An improved representation of the relationship between photosynthesis and stomatal conductance leads to more stable estimation of conductance parameters and improves the goodness-of-fit across diverse data sets

Lamour, Julien; Davidson, Kenneth J.; Ely, Kim S.; Le Moguédec, Gilles; Leakey, Andrew B.; Li, Qianyu; Serbin, Shawn P.; Rogers, Alistair

doi:10.1111/gcb.16103

An improved representation of the relationship between photosynthesis and stomatal conductance leads to more stable estimation of conductance parameters and improves the goodness-of-fit across diverse data sets

Journal Article · Fri Jan 28 04:00:00 EST 2022 · Global Change Biology

DOI:https://doi.org/10.1111/gcb.16103· OSTI ID:1842791

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Brookhaven National Lab. (BNL), Upton, NY (United States)
Brookhaven National Lab. (BNL), Upton, NY (United States); Stony Brook Univ., NY (United States)
Montpellier Univ., (France)
Univ. of Illinois at Urbana-Champaign, IL (United States)

Stomata play a central role in surface-atmosphere exchange by controlling the flux of water and CO₂ between the leaf and the atmosphere. Representation of stomatal conductance (g_sw) is therefore an essential component of models that seek to simulate water and CO₂ exchange in plants and ecosystems. For given environmental conditions at the leaf surface (CO₂ concentration and vapor pressure deficit or relative humidity), models typically assume a linear relationship between g_sw and photosynthetic CO₂ assimilation (A). However, measurement of leaf-level g_sw response curves to changes in A are rare, particularly in the tropics, resulting in only limited data to evaluate this key assumption. Here, we measured the response of g_sw and A to irradiance in six tropical species at different leaf phenological stages. We showed that the relationship between g_sw and A was not linear, challenging the key assumption upon which optimality theory is based-that the marginal cost of water gain is constant. Our data showed that increasing A resulted in a small increase in g_sw at low irradiance, but a much larger increase at high irradiance. We reformulated the popular Unified Stomatal Optimization (USO) model to account for this phenomenon and to enable consistent estimation of the key conductance parameters g₀ and g₁. Our modification of the USO model improved the goodness-of-fit and reduced bias, enabling robust estimation of conductance parameters at any irradiance. In addition, our modification revealed previously undetectable relationships between the stomatal slope parameter g₁ and other leaf traits. We also observed nonlinear behavior between A and g_sw in independent datasets that included data collected from attached and detached leaves, and from plants grown at elevated CO₂ concentration. We propose that this empirical modification of the USO model can improve the measurement of g_sw parameters and the estimation of plant and ecosystem-scale water and CO₂ fluxes.

View Accepted Manuscript (DOE)

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0012704; SC0018277

OSTI ID:: 1842791

Alternate ID(s):: OSTI ID: 2305729
OSTI ID: 1854420

Report Number(s):: BNL--222671-2022-JAAM

Journal Information:: Global Change Biology, Journal Name: Global Change Biology Journal Issue: 11 Vol. 28; ISSN 1354-1013

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (71)

