Impact of mesophyll diffusion on estimated global land CO2 fertilization
Abstract
In C3 plants, CO2 concentrations drop considerably along mesophyll diffusion pathways from substomatal cavities to chloroplasts where CO2 assimilation occurs. Global carbon cycle models have not explicitly represented this internal drawdown and so overestimate CO2 available for carboxylation and underestimate photosynthetic responsiveness to atmospheric CO2. An explicit consideration of mesophyll diffusion increases the modeled cumulative CO2 fertilization effect (CFE) for global gross primary production (GPP) from 915 PgC to 1057 PgC for the period of 1901 to 2010. This increase represents a 16% correction, large enough to explain the persistent overestimation of growth rates of historical atmospheric CO2 by Earth System Models. Without this correction, the CFE for global GPP is underestimated by 0.05 PgC yr-1ppm-1. This finding implies that the contemporary terrestrial biosphere is more CO2-limited than previously thought.
- Authors:
-
- Univ. of Texas at Austin, Austin, TX (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Univ. of Missouri, Columbia, MO (United States). Dept. of Forestry
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Climate Change Science Institute and Computational Earth Sciences Group
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1160002
- Grant/Contract Number:
- FG02- 01ER64746; AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 111; Journal Issue: 44; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences, Washington, DC (United States)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Mesophyll conductance; CO₂ fertilization; carbon cycle; gross primary 42 production; photosynthetic model
Citation Formats
Sun, Ying, Gu, Lianhong, Dickinson, Robert E., Norby, Richard J., Pallardy, Stephen G., and Hoffman, Forrest M. Impact of mesophyll diffusion on estimated global land CO2 fertilization. United States: N. p., 2014.
Web. doi:10.1073/pnas.1418075111.
Sun, Ying, Gu, Lianhong, Dickinson, Robert E., Norby, Richard J., Pallardy, Stephen G., & Hoffman, Forrest M. Impact of mesophyll diffusion on estimated global land CO2 fertilization. United States. https://doi.org/10.1073/pnas.1418075111
Sun, Ying, Gu, Lianhong, Dickinson, Robert E., Norby, Richard J., Pallardy, Stephen G., and Hoffman, Forrest M. Mon .
"Impact of mesophyll diffusion on estimated global land CO2 fertilization". United States. https://doi.org/10.1073/pnas.1418075111. https://www.osti.gov/servlets/purl/1160002.
@article{osti_1160002,
title = {Impact of mesophyll diffusion on estimated global land CO2 fertilization},
author = {Sun, Ying and Gu, Lianhong and Dickinson, Robert E. and Norby, Richard J. and Pallardy, Stephen G. and Hoffman, Forrest M.},
abstractNote = {In C3 plants, CO2 concentrations drop considerably along mesophyll diffusion pathways from substomatal cavities to chloroplasts where CO2 assimilation occurs. Global carbon cycle models have not explicitly represented this internal drawdown and so overestimate CO2 available for carboxylation and underestimate photosynthetic responsiveness to atmospheric CO2. An explicit consideration of mesophyll diffusion increases the modeled cumulative CO2 fertilization effect (CFE) for global gross primary production (GPP) from 915 PgC to 1057 PgC for the period of 1901 to 2010. This increase represents a 16% correction, large enough to explain the persistent overestimation of growth rates of historical atmospheric CO2 by Earth System Models. Without this correction, the CFE for global GPP is underestimated by 0.05 PgC yr-1ppm-1. This finding implies that the contemporary terrestrial biosphere is more CO2-limited than previously thought.},
doi = {10.1073/pnas.1418075111},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 44,
volume = 111,
place = {United States},
year = {Mon Oct 13 00:00:00 EDT 2014},
month = {Mon Oct 13 00:00:00 EDT 2014}
}
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Works referenced in this record:
Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field
journal, April 2009
- Niinemets, Ülo; Díaz-Espejo, Antonio; Flexas, Jaume
- Journal of Experimental Botany, Vol. 60, Issue 8
Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error
journal, September 2003
- Long, S. P.
