When and where soil is important to modify the carbon and water economy of leaves.

least-cost theory nitrogen photosynthesis plant functional traits soil fertility soil pH stomatal conductance

Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
10 2020
Historique:
received: 10 12 2019
accepted: 13 05 2020
pubmed: 27 5 2020
medline: 15 5 2021
entrez: 27 5 2020
Statut: ppublish

Résumé

Photosynthetic 'least-cost' theory posits that the optimal trait combination for a given environment is that where the summed costs of photosynthetic water and nutrient acquisition/use are minimised. The effects of soil water and nutrient availability on photosynthesis should be stronger as climate-related costs for both resources increase. Two independent datasets of photosynthetic traits, Globamax (1509 species, 288 sites) and Glob13C (3645 species, 594 sites), were used to quantify biophysical and biochemical limitations of photosynthesis and the key variable C

Identifiants

pubmed: 32455476
doi: 10.1111/nph.16702
doi:

Substances chimiques

Soil 0
Water 059QF0KO0R
Carbon Dioxide 142M471B3J
Carbon 7440-44-0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

121-135

Informations de copyright

© 2020 The Authors New Phytologist © 2020 New Phytologist Trust.

Références

Atkin OK, Bloomfield KJ, Reich PB, Tjoelker MG, Asner GP, Bonal D, Zaragoza-Castells J. 2015. Global variability in leaf respiration in relation to climate, plant functional types and leaf traits. New Phytologist 206: 614-636.
Atkin OK, Turnbull MH, Zaragoza-Castells J, Fyllas NM, Lloyd J, Meir P, Griffin KL. 2013. Light inhibition of leaf respiration as soil fertility declines along a post-glacial chronosequence in New Zealand: an analysis using the Kok method. Plant and Soil 367: 163-182.
Ball JT, Woodrow IE, Berry JA. 1987. A model predicting stomatal conductance and its contribution to the control of photosynthesis under different environmental conditions. In: Biggins J., ed. Progress in photosynthesis research. Dordrecht, the Netherlands: Martinus-Nijhoff Publishers, 221-224.
Batjes NH. 2012. ISRIC-WISE derived soil properties on a 5 by 5 arc-minutes global grid (ver. 1.2). ISRIC Report 2012/01. Wageningen, the Netherlands: ISRIC - World Soil Information. [WWW document] URL http://www.isric.org.
Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR, Long SP. 2001. Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant, Cell & Environment 24: 253-259.
Brady NC. 1990. The nature and properties of soils, 10th edn New York, NY, USA: MacMillan, 91-152.
Bünemann EK, Bongiorno G, Bai Z, Creamer RE, De Deyn G, de Goede R, Brussaard L. 2018. Soil quality - a critical review. Soil Biology and Biochemistry 120: 105-125.
Cernusak LA, Ubierna N, Winter K. 2013. Environmental and physiological determinants of carbon isotope discrimination in terrestrial plants. New Phytologist 200: 950-965.
Chapin FS, Autumn K, Pugnaire FI. 1993. Evolution of suites of traits in response to environmental stress. The American Naturalist 142: 78-92.
Cheng Y, Wang J, Mary B, Zhang JB, Cai ZC, Chang SX. 2013. Soil pH has contrasting effects on gross and net nitrogen mineralizations in adjacent forest and grassland soils in central Alberta, Canada. Soil Biology and Biochemistry 57: 848-857.
Cornwell WK, Wright IJ, Turner J, Maire V, Barbour M, Cernusak L, Dawson T, Ellsworth D, Farquhar G, Griffiths Het al. 2016. A global dataset of leaf ∆13C values. doi: 10.5281/zenodo.569501.
Cornwell WK, Wright IJ, Turner J, Maire V, Barbour MM, Cernusak LA, Santiago LS. 2018. Climate and soils together regulate photosynthetic carbon isotope discrimination within C3 plants worldwide. Global Ecology and Biogeography 27: 1056-1067.
