Alternative Crassulacean Acid Metabolism Modes Provide Environment-Specific Water-Saving Benefits in a Leaf Metabolic Model

Stoichiometric modeling of leaf metabolism reveals metabolic and morphological determinants for introducing Crassulacean acid metabolism and alternative water-saving flux modes into a C-3 leaf in different environments. Crassulacean acid metabolism (CAM) evolved in arid environments as a water-saving alternative to C-3 photosynthesis. There is great interest in engineering more drought-resistant crops by introducing CAM into C-3 plants. However, it is unknown whether full CAM or alternative water-saving modes would be more productive in the environments typically experienced by C-3 crops. To study the effect of temperature and relative humidity on plant metabolism in the context of water saving, we coupled a time-resolved diel (based on a 24-h day-night cycle) model of leaf metabolism to an environment-dependent gas-exchange model. This combined model allowed us to study the emergence of CAM as a trade-off between leaf productivity and water saving. We show that vacuolar storage capacity in the leaf is a major determinant of the extent of CAM. Moreover, our model identified an alternative CAM cycle involving mitochondrial isocitrate dehydrogenase as a potential contributor to initial carbon fixation at night. Simulations across a range of environmental conditions show that the water-saving potential of CAM strongly depends on the daytime weather conditions and that the additional water-saving effect of carbon fixation by isocitrate dehydrogenase can reach 11% total water saving for the conditions tested.