- Journal of Experimental Botany, Vol. 54, Issue 392
Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer
journal, June 2007
- Warren, C. R.
- Journal of Experimental Botany, Vol. 59, Issue 7
Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion
journal, December 2005
- Terashima, Ichiro; Hanba, Yuko T.; Tazoe, Youshi
- Journal of Experimental Botany, Vol. 57, Issue 2
Resistances along the CO2 diffusion pathway inside leaves
journal, April 2009
- Evans, J. R.; Kaldenhoff, R.; Genty, B.
- Journal of Experimental Botany, Vol. 60, Issue 8
Carbon residence time dominates uncertainty in terrestrial vegetation responses to future climate and atmospheric CO 2
journal, December 2013
- Friend, Andrew D.; Lucht, Wolfgang; Rademacher, Tim T.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 9
An Overview of CMIP5 and the Experiment Design
journal, April 2012
- Taylor, Karl E.; Stouffer, Ronald J.; Meehl, Gerald A.
- Bulletin of the American Meteorological Society, Vol. 93, Issue 4
Reliable estimation of biochemical parameters from C3 leaf photosynthesis-intercellular carbon dioxide response curves: Estimating FvCB model parameters
journal, June 2010
- Gu, Lianhong; Pallardy, Stephen G.; Tu, Kevin
- Plant, Cell & Environment, Vol. 33, Issue 11
Fitting photosynthetic carbon dioxide response curves for C 3 leaves
journal, September 2007
- Sharkey, Thomas D.; Bernacchi, Carl J.; Farquhar, Graham D.
- Plant, Cell & Environment, Vol. 30, Issue 9
Temperature response of carbon isotope discrimination and mesophyll conductance in tobacco: Temperature response of mesophyll conductance
journal, September 2012
- Evans, John R.; Von Caemmerer, Susanne
- Plant, Cell & Environment, Vol. 36, Issue 4
Carbon Isotope Discrimination measured Concurrently with Gas Exchange to Investigate CO2 Diffusion in Leaves of Higher Plants
journal, January 1986
- Evans, Jr; Sharkey, Td; Berry, Ja
- Functional Plant Biology, Vol. 13, Issue 2
What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2: Tansley review
journal, November 2004
- Ainsworth, Elizabeth A.; Long, Stephen P.
- New Phytologist, Vol. 165, Issue 2
Evergreens favored by higher responsiveness to increased CO2
journal, March 2011
- Niinemets, Ülo; Flexas, Jaume; Peñuelas, Josep
- Trends in Ecology & Evolution, Vol. 26, Issue 3
Net primary production of forests: a constant fraction of gross primary production?
journal, February 1998
- Waring, R. H.; Landsberg, J. J.; Williams, M.
- Tree Physiology, Vol. 18, Issue 2
Enhanced Seasonal Exchange of CO2 by Northern Ecosystems Since 1960
journal, August 2013
- Graven, H. D.; Keeling, R. F.; Piper, S. C.
- Science, Vol. 341, Issue 6150
Carbon balance in the tundra, boreal forest and humid tropical forest during climate change: scaling up from leaf physiology and soil carbon dynamics
journal, October 1995
- Wang, Y. P.; Polglase, P. J.
- Plant, Cell and Environment, Vol. 18, Issue 10
Carbon balance of the terrestrial biosphere in the twentieth century: Analyses of CO2, climate and land use effects with four process-based ecosystem models
text, January 2001
- McGuire, A. D.; Sitch, S.; Clein, J. S.
- American Geophysical Union
A Large and Persistent Carbon Sink in the World's Forests
journal, July 2011
- Pan, Y.; Birdsey, R. A.; Fang, J.
- Science, Vol. 333, Issue 6045
Carbon balance of the terrestrial biosphere in the Twentieth Century: Analyses of CO 2 , climate and land use effects with four process-based ecosystem models
journal, March 2001
- McGuire, A. D.; Sitch, S.; Clein, J. S.