Cowan IR. 1986. Economics of carbon fixation in higher plants. In: On the economy of plant form and function. Proceedings of the sixth Maria Moors Cabot symposium. Cambridge, UK: Cambridge University Press, 133-170.
Cowan IR, Farquhar GD. 1977. Stomatal function in relation to leaf metabolism and environment. Symposia of the Society for Experimental Biology 31: 471-505.
Davis TW, Prentice IC, Stocker DB, Thomas RT, Whitley RJ, Wang H, Evans BJ, Gallego-Sala AV, Sykes MT, Cramer W. 2017. Simple process-led algorithms for simulating habitats (SPLASH vol 1.0): robust indices of radiation, evapotranspiration and plant-available moisture. Geoscientific Model Development 10: 689-708.
De Kauwe MG, Lin YS, Wright IJ, Medlyn BE, Crous KY, Ellsworth DS, Maire V, Prentice IC, Atkin OK, Rogers A et al. 2016. A test of the ‘one-point method’ for estimating maximum carboxylation capacity from field-measured, light-saturated photosynthesis. New Phytologist 210: 1130-1144.
Dewar R, Mauranen A, Mäkelä A, Hölttä T, Medlyn B, Vesala T. 2018. New insights into the covariation of stomatal, mesophyll and hydraulic conductances from optimization models incorporating nonstomatal limitations to photosynthesis. New Phytologist 217: 571-585.
Diefendorf AF, Mueller KE, Wing SL, Koch PL, Freeman KH. 2010. Global patterns in leaf 13C discrimination and implications for studies of past and future climate. Proceedings of the National Academy of Sciences, USA 107: 5738-5743.
Evans JR, Sharkey TD, Berry JA, Farquhar GD. 1986. Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants. Functional Plant Biology 13: 281-292.
Farquhar GD, Buckley TN, Miller JM. 2002. Optimal stomatal control in relation to leaf area and nitrogen content. Silva Fennica 36: 625-637.
Farquhar GD, O'Leary MH, Berry JA. 1982. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Functional Plant Biology 9: 121-137.
Field C, Merino J, Mooney HA. 1983. Compromises between water-use efficiency and nitrogen-use in five species of California evergreens. Oecologia 60: 384-389.
Field C, Mooney HA. 1986. The photosynthesis-nitrogen relationship in wild plants. In: Givnish T, ed. On the economy of plant form and function. Cambridge, UK: Cambridge University Press, 25-55.
Fierer N, Jackson RB. 2006. The diversity and biogeography of soil bacterial communities. Proceedings of the National Academy of Sciences, USA 103: 626-631.
Flexas J, Galmes J, Ribas-Carbo M, Medrano H. 2005. The effects of water stress on plant respiration. In: Lambers H, Ribas-Carbo M, eds. Plant respiration: from cell to ecosystem. Dordrecht, the Netherlands: Springer, 85-94.
Franks P, Brodribb TJ. 2005. Stomatal control and water transport in the xylem. In: Holbrook NM, Zwieniecki MA, eds, Vascular transport in plants. New York, NY, USA: Academic Press, 69-89.
Franks PJ, Farquhar GD. 1999. A relationship between humidity response, growth form and photosynthetic operating point in C3 plants. Plant, Cell & Environment 22: 1337-1349.
Friend AD. 1995. PGEN: an integrated model of leaf photosynthesis, transpiration, and conductance. Ecological Modelling 77: 233-255.
Fyllas NM, Patiño S, Baker TR, Nardoto GB, Martinelli LA, Quesada CA, Lloyd J. 2009. Basin-wide variations in foliar properties of Amazonian forest: phylogeny, soils and climate. Biogeosciences 6: 2677-2708.
Gallego-Sala AV, Clark JM, House JI, Orr HG, Prentice IC, Smith P, Chapman SJ. 2010. Bioclimatic envelope model of climate change impacts on blanket peatland distribution in Great Britain. Climate Research 45: 151-162.
