Photorespiration in the context of Rubisco biochemistry, CO₂ diffusion and metabolism

Abstract

Summary Photorespiratory metabolism is essential for plants to maintain functional photosynthesis in an oxygen‐containing environment. Because the oxygenation reaction of Rubisco is followed by the loss of previously fixed carbon, photorespiration is often considered a wasteful process and considerable efforts are aimed at minimizing the negative impact of photorespiration on the plant’s carbon uptake. However, the photorespiratory pathway has also many positive aspects, as it is well integrated within other metabolic processes, such as nitrogen assimilation and C1 metabolism, and it is important for maintaining the redox balance of the plant. The overall effect of photorespiratory carbon loss on the net CO2 fixation of the plant is also strongly influenced by the physiology of the leaf related to CO2 diffusion. This review outlines the distinction between Rubisco oxygenation and photorespiratory CO2 release as a basis to evaluate the costs and benefits of photorespiration.

Photorespiration: The Futile Cycle?

“…The mitochondrial respiration R d is taken to be the rate of 12 CO 2 release after 2 min. This method can provide estimates of both carboxylation and oxygenation if one assumes that the rate of mitochondrial respiration (R d ) is not affected by the sudden high CO 2 concentration, that 0.5 CO 2 is generated per oxygenation reaction when the CO 2 released per oxygenation varies widely with temperature and light level and among species [7], and that leaves do not naturally contain any 13 C [59]. If intracellular reassimilation is significant and it often is [60], substantial errors in the estimate can result.…”

“…Because it produces 2PG, a compound “toxic” to many enzymes in photosynthetic metabolism, and oxidizes organic carbon without seemingly generating ATP, photorespiration is generally considered a wasteful process. The following sections examines how the photorespiratory pathway converts 2PG into glycolate, the only carbon source for the photosynthetic carbon oxidation cycle [ 6 ], a cycle that together with nitrogen assimilation, C 1 metabolism, and sulfur assimilation generates essential amino acids and intermediate compounds [ 7 ]. Moreover, the three enzymes involved in the initial photorespiratory steps within chloroplasts—Rubisco, malic enzyme, and phosphoglycolate phosphatase—have metal binding sites that accommodate either Mg 2+ or Mn 2+ , and balance between the binding of these enzymes to Mg 2+ or Mn 2+ may shift the relative rates and energy efficiencies of photosynthesis and photorespiration [ 8 ].…”

Non‐targeted 13C metabolite analysis demonstrates broad re‐orchestration of leaf metabolism when gas exchange conditions vary

“…Net CO 2 assimilation is the result of carboxylation ( v c ), CO 2 release by photorespiration ( v o / ξ , where v o is the oxygenation rate and ξ is a stoichiometric coefficient, very close to 2 [Abadie, Boex‐Fontvieille, Carroll, & Tcherkez, 2016; Busch, 2020]) and CO 2 production by day respiration ( R d ). In gas‐exchange experiments, the balance between carboxylation and oxygenation is routinely manipulated using CO 2 and O 2 mole fraction, for example using high CO 2 or low O 2 (0.5 or 2%) to suppress photorespiration.…”

Rubisco adaptation is more limited by phylogenetic constraint than by catalytic trade-off

“…Although the oxygenation reaction catalysed by rubisco is not thought to be deleterious in the anoxic environment prevalent when the enzyme first evolved (Nisbet et al ., 2007; Erb and Zarzycki, 2018), under current atmospheric conditions it can comprise a quarter of all rubisco reactions in terrestrial plants (Ehleringer et al ., 1991). Thus, despite oxygenation serving a number of beneficial functions (Busch, 2020), at its current rate it represents a substantial metabolic burden reducing the productivity of some plants by up to 50 % (Ogren, 1984; Bauwe et al ., 2012).…”