A system dynamics model integrating physiology and biochemical regulation predicts extent of crassulacean acid metabolism (CAM) phases

• Published in: The New phytologist Vol. 200; no. 4; pp. 1116 - 1131
• Main Authors: Owen, Nick A., Griffiths, Howard
• Format: Journal Article
• Language: English
• Published: England New Phytologist Trust 01.12.2013; Wiley Subscription Services, Inc
• Subjects: Accumulation; Acids; Agave; Agave - metabolism; Agave - physiology; Agave tequilana; Atmospherics; CAM expression; Carbon dioxide; Carbon Dioxide - metabolism; Complex systems; Computer Simulation; Conductance; Constants; Crassulacean acid metabolism; crassulacean acid metabolism (CAM); Cytosol; Decarboxylation; dynamic models; Dynamics; Empirical analysis; Enzyme kinetics; Enzymes; Feedback; Feedback control; Gas exchange; Kalanchoe - metabolism; Kalanchoe - physiology; Kinetics; Malic acid; Mathematical models; Mesophyll; Metabolic Engineering; Metabolism; Model testing; Modeling; Models, Biological; Multivariate Analysis; Parameters; Phosphoenolpyruvate carboxylase; Photosynthesis - physiology; Physiological regulation; Physiology; Plant Stomata - physiology; Plants; Reproducibility of Results; Resistance; Sensitivity analysis; stem and leaf succulents; Stomata; stomatal movement; System dynamics; Systems Biology; Time Factors; Tissue; tonoplast; Uptake; CAM expression; system dynamics; model; stem and leaf succulents; enzyme kinetics; crassulacean acid metabolism (CAM)
• ISSN: 0028-646X; 1469-8137; 1469-8137
• DOI: 10.1111/nph.12461

A system dynamics (SD) approach was taken to model crassulacean acid metabolism (CAM) expression from measured biochemical and physiological constants. SD emphasizes statedependent feedback interaction to describe the emergent properties of a complex system. These mechanisms maintain biological systems with homeostatic limits on a temporal basis. Previous empirical studies on CAM have correlated biological constants (e.g. enzyme kinetic parameters) with expression over the CAM diel cycle. The SD model integrates these constants within the architecture of the CAM ‘system’. This allowed quantitative causal connections to be established between biological inputs and the four distinct phases of CAM delineated by gas exchange and malic acid accumulation traits. Regulation at flow junctions (e.g. stomatal and mesophyll conductance, and malic acid transport across the tonoplast) that are subject to feedback control (e.g. stomatal aperture, malic acid inhibition of phosphoenolpyruvate carboxylase, and enzyme kinetics) was simulated. Simulated expression for the leaf-succulent Kalanchoё daigremontiana and more succulent tissues of Agave tequilana showed strong correlation with measured gas exchange and malic acid accumulation (R 2 = 0.912 and 0.937, respectively, for K. daigremontiana and R 2 = 0.928 and 0.942, respectively, for A. tequilana). Sensitivity analyseswere conducted to quantitatively identify determinants of dielCO2 uptake. The transition in CAM expression from low to high volume/area tissues (elimination of phase II–IV carbon-uptake signatures)was achieved largely by themanipulation three input parameters.