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Title: Reduced global plant respiration due to the acclimation of leaf dark respiration coupled with photosynthesis

Abstract

Summary Leaf dark respiration ( R d ) acclimates to environmental changes. However, the magnitude, controls and time scales of acclimation remain unclear and are inconsistently treated in ecosystem models. We hypothesized that R d and Rubisco carboxylation capacity ( V cmax ) at 25°C ( R d,25 , V cmax,25 ) are coordinated so that R d,25 variations support V cmax,25 at a level allowing full light use, with V cmax,25 reflecting daytime conditions (for photosynthesis), and R d,25 / V cmax,25 reflecting night‐time conditions (for starch degradation and sucrose export). We tested this hypothesis temporally using a 5‐yr warming experiment, and spatially using an extensive field‐measurement data set. We compared the results to three published alternatives: R d,25 declines linearly with daily average prior temperature; R d at average prior night temperatures tends towards a constant value; and R d,25 / V cmax,25 is constant. Our hypothesis accounted for more variation in observed R d,25 over time ( R 2  = 0.74) and space ( R 2  = 0.68) than the alternatives. Night‐time temperature dominated the seasonal time‐course of R d , with an apparent response time scale of c. 2 wk. V cmax dominated the spatial patterns. Our acclimation hypothesismore » results in a smaller increase in global R d in response to rising CO 2 and warming than is projected by the two of three alternative hypotheses, and by current models.« less