- Global Biogeochemical Cycles, Vol. 15, Issue 1
Causes and implications of persistent atmospheric carbon dioxide biases in Earth System Models
journal, February 2014
- Hoffman, F. M.; Randerson, J. T.; Arora, V. K.
- Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 2
What's the flux? Unraveling how CO 2 fluxes from trees reflect underlying physiological processes
journal, December 2012
- Trumbore, Susan E.; Angert, Alon; Kunert, Norbert
- New Phytologist, Vol. 197, Issue 2
Increase in forest water-use efficiency as atmospheric carbon dioxide concentrations rise
journal, July 2013
- Keenan, Trevor F.; Hollinger, David Y.; Bohrer, Gil
- Nature, Vol. 499, Issue 7458
Evaluation of terrestrial carbon cycle models for their response to climate variability and to CO 2 trends
journal, April 2013
- Piao, Shilong; Sitch, Stephen; Ciais, Philippe
- Global Change Biology, Vol. 19, Issue 7
On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model
journal, February 2004
- Ethier, G. J.; Livingston, N. J.
- Plant, Cell and Environment, Vol. 27, Issue 2
The impact of nitrogen and phosphorous limitation on the estimated terrestrial carbon balance and warming of land use change over the last 156 yr
journal, January 2013
- Zhang, Q.; Pitman, A. J.; Wang, Y. P.
- Earth System Dynamics, Vol. 4, Issue 2
Uncertainties in CMIP5 Climate Projections due to Carbon Cycle Feedbacks
journal, January 2014
- Friedlingstein, Pierre; Meinshausen, Malte; Arora, Vivek K.
- Journal of Climate, Vol. 27, Issue 2
Interannual extremes in the rate of rise of atmospheric carbon dioxide since 1980
journal, June 1995
- Keeling, C. D.; Whorf, T. P.; Wahlen, M.
- Nature, Vol. 375, Issue 6533
Importance of mesophyll diffusion conductance in estimation of plant photosynthesis in the field
journal, March 2009
- Niinemets, Ülo; Díaz-Espejo, Antonio; Flexas, Jaume
- Journal of Experimental Botany, Vol. 60, Issue 8
Temperature Response of Mesophyll Conductance. Implications for the Determination of Rubisco Enzyme Kinetics and for Limitations to Photosynthesis in Vivo
journal, November 2002
- Bernacchi, Carl J.; Portis, Archie R.; Nakano, Hiromi
- Plant Physiology, Vol. 130, Issue 4
Mesophyll conductance: constraint on carbon acquisition by C 3 plants : Editorial
journal, October 2012
- Sharkey, Thomas D.
- Plant, Cell & Environment, Vol. 35, Issue 11
A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species
journal, June 1980
- Farquhar, G. D.; von Caemmerer, S.; Berry, J. A.
- Planta, Vol. 149, Issue 1
Asymmetrical effects of mesophyll conductance on fundamental photosynthetic parameters and their relationships estimated from leaf gas exchange measurements: Asymmetrical mesophyll conductance effects
journal, November 2013
- Sun, Ying; Gu, Lianhong; Dickinson, Robert E.
- Plant, Cell & Environment, Vol. 37, Issue 4
Mesophyll diffusion conductance to CO2: An unappreciated central player in photosynthesis
journal, September 2012
- Flexas, Jaume; Barbour, Margaret M.; Brendel, Oliver
- Plant Science, Vol. 193-194
Improving canopy processes in the Community Land Model version 4 (CLM4) using global flux fields empirically inferred from FLUXNET data
journal, January 2011
- Bonan, Gordon B.; Lawrence, Peter J.; Oleson, Keith W.
- Journal of Geophysical Research, Vol. 116, Issue G2
Limitations of nitrogen and phosphorous on the terrestrial carbon uptake in the 20th century
journal, November 2011
- Zhang, Q.; Wang, Y. P.; Pitman, A. J.
