Photorespiration

Abstract

Photorespiration is an ancient metabolic repair pathway that supplements the Calvin–Benson cycle in all oxygenic phototrophs, that is plants, algae and cyanobacteria. It is necessary because oxygen can substitute for carbon dioxide in the first reaction of the photosynthetic carbon dioxide‐fixation process, catalysed by ribulose‐1,5‐bisphosphate carboxylase (Rubisco), causing the idle synthesis of the powerful enzyme inhibitor 2‐phosphoglycolate. Scavenging of 2‐phosphoglycolate in the photorespiratory pathway recovers three out of four misdirected carbon atoms while the fourth is released as photorespiratory carbon dioxide. Photorespiration involves more enzymes than the Calvin–Benson cycle itself and requires cooperation of different cellular compartments. It thereby represents one of the most complex examples of metabolic organisation and interacts with other metabolism in many ways. Absolute rates vary owing to the absence or presence of carbon concentrating mechanism and they depend on environmental conditions, mainly oxygen, carbon dioxide and temperature.

Key Concepts

  • Photorespiration evolved in cyanobacteria as a supplement to the Calvin–Benson cycle in order to remove the enzyme inhibitor 2‐phosphoglycolate, which is unavoidably produced during oxygenic photosynthesis.
  • Photorespiration was an indispensable condition for the evolution of oxygenic photosynthesis, that is cyanobacteria, algae and plants.
  • When assessed by mass flow, photorespiration constitutes the second most important process in the terrestrial biosphere, excelled only by photosynthesis itself.
  • Energetically, the photosynthetic–photorespiratory supercycle is not wasteful as sometimes perpetuated but, in contradistinction, very efficient as can be seen from the fact that nearly all life on Earth directly or indirectly depends on this pathway.
  • Photorespiration was a key driver for evolutionary innovations such as C4 plants, which are highly productive in warm environments.

Keywords: carbon dioxide; oxygen; phosphoglycolate; photorespiration; photosynthesis; rubisco

Figure 1. Carbon dioxide fixation by ribulose 1,5‐bisphosphate carboxylase (Rubisco) in the presence of oxygen. The enediolate form of the acceptor molecule ribulose 1,5‐bisphosphate (RuBP) can be carboxylated using carbon dioxide leading to the formation of two molecules 3‐phosphoglycerate, or it can be oxidised by oxygen leading to the formation of one molecule each of 2‐phosphoglycolate and 3‐phosphoglycerate. 2‐phosphoglycolate inhibits RuBP regeneration and impairs other processes.
Figure 2. The plant photorespiratory pathway spans three organelles: the chloroplast, the peroxisome, and the mitochondrion. The enzymes of the core pathway (in red) are 2‐phosphoglycolate phosphatase (PGLP), glycolate oxidase (GOX), glutamate‐glyoxylate aminotransferase (GGAT), serine‐glyoxylate aminotransferase (SGAT), the glycine cleavage system (GCS) comprising three enzymes, serine hydroxymethyltransferase (SHMT), peroxisomal hydroxypyruvate reductase (HPR1), and glycerate kinase (GLYK). Catalase (CAT) detoxifies hydrogen peroxide. Known transporters are the glycolate‐glycerate antiporter PLGG1, the glycolate transporter BASS6 and the triosephosphate translocator TPT. At least two reactions of the core pathway can be circumvented in specific conditions. The cytosolic hydroxypyruvate reductase (HPR2) bypass supports HPR1 when the peroxisomal malate dehydrogenase (pMDH) does not provide NADH rapidly enough for hydroxypyruvate reduction. ATP consumption by cytGLYK in the cytosol of shade‐grown plants helps alleviating photoinhibition of chloroplasts.
Figure 3. Photorespiration is embedded into whole cell metabolism and manifold interactions with other metabolic pathways and secondary‐level repair pathways exist. For example, SHMT and other enzymes are inhibited by 5‐formyl THF, which is produced in considerable amounts by SHMT itself (shown in red). Cellular metabolism would rapidly break down if this noxious compound would not be detoxified and recycled to THF (shown in blue). This requires four folate‐interconverting enzymes, 5,10‐CH2THF dehydrogenase combined with 5,10‐methenyl THF cyclohydrolase in a bifunctional enzyme (DHC), 5‐formyl THF cycloligase (5‐FCL) and 10‐formyl THF deformylase (10‐FDF). Formate dehydrogenase (FDH) oxidises the produced formate to carbon dioxide. If 10‐FDF is blocked, plants accumulate massive amounts of glycine in normal air and need elevated carbon dioxide to suppress photorespiration and survive. Adapted from Collakova et al. .
Figure 4. Most cyanobacteria recycle 2‐phosphoglycolate via two partially redundant pathways, a plant‐like photorespiratory pathway (metabolites in blue, enzymes in red) and the bacterial glycerate pathway (orange route). Both pathways start with 2‐phosphoglycolate phosphatase (PGLP) and glycolate dehydrogenase (GlcDH). The glycerate pathway circumvents the glycine‐to‐serine conversion by directly converting glyoxylate into glycerate using glyoxylate carboligase (GCL) and tartronic semialdehyde reductase (TSR). Enzymes of the plant‐like branch are glutamate‐glyoxylate aminotransferase (GGAT), serine‐glyoxylate aminotransferase (SGAT), the glycine system (GCS), serine hydroxymethyltransferase (SHMT) and hydroxypyruvate reductase (HPR). Only few advanced cyanobacteria have a plant‐type 3PGA‐forming glycerate kinase (GLYK); all others use 2PGA‐forming glycerate kinases in combination with phosphoglyceromutase for the generation of 3PGA (not shown). Some cyanobacteria can also completely decompose glyoxylate to carbon dioxide (grey route) via oxalate decarboxylase (ODC) and formate dehydrogenase (FDH). Cyanobacterial mutants without functioning 2‐phosphoglycolate metabolism cannot survive in normal environments. Adapted from Eisenhut et al. .
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Further Reading

Abadie C , Carroll A and Tcherkez G (2017) Interactions between day respiration, photorespiration, and N and S assimilation in leaves. In: Tcherkez G and Ghashghaie J (eds) Plant Respiration: Metabolic Fluxes and Carbon Balance, pp. 1–18. Springer International Publishing.

Bauwe H (2018) Photorespiration – damage repair pathway of the Calvin–Benson cycle. In: Logan DC (ed) Plant Mitochondria, 2nd edn, pp. 293–342. Chichester, UK: John Wiley & Sons, Ltd.

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Bauwe, Hermann(Feb 2019) Photorespiration. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001292.pub3]