Land plants are sessile and have developed sophisticated mechanisms that allow for both immediate and acclimatory responses to changing environments. Partial exposure of low light–adapted Arabidopsis plants to excess light results in a systemic acclimation to excess excitation energy and consequent photooxidative stress in unexposed leaves. Thus, plants possess a mechanism to communicate excess excitation energy systemically, allowing them to mount a defense against further episodes of such stress. Systemic redox changes in the proximity of photosystem II, hydrogen peroxide, and the induction of antioxidant defenses are key determinants of this mechanism of systemic acquired acclimation.

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

Exposure of Arabidopsis plants that were maintained under low light (200 mumol of photons m-2 sec-1) to excess light (2000 mumol of photons m-2 sec-1) for 1 hr caused reversible photoinhibition of photosynthesis. Measurements of photosynthetic parameters and the use of electron transport inhibitors indicated that a novel signal transduction pathway was initiated at plastoquinone and regulated, at least in part, by the redox status of the plastoquinone pool. This signal, which preceded the photooxidative burst of hydrogen peroxide (H2O2) associated with photoinhibition of photosynthesis, resulted in a rapid increase (within 15 min) in mRNA levels of two cytosolic ascorbate peroxidase genes (APX1 and APX2). Treatment of leaves with exogenous reduced glutathione abolished this signal, suggesting that glutathione or the redox status of the glutathione pool has a regulatory impact on this signaling pathway. During recovery from photooxidative stress, transcripts for cytosolic glutathione reductase (GOR2) increased, emphasizing the role of glutathione in this stress.

The mutant regulator of APX2 1-1 (rax1-1) was identified in Arabidopsis thaliana that constitutively expressed normally photooxidative stress-inducible ASCORBATE PEROXIDASE2 (APX2) and had ≥50% lowered foliar glutathione levels. Mapping revealed that rax1-1 is an allele of γ-GLUTAMYLCYSTEINE SYNTHETASE 1 (GSH1), which encodes chloroplastic γ-glutamylcysteine synthetase, the controlling step of glutathione biosynthesis. By comparison of rax1-1 with the GSH1 mutant cadmium hypersensitive 2, the expression of 32 stress-responsive genes was shown to be responsive to changed glutathione metabolism. Under photo-oxidative stress conditions, the expression of a wider set of defense-related genes was altered in the mutants. In wild-type plants, glutathione metabolism may play a key role in determining the degree of expression of defense genes controlled by several signaling pathways both before and during stress. This control may reflect the physiological state of the plant at the time of the onset of an environmental challenge and suggests that changes in glutathione metabolism may be one means of integrating the function of several signaling pathways.

Hydrogen peroxide (H2O2) is produced predominantly in plant cells during photosynthesis and photorespiration, and to a lesser extent, in respiration processes. It is the most stable of the so-called reactive oxygen species (ROS), and therefore plays a crucial role as a signalling molecule in various physiological processes. Intra- and intercellular levels of H2O2 increase during environmental stresses. Hydrogen peroxide interacts with thiol-containing proteins and activates different signalling pathways as well as transcription factors, which in turn regulate gene expression and cell-cycle processes. Genetic systems controlling cellular redox homeostasis and H2O2 signalling are discussed. In addition to photosynthetic and respiratory metabolism, the extracellular matrix (ECM) plays an important role in the generation of H2O2, which regulates plant growth, development, acclimatory and defence responses. During various environmental stresses the highest levels of H2O2 are observed in the leaf veins. Most of our knowledge about H2O2 in plants has been obtained from obligate C3 plants. The potential role of H2O2 in the photosynthetic mode of carbon assimilation, such as C4 metabolism and CAM (Crassulacean acid metabolism) is discussed. We speculate that early in the evolution of oxygenic photosynthesis on Earth, H2O2 could have been involved in the evolution of modern photosystem II.