A quantitative assessment of a terrestrial biosphere model's data needs across North American biomes: PEcAn/ED model-data uncertainty analysis Dietze, Michael C.; Serbin, Shawn P.; Davidson, Carl Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 3 https://doi.org/10.1002/2013JG002392	journal	March 2014
The implications of minimum stomatal conductance on modeling water flux in forest canopies: MINIMUM Barnard, D. M.; Bauerle, W. L. Journal of Geophysical Research: Biogeosciences, Vol. 118, Issue 3 https://doi.org/10.1002/jgrg.20112	journal	July 2013
A Model Predicting Stomatal Conductance and its Contribution to the Control of Photosynthesis under Different Environmental Conditions Ball, J. Timothy; Woodrow, Ian E.; Berry, Joseph A. Progress in Photosynthesis Research https://doi.org/10.1007/978-94-017-0519-6_48	book	January 1987
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
Predicting light-induced stomatal movements based on the redox state of plastoquinone: theory and validation Kromdijk, Johannes; Głowacka, Katarzyna; Long, Stephen P. Photosynthesis Research, Vol. 141, Issue 1 https://doi.org/10.1007/s11120-019-00632-x	journal	March 2019
How should we model plant responses to drought? An analysis of stomatal and non-stomatal responses to water stress Zhou, Shuangxi; Duursma, Remko A.; Medlyn, Belinda E. Agricultural and Forest Meteorology, Vol. 182-183 https://doi.org/10.1016/j.agrformet.2013.05.009	journal	December 2013
Including soil water stress in process-based ecosystem models by scaling down maximum carboxylation rate using accumulated soil water deficit Chen, Bin; Chen, Jing M.; Baldocchi, Dennis D. Agricultural and Forest Meteorology, Vol. 276-277 https://doi.org/10.1016/j.agrformet.2019.107649	journal	October 2019
Temperature responses of photosynthesis and stomatal conductance in rice and wheat plants Huang, Guanjun; Yang, Yuhan; Zhu, Lele Agricultural and Forest Meteorology, Vol. 300 https://doi.org/10.1016/j.agrformet.2021.108322	journal	April 2021
Contrasting responses of stomatal conductance and photosynthetic capacity to warming and elevated CO2 in the tropical tree species Alchornea glandulosa under heatwave conditions Fauset, Sophie; Oliveira, Lauana; Buckeridge, Marcos S. Environmental and Experimental Botany, Vol. 158 https://doi.org/10.1016/j.envexpbot.2018.10.030	journal	February 2019
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
A dynamic global vegetation model for studies of the coupled atmosphere-biosphere system: DVGM FOR COUPLED CLIMATE STUDIES Krinner, G.; Viovy, Nicolas; de Noblet-Ducoudré, Nathalie Global Biogeochemical Cycles, Vol. 19, Issue 1 https://doi.org/10.1029/2003GB002199	journal	February 2005
Improving canopy processes in the Community Land Model version 4 (CLM4) using global flux fields empirically inferred from FLUXNET data Bonan, Gordon B.; Lawrence, Peter J.; Oleson, Keith W. Journal of Geophysical Research, Vol. 116, Issue G2 https://doi.org/10.1029/2010JG001593	journal	January 2011
The role of stomata in sensing and driving environmental change Hetherington, Alistair M.; Woodward, F. Ian Nature, Vol. 424, Issue 6951 https://doi.org/10.1038/nature01843	journal	August 2003
Optimal stomatal behaviour around the world Lin, Yan-Shih; Medlyn, Belinda E.; Duursma, Remko A. Nature Climate Change, Vol. 5, Issue 5 https://doi.org/10.1038/nclimate2550	journal	March 2015
Optimization can provide the fundamental link between leaf photosynthesis, gas exchange and water relations Deans, Ross M.; Brodribb, Timothy J.; Busch, Florian A. Nature Plants, Vol. 6, Issue 9 https://doi.org/10.1038/s41477-020-00760-6	journal	September 2020
An improved theory for calculating leaf gas exchange more precisely accounting for small fluxes Márquez, Diego A.; Stuart-Williams, Hilary; Farquhar, Graham D. Nature Plants, Vol. 7, Issue 3 https://doi.org/10.1038/s41477-021-00861-w	journal	March 2021
Diversity in stomatal function is integral to modelling plant carbon and water fluxes Wolz, Kevin J.; Wertin, Timothy M.; Abordo, Mark Nature Ecology & Evolution, Vol. 1, Issue 9 https://doi.org/10.1038/s41559-017-0238-z	journal	July 2017
The three major axes of terrestrial ecosystem function Migliavacca, Mirco; Musavi, Talie; Mahecha, Miguel D. Nature, Vol. 598, Issue 7881 https://doi.org/10.1038/s41586-021-03939-9	journal	September 2021
Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data Medlyn, B. E.; Dreyer, E.; Ellsworth, D. Plant, Cell and Environment, Vol. 25, Issue 9 https://doi.org/10.1046/j.1365-3040.2002.00891.x	journal	September 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
Convergence in the temperature response of leaf respiration across biomes and plant functional types Heskel, Mary A.; O’Sullivan, Odhran S.; Reich, Peter B. Proceedings of the National Academy of Sciences, Vol. 113, Issue 14 https://doi.org/10.1073/pnas.1520282113	journal	March 2016
Divergent drivers of leaf trait variation within species, among species, and among functional groups Osnas, Jeanne L. D.; Katabuchi, Masatoshi; Kitajima, Kaoru Proceedings of the National Academy of Sciences, Vol. 115, Issue 21 https://doi.org/10.1073/pnas.1803989115	journal	May 2018
Seasonal patterns of leaf-level photosynthetic gas exchange in an eastern Amazonian rain forest Domingues, Tomas F.; Martinelli, Luiz A.; Ehleringer, James R. Plant Ecology & Diversity, Vol. 7, Issue 1-2 https://doi.org/10.1080/17550874.2012.748849	journal	February 2013
Effect of temperature on cuticular transpiration of isolated cuticular membranes and leaf discs Schreiber, L. Journal of Experimental Botany, Vol. 52, Issue 362 https://doi.org/10.1093/jexbot/52.362.1893	journal	September 2001
Seasonal trends in photosynthetic parameters and stomatal conductance of blue oak (Quercus douglasii) under prolonged summer drought and high temperature Xu, L.; Baldocchi, D. D. Tree Physiology, Vol. 23, Issue 13 https://doi.org/10.1093/treephys/23.13.865	journal	September 2003
Stomatal conductance, transpiration and sap flow of tropical montane rain forest trees in the southern Ecuadorian Andes Motzer, T.; Munz, N.; Kuppers, M. Tree Physiology, Vol. 25, Issue 10 https://doi.org/10.1093/treephys/25.10.1283	journal	October 2005
Late day measurement of excised branches results in uncertainty in the estimation of two stomatal parameters derived from response curves in Populus deltoides Bartr. x Populus nigra L. Davidson, Kenneth J.; Lamour, Julien; Rogers, Alistair Tree Physiology https://doi.org/10.1093/treephys/tpac006	journal	February 2022
Seasonal fluctuations and temperature dependence in photosynthetic parameters and stomatal conductance at the leaf scale of Populus euphratica Oliv. Zhu, G. -F.; Li, X.; Su, Y. -H. Tree Physiology, Vol. 31, Issue 2 https://doi.org/10.1093/treephys/tpr005	journal	February 2011
Transpiration and stomatal conductance in a young secondary tropical montane forest: contrasts between native trees and invasive understorey shrubs Ghimire, Chandra Prasad; Bruijnzeel, L. Adrian; Lubczynski, Maciek W. Tree Physiology, Vol. 38, Issue 7 https://doi.org/10.1093/treephys/tpy004	journal	April 2018
Nighttime Stomatal Conductance and Transpiration in C ₃ and C ₄ Plants Caird, Mairgareth A.; Richards, James H.; Donovan, Lisa A. Plant Physiology, Vol. 143, Issue 1 https://doi.org/10.1104/pp.106.092940	journal	January 2007
Leaf Respiration in Light and Darkness (A Comparison of Slow- and Fast-Growing Poa Species) Atkin, O. K.; Westbeek, Mhm.; Cambridge, M. L. Plant Physiology, Vol. 113, Issue 3 https://doi.org/10.1104/pp.113.3.961	journal	March 1997
CO2 and Water Vapor Exchange across Leaf Cuticle (Epidermis) at Various Water Potentials Boyer, J. S.; Wong, S. C.; Farquhar, G. D. Plant Physiology, Vol. 114, Issue 1 https://doi.org/10.1104/pp.114.1.185	journal	May 1997
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
Plasticity influencing the light compensation point offsets the specialization for light niches across shrub species in a tropical forest understorey Sterck, Frank J.; Duursma, Remko A.; Pearcy, Robert W. Journal of Ecology, Vol. 101, Issue 4 https://doi.org/10.1111/1365-2745.12076	journal	June 2013
Global photosynthetic capacity is optimized to the environment Smith, Nicholas G.; Keenan, Trevor F.; Colin Prentice, I. Ecology Letters, Vol. 22, Issue 3 https://doi.org/10.1111/ele.13210	journal	January 2019
Canopy-scale relationships between stomatal conductance and photosynthesis in irrigated rice Ono, Keisuke; Maruyama, Atsushi; Kuwagata, Tsuneo Global Change Biology, Vol. 19, Issue 7 https://doi.org/10.1111/gcb.12188	journal	April 2013
