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Photorespiration and the Potential to Improve Photosynthesis Hagemann and Bauwe 111 Available online at www.sciencedirect.com ScienceDirect Photorespiration and the potential to improve photosynthesis Martin Hagemann and Hermann Bauwe The photorespiratory pathway, in short photorespiration, is an carboxylase (RuBP carboxylase/oxygenase; Rubisco) of essential metabolite repair pathway that allows the the Calvin–Benson cycle (CB cycle) fixes O2 instead of photosynthetic CO2 fixation of plants to occur in the presence CO2 [5]. Oxygenation of RuBP forms 3-phosphoglycer- of oxygen. It is necessary because oxygen is a competing ate (3PGA) and 2-phosphoglycolate (2PG), whereas car- substrate of the CO2-fixing enzyme ribulose 1,5-bisphosphate boxylation of RuBP forms 2 mol 3PGA. In C3 plants, carboxylase, forming 2-phosphoglycolate that negatively every third to fourth molecule of RuBP is oxygenated interferes with photosynthesis. Photorespiration very efficiently rather than carboxylated at the present day air CO2/O2 recycles 2-phosphoglycolate into 3-phosphoglycerate, which ratio (0.04% CO2/20.95% O2) [1,6]. Accordingly, large re-enters the Calvin–Benson cycle to drive sustainable amounts of 2PG are produced during the day. Photores- photosynthesis. Photorespiration however requires extra piration recycles two molecules of 2PG into one molecule energy and re-oxidises one quarter of the 2-phosphoglycolate of 3PGA; thus, only 25% of organic carbon is lost as CO2 carbon to CO2, lowering potential maximum rates of whereas 75% is salvaged and used to synthesize RuBP, photosynthesis in most plants including food and energy crops. refilling the CB cycle. This review discusses natural and artificial strategies to reduce the undesired impact of air oxygen on photosynthesis and in The photorespiratory pathway involves more than 20 dif- turn plant growth. ferent enzymes and (mostly unidentified) transporters that Address are distributed over at least three compartments in plant Universita¨ t Rostock, Institut fu¨ r Biowissenschaften, Abteilung cells, the chloroplast, the peroxisome, and the mitochon- Pflanzenphysiologie, Albert-Einstein-Str. 3, D-18051 Rostock, Germany drion (Figure 1). Rubisco generates 2PG in the chloroplast. Corresponding author: Hagemann, Martin 2PG phosphatase (PGLP) dephosphorylates 2PG into ([email protected]) glycolate, which is exported from the chloroplast into the cytosol by the recently discovered glycolate/glycerate Current Opinion in Chemical Biology 2016, 35:109–116 antiporter [7 ] and then diffuses into the peroxisome. In the peroxisome, glycolate oxidase (GOX) catalyses the O2- This review comes from a themed issue on Energy dependent irreversible oxidation of glycolate to glyoxylate Edited by Wenjun Zhang and David F Savage giving rise to H2O2, which is quickly detoxified by catalase (CAT). Still in the peroxisome, glyoxylate becomes trans- aminated to glycine by the parallel action of glutamate:- http://dx.doi.org/10.1016/j.cbpa.2016.09.014 glyoxylate aminotransferase (GGAT) and serine:glyoxylate aminotransferase (SGAT). The required glutamate is 1367-5931/# 2016 Elsevier Ltd. All rights reserved. imported from the chloroplast by exchange against malate via dicarboxylate antiporters. Glycine then moves into the mitochondrion where the glycine decarboxylase multi- enzyme system (GDC) and serine hydroxymethyltransfer- ase (SHMT) convert two molecules of glycine to one What is photorespiration? molecule of serine, NH3 and CO2. In the oxidative decar- + Photorespiration, in contrast to the light-independent boxylation step, GDC reduces NAD and to NADH. processes of mitochondrial respiration, is the light-de- Serine is exported from the mitochondrion back to the pendent consumption of O2 and coupled release of CO2 peroxisome to return its amino group to glyoxylate in the that occurs simultaneously with photosynthetic CO2 SGAT reaction, producing hydroxypyruvate (HP). Next, uptake and O2 release in all plants, algae and cyanobac- another peroxisomal enzyme, HP reductase (HPR1), teria. Rates of plant photorespiration can be very high, reduces HP to glycerate. The necessary NADH is pro- duced from malate oxidation by peroxisomal malate especially under conditions of high temperature and water shortage. Globally, the process re-liberates an dehydrogenase. The glycerate returns into the chloroplast estimated 29 Gt of freshly assimilated carbon per year to become phosphorylated by glycerate 3-kinase (GLYK) to finally yield 3PGA. This CB cycle intermediate is used into the atmosphere [1,2]. On the molecular level, the term photorespiration also connotes the photorespiratory to regenerate the Rubisco acceptor molecule RuBP. Sev- pathway as an integral component of the photosynthetic- eral more enzymes are essential for the entire photore- spiratory