Temporal-Spatial Interaction between Reactive Oxygen Species and Abscisic Acid Regulates Rapid Systemic Acclimation in Plants  

Abstract

Being sessile organisms, plants evolved sophisticated acclimation mechanisms to cope with abiotic challenges in their environment. These are activated at the initial site of exposure to stress, as well as in systemic tissues that have not been subjected to stress (termed systemic acquired acclimation [SAA]). Although SAA is thought to play a key role in plant survival during stress, little is known about the signaling mechanisms underlying it. Here, we report that SAA in plants requires at least two different signals: an autopropagating wave of reactive oxygen species (ROS) that rapidly spreads from the initial site of exposure to the entire plant and a stress-specific signal that conveys abiotic stress specificity. We further demonstrate that SAA is stress specific and that a temporal-spatial interaction between ROS and abscisic acid regulates rapid SAA to heat stress in plants. In addition, we demonstrate that the rapid ROS signal is associated with the propagation of electric signals in Arabidopsis thaliana. Our findings unravel some of the basic signaling mechanisms underlying SAA in plants and reveal that signaling events and transcriptome and metabolome reprogramming of systemic tissues in response to abiotic stress occur at a much faster rate than previously envisioned.

The Roles of ROS and ABA in Systemic Acquired Acclimation

“…Each cell along the path of the ROS wave activates its own RBOHD proteins generating a systemic autopropagating wave of ROS production that travels in the apoplast from the initiating tissue to the entire plant at rates of up to 8.4 cm/min (Figure 2). Recent analysis of the ROS wave in Arabidopsis demonstrated that it is required for the activation of SAA of plants in response to local stimuli such as high light or heat, as measured by protein and RNA expression as well as enhanced tolerance of systemic leaves (Suzuki et al, 2013). These finding demonstrated that the ROS wave has a biological function in plants.…”

“…This finding prompted the hypothesis that the ROS wave functions to prime the plant for SAA activation and that other stress-specific signals are required to convey specificity to this response. During the SAA response to heat stress, the ROS wave was found to function in coordination with ABA in systemic tissues (Suzuki et al, 2013). This analysis of the ROS wave in Arabidopsis also identified a functional link between ROS production by RBOH proteins and electric signals.…”

“…This analysis of the ROS wave in Arabidopsis also identified a functional link between ROS production by RBOH proteins and electric signals. At least one type of electric signal was found to be suppressed in mutants lacking RBOHD that was required for the ROS wave (Suzuki et al, 2013). The studies described above demonstrated that the ROS wave plays a central role in mediating rapid systemic responses to abiotic stress.…”

“…In addition to the increasing number of compounds and pathways implicated in systemic signaling, new studies have begun to focus on the different tissues involved in generating and perceiving systemic signals and on the speed at which these signals are being mediated . In addition, ABA and stomatal functions have been recently implicated in the regulation of systemic responses to abiotic stress (Suzuki et al, 2013). In this review, we will focus on the role of ROS and calcium in SAA and on their interaction with ABA, NO, and stomatal functions.…”

“…The presumed common outcome of all of these systemic responses is to alert all remote and unstressed tissues of the plant to the existence of a biotic or abiotic threat and to trigger the activation of resistance or acclimation pathways in these tissues. These responses typically are measured by enhanced accumulation of defense or acclimation transcripts and proteins and/or by demonstrating an enhanced level of tolerance or resistance to a subsequent abiotic or biotic stress applied to systemic tissues (Karpi nski et al, 2013;Suzuki et al, 2013;Gilroy et al, 2014;Shah et al, 2014). Activating resistance or acclimation pathways in remote tissues that were not yet subjected to the stress or pathogen would therefore enable the plant to withstand and survive the upcoming biotic or abiotic challenge.…”