Intramolecular carbon isotope signals reflect metabolite allocation in plants

Stable isotopes at natural abundance are key tools to study physiological processes occurring outside the temporal scope of manipulation and monitoring experiments. Whole-molecule carbon isotope ratios (C-13/C-12) enable assessments of plant carbon uptake yet conceal information about carbon allocation. Here, we identify an intramolecular C-13/C-12 signal at tree-ring glucose C-5 and C-6 and develop experimentally testable theories on its origin. More specifically, we assess the potential of processes within C-3 metabolism for signal introduction based (inter alia) on constraints on signal propagation posed by metabolic networks. We propose that the intramolecular signal reports carbon allocation into major metabolic pathways in actively photosynthesizing leaf cells including the anaplerotic, shikimate, and non-mevalonate pathway. We support our theoretical framework by linking it to previously reported whole-molecule C-13/C-12 increases in cellulose of ozone-treated Betula pendula and a highly significant relationship between the intramolecular signal and tropospheric ozone concentration. Our theory postulates a pronounced preference for leaf cytosolic triose-phosphate isomerase to catalyse the forward reaction in vivo (dihydroxyacetone phosphate to glyceraldehyde 3-phosphate). In conclusion, intramolecular C-13/C-12 analysis resolves information about carbon uptake and allocation enabling more comprehensive assessments of carbon metabolism than whole-molecule C-13/C-12 analysis. Intramolecular C-13/C-12 analysis resolves information about carbon uptake and allocation (and associated environmental controls), enabling more comprehensive assessments of carbon metabolism, plant-environment interactions, and environmental variability than whole-molecule C-13/C-12 analysis.

Automated summary

This study demonstrates the use of intramolecular C-13/C-12 analysis to understand carbon uptake and allocation in plants, providing more comprehensive assessments of carbon metabolism than whole-molecule C-13/C-12 analysis. The research also proposes experimentally testable theories on the origin of the intramolecular signal.