The Expression of 2-Oxoglutarate/Malate Translocator in the Bundle-Sheath Mitochondria of Panicum miliaceum, a NAD-Malic Enzyme-Type C4 Plant, Is Regulated by Light and Development

The bundle-sheath mitochondria in NAD-malic enzyme-type C4 plants participate in the C4 dicarboxylate cycle and require high capacities of translocators to accommodate the high rates of exchange of metabolites involved in photosynthesis. In Panicum miliaceum, a NAD-malic enzyme-type C4 plant, the steady-state level of mRNA for the mitochondrial 2-oxoglutarate (2-OG)/malate translocator was higher in leaves than in nonphotosynthetic tissues. Furthermore, the expression of the gene for the mitochondrial 2-OG/malate translocator was restricted to bundle-sheath cells (BSC) but not mesophyll cells. The transcript level of the BSC-located mitochondrial 2-OG/malate translocator increased during greening in accordance with levels of photosynthetic genes, although the relative transcript levels of other mitochondrial membrane proteins decreased. The specific activities of C4 photosynthetic enzymes and the relative abundance of the 2-OG/malate translocator protein in bundle-sheath mitochondria increased in successive sections from the basal meristem to the distal tip, whereas the specific activities of mitochondrial respiratory enzymes remained constant or decreased. These findings indicate that the specific 2-OG/malate translocator in BSC mitochondria of P. miliaceum is expressed in concert with C4 enzymes during the differentiation of BSC and parallels the capacity of C4 photosynthesis. Most unusual, northern analysis showed that significant amounts of unspliced mRNAs, the levels of which are variable during greening, were present in leaf tissues. It is possible that this incomplete splicing is involved in posttranscriptional regulation of expression of this gene.