Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase

Linear electron transport in chloroplasts produces a number of reduced components associated with photosystem I (PS I) that may subsequently participate in reactions that reduce O-2. The two primary reactions that have been extensively studied are: first, the direct reduction of O-2 to superoxide by reduced donors associated with PS I (the Mehler reaction), and second, the rubisco oxygenase (ribulose 1,5-bisphosphate carboxylase oxygenase EC 4.1.1.39) reaction and associated peroxisomal and mitochondrial reactions of the photorespiratory pathway. This paper reviews a number of recent and past studies with higher plants, algae and cyanobacteria that have attempted to quantify O-2 fluxes under various conditions and their contributions to a number of roles, including photon energy dissipation. In C-3 and Crassulacean acid metabolism (CAM) plants, a Mehler O-2 uptake reaction is unlikely to support a significant flow of electron transport (probably less than 10%). In addition, if it were present it would appear to scale with photosynthetic carbon oxidation cycle (PCO) and photosynthetic carbon reduction cycle (PCR) activity. This is supported by studies with antisense tobacco plants with reduced rubisco at low and high temperatures and high light, as well as studies with potatoes, grapes and madrone during water stress. The lack of significant Mehler in these plants directly argues for a strong control of Mehler reaction in the absence of ATP consumption by the PCR and PCO cycles. The difference between C-3 and C-4 plants is primarily that the level of light-dependent O-2 uptake is generally much lower in C-4 plants and is relatively insensitive to the external CO2 concentration. Such a major difference is readily attributed to the operation of the C-4 CO2 concentrating mechanism. Algae show a range of light-dependent O-2 uptake rates, similar to C-4 plants. As in C-4 plants, the O-2 uptake appears to be largely insensitive to CO2, even in species that lack a CO2 concentrating mechanism and under conditions that are clearly limiting with respect to inorganic carbon supply A part explanation for this could be that many algal rubsicos have considerably different oxygenase kinetic properties and exhibit far less oxygenase activity in air. This would lead to the conclusion that perhaps a greater proportion of the observed O-2 uptake may be due to a Mehler reaction and less to rubisco, compared with C-3 plants. In contrast to algae and higher plants, cyanobacteria appear to have a high capacity for Mehler O-2 uptake, which appears to be not well coupled or limited by ATP consumption. It is likely that in all higher plants and algae, which have a well-developed non-photochemical quenching mechanism, non-radiative energy dissipation is the major mechanism for dissipating excess photons absorbed by the light-harvesting complexes under stressful conditions. However, for cyanobacteria, with a lack of significant non-photochemical quenching, the situation may well be different.