Genetic Manipulation of Glycine Decarboxylation

Journal of Experimental Botany, Vol. 54, No. 387, pp. 1523±1535, June 2003 DOI: 10.1093/jxb/erg171 REVIEW ARTICLE Genetic manipulation of glycine decarboxylation Hermann Bauwe1 and UÈ ner Kolukisaoglu Abteilung P¯anzenphysiologie der UniversitaÈt Rostock, Albert-Einstein-Strasse 3, D-18051 Rostock, Germany Received 2 October 2002; Accepted 11 March 2003 Downloaded from https://academic.oup.com/jxb/article/54/387/1523/540368 by guest on 26 September 2021 Abstract complex that occurs in all organisms, prokaryotes and eukaryotes. GDC, together with serine hydroxymethyl- The glycine±serine interconversion, catalysed by gly- transferase (SHMT), is responsible for the inter-conversion cine decarboxylase and serine hydroxymethyltransfer- of glycine and serine, an essential and ubiquitous step of ase, is an important reaction of primary metabolism in primary metabolism. In Escherichia coli, 15% of all all organisms including plants, by providing one-car- carbon atoms assimilated from glucose are estimated to bon units for many biosynthetic reactions. In plants, pass through the glycine±serine pathway (Wilson et al., in addition, it is an integral part of the photorespira- 1993). In eukaryotes, GDC is present exclusively in the tory metabolic pathway and produces large amounts mitochondria, whereas isoforms of SHMT also occur in the of photorespiratory CO within mitochondria. 2 cytosol and, in plants, in plastids. The term `glycine±serine Although controversial, there is signi®cant evidence that this process, by the relocation of glycine decar- interconversion' might suggest that the central importance boxylase within the leaves from the mesophyll to the of this pathway is just the synthesis of serine from glycine and vice versa. However, in both directions of the bundle-sheath, contributed to the evolution of C4 photosynthesis. In this review, some aspects of cur- concerted reaction of GDC and SHMT, tetrahydrofolate 5 10 rent knowledge about glycine decarboxylase and ser- (THF) becomes N ,N -methylenated making these reac- ine hydroxymethyltransferase and the role of these tions the most important source of active one-carbon-units enzymes in metabolism, about the corresponding for a number of biosynthetic processes such as the genes and their expression as well as about mutants biosynthesis of methionine, pyrimidines, and purines and anti-sense plants related to these genes or pro- (Fig. 1). Glycine and serine itself are precursors for cesses will be summarized and discussed. From a chlorophyll, glutathione, tryptophan, phosphatidylcholine comparison of the available information about the and related phospholipids, and ethanolamine. The role of number and organization of GDC and SHMT genes in GDC in all organisms is to interconnect the metabolism of the genomes of Arabidopsis thaliana and Oryza sativa one-, two-, and three-carbon compounds (reviewed by it appears that these and, possibly, other genes Kikuchi, 1973; Oliver, 1994; Cossins, 2000; Hanson and related to photorespiration, are similarly organized Roje, 2001; Douce et al., 2001). It is therefore not even in only very distantly related angiosperms. surprising, that a malfunction of GDC results in serious metabolic consequences. Humans, for example, can suffer from non-ketotic hyperglycinemia, an inherited and Key words: Arabidopsis, genetic engineering, glycine incurable disease with devastating and often lethal symp- decarboxylase, mutant analysis, one-carbon metabolism, photo- toms (Kure et al., 1997). Plants are not able to perform respiration, photosynthesis, serine hydroxymethyltransferase, oxygenic photosynthesis without GDC or SHMT and, with reduced activities of these enzymes, will usually show severe growth retardation (Somerville, 2001; Wingler et al., 1997; Heineke et al., 2001). Introduction Compared with other organisms, the photorespiratory Glycine decarboxylase (GDC, also named glycine-cleav- pathway of plants provides a novel role for both GDC and age-system or glycine dehydrogenase) is a multi-protein SHMT. In plants, GDC and SHMT are integral 1 To whom correspondence should be addressed. Fax: +49 381 498 6112. E-mail: [email protected] 5 10 Abbreviations: CH2-THF, N ,N -methylene tetrahydrofolate; GDC, glycine decarboxylase; LPD, dihydrolipoamide dehydrogenase; SHMT, serine hydroxymethyltransferase. Journal of Experimental Botany, Vol. 54, No. 387, ã Society for Experimental Biology 2003; all rights reserved 1524 Bauwe and Kolukisaoglu understood. Secondly, the glycine±serine interconversion, by providing one-carbon units, is directly related to many biosynthetic processes outside the photorespiratory pathway. Finally, in photosynthesizing organs of C3 plants, GDC is the major source of internally generated CO2 and, as will be discussed