ROS Signaling in Coupled Nonlinear Systems
Today it is well established that ROS exert important functions in signaling pathways within the cells of both plants and animals. The mode of signaling under the participation of ROS depends on the nature of stress. In response to different types of stress, ROS can act in a dual manner: i) by functioning as signal molecules which induce molecular, biochemical, and physiological responses leading to development of adaptive mechanisms and improving the tolerance of the organisms to stress (acclimation) or ii) by inducing reaction sequences that eventually cause programmed cell death (Galvez-Valdivieso and Mullineaux, 2010; Mittler et al., 2011; Vranova et al., 2002; Kreslavski et al., 2007, 2011; Jaspers and Kangasjarvi, 2010; Los et al., 2010; Schmitt et al., 2014a).
In general, significant differences exist in the response to abiotic (light, draught, cold, heat etc.) and biotic (infection by viruses and bacteria) stress. This includes also the type of ROS molecules involved. In case of abiotic stress, :AgO2 is often formed in addition to O 2 and H2O2, while biotic stress mainly leads to enzymatic generation of O 2 and H2O2 which are used as a defense mechanism against biotic stress (Laloi et al., 2004). Different types of ROS give rise to specific signaling, as shown in animal cells (Klotz et al., 2003).
ROS have several advantages in acting as signal molecules (Miller et al., 2009; Mittler et al., 2011): i) Cells are able to rapidly generate and scavenge different forms of ROS in a simultaneous manner, thereby permitting rapid response to stress. ii) The subcellular localization of ROS signals can be strongly controlled within cells, i.e. a spatial control of ROS accumulation exists in a highly specific manner. iii) ROS can be used as rapid long-distance auto-propagating signals to be transferred throughout the plant, as recently reported for Arabidopsis thaliana, in which ROS signals propagate at rates of up to 8.4 cm/min (Miller et al., 2009, Schmitt at al., 2014a). iv) ROS are tightly linked to cellular homeostasis and metabolism.
Most probably, the mechanism of stomatal closure and it spatiotem- poral patterns result from an underlying ROS signaling mechanism. Therefore, it is proposed that ROS are implemented in very general signaling schemes that influence the expression of genes and consequently the molecular biology of green plants. Additionally, ROS are responsible for macroscopic long range effects that are directly observable on the cellular level like stomatal closure. It is a trigger for adaption of the whole cell metabolism and, in case of biotic stress, actively produced with respect to long range interaction as found for O 2 and H2O2 (in contrast to singlet oxygen which has a much shorter lifetime) to be used as oxide- zing defense molecules against the biotic stressors.
A comparison with ROS signaling in animal cells revealed that the communication of mitochondria in heart cells occurs via ROS-induced waves. An abrupt collapse or oscillation of the mitochondrial energy state is assumed to be synchronized across the mitochondrial network by local ROS-mediated interactions (Zhou et al., 2010; Zhou and O’Rourke, 2012). This model is based on the idea that a depolarization of the electrical potential difference across the coupling membrane is specifically mediated by O 2 via its diffusion and the O 2 -dependent activation of an inner membrane anion channel. This is in agreement with experimental data. This mode of ROS-induced ROS release mechanisms in animal cells can also be used in plants for propagation of cell-to-cell ROS signaling over long distances (Miller et al., 2009, Mittler et al., 2011). The concept of a transient ROS burst occurring in selected cells can be further extended to the more general concept of a ROS wave propagating in time and space as response to different types of stress (Schmitt et al., 2014a).