Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale

Dushan P. Kumarathunge; Belinda E. Medlyn; John E. Drake; Mark G. Tjoelker; Michael J. Aspinwall; Michael Battaglia; Francisco J. Cano; Kelsey R. Carter; Molly A. Cavaleri; Lucas A. Cernusak; Jeffrey Q. Chambers; Kristine Y. Crous; Martin G. De Kauwe; Dylan N. Dillaway; Erwin Dreyer; David S. Ellsworth; Oula Ghannoum; Qingmin Han; Kouki Hikosaka; Anna M. Jensen; Jeff W.G. Kelly; Eric L. Kruger; Lina M. Mercado; Yusuke Onoda; Peter B. Reich; Alistair Rogers; Martijn Slot; Nicholas G. Smith; Lasse Tarvainen; David T. Tissue; Henrique F. Togashi; Edgard S. Tribuzy; Johan Uddling; Angelica Vårhammar; Göran Wallin; Jeffrey M. Warren; Danielle A. Way

doi:10.1111/nph.15668

Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale

Dushan P. Kumarathunge, Belinda E. Medlyn, John E. Drake, Mark G. Tjoelker, Michael J. Aspinwall, Michael Battaglia, Francisco J. Cano, Kelsey R. Carter, Molly A. Cavaleri, Lucas A. Cernusak, Jeffrey Q. Chambers, Kristine Y. Crous, Martin G. De Kauwe, Dylan N. Dillaway, Erwin Dreyer, David S. Ellsworth, Oula Ghannoum, Qingmin Han, Kouki Hikosaka, Anna M. JensenJeff W.G. Kelly, Eric L. Kruger, Lina M. Mercado, Yusuke Onoda, Peter B. Reich, Alistair Rogers, Martijn Slot, Nicholas G. Smith, Lasse Tarvainen, David T. Tissue, Henrique F. Togashi, Edgard S. Tribuzy, Johan Uddling, Angelica Vårhammar, Göran Wallin, Jeffrey M. Warren, Danielle A. Way

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Abstract

The temperature response of photosynthesis is one of the key factors determining predicted responses to warming in global vegetation models (GVMs). The response may vary geographically, owing to genetic adaptation to climate, and temporally, as a result of acclimation to changes in ambient temperature. Our goal was to develop a robust quantitative global model representing acclimation and adaptation of photosynthetic temperature responses. We quantified and modelled key mechanisms responsible for photosynthetic temperature acclimation and adaptation using a global dataset of photosynthetic CO ₂ response curves, including data from 141 C ₃ species from tropical rainforest to Arctic tundra. We separated temperature acclimation and adaptation processes by considering seasonal and common-garden datasets, respectively. The observed global variation in the temperature optimum of photosynthesis was primarily explained by biochemical limitations to photosynthesis, rather than stomatal conductance or respiration. We found acclimation to growth temperature to be a stronger driver of this variation than adaptation to temperature at climate of origin. We developed a summary model to represent photosynthetic temperature responses and showed that it predicted the observed global variation in optimal temperatures with high accuracy. This novel algorithm should enable improved prediction of the function of global ecosystems in a warming climate.

Original language	English (US)
Pages (from-to)	768-784
Number of pages	17
Journal	New Phytologist
Volume	222
Issue number	2
DOIs	https://doi.org/10.1111/nph.15668
State	Published - Apr 2019

