Coupled Gas-Exchange Model for C4 Leaves Comparing Stomatal Conductance Models

Yun, Kyungdahm; Timlin, Dennis; Kim, Soo-Hyung

doi:10.3390/plants9101358

Coupled Gas-Exchange Model for C4 Leaves Comparing Stomatal Conductance Models

Journal Article · Wed Oct 14 00:00:00 EDT 2020 · Plants

DOI:https://doi.org/10.3390/plants9101358· OSTI ID:1681046

; ;

Plant simulation models are abstractions of plant physiological processes that are useful for investigating the responses of plants to changes in the environment. Because photosynthesis and transpiration are fundamental processes that drive plant growth and water relations, a leaf gas-exchange model that couples their interdependent relationship through stomatal control is a prerequisite for explanatory plant simulation models. Here, we present a coupled gas-exchange model for C4 leaves incorporating two widely used stomatal conductance submodels: Ball–Berry and Medlyn models. The output variables of the model includes steady-state values of CO2 assimilation rate, transpiration rate, stomatal conductance, leaf temperature, internal CO2 concentrations, and other leaf gas-exchange attributes in response to light, temperature, CO2, humidity, leaf nitrogen, and leaf water status. We test the model behavior and sensitivity, and discuss its applications and limitations. The model was implemented in Julia programming language using a novel modeling framework. Our testing and analyses indicate that the model behavior is reasonably sensitive and reliable in a wide range of environmental conditions. The behavior of the two model variants differing in stomatal conductance submodels deviated substantially from each other in low humidity conditions. The model was capable of replicating the behavior of transgenic C4 leaves under moderate temperatures as found in the literature. The coupled model, however, underestimated stomatal conductance in very high temperatures. This is likely an inherent limitation of the coupling approaches using Ball–Berry type models in which photosynthesis and stomatal conductance are recursively linked as an input of the other.

View Journal Article

Research Organization:: University of Florida, Gainesville, FL (United States)

Sponsoring Organization:: USDOE; USDOE Advanced Research Projects Agency - Energy (ARPA-E)

Grant/Contract Number:: AR0000820

OSTI ID:: 1681046

Alternate ID(s):: OSTI ID: 1848271

Journal Information:: Plants, Journal Name: Plants Journal Issue: 10 Vol. 9; ISSN PLANCD; ISSN 2223-7747

Publisher:: MDPI AGCopyright Statement

Country of Publication:: Netherlands

Language:: English

References (54)

