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

Abstract

ROS, calcium, and electric signals mediate rapid systemic signaling in plants.

Figure 1.

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).

Figure 2.

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 suppression in the level of a particular chemical or transcript/protein, and dashed, dotted, and wide red arrows indicate direction of the signal.

Figure 3.

Integration of the different waves that mediate rapid systemic signaling during SAA. Local stimuli are shown to trigger the ROS/calcium/electric wave, as well as a hydraulic wave that in turn triggers the calcium wave via mechano-sensors. The calcium and ROS waves are shown to be linked (possibly via RBOH and TPC1/CPK function), the ROS and electric waves are shown to be linked (possibly through RBOHD and GLR function), and the calcium and electric waves are shown to be linked (possibly via channels such as GLRs or similar). The different waves are shown to mediate the propagation of each other and to trigger a response in the systemic tissue.