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
The response of stomatal conductance to seasonal drought in tropical forests Wu, Jin; Serbin, Shawn P.; Ely, Kim S. Global Change Biology, Vol. 26, Issue 2 https://doi.org/10.1111/gcb.14820	journal	October 2019
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
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
Long-term growth of soybean at elevated [CO2] does not cause acclimation of stomatal conductance under fully open-air conditions Leakey, Andrew D. B.; Bernacchi, Carl J.; Ort, Donald R. Plant, Cell and Environment, Vol. 29, Issue 9 https://doi.org/10.1111/j.1365-3040.2006.01556.x	journal	September 2006
The response of photosynthesis and stomatal conductance to rising [CO ₂ ]: mechanisms and environmental interactions : Photosynthesis and stomatal conductance responses to rising [CO Ainsworth, Elizabeth A.; Rogers, Alistair Plant, Cell & Environment, Vol. 30, Issue 3 https://doi.org/10.1111/j.1365-3040.2007.01641.x	journal	January 2007
The stomatal response to evaporative demand persists at night in Ricinus communis plants with high nocturnal conductance Barbour, Margaret M.; Buckley, Thomas N. Plant, Cell & Environment, Vol. 30, Issue 6 https://doi.org/10.1111/j.1365-3040.2007.01658.x	journal	June 2007
An overview of models of stomatal conductance at the leaf level: Models of stomatal conductance Damour, GaËLle; Simonneau, Thierry; Cochard, HervÉ Plant, Cell & Environment https://doi.org/10.1111/j.1365-3040.2010.02181.x	journal	July 2010
Optimal stomatal conductance in relation to photosynthesis in climatically contrasting Eucalyptus species under drought : Stomatal responses of eucalyptus under drought HÉRoult, Arnaud; Lin, Yan-Shih; Bourne, Aimee Plant, Cell & Environment, Vol. 36, Issue 2 https://doi.org/10.1111/j.1365-3040.2012.02570.x	journal	August 2012
Leaf-level light compensation points in shade-tolerant woody seedlings: Letters Craine, Joseph M.; Reich, Peter B. New Phytologist, Vol. 166, Issue 3 https://doi.org/10.1111/j.1469-8137.2005.01420.x	journal	May 2005
Nocturnal stomatal conductance responses to rising [CO2], temperature and drought Zeppel, Melanie J. B.; Lewis, James D.; Chaszar, Brian New Phytologist, Vol. 193, Issue 4 https://doi.org/10.1111/j.1469-8137.2011.03993.x	journal	December 2011
A test of the ‘one-point method’ for estimating maximum carboxylation capacity from field-measured, light-saturated photosynthesis De Kauwe, Martin G.; Lin, Yan-Shih; Wright, Ian J. New Phytologist, Vol. 210, Issue 3 https://doi.org/10.1111/nph.13815	journal	December 2015
Convergence in relationships between leaf traits, spectra and age across diverse canopy environments and two contrasting tropical forests Wu, Jin; Chavana-Bryant, Cecilia; Prohaska, Neill New Phytologist, Vol. 214, Issue 3 https://doi.org/10.1111/nph.14051	journal	July 2016
A roadmap for improving the representation of photosynthesis in Earth system models Rogers, Alistair; Medlyn, Belinda E.; Dukes, Jeffrey S. New Phytologist, Vol. 213, Issue 1 https://doi.org/10.1111/nph.14283	journal	November 2016
In situ temperature response of photosynthesis of 42 tree and liana species in the canopy of two Panamanian lowland tropical forests with contrasting rainfall regimes Slot, Martijn; Winter, Klaus New Phytologist, Vol. 214, Issue 3 https://doi.org/10.1111/nph.14469	journal	February 2017
Changes in the chloroplastic CO ₂ concentration explain much of the observed Kok effect: a model Farquhar, Graham D.; Busch, Florian A. New Phytologist, Vol. 214, Issue 2 https://doi.org/10.1111/nph.14512	journal	March 2017
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
Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale Kumarathunge, Dushan P.; Medlyn, Belinda E.; Drake, John E. New Phytologist, Vol. 222, Issue 2 https://doi.org/10.1111/nph.15668	journal	February 2019
Phylogenetic and biogeographic controls of plant nighttime stomatal conductance Yu, Kailiang; Goldsmith, Gregory R.; Wang, Yujie New Phytologist, Vol. 222, Issue 4 https://doi.org/10.1111/nph.15755	journal	March 2019
Assessing the potential functions of nocturnal stomatal conductance in C ₃ and C ₄ plants Resco de Dios, Víctor; Chowdhury, Faqrul I.; Granda, Elena New Phytologist, Vol. 223, Issue 4 https://doi.org/10.1111/nph.15881	journal	May 2019
