Leaf-level metabolic changes in response to drought affect daytime CO2 emission and isoprenoid synthesis

Daytime production of CO2 in leaves is primarily a byproduct of secondary metabolite synthesis, including the production of volatile organic compounds (VOCs). It remains unclear how the carbon fluxes associated with daytime CO2 production and VOC emission vary among mature trees, and how they are influenced by drought. We used position-specific 13C-pyruvate labeling to investigate leaf CO2 and VOC fluxes from four tropical species before and during a controlled drought in an enclosed rainforest. Although daytime CO2 production was always dominated by non-mitochondrial processes, the relative contribution of CO2 from mitochondria (i.e., the tricarboxylic acid cycle) tended to increase under drought. The legume tree Clitoria fairchildiana had less anabolic CO2 production than the other species, and was also the only one to allocate detectable amounts of the 13C label to VOCs. In C. fairchildiana leaves, our data indicate that intermediates from the mevalonic acid pathway are used to produce the volatile monoterpene trans-β-ocimene, but not isoprene. This suggests that geranyl pyrophosphate is the more important intermediate for crosstalk between cytosolic and plastidic isoprenoid synthesis, not isopentenyl pyrophosphate. This apparent crosstalk declined with drought, and although trans-β-ocimene emissions increased, they were primarily sourced from stored intermediates and not de novo synthesis.