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [5]; ORCiD logo [6]; ORCiD logo [7]; ORCiD logo [8]
  1. Department of Earth System Science, Ministry of Education Key Laboratory for Earth System Modeling, Institute for Global Change Studies Tsinghua University Beijing 100084 China
  2. Department of Earth System Science, Ministry of Education Key Laboratory for Earth System Modeling, Institute for Global Change Studies Tsinghua University Beijing 100084 China, School of Archaeology, Geography and Environmental Sciences (SAGES) University of Reading Reading RG6 6AH UK
  3. Department of Earth System Science, Ministry of Education Key Laboratory for Earth System Modeling, Institute for Global Change Studies Tsinghua University Beijing 100084 China, Department of Life Sciences, Georgina Mace Centre for the Living Planet Imperial College London Silwood Park Campus, Buckhurst Road Ascot SL5 7PY UK
  4. ARC Centre of Excellence in Plant Energy Biology, Research School of Biology The Australian National University Building 134 Canberra ACT 2601 Australia, Division of Plant Sciences, Research School of Biology The Australian National University Building 46 Canberra ACT 2601 Australia
  5. Department of Biological Sciences Texas Tech University Lubbock TX 79409 USA
  6. Department of Life Sciences, Georgina Mace Centre for the Living Planet Imperial College London Silwood Park Campus, Buckhurst Road Ascot SL5 7PY UK
  7. Department of Forest Resources University of Minnesota St Paul MN 55108 USA
  8. Department of Forest Resources University of Minnesota St Paul MN 55108 USA, Institute for Global Change Biology, and School for the Environment and Sustainability University of Michigan Ann Arbor MI 48109 USA, Hawkesbury Institute for the Environment Western Sydney University Penrith NSW 2753 Australia
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
2203997
Alternate Identifier(s):
OSTI ID: 2274722
Grant/Contract Number:  
DE‐FG02‐07ER644456
Resource Type:
Published Article
Journal Name:
New Phytologist
Additional Journal Information:
Journal Name: New Phytologist Journal Volume: 241 Journal Issue: 2; Journal ID: ISSN 0028-646X
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Ren, Yanghang, Wang, Han, Harrison, Sandy P., Prentice, I. Colin, Atkin, Owen K., Smith, Nicholas G., Mengoli, Giulia, Stefanski, Artur, and Reich, Peter B. Reduced global plant respiration due to the acclimation of leaf dark respiration coupled with photosynthesis. United Kingdom: N. p., 2023. Web. doi:10.1111/nph.19355.
Ren, Yanghang, Wang, Han, Harrison, Sandy P., Prentice, I. Colin, Atkin, Owen K., Smith, Nicholas G., Mengoli, Giulia, Stefanski, Artur, & Reich, Peter B. Reduced global plant respiration due to the acclimation of leaf dark respiration coupled with photosynthesis. United Kingdom. https://doi.org/10.1111/nph.19355
Ren, Yanghang, Wang, Han, Harrison, Sandy P., Prentice, I. Colin, Atkin, Owen K., Smith, Nicholas G., Mengoli, Giulia, Stefanski, Artur, and Reich, Peter B. Sat . "Reduced global plant respiration due to the acclimation of leaf dark respiration coupled with photosynthesis". United Kingdom. https://doi.org/10.1111/nph.19355.
@article{osti_2203997,
title = {Reduced global plant respiration due to the acclimation of leaf dark respiration coupled with photosynthesis},
author = {Ren, Yanghang and Wang, Han and Harrison, Sandy P. and Prentice, I. Colin and Atkin, Owen K. and Smith, Nicholas G. and Mengoli, Giulia and Stefanski, Artur and Reich, Peter B.},
abstractNote = {Summary Leaf dark respiration ( R d ) acclimates to environmental changes. However, the magnitude, controls and time scales of acclimation remain unclear and are inconsistently treated in ecosystem models. We hypothesized that R d and Rubisco carboxylation capacity ( V cmax ) at 25°C ( R d,25 , V cmax,25 ) are coordinated so that R d,25 variations support V cmax,25 at a level allowing full light use, with V cmax,25 reflecting daytime conditions (for photosynthesis), and R d,25 / V cmax,25 reflecting night‐time conditions (for starch degradation and sucrose export). We tested this hypothesis temporally using a 5‐yr warming experiment, and spatially using an extensive field‐measurement data set. We compared the results to three published alternatives: R d,25 declines linearly with daily average prior temperature; R d at average prior night temperatures tends towards a constant value; and R d,25 / V cmax,25 is constant. Our hypothesis accounted for more variation in observed R d,25 over time ( R 2  = 0.74) and space ( R 2  = 0.68) than the alternatives. Night‐time temperature dominated the seasonal time‐course of R d , with an apparent response time scale of c. 2 wk. V cmax dominated the spatial patterns. Our acclimation hypothesis results in a smaller increase in global R d in response to rising CO 2 and warming than is projected by the two of three alternative hypotheses, and by current models.},
doi = {10.1111/nph.19355},
journal = {New Phytologist},
number = 2,
volume = 241,
place = {United Kingdom},
year = {Sat Oct 28 00:00:00 EDT 2023},
month = {Sat Oct 28 00:00:00 EDT 2023}
}

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Works referenced in this record:

Forest production efficiency increases with growth temperature
journal, October 2020


Acclimation of leaf respiration consistent with optimal photosynthetic capacity
journal, February 2020

  • Wang, Han; Atkin, Owen K.; Keenan, Trevor F.
  • Global Change Biology, Vol. 26, Issue 4
  • DOI: 10.1111/gcb.14980

An optimality‐based model explains seasonal variation in C3 plant photosynthetic capacity
journal, September 2020

  • Jiang, Chongya; Ryu, Youngryel; Wang, Han
  • Global Change Biology, Vol. 26, Issue 11
  • DOI: 10.1111/gcb.15276

LCE: leaf carbon exchange data set for tropical, temperate, and boreal species of North and Central America
journal, September 2017

  • Smith, Nicholas G.; Dukes, Jeffrey S.
  • Ecology, Vol. 98, Issue 11
  • DOI: 10.1002/ecy.1992

WFDE5: bias-adjusted ERA5 reanalysis data for impact studies
journal, January 2020

  • Cucchi, Marco; Weedon, Graham P.; Amici, Alessandro
  • Earth System Science Data, Vol. 12, Issue 3
  • DOI: 10.5194/essd-12-2097-2020

Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species
journal, August 2004


Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale
journal, February 2019

  • Kumarathunge, Dushan P.; Medlyn, Belinda E.; Drake, John E.
  • New Phytologist, Vol. 222, Issue 2
  • DOI: 10.1111/nph.15668

Rapid temperature acclimation of leaf respiration rates in Quercus alba and Quercus rubra
journal, October 2003


Drivers of leaf carbon exchange capacity across biomes at the continental scale
journal, June 2018

  • Smith, Nicholas G.; Dukes, Jeffrey S.
  • Ecology, Vol. 99, Issue 7
  • DOI: 10.1002/ecy.2370

Photosynthetic responses to altitude: an explanation based on optimality principles
journal, November 2016

  • Wang, Han; Prentice, I. Colin; Davis, Tyler W.
  • New Phytologist, Vol. 213, Issue 3
  • DOI: 10.1111/nph.14332

Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency
journal, June 2004


New Equations for Computing Vapor Pressure and Enhancement Factor
journal, December 1981


A General Model for the Light-Use Efficiency of Primary Production
journal, October 1996

  • Haxeltine, A.; Prentice, I. C.
  • Functional Ecology, Vol. 10, Issue 5
  • DOI: 10.2307/2390165

Short-term thermal acclimation of dark respiration is greater in non-photosynthetic than in photosynthetic tissues
journal, October 2019

  • Smith, Nicholas G.; Li, Guoyong; Dukes, Jeffrey S.
  • AoB PLANTS, Vol. 11, Issue 6
  • DOI: 10.1093/aobpla/plz064

Global photosynthetic capacity is optimized to the environment
journal, January 2019

  • Smith, Nicholas G.; Keenan, Trevor F.; Colin Prentice, I.
  • Ecology Letters, Vol. 22, Issue 3
  • DOI: 10.1111/ele.13210

A dynamic global vegetation model for studies of the coupled atmosphere-biosphere system: DVGM FOR COUPLED CLIMATE STUDIES
journal, February 2005

  • Krinner, G.; Viovy, Nicolas; de Noblet-Ducoudré, Nathalie
  • Global Biogeochemical Cycles, Vol. 19, Issue 1
  • DOI: 10.1029/2003GB002199

Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants
journal, August 2008


Reprocessing the MODIS Leaf Area Index products for land surface and climate modelling
journal, May 2011


Thermal acclimation and the dynamic response of plant respiration to temperature
journal, July 2003


Recent trends in gross primary production and their drivers: analysis and modelling at flux-site and global scales
journal, December 2020


A Generalized Relationship between Photosynthetically Active Radiation and Solar Radiation 1
journal, March 1907


The Joint UK Land Environment Simulator (JULES), model description – Part 2: Carbon fluxes and vegetation dynamics
journal, January 2011

  • Clark, D. B.; Mercado, L. M.; Sitch, S.
  • Geoscientific Model Development, Vol. 4, Issue 3
  • DOI: 10.5194/gmd-4-701-2011

Forest carbon balance under elevated CO2
journal, April 2002


Coordination theory of leaf nitrogen distribution in a canopy
journal, February 1993

  • Chen, Jia-Lin; Reynolds, James F.; Harley, Peter C.
  • Oecologia, Vol. 93, Issue 1
  • DOI: 10.1007/BF00321192

Robust satisficing linear regression: Performance/robustness trade-off and consistency criterion
journal, August 2009

  • Zacksenhouse, Miriam; Nemets, Simona; Lebedev, Mikhail A.
  • Mechanical Systems and Signal Processing, Vol. 23, Issue 6
  • DOI: 10.1016/j.ymssp.2008.09.008

Boreal and temperate trees show strong acclimation of respiration to warming
journal, March 2016

  • Reich, Peter B.; Sendall, Kerrie M.; Stefanski, Artur
  • Nature, Vol. 531, Issue 7596
  • DOI: 10.1038/nature17142

