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Title: Interactions of C4 subtype metabolic activities and transport in maize are revealed through the characterization of DCT2 mutants

item WEISSMANN, SARIT - Danforth Plant Science Center
item MA, FANGFANG - Danforth Plant Science Center
item FURUYAMA, KOKI - Nagoya University
item Gierse, James
item BERG, HOWARD - Danforth Plant Science Center
item SHAO, YING - Danforth Plant Science Center
item TANIGUCHI, MITSUTAKA - Nagoya University
item Allen, Douglas - Doug
item BRUTNELL, THOMAS - Danforth Plant Science Center

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/21/2016
Publication Date: 2/1/2016
Publication URL:
Citation: Weissmann, S., Ma, F., Furuyama, K., Gierse, J.K., Berg, H., Shao, Y., Taniguchi, M., Allen, D.K., Brutnell, T.P. 2016. Interactions of C4 subtype metabolic activities and transport in maize are revealed through the characterization of DCT2 mutants. The Plant Cell. 28:466-484.

Interpretive Summary: Photosynthesis is a complex process that balances the harvesting of light energy with carbon assimilation (into sugars and other metabolites from CO2) in plants. The efficiency of photosynthesis constrains plant biomass production (vegetative growth) and ultimately yield. Some plants have special anatomical and biochemical mechanisms to improve their capacity to perform photosynthesis and are known as C4 plants because the improvements involve the shuttling of four carbon organic and amino acids between cells and chloroplasts. The C4 metabolites are involved in assimilating carbon dioxide and transferring it to RuBisCO which is the enzyme in nature that plants rely upon to fix CO2 and produce biomass. Though this special C4 anatomy results in improved photosynthetic performance it is complex and the shuttling of elements such as carbon between locations are not well understood. In addition there are several subtypes of metabolic pathways that use different metabolites (i.e. organic acids vs. amino acids) to move the carbon, which we studied through a set of genetic mutants. In particular the transporters involved in moving carbon compounds between different cell types have not been conclusively identified or characterized so we investigated an altered maize line deficient in one of the transporters. Our results provide evidence that the genetic mutant we studied, ZmDCT2, is a transporter of the organic acid malate and functions to move it into the chloroplast of one of the special cell types called a bundle sheath cell. This is the location where RuBisCO is located in maize and where carbon fixation ultimately occurs. These studies are important because the data describe the operation of C4 photosynthesis in an important crop, providing insight on how maize might be engineered for improved biomass production.

Technical Abstract: 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.