CAM Models: Lessons and Implications for CAM Evolution

Abstract

The evolution of Crassulacean acid metabolism (CAM) by plants has been one of the most successful strategies in response to aridity. On the onset of climate change, expanding the use of water efficient crops and engineering higher water use efficiency into C3 and C4 crops constitute a plausible solution for the problems of agriculture in hotter and drier environments. A firm understanding of CAM is thus crucial for the development of agricultural responses to climate change. Computational models on CAM can contribute significantly to this understanding. Two types of models have been used so far. Early CAM models based on ordinary differential equations (ODE) reproduced the typical diel CAM features with a minimal set of components and investigated endogenous day/night rhythmicity. This line of research brought to light the preponderant role of vacuolar malate accumulation in diel rhythms. A second wave of CAM models used flux balance analysis (FBA) to better understand the role of CO₂ uptake in flux distribution. They showed that flux distributions resembling CAM metabolism emerge upon constraining CO₂ uptake by the system. We discuss the evolutionary implications of this and also how CAM components from unrelated pathways could have integrated along evolution.

Keywords: CAM; CAM evolution; FBA models; ODE models; carbon concentration mechanism.

Figure 1

(A) Regulatory interactions sufficient to give rise to diel oscillations of malate accumulation and CO₂ uptake adapted from Nungesser et al. (1984) skeleton model: malate inhibition of PEPC (1); Glc6P activation of PEPC (2); PEP inhibition of glycolysis (3); light activation of photosynthesis (4); induction of stomatal closure by high C_i (5); and the autonomous vacuolar oscillator (6). (B) Pathways that articulated during CAM evolution. The anapleurotic fixation of CO₂ by PEPC in unicellular algae occurs to provide carbon skeletons for amino acid synthesis (magenta). The same pathway is found in C3 plants, which store in the vacuole malic acid resulting from CO₂ fixation during the night to be used for amino acid synthesis the next day. C3 plants are also able to close stomata upon high C_i (green). Three events could have closed the cycle to give rise to CAM (brown): an increased flux through PEPC; an increase in decarboxylation activity, e.g., NAD(P)-ME, and its delay to not overlap with PEPC fixation; and finally, an increased vacuolar capacity that allows the concentration of CO₂.