Photorespiration

Abstract

Photorespiration is the light‐dependent release of carbon dioxide initiated by ribulose‐1,5‐bisphosphate carboxylase/oxygenase (Rubisco) in oxygen‐producing photosynthetic organisms. It occurs because oxygen can substitute for carbon dioxide in the first reaction of the photosynthetic carbon dioxide‐fixation process, causing the idle synthesis of phosphoglycolate. Phosphoglycolate is scavenged in the photorespiratory C2 cycle, which is an essential auxiliary metabolic pathway that allows photosynthesis in oxygen‐containing environments. Three out of four misdirected carbon atoms are recovered and the fourth is released as photorespiratory carbon dioxide. Absolute rates vary in different organisms and they also depend on environmental conditions, mainly oxygen, carbon dioxide and temperature. They are highest in C3 plants and much reduced in other organisms, such as C4 plants, algae and cyanobacteria. In the presence of oxygen, phosphoglycolate production is unavoidable and cannot be eliminated.

Key concepts:

  • Nearly all photosynthetic activity on earth is oxygen‐producing photosynthesis. Dictated by the biochemistry of carbon dioxide fixation, this unavoidably comes with the production of phosphoglycolate.

  • When assessed by mass flow, excelled only by photosynthesis, phosphoglycolate production constitutes the second‐most important process in the land‐based biosphere.

  • The scavenging of phosphoglycolate was a condition for the evolution of cyanobacteria, algae and plants.

  • Oxygenic photosynthesis is only possible on the condition of adequate photorespiratory metabolism and life on earth would look very different without it.

  • Oxygenic photosynthesis is coupled to photorespiratory carbon dioxide losses and this reduces competitiveness of C3 plants in warm environments. Gene technology‐assisted breeding hopes to reduce these losses in crops.

Keywords: C2 cycle; carbon dioxide; glycolate; oxygen; photorespiration; photosynthesis; Rubisco

Figure 1.

The plant photorespiratory C2 cycle spans three organelles: the chloroplast, the peroxisome and the mitochondrion. The enzymes of the core cycle are Rubisco, phosphoglycolate phosphatase (PGP), glycolate oxidase (GOX), serine‐glyoxylate aminotransferase (SGT), glutamate‐glyoxylate aminotransferase (GGT), glycine decarboxylase (GDC), serine hydroxymethyltransferase (SHMT), peroxisomal hydroxypyruvate reductase (HPR1) and glycerate kinase (GLYK). Catalase (CAT) detoxifies hydrogen peroxide. A cytosolic hydroxypyruvate reductase (HPR2) supports HPR1 when the peroxisomal malate dehydrogenase (pMDH) does not provide NADH rapidly enough for hydroxypyruvate reduction. Photorespiratory ammonia is captured by glutamine synthetase (GS2). The produced glutamine is then used by ferredoxin‐dependent glutamate synthase (GOGAT) to recycle 2‐oxoglutarate into fresh glutamate for peroxisomal transamination.

Figure 2.

Photorespiration is embedded into whole cell metabolism and manifold interactions with other metabolic pathways exist. For example, SHMT and other enzymes are strongly inhibited by 5‐formyl‐THF, which is produced in considerable amounts by SHMT itself. Cellular metabolism would rapidly break down if this noxious compound would not be detoxified and recycled to THF. This requires four folate‐interconverting enzymes, 5,10‐CH2THF dehydrogenase combined with 5,10‐methenyl‐THF cyclohydrolase in a bifunctional enzyme (E1), 5‐formyl‐THF cycloligase (E2) and 10‐formyl‐THF deformylase (E3). If E3 is blocked, plants accumulate massive amounts of glycine in normal air and need elevated carbon dioxide to survive (Collakova et al., ).

Figure 3.

Cyanobacteria recycle phosphoglycolate via two partially redundant pathways, a plant‐like C2 cycle (metabolites in blue, enzymes in red) and the bacterial glycerate pathway (black route). Both pathways start with phosphoglycolate phosphatase (PGP) and glycolate dehydrogenase (GLCDH). The glycerate pathway circumvents the glycine‐to‐serine conversion by directly converting glyoxylate into glycerate using tartronic semialdehyde synthase (TSS) and tartronic semialdehyde reductase (TSR). Enzymes of the plant‐like branch are serine‐glyoxylate aminotransferase (SGT), glutamate‐glyoxylate aminotransferase (GGT), glycine decarboxylase (GDC), serine hydroxymethyltransferase (SHMT) and hydroxypyruvate reductase (HPR). Only few advanced cyanobacteria have a plant‐type 3PGA‐forming glycerate kinase (GLYK, green route); all others use 2PGA‐forming glycerate kinases (GK) in combination with phosphoglyceromutase (PGM) for the generation of 3PGA. Some cyanobacteria can also completely decompose glyoxylate to carbon dioxide (grey route) via oxalate decarboxylase (ODC) and formate dehydrogenase (FDH). Cyanobacterial mutants without functioning phosphoglycolate metabolism cannot survive in normal environments (Eisenhut et al., ).