- Geophysical Research Letters, Vol. 38, Issue 22
Works referencing / citing this record:
Revisiting ocean carbon sequestration by direct injection: a global carbon budget perspective
journal, January 2016
- Reith, Fabian; Keller, David P.; Oschlies, Andreas
- Earth System Dynamics, Vol. 7, Issue 4
The response of stomatal conductance to seasonal drought in tropical forests
journal, October 2019
- Wu, Jin; Serbin, Shawn P.; Ely, Kim S.
- Global Change Biology, Vol. 26, Issue 2
The interaction between nitrogen and phosphorous is a strong predictor of intra-plant variation in nitrogen isotope composition in a desert species
journal, January 2017
- Zhang, Jinxin; Gu, Lianhong; Zhang, Jingbo
- Biogeosciences, Vol. 14, Issue 1
Understanding regulation of leaf internal carbon and water transport using online stable isotope techniques
journal, September 2016
- Barbour, Margaret M.
- New Phytologist, Vol. 213, Issue 1
Revisiting ocean carbon sequestration by direct injection: A global carbon budget perspective
journal, April 2016
- Reith, Fabian; Keller, David P.; Oschlies, Andreas
- Earth Systems Dynamics Discussions
Mesophyll conductance and accurate photosynthetic carbon gain calculations
journal, November 2018
- Tosens, Tiina; Laanisto, Lauri
- Journal of Experimental Botany, Vol. 69, Issue 22
Elevated [ CO 2 ] effects on crops: Advances in understanding acclimation, nitrogen dynamics and interactions with drought and other organisms
journal, January 2019
- Tausz‐Posch, S.; Tausz, M.; Bourgault, M.
- Plant Biology, Vol. 22, Issue S1
Reliable, robust and realistic: the three R's of next-generation land-surface modelling
journal, January 2015
- Prentice, I. C.; Liang, X.; Medlyn, B. E.
- Atmospheric Chemistry and Physics, Vol. 15, Issue 10
Ecosystem functioning is enveloped by hydrometeorological variability
journal, August 2017
- Pappas, Christoforos; Mahecha, Miguel D.; Frank, David C.
- Nature Ecology & Evolution, Vol. 1, Issue 9
Carbon storage dynamics of temperate freshwater wetlands in Pennsylvania
journal, July 2018
- Mazurczyk, Tara; Brooks, Robert P.
- Wetlands Ecology and Management, Vol. 26, Issue 5
Sun‐induced Chl fluorescence and its importance for biophysical modeling of photosynthesis based on light reactions
journal, April 2019
- Gu, Lianhong; Han, Jimei; Wood, Jeffrey D.
- New Phytologist, Vol. 223, Issue 3
An Excel tool for deriving key photosynthetic parameters from combined gas exchange and chlorophyll fluorescence: theory and practice: Descriptive modelling of gas exchange data
journal, June 2015
- Bellasio, Chandra; Beerling, David J.; Griffiths, Howard
- Plant, Cell & Environment, Vol. 39, Issue 6
High mesophyll conductance in the high-yielding rice cultivar Takanari quantified with the combined gas exchange and chlorophyll fluorescence measurements under free-air CO 2 enrichment
journal, July 2019
- Ikawa, Hiroki; Sakai, Hidemitsu; Chen, Charles P.
- Plant Production Science, Vol. 22, Issue 3
What gas exchange data can tell us about photosynthesis: Gas exchange data and photosynthesis
journal, December 2015
- Sharkey, Thomas D.
- Plant, Cell & Environment, Vol. 39, Issue 6
Elevated CO 2 does not stimulate carbon sink in a semi-arid grassland
journal, January 2019
- Song, Jian; Wan, Shiqiang; Piao, Shilong
- Ecology Letters, Vol. 22, Issue 3
The many meanings of gross photosynthesis and their implication for photosynthesis research from leaf to globe: Definition of gross photosynthesis
journal, June 2015
- Wohlfahrt, Georg; Gu, Lianhong
- Plant, Cell & Environment, Vol. 38, Issue 12
The temperature response of mesophyll conductance, and its component conductances, varies between species and genotypes
journal, February 2019
- Shrestha, Arjina; Song, Xin; Barbour, Margaret M.