Galmés J, Ribas-Carbó M, Medrano H, Flexas J. 2007. Response of leaf respiration to water stress in Mediterranean species with different growth forms. Journal of Arid Environments 68: 206-222.
Givnish TJ. 1986. Optimal stomatal conductance, allocation of energy between leaves and roots, and the marginal cost of transpiration. In: Givnish TJ, ed. On the economy of plant form and function. Cambridge, UK: Cambridge University Press, 171-213.
Givnish TJ. 2002. Adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox. Silva Fennica 36: 703-743.
Han WX, Fang JY, Reich PB, Ian Woodward F, Wang ZH. 2011. Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China. Ecology Letters 14: 788-796.
Hartmann J, Moosdorf N, Lauerwald R, Hinderer M, West AJ. 2014. Global chemical weathering and associated P-release - the role of lithology, temperature and soil properties. Chemical Geology 363: 145-163.
Hengl T, De Jesus JM, Heuvelink GBM, Gonzalez MR, Kilibarda M, Blagotić A, Kempen B. 2017. SoilGrids250m: global gridded soil information based on machine learning. PLoS ONE 12: e0169748.
Hengl T, de Jesus JM, MacMillan R, Batjes NH, Heuvelink GBM, Ribeiro E, Gonzalez MR. 2014. SoilGrids1km - global soil information based on automated mapping. PLoS ONE 9: e105992.
Hengl T, Heuvelink GB, Kempen B, Leenaars JG, Walsh MG, Shepherd KD, Sila A, MacMillan RA, Mendes de Jesus J, Tamene L et al. 2015. Mapping soil properties of Africa at 250 m resolution: random forests significantly improve current predictions. PLoS One 10: e0125814.
Hillel D. 1980. Fundamentals of soil physics. New York, NY, USA: Academic Press.
Huntingford C, Monteith JL. 1998. The behaviour of a mixed-layer model of the convective boundary layer coupled to a big leaf model of surface energy partitioning. Boundary-layer meteorology 88: 87-101.
Husson O. 2013. Redox potential (Eh) and pH as drivers of soil/plant/microorganism systems: a transdisciplinary overview pointing to integrative opportunities for agronomy. Plant and Soil 362: 389-417.
Huston MA. 2012. Precipitation, soils, NPP, and biodiversity: resurrection of albrecht’s curve. Ecological Monographs 82: 277-296.
Jenny H. 1941. Factors of soil formation a system of quantitative pedology. New York, NY, USA: Dover Publications.
Kattge J, Knorr W, Raddatz T, Wirth C. 2009. Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global-scale terrestrial biosphere models. Global Change Biology 15: 976-991.
Katul G, Manzoni S, Palmroth S, Oren R. 2010. A stomatal optimization theory to describe the effects of atmospheric CO2 on leaf photosynthesis and transpiration. Annals of Botany 105: 431-442.
Kennedy D, Swenson S, Oleson KW, Lawrence DM, Fisher R, Lola da Costa AC, Gentine P. 2019. Implementing plant hydraulics in the community land model, version 5. Journal of Advances in Modeling Earth Systems 11: 485-513.
Laliberté E, Turner BL, Costes T, Pearse SJ, Wyrwoll KH, Zemunik G, Lambers H. 2012. Experimental assessment of nutrient limitation along a 2-million-year dune chronosequence in the south-western Australia biodiversity hotspot. Journal of Ecology 100: 631-642.
Leuning R. 1995. A critical appraisal of a coupled stomatal-photosynthesis model for C3 plants. Plant, Cell & Environment 18: 339-357.
Lin H. 2011. Three principles of soil change and pedogenesis in time and space. Soil Science Society of America Journal 75: 2049.
Lin YS, Medlyn BE, Duursma RA, Prentice IC, Wang H, Baig S, De Beeck MO. 2015. Optimal stomatal behaviour around the world. Nature Climate Change 5: 459-464.
Maire V, