Journal
JOURNAL OF EXPERIMENTAL BOTANY
Volume 68, Issue 2, Pages 283-298Publisher
OXFORD UNIV PRESS
DOI: 10.1093/jxb/erw414
Keywords
C-13 labeling; C-4 photosynthesis; carbon flow; CO2-concentrating shuttle; maize
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Funding
- European Commission [289582]
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Worldwide efforts to engineer C-4 photosynthesis into C-3 crops require a deep understanding of how this complex pathway operates. CO2 is incorporated into four-carbon metabolites in the mesophyll, which move to the bundle sheath where they are decarboxylated to concentrate CO2 around RuBisCO. We performed dynamic (CO2)-C-13 labeling in maize to analyze C flow in C-4 photosynthesis. The overall labeling kinetics reflected the topology of C-4 photosynthesis. Analyses of cell-specific labeling patterns after fractionation to enrich bundle sheath and mesophyll cells revealed concentration gradients to drive intercellular diffusion of malate, but not pyruvate, in the major CO2-concentrating shuttle. They also revealed intercellular concentration gradients of aspartate, alanine, and phosphenolpyruvate to drive a second phosphoenolpyruvate carboxykinase (PEPCK)-type shuttle, which carries 10-14% of the carbon into the bundle sheath. Gradients also exist to drive intercellular exchange of 3-phosphoglycerate and triose-phosphate. similar to 10% of carbon gain. In contrast, very little C leaks from the large pools of metabolites in the C concentration shuttle into respiratory metabolism. We postulate that the presence of multiple shuttles, alongside carbon transfer between them and the Calvin-Benson cycle, confers great flexibility in C-4 photosynthesis.
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