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Interactions of C4 Subtype Metabolic Activities and Transport in Maize Are Revealed through the Characterization of DCT2 Mutants

Weissmann, Sarit, Ma, Fangfang, Furuyama, Koki, Gierse, James, Berg, Howard, Shao, Ying, Taniguchi, Mitsutaka, Allen, Doug K., Brutnell, Thomas P.
The Plant cell 2016 v.28 no.2 pp. 466-484
C4 photosynthesis, Zea mays, carbon, carbon dioxide, chloroplasts, corn, gene expression, gene expression regulation, insertional mutagenesis, isotope labeling, leaves, malates, mesophyll, metabolites, mutants, nitrogen, physiological transport, ribulose-bisphosphate carboxylase, transporters
C4 photosynthesis is an elaborate set of metabolic pathways that utilize specialized anatomical and biochemical adaptations to concentrate CO2 around RuBisCO. The activities of the C4 pathways are coordinated between two specialized leaf cell types, mesophyll (M) and bundle sheath (BS), and rely heavily on movement of metabolites between locations, although the identity of most transporters is unknown. ZmDCT2 is a dicarboxylate transporter that can move malate at high efficiency. It is differentially expressed in the BS cells in maize, has a photosynthetic gene expression pattern along the leaf gradient, and is light responsive, making it a good candidate for malate transport into the BS chloroplast during C4 photosynthesis in maize. We characterized the role of ZmDCT2 in maize leaves via insertional mutagenesis. We show that ZmDCT2 is expressed in the BS and is essential for transport of malate into the BS chloroplast. We also show, through combined 13C and 14C isotopic labeling experiments, that both WT and mutant maize leaves have an active PEPCK C4 photosynthesis pathway that accounts for approximately 25% of the photosynthetic activity of the plant. Our results emphasize the importance of malate transport during C4 photosynthesis and genetically define the first malate transporter in maize. Additionally, our data suggest the presence of multiple C4 subtypes may enable survival when one of the paths is compromised and that the balance between pathways involves allocation of nitrogen as well as carbon.