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

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 syst...

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Published inThe New phytologist Vol. 200; no. 4; pp. 1116 - 1131
Main Authors Owen, Nick A., Griffiths, Howard
Format Journal Article
LanguageEnglish
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)
Online AccessGet full text
ISSN0028-646X
1469-8137
1469-8137
DOI10.1111/nph.12461

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Abstract 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.
AbstractList A system dynamics (SD) approach was taken to model crassulacean acid metabolism (CAM) expression from measured biochemical and physiological constants. SD emphasizes state-dependent 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 Kalanchoee daigremontiana and more succulent tissues of Agave tequilana showed strong correlation with measured gas exchange and malic acid accumulation (R2 = 0.912 and 0.937, respectively, for K. daigremontiana and R2 = 0.928 and 0.942, respectively, for A. tequilana).Sensitivity analyses were conducted to quantitatively identify determinants of diel CO2 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 the manipulation three input parameters. See also the Commentary by Borland and Yang
A system dynamics (SD) approach was taken to model crassulacean acid metabolism (CAM) expression from measured biochemical and physiological constants. SD emphasizes state‐dependent 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 Kalanchoë daigremontiana and more succulent tissues of Agave tequilana showed strong correlation with measured gas exchange and malic acid accumulation (R² = 0.912 and 0.937, respectively, for K. daigremontiana and R² = 0.928 and 0.942, respectively, for A. tequilana). Sensitivity analyses were conducted to quantitatively identify determinants of diel CO₂ 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 the manipulation three input parameters.
A system dynamics (SD) approach was taken to model crassulacean acid metabolism (CAM) expression from measured biochemical and physiological constants. SD emphasizes state‐dependent 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 Kalanchoë daigremontiana and more succulent tissues of Agave tequilana showed strong correlation with measured gas exchange and malic acid accumulation (R2 = 0.912 and 0.937, respectively, for K. daigremontiana and R2 = 0.928 and 0.942, respectively, for A. tequilana).Sensitivity analyses were conducted to quantitatively identify determinants of diel CO2 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 the manipulation three input parameters.
Summary A system dynamics (SD) approach was taken to model crassulacean acid metabolism (CAM) expression from measured biochemical and physiological constants. SD emphasizes state-dependent 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 Kalanchoë daigremontiana and more succulent tissues of Agave tequilana showed strong correlation with measured gas exchange and malic acid accumulation (R2 = 0.912 and 0.937, respectively, for K. daigremontiana and R2 = 0.928 and 0.942, respectively, for A. tequilana). Sensitivity analyses were conducted to quantitatively identify determinants of diel CO2 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 the manipulation three input parameters. See also the Commentary by Borland and Yang [PUBLICATION ABSTRACT]
A system dynamics (SD) approach was taken to model crassulacean acid metabolism (CAM) expression from measured biochemical and physiological constants. SD emphasizes state-dependent 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 Kalanchoë 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 analyses were conducted to quantitatively identify determinants of diel CO2 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 the manipulation three input parameters.A system dynamics (SD) approach was taken to model crassulacean acid metabolism (CAM) expression from measured biochemical and physiological constants. SD emphasizes state-dependent 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 Kalanchoë 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 analyses were conducted to quantitatively identify determinants of diel CO2 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 the manipulation three input parameters.
A system dynamics (SD) approach was taken to model crassulacean acid metabolism (CAM) expression from measured biochemical and physiological constants. SD emphasizes state-dependent 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 Kalanchoë 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 analyses were conducted to quantitatively identify determinants of diel CO2 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 the manipulation three input parameters.
Summary A system dynamics (SD) approach was taken to model crassulacean acid metabolism (CAM) expression from measured biochemical and physiological constants. SD emphasizes state‐dependent 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 Kalanchoë daigremontiana and more succulent tissues of Agave tequilana showed strong correlation with measured gas exchange and malic acid accumulation (R2 = 0.912 and 0.937, respectively, for K. daigremontiana and R2 = 0.928 and 0.942, respectively, for A. tequilana). Sensitivity analyses were conducted to quantitatively identify determinants of diel CO2 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 the manipulation three input parameters. See also the Commentary by Borland and Yang
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.
A system dynamics ( SD ) approach was taken to model crassulacean acid metabolism ( CAM ) expression from measured biochemical and physiological constants. SD emphasizes state‐dependent 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 Kalanchoë 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 analyses were conducted to quantitatively identify determinants of diel CO 2 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 the manipulation three input parameters. See also the Commentary by Borland and Yang
Author Howard Griffiths
Nick A. Owen
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/23992169$$D View this record in MEDLINE/PubMed
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Issue 4
Keywords CAM expression
system dynamics
model
stem and leaf succulents
enzyme kinetics
crassulacean acid metabolism (CAM)
Language English
License http://onlinelibrary.wiley.com/termsAndConditions#vor
2013 The Authors. New Phytologist © 2013 New Phytologist Trust.
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Snippet A system dynamics (SD) approach was taken to model crassulacean acid metabolism (CAM) expression from measured biochemical and physiological constants. SD...
Summary A system dynamics (SD) approach was taken to model crassulacean acid metabolism (CAM) expression from measured biochemical and physiological constants....
A system dynamics ( SD ) approach was taken to model crassulacean acid metabolism ( CAM ) expression from measured biochemical and physiological constants. SD...
Summary A system dynamics (SD) approach was taken to model crassulacean acid metabolism (CAM) expression from measured biochemical and physiological constants....
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StartPage 1116
SubjectTerms 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
Title A system dynamics model integrating physiology and biochemical regulation predicts extent of crassulacean acid metabolism (CAM) phases
URI https://www.jstor.org/stable/newphytologist.200.4.1116
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fnph.12461
https://www.ncbi.nlm.nih.gov/pubmed/23992169
https://www.proquest.com/docview/1448206300
https://www.proquest.com/docview/2513008889
https://www.proquest.com/docview/1468376879
https://www.proquest.com/docview/1503550906
https://www.proquest.com/docview/2524284213
Volume 200
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