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 comp onents associated with photosystem I (PS I) that may subsequently participa te in reactions that reduce O-2. The two primary reactions that have been e xtensively 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 th e 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 n umber of roles, including photon energy dissipation. In C-3 and Crassulacea n 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 photosynthet ic carbon oxidation cycle (PCO) and photosynthetic carbon reduction cycle ( PCR) activity. This is supported by studies with antisense tobacco plants w ith 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 cycle s. 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 re latively insensitive to the external CO2 concentration. Such a major differ ence is readily attributed to the operation of the C-4 CO2 concentrating me chanism. 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 insensi tive to CO2, even in species that lack a CO2 concentrating mechanism and un der conditions that are clearly limiting with respect to inorganic carbon s upply A part explanation for this could be that many algal rubsicos have co nsiderably different oxygenase kinetic properties and exhibit far less oxyg enase activity in air. This would lead to the conclusion that perhaps a gre ater 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 hig her plants, cyanobacteria appear to have a high capacity for Mehler O-2 upt ake, 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-h arvesting complexes under stressful conditions. However, for cyanobacteria, with a lack of significant non-photochemical quenching, the situation may well be different.