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References

Andrews TJ and Whitney SM (2003) Manipulating ribulose bisphosphate carboxylase/oxygenase in the chloroplasts of higher plants. Archives of Biochemistry and Biophysics 414: 159–169.

Ashida H, Danchin A and Yokota A (2005) Was photosynthetic RuBisCO recruited by acquisitive evolution from RuBisCO‐like proteins involved in sulfur metabolism? Research in Microbiology 156: 611–618.

Bartsch O, Hagemann M and Bauwe H (2008) Only plant‐type (GLYK) glycerate kinases produce d‐glycerate 3‐phosphate. FEBS Letters 582: 3025–3028.

Bauwe H (2010) Photorespiration – the bridge to C4 photosynthesis. In: Raghavendra AS and Sage R (eds) C4 Photosynthesis and Related CO2 Concentrating Mechanisms. New York: Springer.

Berner RA (2006) GEOCARBSULF: a combined model for Phanerozoic atmospheric O2 and CO2. Geochimica et Cosmochimica Acta 70: 5653–5664.

Blackwell RD, Murray AJS, Lea PJ et al. (1988) The value of mutants unable to carry out photorespiration. Photosynthesis Research 16: 155–176.

Boldt R, Edner C, Kolukisaoglu Ü et al. (2005) d‐glycerate 3‐kinase, the last unknown enzyme in the photorespiratory cycle in Arabidopsis, belongs to a novel kinase family. Plant Cell 17: 2413–2420.

Bowes G, Ogren WL and Hageman RH (1971) Phosphoglycolate production catalysed by ribulose diphosphate carboxylase. Biochemical and Biophysical Research Communications 45: 716–722.

Brestic M, Cornic G, Fryer MJ et al. (1995) Does photorespiration protect the photosynthetic apparatus in french bean leaves from photoinhibition during drought stress. Planta 196: 450–457.

Cegelski L and Schaefer J (2006) NMR determination of photorespiration in intact leaves using in vivo 13CO2 labeling. Journal of Magnetic Resonance 178: 1–10.

Collakova E, Goyer A, Naponelli V et al. (2008) Arabidopsis 10‐formyl tetrahydrofolate deformylases are essential for photorespiration. Plant Cell 20: 1818–1832.

Coschigano KT, Melo‐Oliveira R, Lim J et al. (1998) Arabidopsis gls mutants and distinct Fd‐GOGAT genes: implications for photorespiration and primary nitrogen assimilation. Plant Cell 10: 741–752.

Cousins AB, Pracharoenwattana I, Zhou W et al. (2008) Peroxisomal malate dehydrogenase is not essential for photorespiration in Arabidopsis but its absence causes an increase in the stoichiometry of photorespiratory CO2 release. Plant Physiology 148: 786–795.

Douce R, Bourguignon J, Neuburger M et al. (2001) The glycine decarboxylase system: a fascinating complex. Trends in Plant Science 6: 167–176.

Dutilleul C, Lelarge C, Prioul JL et al. (2005) Mitochondria‐driven changes in leaf NAD status exert a crucial influence on the control of nitrate assimilation and the integration of carbon and nitrogen metabolism. Plant Physiology 139: 64–78.

Eisenhut M, Ruth W, Haimovich M et al. (2008) The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants. Proceedings of the National Academy of Sciences of the USA 105: 17199–17204.

Foyer CH, Bloom AJ, Queval G et al. (2009) Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annual Review of Plant Biology 60: 455.

Hanson AD and Roje S (2001) One‐carbon metabolism in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 52: 119–137.

Heber U, Bligny R, Streb P et al. (1996) Photorespiration is essential for the protection of the photosynthetic apparatus of C3 plants against photoinactivation under sunlight. Botanica Acta 109: 307–315.

Husic DW, Husic HD and Tolbert NE (1987) The oxidative photosynthetic carbon cycle or C2 cycle. Critical Reviews in Plant Sciences 5: 45–100.

Igamberdiev AU and Gardeström P (2003) Regulation of NAD‐ and NADP‐dependent isocitrate dehydrogenases by reduction levels of pyridine nucleotides in mitochondria and cytosol of pea leaves. Biochimica et Biophysica Acta 1606: 117–125.

Kebeish R, Niessen M, Thiruveedhi K et al. (2007) Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nature Biotechnology 25: 593–599.

Keys AJ, Bird IF, Cornelius MJ et al. (1978) Photorespiratory nitrogen cycle. Nature 275: 741–743.

Kleczkowski LA (1994) Inhibitors of photosynthetic enzymes/carriers and metabolism. Annual Review of Plant Physiology 45: 339–367.

Kürschner WM, Kvacek Z and Dilcher DL (2008) The impact of Miocene atmospheric carbon dioxide fluctuations on climate and the evolution of terrestrial ecosystems. Proceedings of the National Academy of Sciences of the USA 105: 449–453.