metabolism for example to re-assimilate the photorespiratory supercycle [3,4]. Photorespiration starts when the CO2 fixation enzyme ribulose 1,5-bisphosphate photorespiratory NH3 in the photorespiratory nitrogen www.sciencedirect.com Current Opinion in Chemical Biology 2016, 35:109–116 110 Energy Figure 1 NADPH ATP Triose phosphate Calvin-Benson cycle CO 2 3PGA Glutamate synthase O2 Photorespiratory cycle 2– CH2O-PO3 pathway ATP ADP Phosphoglycolate COO– NH+ 4 GS2 ADP PGLP GLYK Glu Gln Pi ATP Fd-GltS CH2OH Fd Fd ox red Glycolate COO– Glu 20G Chloroplast CH2OH H-C-OH COO– Glycerate O NAD+ GOX 2 CAT pMDH HPR1 H2O2 NADH CH OH ½O2 H2O 2 CHO C=O Glyoxylate COO– COO– Hydroxypyruvate GGAT SGAT Glu 20G Gln Glu ASNS SGAT SGAT Asp Asn Ala OAA 2-OS Pyr ω-Amidase + NH4 Peroxisome + CH2-NH3 SHMT CH2OH Glycine COO– H-C-NH+ THF 3 P T COO– Serine GDC CH2-THF NAD+ L NADH CO2 NH3 Mitochondrion Current Opinion in Chemical Biology The photorespiratory pathway and its interconnection with photosynthetic Calvin–Benson cycle and NH3 assimilation in higher plants. (2OG, 2- oxoglutarate; 2-OS, 2-oxosuccinamate; 3PGA, 3-phosphoglycerate; Ala, alanine; Asn, asparagine; ASNS, asparagine synthetase; Asp, aspartate; CAT, catalase; FD-GltS, ferredoxin-dependent glutamate synthase; GDC, glycine decarboxylase complex; GGAT, glutamate:glyoxylate aminotransferase; Gln, glutamine; Glu, glutamate; GLYK, glycerate 3-kinase; GOX, glycolate oxidase; GS2, glutamine synthetase; HPR1, hydroxypyruvate reductase; OAA, oxaloacetate; PGLP, phosphoglycolate phosphatase; Pyr, pyruvate; Rubisco, ribulose 1,5-bisphosphate carboxylase/oxygenase; SGAT, serine:glyoxylate aminotransferase; SHMT, serine hydroxymethyltransferase.) Current Opinion in Chemical Biology 2016, 35:109–116 www.sciencedirect.com Photorespiration and the potential to improve photosynthesis Hagemann and Bauwe 111 cycle [8] or to remove inhibitory 5-formyl tetrahydrofolate algae [17] and more recently in red algae [18 ]. Second, produced in a side-reaction of SHMT [9 ]. the reconstructed phylogenies of photorespiratory enzymes reflect their ancient origins in different groups Photorespiration is an energy-demanding process that of prokaryotes that served as eukaryotic host cell or as formally requires a total of 3.25 mol ATP and 2 mol endosymbionts for the origin of mitochondria and plastids NADPH per one oxygenation of RuBP, which is about [19]. one-third of the total energetic costs of CO2 fixation in air [10]. Whereas the photorespiratory core pathway (net Over geologic times, a number of adaptations occurred reaction: 2 mol 2PG + O2 ! 3PGA + CO2 + NH3; see leading to variations in the photorespiratory metabolism. Figure 1) consumes 1 mol of ATP for the phosphorylation Most cyanobacteria metabolize 2PG not only by the of glycerate to 3PGA via GLYK (0.5 mol ATP per oxy- plant-like photorespiratory cycle, but can also convert genation event), the reassimilation of the released am- 2 mol glyoxylate into glycerate using the bacterial glyce- monia into glutamine and the conversion of 3PGA into rate pathway with tartronate-semialdehyde as intermedi- RuBP via the CB cycle is highly energy-demanding. ate [16 ]. This pathway also releases one CO2 per two molecules of 2PG but does not require transamination of Why is there photorespiration? glyoxylate and hence does not release ammonia, which The high energy demand of photorespiration and partic- makes it more energy efficient. Moreover, some cyano- ularly the inherent loss of freshly assimilated CO2 raise bacterial strains have the potential to completely oxidize the question why this process exists? The answer is glyoxylate into CO2 [16 ]. Cyanobacteria as well as relatively simple: the photorespiratory pathway in es- chlorophytes evolved glycolate dehydrogenase-(GDH)- sence renders the CB cycle insensitive towards oxygen. based photorespiration, which is not producing the by- All oxygenic phototrophs rely on the CB cycle with product H2O2 and gains NAD(P)H, in contrast to GOX- Rubisco as the key carboxylating enzyme. The chemistry based photorespiration in other eukaryotic alga [18 ,20] of the Rubisco-catalysed reaction dictates that competi- and plants. tive oxygenation occurs whenever O2 is present. The essential role of photorespiration for enabling oxygenic Photorespiration is a major metabolic photosynthesis is clearly supported by many mutant pathway and a target for crop improvement studies, which showed that knocking out genes encoding As outlined before, the repair of the consequences of photorespiratory enzymes results in the so-called ‘photo- RuBP oxygenation occurs very efficiently, salvaging three respiratory phenotype’, that is such mutants cannot grow out of four glycolate carbons for photosynthesis [12], but in ambient air but can be rescued in air with a 20-fold to
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