The relative impacts of daytime and night-time warming on photosynthetic capacity in Populus deltoides
journal, December 2002


Temperature responses of photosynthesis and respiration in evergreen trees from boreal to tropical latitudes
journal, January 2022

  • Crous, Kristine Y.; Uddling, Johan; De Kauwe, Martin G.
  • New Phytologist, Vol. 234, Issue 2
  • DOI: 10.1111/nph.17951

Eco‐evolutionary optimality as a means to improve vegetation and land‐surface models
journal, July 2021

  • Harrison, Sandy P.; Cramer, Wolfgang; Franklin, Oskar
  • New Phytologist, Vol. 231, Issue 6
  • DOI: 10.1111/nph.17558

Plant RuBisCo: An Underutilized Protein for Food Applications
journal, August 2018

  • Di Stefano, Elisa; Agyei, Dominic; Njoku, Emmanuel N.
  • Journal of the American Oil Chemists' Society, Vol. 95, Issue 8
  • DOI: 10.1002/aocs.12104

Leaf respiration and alternative oxidase in field-grown alpine grasses respond to natural changes in temperature and light
journal, December 2010


Temperature acclimation of photosynthesis and respiration: A key uncertainty in the carbon cycle-climate feedback: PHYSIOLOGICAL TEMPERATURE ACCLIMATION
journal, October 2015

  • Lombardozzi, Danica L.; Bonan, Gordon B.; Smith, Nicholas G.
  • Geophysical Research Letters, Vol. 42, Issue 20
  • DOI: 10.1002/2015GL065934

The use and misuse of V c,max in Earth System Models
journal, April 2013


Plant respiration and photosynthesis in global-scale models: incorporating acclimation to temperature and CO 2
journal, September 2012


The community Noah land surface model with multiparameterization options (Noah-MP): 1. Model description and evaluation with local-scale measurements
journal, January 2011

  • Niu, Guo-Yue; Yang, Zong-Liang; Mitchell, Kenneth E.
  • Journal of Geophysical Research, Vol. 116, Issue D12
  • DOI: 10.1029/2010JD015139

Updated respiration routines alter spatio-temporal patterns of carbon cycling in a global land surface model
journal, September 2021

  • Butler, Ethan E.; Wythers, Kirk R.; Flores-Moreno, Habacuc
  • Environmental Research Letters, Vol. 16, Issue 10
  • DOI: 10.1088/1748-9326/ac2528

Towards a universal model for carbon dioxide uptake by plants
journal, September 2017


Convergence in the temperature response of leaf respiration across biomes and plant functional types
journal, March 2016

  • Heskel, Mary A.; O’Sullivan, Odhran S.; Reich, Peter B.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 14
  • DOI: 10.1073/pnas.1520282113

Global Carbon Budget 2021
journal, April 2022

  • Friedlingstein, Pierre; Jones, Matthew W.; O'Sullivan, Michael
  • Earth System Science Data, Vol. 14, Issue 4
  • DOI: 10.5194/essd-14-1917-2022

Balancing the costs of carbon gain and water transport: testing a new theoretical framework for plant functional ecology
journal, November 2013

  • Prentice, I. Colin; Dong, Ning; Gleason, Sean M.
  • Ecology Letters, Vol. 17, Issue 1
  • DOI: 10.1111/ele.12211

Evaluating the convergence between eddy-covariance and biometric methods for assessing carbon budgets of forests
journal, December 2016

  • Campioli, M.; Malhi, Y.; Vicca, S.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms13717

Leaf nitrogen from first principles: field evidence for adaptive variation with climate
journal, January 2017

  • Dong, Ning; Prentice, Iain Colin; Evans, Bradley J.
  • Biogeosciences, Vol. 14, Issue 2
  • DOI: 10.5194/bg-14-481-2017

Global variation in diurnal asymmetry in temperature, cloud cover, specific humidity and precipitation and its association with leaf area index
journal, September 2020