A refined index of model performance Willmott, Cort J.; Robeson, Scott M.; Matsuura, Kenji International Journal of Climatology, Vol. 32, Issue 13 https://doi.org/10.1002/joc.2419	journal	September 2011
An Introduction to Environmental Biophysics Campbell, Gaylon S.; Norman, John M. Springer New York, NY https://doi.org/10.1007/978-1-4612-1626-1	book	January 1998
A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species Farquhar, G. D.; von Caemmerer, S.; Berry, J. A. Planta, Vol. 149, Issue 1 https://doi.org/10.1007/BF00386231	journal	June 1980
Interactive Effects of Elevated CO2, Drought, and Warming on Plants Xu, Zhenzhu; Shimizu, Hideyuki; Yagasaki, Yasumi Journal of Plant Growth Regulation, Vol. 32, Issue 4 https://doi.org/10.1007/s00344-013-9337-5	journal	April 2013
River flow forecasting through conceptual models part I — A discussion of principles Nash, J. E.; Sutcliffe, J. V. Journal of Hydrology, Vol. 10, Issue 3 https://doi.org/10.1016/0022-1694(70)90255-6	journal	April 1970
Physiological and environmental regulation of stomatal conductance, photosynthesis and transpiration: a model that includes a laminar boundary layer Collatz, G. James; Ball, J. Timothy; Grivet, Cyril Agricultural and Forest Meteorology, Vol. 54, Issue 2-4 https://doi.org/10.1016/0168-1923(91)90002-8	journal	April 1991
Coupling biochemical and biophysical processes at the leaf level: an equilibrium photosynthesis model for leaves of C3 plants Nikolov, Nedialko T.; Massman, William J.; Schoettle, Anna W. Ecological Modelling, Vol. 80, Issue 2-3 https://doi.org/10.1016/0304-3800(94)00072-P	journal	July 1995
Effects of Nitrogen Nutrition and Water Deficit on Net Photosynthetic Rate and Chlorophyll Fluorescence in Winter Wheat Shangguan, Zhouping; Shao, Mingan; Dyckmans, Jens Journal of Plant Physiology, Vol. 156, Issue 1 https://doi.org/10.1016/S0176-1617(00)80271-0	journal	January 2000
Nitrogen Deficiency Limited the Improvement of Photosynthesis in Maize by Elevated CO2 Under Drought Zong, Yu-zheng; Shangguan, Zhou-ping Journal of Integrative Agriculture, Vol. 13, Issue 1 https://doi.org/10.1016/S2095-3119(13)60349-4	journal	January 2014
Maize yield under a changing climate: The hidden role of vapor pressure deficit Hsiao, Jennifer; Swann, Abigail L. S.; Kim, Soo-Hyung Agricultural and Forest Meteorology, Vol. 279 https://doi.org/10.1016/j.agrformet.2019.107692	journal	December 2019
Unified representation of the C3, C4, and CAM photosynthetic pathways with the Photo3 model Hartzell, Samantha; Bartlett, Mark S.; Porporato, Amilcare Ecological Modelling, Vol. 384 https://doi.org/10.1016/j.ecolmodel.2018.06.012	journal	September 2018
Interactive effects of free-air CO2 enrichment and drought stress on maize growth Manderscheid, Remy; Erbs, Martin; Weigel, Hans-Joachim European Journal of Agronomy, Vol. 52 https://doi.org/10.1016/j.eja.2011.12.007	journal	January 2014
Temperature dependence of growth, development, and photosynthesis in maize under elevated CO2 Kim, S.; Gitz, D.; Sicher, R. Environmental and Experimental Botany, Vol. 61, Issue 3 https://doi.org/10.1016/j.envexpbot.2007.06.005	journal	December 2007
Growth and yield stimulation under elevated CO 2 and drought: A meta-analysis on crops van der Kooi, Casper J.; Reich, Martin; Löw, Markus Environmental and Experimental Botany, Vol. 122 https://doi.org/10.1016/j.envexpbot.2015.10.004	journal	February 2016
Effect of nitrogen supply on leaf appearance, leaf growth, leaf nitrogen economy and photosynthetic capacity in maize (Zea mays L.) Vos, J.; Putten, P. E. L. van der; Birch, C. J. Field Crops Research, Vol. 93, Issue 1 https://doi.org/10.1016/j.fcr.2004.09.013	journal	July 2005
Nitrogen and water resources commonly limit crop yield increases, not necessarily plant genetics Sinclair, Thomas R.; Rufty, Thomas W. Global Food Security, Vol. 1, Issue 2 https://doi.org/10.1016/j.gfs.2012.07.001	journal	December 2012
C3 and C4 photosynthesis models: An overview from the perspective of crop modelling Yin, X.; Struik, P. C. NJAS - Wageningen Journal of Life Sciences, Vol. 57, Issue 1 https://doi.org/10.1016/j.njas.2009.07.001	journal	December 2009
Plants and Microclimate Jones, Hamlyn G. Cambridge University Press https://doi.org/10.1017/CBO9780511845727	book	January 2013
Differential Evolution – A Simple and Efficient Heuristic for global Optimization over Continuous Spaces Storn, Rainer; Price, Kenneth Journal of Global Optimization, Vol. 11, Issue 4, p. 341-359 https://doi.org/10.1023/A:1008202821328	journal	January 1997
