, outside of the mammalian cells, were fumigated with 50 µM H2DCFDA (Millipore-Sigma, St. Louis, MO, USA) in 0.05 M Phosphate buffer pH 7.4 with 0.01% Silwet L-77. Fumigation was carried out for 30 min using nebulizers (Punasi Direct, Hong Kong, China) [20][21][22][23][24]37,38 . For mammalian cells 10 µM H2DCFDA (final concentration) was applied to the medium and incubated for 30 min.…”