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The Plant Cell 17:2139-2141 (2005)
© 2005 American Society of Plant Biologists

IN THIS ISSUE

Photorespiration Revisited

Nancy A. Eckardt, News and Reviews Editor

neckardt{at}aspb.org

As early as 1920, Otto Warburg made the observation that O2 inhibits photosynthesis (Warburg, 1920Go). This phenomenon, originally known as the "Warburg effect," was later recognized as the light-dependent release of CO2 by photosynthetic organisms, or photorespiration, and was the subject of intense investigation and debate for many decades (reviewed in Ogren, 1984Go). The mechanistic basis of photorespiration was found in the dual nature of ribulose bisphosphate (RuBP) carboxylase/oxygenase (Andrews et al., 1971Go; Bowes et al., 1971Go). The photosynthetic carboxylation reaction yields two molecules of 3-phosphoglycerate (3PGA), which enter the C3 carbon reduction or Calvin cycle, whereas oxygenation, which competitively inhibits carboxylation, produces one molecule of 3PGA and one molecule of the 2-carbon compound phosphoglycolate. The photorespiratory pathway is the conversion of phosphoglycolate to CO2 and 3PGA, a complex series of reactions that takes place across three separate subcellular compartments; chloroplasts, peroxisomes, and mitochondria (Kisaki and Tolbert, 1969Go). Photorespiration results in the loss of up to 25% of the carbon that is fixed during photosynthetic carbon assimilation (Ludwig and Canvin, 1971Go). Despite the net loss of carbon, the photorespiratory cycle allows for recovery into the C3 carbon assimilation cycle of three moles of carbon (as 3PGA) for every one that is respired as CO2 (Berry et al., 1978Go). The photorespiratory cycle is essential for plant growth, as demonstrated by photorespiration mutants that are inviable in normal air (~0.04% CO2) and grow only in elevated CO2 (1 to 2% CO2), conditions under which RuBP oxygenation is suppressed (Somerville and Ogren, 1982Go).

The study of photorespiration also occupies a central position in the history of modern plant biology. Somerville (2001)Go presents an excellent brief history of the early work on photorespiration and the development of Arabidopsis as a model organism. Somerville and colleagues focused on unsolved problems of photorespiration to demonstrate the utility of a genetic approach (i.e., mutant screening) to investigating fundamental questions in plant biology. The collection of photorespiration mutants isolated was instrumental in proving that Rubisco oxygenase activity is the entry point of glycolate into the photorespiratory pathway and that operation of the pathway is essential for plant growth. The isolation of photorespiratory mutants led to the confirmation and characterization of many of the enzymes and some of the transporters involved in this complex pathway (see figure; Somerville, 2001Go).



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  		An Abbreviated Scheme of the Photorespiratory Pathway.

Phosphoglycolate produced by RuBP oxygenase activity is converted to glycolate by phosphoglycolate phosphatase in the chloroplast. Glycolate enters peroxisomes and is converted to glyoxylate by glycolate oxidase. Glyoxylate is transaminated to Gly by either Ser:glyoxylate aminotransferase or Glu:glyoxylate aminotransferase. In mitochondria, Gly is converted to CO2, ammonia, and the methylene group of methylene tetrahydrofolate (C1-THF). Gly and C1-THF condense to produce Ser. Peroxisomal Ser is deaminated to hydroxypyruvate, which is reduced to glycerate by hydroxypyruvate reductase. Glycerate enters the chloroplast and is phosphorylated to 3PGA, an intermediate of the Calvin cycle. Ammonia released during Gly decarboxylation is used by Gln synthetase to produce Gln. Glu synthase condenses 2-oxoglutarate (2-OG) and Gln to produce two molecules of Glu. A dicarboxylate transporter (DT) in the chloroplast envelope consisting of two transporters transfers oxoglutarate, Glu, and Gln across the chloroplast envelope. Overall, two molecules of phosphoglycolate are converted to one molecule of phosphoglycerate and one molecule of CO2. (Reproduced with permission from Somerville, 2001Go.)