- Photosynthesis Research, Vol. 141, Issue 1
The interaction between nitrogen and phosphorous is a strong predictor of intra-plant variation in nitrogen isotope composition in a desert species
preprint, November 2015
- Zhang, J.; Gu, L.; Zhang, J.
Towards a universal model for carbon dioxide uptake by plants
journal, September 2017
- Wang, Han; Prentice, I. Colin; Keenan, Trevor F.
- Nature Plants, Vol. 3, Issue 9
Evaluation of Forest Conversion Effects on Soil Erosion, Soil Organic Carbon and Total Nitrogen Based on 137Cs Tracer Technique
journal, May 2019
- Zhu, Xi; Lin, Jie; Dai, Qiao
- Forests, Vol. 10, Issue 5
Historical carbon dioxide emissions caused by land-use changes are possibly larger than assumed
journal, January 2017
- Arneth, A.; Sitch, S.; Pongratz, J.
- Nature Geoscience, Vol. 10, Issue 2
Mesophyll conductance in land surface models: effects on photosynthesis and transpiration
journal, December 2019
- Knauer, Jürgen; Zaehle, Sönke; De Kauwe, Martin G.
- The Plant Journal, Vol. 101, Issue 4
Spatiotemporal pattern of gross primary productivity and its covariation with climate in China over the last thirty years
journal, September 2017
- Yao, Yitong; Wang, Xuhui; Li, Yue
- Global Change Biology, Vol. 24, Issue 1
Description and validation of an intermediate complexity model for ecosystem photosynthesis and evapotranspiration: ACM-GPP-ETv1
journal, January 2019
- Smallman, Thomas Luke; Williams, Mathew
- Geoscientific Model Development, Vol. 12, Issue 6
Critical review: incorporating the arrangement of mitochondria and chloroplasts into models of photosynthesis and carbon isotope discrimination
journal, April 2019
- Ubierna, Nerea; Cernusak, Lucas A.; Holloway-Phillips, Meisha
- Photosynthesis Research, Vol. 141, Issue 1
High mesophyll conductance in the high-yielding rice cultivar Takanari quantified with the combined gas exchange and chlorophyll fluorescence measurements under free-air CO2 enrichment
text, January 2019
- Ikawa, Hiroki; Sakai, Hidemitsu; Chen, Charles P.
- Taylor & Francis
A meta-analysis of crop response patterns to nitrogen limitation for improved model representation
journal, October 2019
- Seufert, Verena; Granath, Gustaf; Müller, Christoph
- PLOS ONE, Vol. 14, Issue 10
A vertically discretised canopy description for ORCHIDEE (SVN r2290) and the modifications to the energy, water and carbon fluxes
journal, January 2015
- Naudts, K.; Ryder, J.; McGrath, M. J.
- Geoscientific Model Development, Vol. 8, Issue 7
Atmospheric evidence for a global secular increase in carbon isotopic discrimination of land photosynthesis
journal, September 2017
- Keeling, Ralph F.; Graven, Heather D.; Welp, Lisa R.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 39
Is NPP proportional to GPP? Waring’s hypothesis 20 years on
journal, May 2019
- Collalti, A.; Prentice, I. C.
- Tree Physiology, Vol. 39, Issue 8
The interaction between nitrogen and phosphorous is a strong predictor of 2 intra-plant variation in nitrogen isotope composition in a desert species
posted_content, June 2016
- Zhang, Jinxin; Gu, Lianhong; Zhang, Jingbo
- Biogeosciences
Using photorespiratory oxygen response to analyse leaf mesophyll resistance
journal, February 2020
- Yin, Xinyou; van der Putten, Peter E. L.; Belay, Daniel
- Photosynthesis Research, Vol. 144, Issue 1