Second Messengers and Signaling Molecules in H2O2 Signaling Chains and (Nonlinear) Networking
Although our current knowledge on the signalling networks of ROS is still rather fragmentary, Figure 71 summarizes some pathways in the signal networks including the interference between various pathways.
It was found that H2O2 stimulates a rapid increase of intracellular Ca2+ concentration (Kim et al., 2009). The development of oxidative stress controls the activity of several isoforms of calmodulin. In plant cells, on the other hand, the ROS generation in mitochondria is activated by an increase of the Ca2+ concentration. Likewise, under certain conditions, the Ca2+ concentration depends on the actual ROS level and additionally Ca2+ stimulates the formation of ROS in plant cells (Bowler and Fluhr, 2000). These findings indicate that ROS/redox state and calcium-dependent signaling pathways are closely interconnected in a strongly nonlinear way (Yin et al., 2000). Heat hardening, at least a short-term treatment, can also be accompanied by an increase of the ROS content in cells (Dat et al., 1998), i.e. ROS might function in transduction of a temperature signal (Suzuki and Mittler, 2006; Yu et al., 2008). It is also suggested that ROS participate in acclimation of the photosynthetic apparatus to high light under conditions similar to heat hardening (Kuznetsov and Shevyakova, 1999; Allakhverdiev et al., 2007; Kreslavski et al., 2009, 2012a).
Common intermediates were found to participate in mechanism(s) of ROS and phytohormone action (Jung et al., 2009), as is shown by the involvement of the species O 2 and O3 in programmed cell death together with ethylene- and jasmonate-dependent metabolic pathways. On the other hand, ROS can function as second messengers in the transduction of hormonal signals, as was shown for the auxin affect on gene expression, where ROS are used as second messengers, which simultaneously regulate activity and expression of glutathione transferase (Tognetti et al., 2012).
H2O2 induces the phosphoinositide cycle that switches signaling pathways associated with the secondary messengers, IP3 and diacylglycerol (DAG) (Munnik et al., 1998), whereas phospholipase D was reported to stimulate H2O2 production in A. thaliana leaves via generation of phosphatidic acid acting as lipid messenger (Sang et al., 2001).
It is well known that exogenous salicylic acid and pathogens induce a burst of ROS generation in plant tissues (Dmitriev, 2003). However, it remains unclear how and to what extent ROS are involved in the improvement of plant stress resistance. Exogenous salicylic acid was found to give rise to enhanced plant cold tolerance (Horvath et al., 2002). This effect is attributed to the inhibition of catalase and related to oxidative stress leading to accumulation of H2O2. Studies on two maize genotypes revealed that the cold-resistant line had a molecular form of catalase, which was more severely inhibited by salicylic acid than the catalase of the sensitive line (Horvath et al., 2002). Oxidative stress caused by exogenous salicylic acid depends on the calcium status of the cells and is not manifested in the presence of calcium channel blockers.
When considering the existence of signaling networks, it must be emphasized that different hierarchies of complexity exist in ROS-induced signaling depending primarily on the evolutionary level of the organism. Networking is evidently simpler in prokaryotic than in eukaryotic cells, which contain various cell organelles (chloroplasts, mitochondria, peroxisomes, nucleus, endoplasmatic reticulum) and loci of genomic information (e.g. plastids and nucleus in plants). An even more complex signal network exists in multi-cellular organisms, e.g. in leaves of higher plants with different cell types (mesophyll, bundle sheath, guard cells). The deciphering of the latter type of networks requires detailed analyses, and this topic is just at the beginning to reach a level of deeper understanding.