Bibliographical note

Funding Information:
This research was supported by a Western Sydney University PhD scholarship to DPK. AR was supported by the Next Generation Ecosystem Experiments (NGEE Arctic) project, which is supported by the Office of Biological and Environmental Research in the United States Department of Energy (DOE), Office of Science, and through the United States Department of Energy contract no. DE-SC0012704 to Brookhaven National Laboratory. KYC was supported by an Australian Research Council DECRA (DE160101484). DAW acknowledges an NSERC Discovery grant and funding from the Hawkesbury Institute Research Exchange Program. JU, LT and GW were supported by the Swedish strategic research area BECC (Biodiversity and Ecosystem Services in a Changing Climate; www.becc.lu.se). JQC was supported by the NGEE-Tropics, United States DOE. MDK was supported by Australian Research Council Centre of Excellence for Climate Extremes (CE170100023). MS was supported by an Earl S Tupper postdoctoral fellowship. AMJ and JMW were supported by the Biological and Environmental Research Program in the Office of Science, United States DOE under contract DEAC05-00OR22725. MAC was supported by United States DOE grant DE-SC-0011806 and USDA Forest Service 13-JV-11120101-03. Several of the Eucalyptus datasets included in this study were supported by the Australian Commonwealth Department of the Environment or Department of Agriculture, and the Australian Research Council (including DP140103415). We are grateful to Jens Kattge, Yan Shih-Lin, Alida C. Mau and Remko Duursma for useful discussions.

Publisher Copyright:
© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust

Keywords

AC curves
J
V
climate of origin
global vegetation models (GVMs)
growth temperature
maximum carboxylation capacity
maximum electron transport rate

Publisher link

10.1111/nph.15668

http://nora.nerc.ac.uk/id/eprint/522432/1/N522432PP.pdf

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Kumarathunge, D. P., Medlyn, B. E., Drake, J. E., Tjoelker, M. G., Aspinwall, M. J., Battaglia, M., Cano, F. J., Carter, K. R., Cavaleri, M. A., Cernusak, L. A., Chambers, J. Q., Crous, K. Y., De Kauwe, M. G., Dillaway, D. N., Dreyer, E., Ellsworth, D. S., Ghannoum, O., Han, Q., Hikosaka, K., ... Way, D. A. (2019). Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale. New Phytologist, 222(2), 768-784. https://doi.org/10.1111/nph.15668

Kumarathunge, DP, Medlyn, BE, Drake, JE, Tjoelker, MG, Aspinwall, MJ, Battaglia, M, Cano, FJ, Carter, KR, Cavaleri, MA, Cernusak, LA, Chambers, JQ, Crous, KY, De Kauwe, MG, Dillaway, DN, Dreyer, E, Ellsworth, DS, Ghannoum, O, Han, Q, Hikosaka, K, Jensen, AM, Kelly, JWG, Kruger, EL, Mercado, LM, Onoda, Y, Reich, PB, Rogers, A, Slot, M, Smith, NG, Tarvainen, L, Tissue, DT, Togashi, HF, Tribuzy, ES, Uddling, J, Vårhammar, A, Wallin, G, Warren, JM & Way, DA 2019, 'Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale', New Phytologist, vol. 222, no. 2, pp. 768-784. https://doi.org/10.1111/nph.15668

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title = "Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale",

abstract = " The temperature response of photosynthesis is one of the key factors determining predicted responses to warming in global vegetation models (GVMs). The response may vary geographically, owing to genetic adaptation to climate, and temporally, as a result of acclimation to changes in ambient temperature. Our goal was to develop a robust quantitative global model representing acclimation and adaptation of photosynthetic temperature responses. We quantified and modelled key mechanisms responsible for photosynthetic temperature acclimation and adaptation using a global dataset of photosynthetic CO 2 response curves, including data from 141 C 3 species from tropical rainforest to Arctic tundra. We separated temperature acclimation and adaptation processes by considering seasonal and common-garden datasets, respectively. The observed global variation in the temperature optimum of photosynthesis was primarily explained by biochemical limitations to photosynthesis, rather than stomatal conductance or respiration. We found acclimation to growth temperature to be a stronger driver of this variation than adaptation to temperature at climate of origin. We developed a summary model to represent photosynthetic temperature responses and showed that it predicted the observed global variation in optimal temperatures with high accuracy. This novel algorithm should enable improved prediction of the function of global ecosystems in a warming climate.",