in more detail later, may in¯uence CO2 concentration gradients within leaves. Several excellent recent reviews cover different aspects of the biochemistry and enzymology of glycine decarboxylation and its relation to plant metabolism (for example Douce et al., 2001; Mouillon et al., 1999; Hanson and Roje, 2001). In this review, these aspects will only be Downloaded from https://academic.oup.com/jxb/article/54/387/1523/540368 by guest on 26 September 2021 Fig. 1. Schematic presentation of the glycine±serine interconversion and its connection to one-carbon metabolism in different subcellular discussed brie¯y, instead the focus will be on the compartments. Circles P, T, H, and L represent the four protein underlying genetics and on the results obtained with components of glycine decarboxylase and circle S represents serine mutants and transgenic plants. As stated above, GDC hydroxymethyltransferase (Cossins, 2000; Ravanel et al., 2001). closely co-operates with SHMT both during the photorespiratory decarboxylation of glycine and the supply of components of primary metabolism not only in the context one-carbon units for other biosynthetic processes. of `house-keeping' glycine±serine interconversion as dis- Therefore, both GDC and SHMT will be covered in this cussed above. Their additional function in plants is the survey. breakdown of glycine that originates, after several enzymatic reactions, from the oxygenase reaction of Rubisco (Bowes et al., 1971; Tolbert, 1973). By this side Protein components and reactions of the glycine±serine interconversion reaction of oxygenic photosynthesis, 2-phosphoglycolate is produced and, by the action of ten different enzymes The general course of the individual reactions is well including GDC and SHMT, is subsequently recycled as 3- known from the work of several groups over many years phosphoglycerate to the Calvin cycle. The contributing (Kikuchi, 1973; Oliver, 1994; Bourguignon et al., 1988; enzymes are localized in three different organelles, Walker and Oliver, 1986a). More details of the involved chloroplasts, peroxisomes, and mitochondria. In C3 plants, catalytic mechanisms can be expected from crystallo- if grown under illumination in ambient air, glycine graphic data in the near future. Strongly simpli®ed, the synthesis occurs at very high rates and requires a high course of the reactions in the context of the photorespira- capacity for mitochondrial glycine oxidation. In fact, tory pathway can be described by the following equations: glycine is the preferred substrate of mitochondria and becomes very rapidly oxidized (Day et al., 1985; KroÈmer GDC: + and Heldt, 1991) leading to relatively low glycine Glycine + NAD + THF ® Methylene-THF + CO2 + concentrations in leaves (Leidreiter et al., 1995). NH3 + NADH GDC, under unstressed conditions, represents the sole SHMT: source of photorespiratory CO2 and NH3 and functions as Glycine + Methylene-THF + H2O ® Serine + THF an important link between photorespiration and other GDC/SHMT: + metabolic pathways such as nitrate and ammonia assimi- 2 Glycine + NAD ® Serine + CO2 +NH3 + NADH lation. Much of the earlier work on photorespiration was directed towards attempts to reduce the massive net CO GDC comprises four protein components (Fig. 1). All 2 four individual proteins, which have been designated P, T, losses that occur in C3 plants especially in warm environ- ments. From research conducted over the past 20 years, it H, and L protein, are nuclear encoded and targeted into the is now clear that attempts to abolish or even reduce mitochondrial matrix. photorespiration by reducing the activity of individual enzymes of the photorespiratory pathway, except ribulose- P protein (EC 1.4.4.2) 1,5-bisphosphate oxygenase, will not lead to improved P protein, a pyridoxal-5-phosphate containing homodimer plant performance. of about 200 kDa, is the actual glycine decarboxylating What then can be the purpose of continuing attempts to subunit. P protein has also been identi®ed as the binding manipulate glycine decarboxylation genetically? Firstly, it protein of a host-speci®c toxin, victorin (Wolpert et al., appears that regulatory interactions exist between photo- 1994). The product of the P protein-catalysed decarbox- respiration and photosynthesis triggered by metabolite ylation of glycine is CO2 and not bicarbonate (Sarojini and levels. The nature of these interactions is not well Oliver, 1983). The remaining amino methylene moiety is Manipulation of glycine decarboxylation 1525 transferred to the distal sulphur atom of the oxidized dehydrogenase complex (Luethy et al., 1996). By contrast lipoamide arm of H protein (Douce et al., 2001). with pea, where it was reported that mitochondrial L protein is encoded by a single gene

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