Abstract
Glycine decarboxylase (GDC) plays an important role in the photorespiratory metabolism of plants. GDC is composed of four subunits (P, H, L, and T) with the P-subunit (GLDP) serving as the actual decarboxylating unit. In C(3) plants, GDC can be found in all photosynthetic cells, whereas in leaves of C(3)-C(4) intermediate and C(4) species its occurrence is restricted to bundle-sheath cells. The specific expression of GLDP in bundle-sheath cells might have constituted a biochemical starting point for the evolution of C(4) photosynthesis. To understand the molecular mechanisms responsible for restricting GLDP expression to bundle-sheath cells, we performed a functional analysis of the GLDPA promoter from the C(4) species Flaveria trinervia. Expression of a promoter-reporter gene fusion in transgenic plants of the transformable C(4) species Flaveria bidentis (C(4)) showed that 1,571 bp of the GLDPA 5' flanking region contain all the necessary information for the specific expression in bundle-sheath cells and vascular bundles. Interestingly, we found that the GLDPA promoter of F. trinervia exhibits a C(4)-like spatial activity also in the C(3) plant Arabidopsis (Arabidopsis thaliana), indicating that a mechanism for bundle-sheath-specific expression is also present in this C(3) species. Using transgenic Arabidopsis, promoter deletion studies identified two regions in the GLDPA promoter, one conferring repression of gene expression in mesophyll cells and one functioning as a general transcriptional enhancer. Subsequent analyses in transgenic F. bidentis confirmed that these two segments fulfill the same function also in the C(4) context.
Highlights
Glycine decarboxylase (GDC) plays an important role in the photorespiratory metabolism of plants
Immunolabeling studies have shown that, in C4 plants, GLDP accumulates exclusively in bundle-sheath cells of leaves (Hylton et al, 1988; Morgan et al, 1993; Yoshimura et al, 2004). To examine whether this C4-characteristic localization of the P-protein is due to specific accumulation of GLDPA mRNA in this compartment, we analyzed the expression pattern of the GLDPA gene in leaves of the C4 species F. trinervia by in situ hybridization
In leaves of F. trinervia, transcripts of the GLDPA gene could only be detected in bundle-sheath and not in mesophyll cells (Fig. 1A)
Summary
Glycine decarboxylase (GDC) plays an important role in the photorespiratory metabolism of plants. To understand the molecular mechanisms responsible for restricting GLDP expression to bundle-sheath cells, we performed a functional analysis of the GLDPA promoter from the C4 species Flaveria trinervia. There are indications that photorespiration exists in C4 plants, albeit at a much lower level than in C3 plants (Osmond and Harris, 1971; Furbank and Badger, 1983; de Veau and Burris, 1989) This is likely due to the fact that photorespiration in C4 species is strictly confined to the bundle-sheath cells in the leaves, while in. Consistent with the compartmentation of the photorespiratory cycle, GDC is present in all photosynthetic cells of C3 plant leaves, but strictly confined to the bundle-sheath cells in C4 species (Ohnishi and Kanai, 1983). None of the GDC subunits has been detected in the mesophyll cells of C4 plants (Morgan et al, 1993)
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