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author = "Kumarathunge, {Dushan P.} and Medlyn, {Belinda E.} and Drake, {John E.} and Tjoelker, {Mark G.} and Aspinwall, {Michael J.} and Michael Battaglia and Cano, {Francisco J.} and Carter, {Kelsey R.} and Cavaleri, {Molly A.} and Cernusak, {Lucas A.} and Chambers, {Jeffrey Q.} and Crous, {Kristine Y.} and {De Kauwe}, {Martin G.} and Dillaway, {Dylan N.} and Erwin Dreyer and Ellsworth, {David S.} and Oula Ghannoum and Qingmin Han and Kouki Hikosaka and Jensen, {Anna M.} and Kelly, {Jeff W.G.} and Kruger, {Eric L.} and Mercado, {Lina M.} and Yusuke Onoda and Reich, {Peter B.} and Alistair Rogers and Martijn Slot and Smith, {Nicholas G.} and Lasse Tarvainen and Tissue, {David T.} and Togashi, {Henrique F.} and Tribuzy, {Edgard S.} and Johan Uddling and Angelica V{\aa}rhammar and G{\"o}ran Wallin and Warren, {Jeffrey M.} and Way, {Danielle A.}",

note = "Funding Information: This research was supported by a Western Sydney University PhD scholarship to DPK. AR was supported by the Next Generation Ecosystem Experiments (NGEE Arctic) project, which is supported by the Office of Biological and Environmental Research in the United States Department of Energy (DOE), Office of Science, and through the United States Department of Energy contract no. DE-SC0012704 to Brookhaven National Laboratory. KYC was supported by an Australian Research Council DECRA (DE160101484). DAW acknowledges an NSERC Discovery grant and funding from the Hawkesbury Institute Research Exchange Program. JU, LT and GW were supported by the Swedish strategic research area BECC (Biodiversity and Ecosystem Services in a Changing Climate; www.becc.lu.se). JQC was supported by the NGEE-Tropics, United States DOE. MDK was supported by Australian Research Council Centre of Excellence for Climate Extremes (CE170100023). MS was supported by an Earl S Tupper postdoctoral fellowship. AMJ and JMW were supported by the Biological and Environmental Research Program in the Office of Science, United States DOE under contract DEAC05-00OR22725. MAC was supported by United States DOE grant DE-SC-0011806 and USDA Forest Service 13-JV-11120101-03. Several of the Eucalyptus datasets included in this study were supported by the Australian Commonwealth Department of the Environment or Department of Agriculture, and the Australian Research Council (including DP140103415). We are grateful to Jens Kattge, Yan Shih-Lin, Alida C. Mau and Remko Duursma for useful discussions. Publisher Copyright: {\textcopyright} 2018 The Authors. New Phytologist {\textcopyright} 2018 New Phytologist Trust",

year = "2019",

month = apr,

doi = "10.1111/nph.15668",

language = "English (US)",

volume = "222",

pages = "768--784",

journal = "New Phytologist",

issn = "0028-646X",

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T1 - Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale

AU - Kumarathunge, Dushan P.

AU - Medlyn, Belinda E.

AU - Drake, John E.

AU - Tjoelker, Mark G.

AU - Aspinwall, Michael J.

AU - Battaglia, Michael

AU - Cano, Francisco J.

AU - Carter, Kelsey R.

AU - Cavaleri, Molly A.

AU - Cernusak, Lucas A.

AU - Chambers, Jeffrey Q.

AU - Crous, Kristine Y.

AU - De Kauwe, Martin G.

AU - Dillaway, Dylan N.

AU - Dreyer, Erwin

AU - Ellsworth, David S.

AU - Ghannoum, Oula

AU - Han, Qingmin

AU - Hikosaka, Kouki

AU - Jensen, Anna M.

AU - Kelly, Jeff W.G.

AU - Kruger, Eric L.

AU - Mercado, Lina M.

AU - Onoda, Yusuke

AU - Reich, Peter B.

AU - Rogers, Alistair

AU - Slot, Martijn

AU - Smith, Nicholas G.

AU - Tarvainen, Lasse

AU - Tissue, David T.

AU - Togashi, Henrique F.

AU - Tribuzy, Edgard S.

AU - Uddling, Johan

AU - Vårhammar, Angelica

AU - Wallin, Göran

AU - Warren, Jeffrey M.

AU - Way, Danielle A.

