The metabolic origins of non-photorespiratory CO2 release during photosynthesis: a metabolic flux analysis

Respiration in the light (R-L) releases CO2 in photosynthesizing leaves and is a phenomenon that occurs independently from photorespiration. Since R-L lowers net carbon fixation, understanding R-L could help improve plant carbon-use efficiency and models of crop photosynthesis. Although R-L was identified more than 75 years ago, its biochemical mechanisms remain unclear. To identify reactions contributing to R-L, we mapped metabolic fluxes in photosynthesizing source leaves of the oilseed crop and model plant camelina (Camelina sativa). We performed a flux analysis using isotopic labeling patterns of central metabolites during (CO2)-C-13 labeling time course, gas exchange, and carbohydrate production rate experiments. To quantify the contributions of multiple potential CO2 sources with statistical and biological confidence, we increased the number of metabolites measured and reduced biological and technical heterogeneity by using single mature source leaves and quickly quenching metabolism by directly injecting liquid N-2; we then compared the goodness-of-fit between these data and data from models with alternative metabolic network structures and constraints. Our analysis predicted that R-L releases 5.2 mu mol CO2 g(-1) FW h(-1) of CO2, which is relatively consistent with a value of 9.3 mu mol CO2 g(-1) FW h(-1) measured by CO2 gas exchange. The results indicated that <= 10% of R-L results from TCA cycle reactions, which are widely considered to dominate R-L. Further analysis of the results indicated that oxidation of glucose-6-phosphate to pentose phosphate via 6-phosphogluconate (the G6P/OPP shunt) can account for >93% of CO2 released by R-L.

Automated summary

By analyzing metabolic fluxes in photosynthesizing source leaves of the oilseed crop camelina, it was determined that the majority of CO2 released in R-L is attributed to the G6P/OPP shunt pathway, rather than TCA cycle reactions.