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Christoph Peterhansel, Veronica G. Maurino, Photorespiration Redesigned, Plant Physiology, Volume 155, Issue 1, January 2011, Pages 49–55, https://doi.org/10.1104/pp.110.165019
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Photorespiration has been a target for crop improvement ever since the energy losses associated with this pathway were identified in the 1970s. However, recent research highlights the importance of photorespiration as a recycling pathway for the products of ribulose-1,5-bisphosphate (RuBP) oxygenation and its intimate interconnection with primary metabolism. Nevertheless, reducing photorespiratory losses by installation of alternative salvage pathways in Arabidopsis (Arabidopsis thaliana) resulted in enhanced growth and biomass. Such approaches will probably also prove useful under field conditions, and in a future atmosphere containing higher CO2 concentrations combined with high temperature or limiting water.
PHOTORESPIRATION EVOLVED AS A METABOLITE RECYCLING PATHWAY
Photorespiration is an exceptional biochemical pathway as it starts with what might be considered an erroneous reaction: Rubisco fixes molecular oxygen (O2) instead of executing its intrinsic function in photosynthesis, fixation of carbon dioxide (CO2). CO2 uptake results in the formation of two molecules of 3-phosphoglycerate (3-PGA) that is used for biosynthetic reactions and the recycling of the acceptor molecule RuBP. During O2 fixation, one molecule of 3-PGA and one molecule of 2-phosphoglycolate (2-PG) are formed. The latter cannot be used by plants for biosynthetic reactions and it is a potent inhibitor of chloroplastic function (Anderson, 1971). The catalytic activity of Rubisco with O2 as a substrate is some 100-fold lower than with CO2 at equivalent concentrations of the two gases (Tcherkez et al., 2006); thus, at a first glance, O2 fixation does not cause a major problem. This was probably true during early evolutionary times when the atmosphere was essentially free of O2 and contained much higher amounts of CO2 than nowadays (Kasting and Ono, 2006). However, oxygenic photosynthesis was a great evolutionary success that resulted in a drastic change of the atmospheric composition. Essentially all CO2 was fixed from the atmosphere down to levels clearly below 0.1% on a molar basis. Much of this fixed carbon was not released back to the atmosphere by decomposition of organic matter, but removed from the biogeochemical carbon cycle by sedimentation and fossilization. Concomitantly, the light reactions of oxygenic photosynthesis, as the name implies, produced immense amounts of O2 by using water as the primary electron donor. After saturation of mineral deposits and the seawater, O2 started to accumulate in the atmosphere (Buick, 2008). Today, atmospheric O2 is roughly 500-fold more abundant than CO2. Fortunately, some other factors such as increased solubility of CO2 compared to O2 in the aqueous cytosol and the chloroplast stroma (Ku and Edwards, 1977) again favor CO2 fixation by Rubisco. All this ends up with approximately 25% oxygenase reaction under moderate growth conditions. This rate seems to be a balanced trade-off of atmospheric CO2 and O2 concentrations, resulting in acceptable rates of RuBP oxygenation at highest possible rates of carboxylation. However, the fraction of oxygenase reactions can significantly rise in warm and dry habitats. Under increasing temperatures, the affinity of Rubisco for CO2 decreases (Jordan and Ogren, 1984). Moreover, plants tend to close stomata to reduce transpiratory losses. The remaining level of CO2 inside the leaf is rapidly decreased and O2 is available in excess, resulting in high rates of RuBP oxygenation.