 
In this issue of The Plant Cell, Boldt et al. (pages 2413–2420) present the identification of the last previously uncharacterized gene in the photorespiratory cycle in Arabidopsis, D-GLYCERATE 3-KINASE (GLYK), which encodes the enzyme that catalyzes that last step in the pathway, the phosphorylation of glycerate to 3PGA. Glycerate kinases (GKs) are also present in nonplant organisms, such as animals and bacteria, in which they participate in a number of carbon metabolism reactions. Interestingly, GLYK mutants have never turned up in plant photorespiratory mutant screens, and Boldt et al. could find no plant proteins or DNA sequences homologous to animal or bacterial GKs. The authors therefore identified the gene from the amino acid sequence obtained from mass spectrographic analysis of the enzyme purified from Arabidopsis leaves. The sequence corresponded to the previously uncharacterized gene At1g80380 on chromosome 1, now named AtGLYK. The enzyme purified from Arabidopsis leaves or produced in recombinant form from the GLYK sequence expressed in Escherichia coli functions specifically as a GK in vitro.

Boldt et al. then analyzed T-DNA insertional knockout mutants of GLYK and found that they show no GLYK activity and accumulate glycerate. Like many other photorespiratory mutants, the glyk mutants were found to be inviable in normal air and grew only in a high CO2 atmosphere, indicating that this single-copy gene is the exclusive source of GLYK activity in Arabidopsis. The results provide conclusive evidence that the recovery of carbon into the C3 carbon reduction cycle in the form of 3PGA is an essential feature of the photorespiratory pathway, and this last step in the pathway is catalyzed solely by GLYK in Arabidopsis. As explained by Ogren (1984)Go, "it is essential that carbon remaining after glycine decarboxylation be returned to the photosynthetic cycle so as to maintain a concentration of photosynthesis intermediates sufficient to support the steady state of CO2 fixation." Thus, the work of Boldt et al. provides satisfying closure (at least in a narrow sense) to the problem of photorespiration, a problem long ago described as "a nightmare oppressing all who are concerned with the exact measurement of photosynthesis" (Rabinowitch, 1945Go).

Although all of the Arabidopsis genes encoding enzymes that catalyze the basic steps of the photorespiratory pathway have been cloned, questions remain, for example, concerning the nature and regulation of the transporters required for movement of substrates and products in and out of chloroplasts, peroxisomes, and mitochondria (only some of which have been characterized), the evolutionary origins of components of the pathway, and what has often been described as the holy grail of photosynthesis research, the possibility of increasing photosynthesis by reducing photorespiration.

The identification of GLYK and phylogenetic analysis by Boldt et al. provides fodder for stimulating further research on the evolutionary origin of photorespiration. Homologous proteins were found in other higher plants and green algae, filamentous cyanobacteria (Nostoc and Anabaena), and fungi (Saccharomyces). The authors constructed a phylogenetic tree using plant and nonplant GK amino acid sequences. The GK proteins fell into three distinct clades: the higher plant GLYKs, which include homologs from cyanobacteria Nostoc and Anabaena and the yeast Saccharomyces; animal GKs, which include homologs from specialized bacteria such as Thermotoga; and bacterial GKs, which include homologs from Escherichia, Erwinia, and Klebsiella. The higher plant GLYKs appear to be only distantly related to the other two GK clades, suggesting that plant GLYKs constitute a novel kinase family.

Notably, Synechocystis, a unicellular non-nitrogen-fixing cyanobacterium, contains a GK enzyme that falls within the bacterial clade, only distantly related to the higher plant and yeast GLYKs, and more closely related to GKs from animals and specialized bacteria. Hagemann et al. (2005)Go recently showed that null mutations in the genes encoding the subunits of Gly decarboxylase, an essential photorespiratory enzyme in higher plants, do not significantly affect viability or growth of Synechocystis. These results suggest that the photorespiratory pathway is not essential in Synechocystis. Cyanobacteria have evolved highly complex CO2 concentrating mechanisms that operate to increase the CO2 concentration around Rubisco inside subcellular compartments called carboxysomes (reviewed in Badger and Price, 2003Go), which might be expected to relax the requirement for the photorespiratory cycle. The phylogenetic analysis of Boldt et al. supports the notion that Synechocystis GK has a function in carbon metabolism similar to that in bacteria and animals, rather than a primary role in photorespiration, but this remains to be investigated.