Effects of elevated [CO2] on photosynthesis in European forest species: a meta-analysis of model parameters: Photosynthetic acclimation to elevated CO2 Medlyn, B. E.; Badeck, F. -W.; De Pury, D. G. G. Plant, Cell & Environment, Vol. 22, Issue 12 https://doi.org/10.1046/j.1365-3040.1999.00523.x	journal	December 1999
Temperature response of parameters of a biochemically based model of photosynthesis. I. Seasonal changes in mature maritime pine (Pinus pinaster Ait.) Medlyn, B. E.; Loustau, D.; Delzon, S. Plant, Cell and Environment, Vol. 25, Issue 9 https://doi.org/10.1046/j.1365-3040.2002.00890.x	journal	September 2002
The Ball-Berry-Leuning and Tardieu-Davies stomatal models: synthesis and extension within a spatially aggregated picture of guard cell function Dewar, R. C. Plant, Cell and Environment, Vol. 25, Issue 11 https://doi.org/10.1046/j.1365-3040.2002.00909.x	journal	November 2002
A coupled model of stomatal conductance, photosynthesis and transpiration Tuzet, A.; Perrier, A.; Leuning, R. Plant, Cell and Environment, Vol. 26, Issue 7 https://doi.org/10.1046/j.1365-3040.2003.01035.x	journal	July 2003
A hydromechanical and biochemical model of stomatal conductance Buckley, T. N.; Mott, K. A.; Farquhar, G. D. Plant, Cell and Environment, Vol. 26, Issue 10 https://doi.org/10.1046/j.1365-3040.2003.01094.x	journal	October 2003
Biochemical Models of Leaf Photosynthesis von Caemmerer, S. https://doi.org/10.1071/9780643103405	book	January 2000
Coupled Photosynthesis-Stomatal Conductance Model for Leaves of C4 Plants Collatz, Gj; Ribas-Carbo, M.; Berry, Ja Functional Plant Biology, Vol. 19, Issue 5 https://doi.org/10.1071/PP9920519	journal	January 1992
A Coupled Model of Photosynthesis, Stomatal Conductance and Transpiration for a Rose Leaf (Rosa hybrida L.) Kim, S. -H. Annals of Botany, Vol. 91, Issue 7 https://doi.org/10.1093/aob/mcg080	journal	March 2003
C4 photosynthesis and water stress Ghannoum, O. Annals of Botany, Vol. 103, Issue 4 https://doi.org/10.1093/aob/mcn093	journal	May 2008
Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature Sage, Rowan F. Journal of Experimental Botany, Vol. 53, Issue 369 https://doi.org/10.1093/jexbot/53.369.609	journal	April 2002
Impairment of C4 photosynthesis by drought is exacerbated by limiting nitrogen and ameliorated by elevated [CO2] in maize Markelz, R. J. Cody; Strellner, Reid S.; Leakey, Andrew D. B. Journal of Experimental Botany, Vol. 62, Issue 9 https://doi.org/10.1093/jxb/err056	journal	March 2011
Increase in leaf temperature opens stomata and decouples net photosynthesis from stomatal conductance in Pinus taeda and Populus deltoides x nigra Urban, Josef; Ingwers, Miles W.; McGuire, Mary Anne Journal of Experimental Botany, Vol. 68, Issue 7 https://doi.org/10.1093/jxb/erx052	journal	March 2017
Sensitivity of Photosynthesis in a C4 Plant, Maize, to Heat Stress Crafts-Brandner, Steven J.; Salvucci, Michael E. Plant Physiology, Vol. 129, Issue 4 https://doi.org/10.1104/pp.002170	journal	June 2002
C ₄ Photosynthesis at Low Temperature. A Study Using Transgenic Plants with Reduced Amounts of Rubisco Kubien, David S.; von Caemmerer, Susanne; Furbank, Robert T. Plant Physiology, Vol. 132, Issue 3 https://doi.org/10.1104/pp.103.021246	journal	June 2003
Photosynthesis, Productivity, and Yield of Maize Are Not Affected by Open-Air Elevation of CO ₂ Concentration in the Absence of Drought Leakey, Andrew D. B.; Uribelarrea, Martin; Ainsworth, Elizabeth A. Plant Physiology, Vol. 140, Issue 2 https://doi.org/10.1104/pp.105.073957	journal	January 2006
Stomatal Function across Temporal and Spatial Scales: Deep-Time Trends, Land-Atmosphere Coupling and Global Models Franks, Peter J.; Berry, Joseph A.; Lombardozzi, Danica L. Plant Physiology, Vol. 174, Issue 2 https://doi.org/10.1104/pp.17.00287	journal	April 2017
Interaction of Water Supply and N in Wheat Morgan, Jack A. Plant Physiology, Vol. 76, Issue 1 https://doi.org/10.1104/pp.76.1.112	journal	September 1984
Comparing optimal and empirical stomatal conductance models for application in Earth system models Franks, Peter J.; Bonan, Gordon B.; Berry, Joseph A. Global Change Biology, Vol. 24, Issue 12 https://doi.org/10.1111/gcb.14445	journal	October 2018
Canopy photosynthesis, evapotranspiration, leaf nitrogen, and transcription profiles of maize in response to CO2 enrichment Kim, Soo-Hyung; Sicher, Richard C.; Bae, Hanhong Global Change Biology, Vol. 12, Issue 3 https://doi.org/10.1111/j.1365-2486.2006.01110.x	journal	March 2006
Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global-scale terrestrial biosphere models Kattge, Jens; Knorr, Wolfgang; Raddatz, Thomas Global Change Biology, Vol. 15, Issue 4 https://doi.org/10.1111/j.1365-2486.2008.01744.x	journal	April 2009
Reconciling the optimal and empirical approaches to modelling stomatal conductance: RECONCILING OPTIMAL AND EMPIRICAL STOMATAL MODELS Medlyn, Belinda E.; Duursma, Remko A.; Eamus, Derek Global Change Biology, Vol. 17, Issue 6 https://doi.org/10.1111/j.1365-2486.2010.02375.x	journal	January 2011
The sensitivity of C3 photosynthesis to increasing CO2 concentration: a theoretical analysis of its dependence on temperature and background CO2 concentration Kirschbaum, M. U. F. Plant, Cell and Environment, Vol. 17, Issue 6 https://doi.org/10.1111/j.1365-3040.1994.tb00167.x	journal	June 1994
A critical appraisal of a combined stomatal-photosynthesis model for C3 plants Leuning, R. Plant, Cell and Environment, Vol. 18, Issue 4 https://doi.org/10.1111/j.1365-3040.1995.tb00370.x	journal	April 1995
Simple scaling of photosynthesis from leaves to canopies without the errors of big-leaf models De Pury, D. G. G.; Farquhar, G. D. Plant, Cell and Environment, Vol. 20, Issue 5 https://doi.org/10.1111/j.1365-3040.1997.00094.x	journal	May 1997
A new, vapour-phase mechanism for stomatal responses to humidity and temperature: Vapour-phase mechanism Peak, David; Mott, Keith A. Plant, Cell & Environment, Vol. 34, Issue 1 https://doi.org/10.1111/j.1365-3040.2010.02234.x	journal	November 2010
On the minimum leaf conductance: its role in models of plant water use, and ecological and environmental controls Duursma, Remko A.; Blackman, Christopher J.; Lopéz, Rosana New Phytologist, Vol. 221, Issue 2 https://doi.org/10.1111/nph.15395	journal	August 2018
Modelling stomatal conductance in response to environmental factors: Modelling stomatal conductance Buckley, Thomas N.; Mott, Keith A. Plant, Cell & Environment, Vol. 36, Issue 9 https://doi.org/10.1111/pce.12140	journal	June 2013
Julia: A Fresh Approach to Numerical Computing Bezanson, Jeff; Edelman, Alan; Karpinski, Stefan SIAM Review, Vol. 59, Issue 1 https://doi.org/10.1137/141000671	journal	January 2017
A Revised Land Surface Parameterization (SiB2) for Atmospheric GCMS. Part I: Model Formulation Sellers, P. J.; Randall, D. A.; Collatz, G. J. Journal of Climate, Vol. 9, Issue 4 https://doi.org/10.1175/1520-0442(1996)009<0676:ARLSPF>2.0.CO;2	journal	April 1996
Plantecophys - An R Package for Analysing and Modelling Leaf Gas Exchange Data Duursma, Remko A. PLOS ONE, Vol. 10, Issue 11 https://doi.org/10.1371/journal.pone.0143346	journal	November 2015
Modeling Temperature Responses of Leaf Growth, Development, and Biomass in Maize with MAIZSIM Kim, Soo-Hyung; Yang, Yang; Timlin, Dennis J. Agronomy Journal, Vol. 104, Issue 6 https://doi.org/10.2134/agronj2011.0321	journal	November 2012
Physiological Evaluations of Recent Drought‐Tolerant Maize Hybrids at Varying Stress Levels Roth, Jason A.; Ciampitti, Ignacio A.; Vyn, Tony J. Agronomy Journal, Vol. 105, Issue 4 https://doi.org/10.2134/agronj2013.0066	journal	July 2013
Proposed Standards for Peer-Reviewed Publication of Computer Code Timlin, Dennis; David, Olaf; Green, Timothy R. Agronomy Journal, Vol. 108, Issue 5 https://doi.org/10.2134/agronj2015.0481	journal	September 2016
Maize Leaf Absorptance of Photosynthetically Active Radiation and Its Estimation Using a Chlorophyll Meter Earl, H. J.; Tollenaar, M. Crop Science, Vol. 37, Issue 2 https://doi.org/10.2135/cropsci1997.0011183X003700020022x	journal	March 1997
Connecting Biochemical Photosynthesis Models with Crop Models to Support Crop Improvement Wu, Alex; Song, Youhong; van Oosterom, Erik J. Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01518	journal	October 2016

Similar Records

Increasing water use efficiency along the C3 to C4 evolutionary pathway: a stomatal optimization perspective

Journal Article · Thu May 22 20:00:00 EDT 2014 · Journal of Experimental Botany · OSTI ID:1625386

Effect of ozone on stomatal aperture and transpiration

Book · Sun Dec 31 23:00:00 EST 1967 · OSTI ID:5014996

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Ball–Berry
C4 photosynthesis
Medlyn
gas-exchange
plant sciences
stomatal conductance

Coupled Gas-Exchange Model for C4 Leaves Comparing Stomatal Conductance Models

Citation Formats

References (54)

Similar Records

Related Subjects