N1 - Funding Information: This research was supported by a Western Sydney University PhD scholarship to DPK. AR was supported by the Next Generation Ecosystem Experiments (NGEE Arctic) project, which is supported by the Office of Biological and Environmental Research in the United States Department of Energy (DOE), Office of Science, and through the United States Department of Energy contract no. DE-SC0012704 to Brookhaven National Laboratory. KYC was supported by an Australian Research Council DECRA (DE160101484). DAW acknowledges an NSERC Discovery grant and funding from the Hawkesbury Institute Research Exchange Program. JU, LT and GW were supported by the Swedish strategic research area BECC (Biodiversity and Ecosystem Services in a Changing Climate; www.becc.lu.se). JQC was supported by the NGEE-Tropics, United States DOE. MDK was supported by Australian Research Council Centre of Excellence for Climate Extremes (CE170100023). MS was supported by an Earl S Tupper postdoctoral fellowship. AMJ and JMW were supported by the Biological and Environmental Research Program in the Office of Science, United States DOE under contract DEAC05-00OR22725. MAC was supported by United States DOE grant DE-SC-0011806 and USDA Forest Service 13-JV-11120101-03. Several of the Eucalyptus datasets included in this study were supported by the Australian Commonwealth Department of the Environment or Department of Agriculture, and the Australian Research Council (including DP140103415). We are grateful to Jens Kattge, Yan Shih-Lin, Alida C. Mau and Remko Duursma for useful discussions. Publisher Copyright: © 2018 The Authors. New Phytologist © 2018 New Phytologist Trust

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Y1 - 2019/4

N2 - The temperature response of photosynthesis is one of the key factors determining predicted responses to warming in global vegetation models (GVMs). The response may vary geographically, owing to genetic adaptation to climate, and temporally, as a result of acclimation to changes in ambient temperature. Our goal was to develop a robust quantitative global model representing acclimation and adaptation of photosynthetic temperature responses. We quantified and modelled key mechanisms responsible for photosynthetic temperature acclimation and adaptation using a global dataset of photosynthetic CO 2 response curves, including data from 141 C 3 species from tropical rainforest to Arctic tundra. We separated temperature acclimation and adaptation processes by considering seasonal and common-garden datasets, respectively. The observed global variation in the temperature optimum of photosynthesis was primarily explained by biochemical limitations to photosynthesis, rather than stomatal conductance or respiration. We found acclimation to growth temperature to be a stronger driver of this variation than adaptation to temperature at climate of origin. We developed a summary model to represent photosynthetic temperature responses and showed that it predicted the observed global variation in optimal temperatures with high accuracy. This novel algorithm should enable improved prediction of the function of global ecosystems in a warming climate.

AB - The temperature response of photosynthesis is one of the key factors determining predicted responses to warming in global vegetation models (GVMs). The response may vary geographically, owing to genetic adaptation to climate, and temporally, as a result of acclimation to changes in ambient temperature. Our goal was to develop a robust quantitative global model representing acclimation and adaptation of photosynthetic temperature responses. We quantified and modelled key mechanisms responsible for photosynthetic temperature acclimation and adaptation using a global dataset of photosynthetic CO 2 response curves, including data from 141 C 3 species from tropical rainforest to Arctic tundra. We separated temperature acclimation and adaptation processes by considering seasonal and common-garden datasets, respectively. The observed global variation in the temperature optimum of photosynthesis was primarily explained by biochemical limitations to photosynthesis, rather than stomatal conductance or respiration. We found acclimation to growth temperature to be a stronger driver of this variation than adaptation to temperature at climate of origin. We developed a summary model to represent photosynthetic temperature responses and showed that it predicted the observed global variation in optimal temperatures with high accuracy. This novel algorithm should enable improved prediction of the function of global ecosystems in a warming climate.

KW - AC curves

KW - J

KW - V

KW - climate of origin

KW - global vegetation models (GVMs)

KW - growth temperature

KW - maximum carboxylation capacity

KW - maximum electron transport rate

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Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale

Abstract

Bibliographical note

Keywords

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