It is also interesting that the GLYK homolog in Saccharomyces (yeast) appears to be more closely related to the higher plant GLYKs than are the cyanobacterial GLYKs and only distantly related to animal and bacterial GKs. The function of the GLYK homolog in Saccharomyces, which lacks photosynthesis and photorespiration, also remains to be determined. Thus, the work of Boldt et al. closes one chapter in the long and interesting tale of photorespiration and opens several others.


   REFERENCES
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Andrews, T.J., Lorimer, G.H., and Tolbert, N.E. (1971). Incorporation of molecular oxygen into glycine and serine during photorespiration in spinach leaves. Biochemistry 10, 4777–4782.[CrossRef][Medline]

Badger, M.R., and Price, G.D. (2003). CO2 concentrating mechanisms in cyanobacteria: Molecular components, their diversity and evolution. J. Exp. Bot. 54, 609–622.[Abstract/Free Full Text]

Berry, J.A., Osmond, C.B., and Lorimer, G.H. (1978). Fixation of 18O2 during photorespiration. Kinetic and steady state studies of the photorespiratory carbon oxidation cycle with intact leaves and isolated chloroplasts of C3 plants. Plant Physiol. 62, 954–967.[Abstract/Free Full Text]

Boldt, R., Edner, C., Kolukisaoglu, U., Hagemann, M., Weckwerth, W., Wienkoop, S., Morgenthal, K., and Bauwe, H. (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.[Abstract/Free Full Text]

Bowes, G., Ogren, W.L., and Hageman, R.H. (1971). Phosphoglycolate production catalyzed by ribulose diphosphate carboxylase. Biochem. Biophys. Res. Commun. 45, 716–722.[CrossRef][Web of Science][Medline]

Hagemann, M., Vinnemeier, J., Oberpichler, I., Boldt, R., and Bauwe, H. (2005). The glycine decarboxylase complex is not essential for the cyanobacterium Synechocystis sp strain PCC 6803. Plant Biol. 7, 15–22.

Kisaki, T., and Tolbert, N.E. (1969). Glycolate and glyoxylate metabolism by isolated peroxisomes or chloroplasts. Plant Physiol. 44, 242–250.[Abstract/Free Full Text]

Ludwig, J., and Canvin, D.T. (1971). The rate of photorespiration during photosynthesis and the relationship of the substrate of light respiration to the products of photosynthesis in sunflower leaves. Plant Physiol. 48, 712–719.[Abstract/Free Full Text]

Ogren, W.L. (1984). Photorespiration: Pathways, regulation, and modification. Annu. Rev. Plant Physiol. 35, 415–442.[CrossRef][Web of Science]

Rabinowitch, E.I. (1945). Photosynthesis and Related Processes, Vol. I. (New York: Interscience Publishers).

Somerville, C. (2001). An early Arabidopsis demonstration. Resolving a few issues concerning photorespiration. Plant Physiol. 125, 20–24.[Free Full Text]

Somerville, C., and Ogren, W.L. (1982). Genetic modification of photorespiration. Trends Biochem. Sci. 7, 171–174.

Warburg, O. (1920). Über die Geschwindigkeit der photochemischen Kohlensäurezersetzung in lebenden Zellen. II. Biochem. Z. 103, 188–217.


Related articles in Plant Cell:

D-GLYCERATE 3-KINASE, the Last Unknown Enzyme in the Photorespiratory Cycle in Arabidopsis, Belongs to a Novel Kinase Family
Ralf Boldt, Christoph Edner, Üner Kolukisaoglu, Martin Hagemann, Wolfram Weckwerth, Stefanie Wienkoop, Katja Morgenthal, and Hermann Bauwe
Plant Cell 2005 17: 2413-2420. [Abstract] [Full Text]  



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