Linka M and Weber APM (2005) Shuffling ammonia between mitochondria and plastids during photorespiration. Trends in Plant Science 10: 461–465.

Long SP, Zhu XG, Naidu SL et al. (2006) Can improvement in photosynthesis increase crop yields? Plant, Cell and Environment 29: 315–330.

Marti MC, Olmos E, Calvete JJ et al. (2009) Mitochondrial and nuclear localization of a novel pea thioredoxin: identification of its mitochondrial target proteins. Plant Physiology 150: 646–657.

Noctor G, Arisi AM, Jouanin L et al. (1999) Photorespiratory glycine enhances glutathione accumulation in both the chloroplastic and cytosolic compartments. Journal of Experimental Botany 50: 1157–1167.

Nunes‐Nesi A, Sulpice R, Gibon Y et al. (2008) The enigmatic contribution of mitochondrial function in photosynthesis. Journal of Experimental Botany 59: 1675–1684.

Osmond CB, Badger M, Maxwell K et al. (1997) Too many photons: photorespiration, photoinhibition and photooxidation. Trends in Plant Science 2: 119–121.

Price GD, Badger MR, Woodger FJ et al. (2008) Advances in understanding the cyanobacterial CO2‐concentrating‐mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. Journal of Experimental Botany 59: 1441–1461.

Rachmilevitch S, Cousins AB and Bloom AJ (2004) Nitrate assimilation in plant shoots depends on photorespiration. Proceedings of the National Academy of Sciences of the USA 101: 11506–11510.

Rawsthorne S (1992) C3‐C4 intermediate photosynthesis – linking physiology to gene expression. Plant Journal 2: 267–274.

Reumann S and Weber AP (2006) Plant peroxisomes respire in the light: some gaps of the photorespiratory C2 cycle have become filled – others remain. Biochimica et Biophysica Acta 1763: 1496–1510.

Rodriguez‐Ezpeleta N, Brinkmann H, Burey SC et al. (2005) Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Current Biology 15: 1325–1330.

Scheibe R, Backhausen JE, Emmerlich V et al. (2005) Strategies to maintain redox homeostasis during photosynthesis under changing conditions. Journal of Experimental Botany 56: 1481–1489.

Sharkey TD (1988) Estimating the rate of photorespiration in leaves. Physiologia Plantarum 73: 147–152.

Somerville CR (1986) Analysis of photosynthesis with mutants of higher plants and algae. Annual Review of Plant Physiology 37: 467–506.

Somerville CR (2001) An early Arabidopsis demonstration resolving a few issues concerning photorespiration. Plant Physiology 125: 20–24.

Tabita FR, Satagopan S, Hanson TE et al. (2008) Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships. Journal of Experimental Botany 59: 1515–1524.

Taira M, Valtersson U, Burkhardt B et al. (2004) Arabidopsis thaliana GLN2‐encoded glutamine synthetase is dual targeted to leaf mitochondria and chloroplasts. Plant Cell 16: 2048–2058.

Taylor NL, Day DA and Millar AH (2004) Targets of stress‐induced oxidative damage in plant mitochondria and their impact on cell carbon/nitrogen metabolism. Journal of Experimental Botany 55: 1–10.

Tcherkez GGB, Farquhar GD and Andrews TJ (2006) Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proceedings of the National Academy of Sciences of the USA 103: 7246–7251.

Timm S, Nunes‐Nesi A, Pärnik T et al. (2008) A cytosolic pathway for the conversion of hydroxypyruvate to glycerate during photorespiration in Arabidopsis. Plant Cell 20: 2848–2859.

Zelitch I, Schultes NP, Peterson RB et al. (2009) High glycolate oxidase activity is required for survival of maize in normal air. Plant Physiology 149: 195–204.

Further Reading

Allen JF and Martin W (2007) Evolutionary biology: out of thin air. Nature 445: 610–612.

Andrews TJ and Lorimer GH (1978) Photorespiration – still unavoidable? FEBS Letters 90: 1–9.

Canfield DE (2005) The early history of atmospheric oxygen: homage to Robert M. Garrels. Annual Review of Earth and Planetary Sciences 33: 1–36.

Giordano M, Beardall J and Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annual Review of Plant Biology 56: 99–131.

Gould SB, Waller RF and McFadden GI (2008) Plastid evolution. Annual Review of Plant Biology 59: 491–517.

Hetherington AM and Raven JA (2005) The biology of carbon dioxide. Current Biology 15: R406–R410.

Schwartzman D, Caldeira K and Pavlov A (2008) Cyanobacterial emergence at 2.8 Gya and greenhouse feedbacks. Astrobiology 8: 187–203.

Tolbert NE (1997) The C2 oxidative photosynthetic carbon cycle. Annual Review of Plant Physiology and Plant Molecular Biology 48: 1–25.

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Bauwe, Hermann(Feb 2010) Photorespiration. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001292.pub2]