Regulation of the Photorespiratory GLDPA Gene in C4 Flaveria: An Intricate Interplay of Transcriptional and Posttranscriptional Processes

The mitochondrial Gly decarboxylase complex (GDC) is a key component of the photorespiratory pathway that occurs in all photosynthetically active tissues of C-3 plants but is restricted to bundle sheath cells in C-4 species. GDC is also required for general cellular C-1 metabolism. In the Asteracean C-4 species Flaveria trinervia, a single functional GLDP gene, GLDPA, encodes the P-subunit of GDC, a decarboxylating Gly dehydrogenase. GLDPA promoter reporter gene fusion studies revealed that this promoter is active in bundle sheath cells and the vasculature of transgenic Flaveria bidentis (C-4) and the Brassicacean C-3 species Arabidopsis thaliana, suggesting the existence of an evolutionarily conserved gene regulatory system in the bundle sheath. Here, we demonstrate that GLDPA gene regulation is achieved by an intricate interplay of transcriptional and posttranscriptional mechanisms. The GLDPA promoter is composed of two tandem promoters, P-R2 and P-R7, that together ensure a strong bundle sheath expression. While the proximal promoter (P-R7) is active in the bundle sheath and vasculature, the distal promoter (P-R2) drives uniform expression in all leaf chlorenchyma cells and the vasculature. An intron in the 5' untranslated leader of P-R2-derived transcripts is inefficiently spliced and apparently suppresses the output of P-R2 by eliciting RNA decay.