  • Cox, Daniel T. C.; Maclean, Ilya M. D.; Gardner, Alexandra S.
  • Global Change Biology, Vol. 26, Issue 12
  • DOI: 10.1111/gcb.15336

Rising CO2 and warming reduce global canopy demand for nitrogen
journal, April 2022

  • Dong, Ning; Wright, Ian J.; Chen, Jing M.
  • New Phytologist, Vol. 235, Issue 5
  • DOI: 10.1111/nph.18076

Acclimation of photosynthesis and respiration is asynchronous in response to changes in temperature regardless of plant functional group
journal, October 2007


Ecosystem Photosynthesis in Land‐Surface Models: A First‐Principles Approach Incorporating Acclimation
journal, January 2022

  • Mengoli, Giulia; Agustí‐Panareda, Anna; Boussetta, Souhail
  • Journal of Advances in Modeling Earth Systems, Vol. 14, Issue 1
  • DOI: 10.1029/2021MS002767

Physiological and environmental regulation of stomatal conductance, photosynthesis and transpiration: a model that includes a laminar boundary layer
journal, April 1991

  • Collatz, G. James; Ball, J. Timothy; Grivet, Cyril
  • Agricultural and Forest Meteorology, Vol. 54, Issue 2-4
  • DOI: 10.1016/0168-1923(91)90002-8

Implications of improved representations of plant respiration in a changing climate
journal, November 2017

  • Huntingford, Chris; Atkin, Owen K.; Martinez-de la Torre, Alberto
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/s41467-017-01774-z

R UBISCO : Structure, Regulatory Interactions, and Possibilities for a Better Enzyme
journal, June 2002


Does physiological acclimation to climate warming stabilize the ratio of canopy respiration to photosynthesis?
journal, April 2016

  • Drake, John E.; Tjoelker, Mark G.; Aspinwall, Michael J.
  • New Phytologist, Vol. 211, Issue 3
  • DOI: 10.1111/nph.13978

Global convergence in leaf respiration from estimates of thermal acclimation across time and space
journal, April 2015

  • Vanderwel, Mark C.; Slot, Martijn; Lichstein, Jeremy W.
  • New Phytologist, Vol. 207, Issue 4
  • DOI: 10.1111/nph.13417

The Coordination of Leaf Photosynthesis Links C and N Fluxes in C3 Plant Species
journal, June 2012


Representing Nitrogen, Phosphorus, and Carbon Interactions in the E3SM Land Model: Development and Global Benchmarking
journal, July 2019

  • Zhu, Qing; Riley, William J.; Tang, Jinyun
  • Journal of Advances in Modeling Earth Systems, Vol. 11, Issue 7
  • DOI: 10.1029/2018MS001571

Acclimation of leaf respiration temperature responses across thermally contrasting biomes
journal, October 2020

  • Zhu, Lingling; Bloomfield, Keith J.; Asao, Shinichi
  • New Phytologist, Vol. 229, Issue 3
  • DOI: 10.1111/nph.16929

Leaf Respiration in Terrestrial Biosphere Models
book, January 2017


Global distribution of C 3 and C 4 vegetation: Carbon cycle implications : C
journal, January 2003

  • Still, Christopher J.; Berry, Joseph A.; Collatz, G. James
  • Global Biogeochemical Cycles, Vol. 17, Issue 1
  • DOI: 10.1029/2001GB001807

Transpiration and Leaf Temperature
journal, June 1968


Assessing the relevant time frame for temperature acclimation of leaf dark respiration: A test with 10 boreal and temperate species
journal, April 2021

  • Reich, Peter B.; Stefanski, Artur; Rich, Roy L.
  • Global Change Biology, Vol. 27, Issue 12
  • DOI: 10.1111/gcb.15609

Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology
journal, May 1994


Global climatic drivers of leaf size
journal, August 2017


The influence of leaf size and shape on leaf thermal dynamics: does theory hold up under natural conditions?: Leaf size, shape and temperature
journal, December 2016

