ROS, Calcium, and Electric Signals: Key Mediators of Rapid Systemic Signaling in Plants

Abstract

The systemic response of plants to pathogen infection (systemic acquired resistance [SAR]), or wounding has been extensively studied with a network of numerous compounds and signals implicated (for review, see Dempsey and Klessig, 2012; Shah and Zeier, 2013). In recent years a new type of systemic response, termed systemic acquired acclimation (SAA), has emerged as an important acclimation response of plants to abiotic stresses (e.g. Karpiński et al., 1999; Szechyńska-Hebda et al., 2010; Suzuki et al., 2013). This response is characterized by a rapid spread of the systemic signal(s) that can reach the systemic tissue within minutes from the application of abiotic stress to a local tissue. A number of different signaling mechanisms were implicated in this response, including the reactive oxygen species (ROS) wave (Miller et al., 2009), the calcium (Ca2+) wave (Choi et al., 2014), and electric signals (Szechyńska-Hebda et al., 2010). In this review we will focus on recent findings regarding each of these signals, as well as their integration, and attempt to propose a model for the propagation of rapid systemic signals during SAA and SAR. Due to space limitations, we will not address many other important aspects of ROS signaling that have been covered by a number of recent excellent reviews (for review, see Foyer and Noctor, 2013; Vaahtera et al., 2014; Considine et al., 2015; Dietz, 2015; Mignolet-Spruyt et al., 2016). The ROS wave is an autopropagating wave of ROS production mediated via RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD) activation in each cell along its systemic path (Fig. 1). It was initially discovered by Miller et al. (2009), and was extensively reviewed by Mittler et al. (2011), Gilroy et al. (2014), and Mittler and Blumwald (2015). It can reach rates of up to 8.4 cm/min and is directly linked to the calcium wave (for review, see Gilroy et al., 2014) and possibly to electric signals (Suzuki et al., 2013; Fig. 2). It is required for SAA, but by itself it likely does not convey specificity to the systemic response of plants to different abiotic stresses (Suzuki et al., 2013; for review, see Mittler et al., 2011). The ROS wave is currently thought to be integrated with additional metabolic/signaling pathways and to enable rapid SAA responses and acclimation of plants, improving their overall fitness (Suzuki et al., 2013; for review, see Mittler et al., 2011; Mittler and Blumwald, 2015). Activation of the ROS wave by a local heat stress was shown, for example, to enhance the acclimation of systemic tissues to heat stress, and to be regulated by temporal and special interactions with ABA signaling (Suzuki et al., 2013; for review, see Mittler and Blumwald, 2015). In addition, local application of high light resulted in the activation of a ROS wave that enabled systemic tissues to withstand light stress, and was accompanied by the accumulation of photorespiratory amino acids, including Gly and Ser, in nonstressed systemic tissues (Suzuki et al., 2013). Integration of the ROS, Ca2+, and electric waves in and between cells via the function of RBOH proteins and superoxide dismutases (SODs; yellow), Ca2+-dependent protein kinases (CPK/CBL-CIPKs; green), calcium channels such as TPC1 and H2O2-activated plasma membrane calcium channels (red), and GLRs and/or plasma membrane H2O2 channels (blue). Activation of RBOHD is shown to be mediated by CPK/CBL-CIPKs, Cys-rich receptor kinases (CRKs), or directly by Ca2+. Activation of Ca2+ channels is shown to be mediated by H2O2 or by calcium via calcium-induced calcium release. Activation of GLRs is proposed to be mediated by H2O2 and/or calcium levels via calcium-induced calcium release. The level of ROS in cells is proposed to be regulated by NO-ROS and NO-RBOH interactions, retrograde signaling, and ROS removal/production in the chloroplast (Cp), mitochondria (Mt), and peroxisomes (Px). The regulation of gene expression in the nuclei is shown to be mediated via redox/ROS changes, LESION SIMULATING DISEASE1 (LSD), ENHANCED DISEASE SUSCEPTIBILITY1 (EDS), MITOGEN-ACTIVATED PROTEIN KINASEs (MPKs), WRKY, and RRTF1. The electric signal is depicted as a sinus-like wave that travels along the plasma membrane and through the plasmodesmata (PD). Copropagation of the ROS, calcium, hydraulic, and electric waves during rapid systemic signaling. The ROS wave is shown as a series of red arrows, the calcium wave is shown as a dashed green arrow, the hydraulic wave is shown as a dotted blue arrow, and the electric wave is shown as a dotted black arrow. Different sections along the path of the signal (yellow arrows) are also shown to have alternating levels of NPQ and ROS/APX1 levels, and JA is shown to accumulate in cells along the systemic path. The local tissue is shown to have alterations in ROS, calcium, and membrane depolarization potential, and the systemic tissue is shown to have accumulation of ROS and abscisic acid (ABA). Black arrows indicate accumulation or suppressi