How do stomata respond to water status? Buckley, Thomas N. New Phytologist, Vol. 224, Issue 1 https://doi.org/10.1111/nph.15899	journal	June 2019
Where do leaf water leaks come from? Trade‐offs underlying the variability in minimum conductance across tropical savanna species with contrasting growth strategies Machado, Renan; Loram‐Lourenço, Lucas; Farnese, Fernanda Santos New Phytologist, Vol. 229, Issue 3 https://doi.org/10.1111/nph.16941	journal	October 2020
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
Cutting-edge research or cutting-edge artefact? An overdue control experiment complicates the xylem refilling story: Xylem-refilling artefacts Sperry, John Plant, Cell & Environment https://doi.org/10.1111/pce.12148	journal	August 2013
Optimal plant water economy: Optimal plant water economy Buckley, Thomas N.; Sack, Lawren; Farquhar, Graham D. Plant, Cell & Environment, Vol. 40, Issue 6 https://doi.org/10.1111/pce.12823	journal	October 2016
Estimating the sensitivity of stomatal conductance to photosynthesis: a review: The sensitivity of conductance to photosynthesis Miner, Grace L.; Bauerle, William L.; Baldocchi, Dennis D. Plant, Cell & Environment, Vol. 40, Issue 7 https://doi.org/10.1111/pce.12871	journal	February 2017
Seasonal variability of the parameters of the Ball-Berry model of stomatal conductance in maize ( Zea mays L . ) and sunflower ( Helianthus annuus L.) under well-watered and water-stressed conditions: Ball-Berry model parameters Miner, Grace L.; Bauerle, William L. Plant, Cell & Environment, Vol. 40, Issue 9 https://doi.org/10.1111/pce.12990	journal	July 2017
The “one‐point method” for estimating maximum carboxylation capacity of photosynthesis: A cautionary tale Burnett, Angela C.; Davidson, Kenneth J.; Serbin, Shawn P. Plant, Cell & Environment, Vol. 42, Issue 8 https://doi.org/10.1111/pce.13574	journal	June 2019
Modeling the Exchanges of Energy, Water, and Carbon Between Continents and the Atmosphere Sellers, P. J. Science, Vol. 275, Issue 5299 https://doi.org/10.1126/science.275.5299.502	journal	January 1997
Plant water potential improves prediction of empirical stomatal models Anderegg, William R. L.; Wolf, Adam; Arango-Velez, Adriana PLOS ONE, Vol. 12, Issue 10 https://doi.org/10.1371/journal.pone.0185481	journal	October 2017
Genotypic Variation in Epidermal Conductance and its Associated Traits among Oryza sativa and O. glaberrima Cultivars and their Interspecific Progenies Saito, Kazuki; Futakuchi, Koichi Crop Science, Vol. 50, Issue 1 https://doi.org/10.2135/cropsci2009.06.0284	journal	January 2010
Representing nighttime and minimum conductance in CLM4.5: global hydrology and carbon sensitivity analysis using observational constraints Lombardozzi, Danica L.; Zeppel, Melanie J. B.; Fisher, Rosie A. Geoscientific Model Development, Vol. 10, Issue 1 https://doi.org/10.5194/gmd-10-321-2017	journal	January 2017
The Joint UK Land Environment Simulator (JULES), model description – Part 2: Carbon fluxes and vegetation dynamics Clark, D. B.; Mercado, L. M.; Sitch, S. Geoscientific Model Development, Vol. 4, Issue 3 https://doi.org/10.5194/gmd-4-701-2011	journal	January 2011
Modeling stomatal conductance in the earth system: linking leaf water-use efficiency and water transport along the soil–plant–atmosphere continuum Bonan, G. B.; Williams, M.; Fisher, R. A. Geoscientific Model Development, Vol. 7, Issue 5 https://doi.org/10.5194/gmd-7-2193-2014	journal	January 2014
A test of an optimal stomatal conductance scheme within the CABLE land surface model De Kauwe, M. G.; Kala, J.; Lin, Y. -S. Geoscientific Model Development, Vol. 8, Issue 2 https://doi.org/10.5194/gmd-8-431-2015	journal	January 2015

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54 ENVIRONMENTAL SCIENCES
leaf gas exchange
minimum conductance
optimality model
residual conductance
stomatal conductance
trait covariation
transpiration
water use efficiency

An improved representation of the relationship between photosynthesis and stomatal conductance leads to more stable estimation of conductance parameters and improves the goodness-of-fit across diverse data sets

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