  • Leigh, A.; Sevanto, S.; Close, J. D.
  • Plant, Cell & Environment, Vol. 40, Issue 2
  • DOI: 10.1111/pce.12857

Accelerating net terrestrial carbon uptake during the warming hiatus due to reduced respiration
journal, January 2017

  • Ballantyne, Ashley; Smith, William; Anderegg, William
  • Nature Climate Change, Vol. 7, Issue 2
  • DOI: 10.1038/nclimate3204

Global patterns of vegetation carbon use efficiency and their climate drivers deduced from MODIS satellite data and process-based models
journal, June 2018


The energetic and carbon economic origins of leaf thermoregulation
journal, August 2016

  • Michaletz, Sean T.; Weiser, Michael D.; McDowell, Nate G.
  • Nature Plants, Vol. 2, Issue 9
  • DOI: 10.1038/nplants.2016.129

Leaf day respiration: low CO 2 flux but high significance for metabolism and carbon balance
journal, October 2017

  • Tcherkez, Guillaume; Gauthier, Paul; Buckley, Thomas N.
  • New Phytologist, Vol. 216, Issue 4
  • DOI: 10.1111/nph.14816

Increase in observed net carbon dioxide uptake by land and oceans during the past 50 years
journal, August 2012

  • Ballantyne, A. P.; Alden, C. B.; Miller, J. B.
  • Nature, Vol. 488, Issue 7409
  • DOI: 10.1038/nature11299

Robust regression methods for intensive care monitoring
journal, January 2007

  • Imhoff, M.; Schettlinger, K.; Fried, R.
  • Critical Care, Vol. 11, Issue Suppl 2
  • DOI: 10.1186/cc5598

In vivo temperature response functions of parameters required to model RuBP-limited photosynthesis
journal, September 2003


Diurnal asymmetry to the observed global warming: DIURNAL ASYMMERTRYR IN THE OBSERVED GLOBAL WARMING
journal, February 2016

  • Davy, Richard; Esau, Igor; Chernokulsky, Alexander
  • International Journal of Climatology, Vol. 37, Issue 1
  • DOI: 10.1002/joc.4688

Measurement of Protein Degradation in Leaves of Zea mays Using [3H]Acetic Anhydride and Tritiated Water
journal, June 1981

  • Simpson, Ellen; Cooke, Robert J.; Davies, David D.
  • Plant Physiology, Vol. 67, Issue 6
  • DOI: 10.1104/pp.67.6.1214

Nocturnal plant respiration is under strong non-temperature control
journal, September 2022


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
  • DOI: 10.1007/BF00386231

Global variability in leaf respiration in relation to climate, plant functional types and leaf traits
journal, January 2015

  • Atkin, Owen K.; Bloomfield, Keith J.; Reich, Peter B.
  • New Phytologist, Vol. 206, Issue 2
  • DOI: 10.1111/nph.13253

Wheat respiratory O2 consumption falls with night warming alongside greater respiratory CO2 loss and reduced biomass
journal, October 2021

  • Posch, Bradley C.; Zhai, Deping; Coast, Onoriode
  • Journal of Experimental Botany, Vol. 73, Issue 3
  • DOI: 10.1093/jxb/erab454

A Model of C4 Photosynthetic Acclimation Based on Least‐Cost Optimality Theory Suitable for Earth System Model Incorporation
journal, March 2022

  • Scott, Helen G.; Smith, Nicholas G.
  • Journal of Advances in Modeling Earth Systems, Vol. 14, Issue 3
  • DOI: 10.1029/2021MS002470

Quantifying carbon-nitrogen feedbacks in the Community Land Model (CLM4): CARBON-NITROGEN FEEDBACKS IN CLM4
journal, April 2010

  • Bonan, Gordon B.; Levis, Samuel
  • Geophysical Research Letters, Vol. 37, Issue 7
  • DOI: 10.1029/2010GL042430

Improved temperature response functions for models of Rubisco-limited photosynthesis
journal, February 2001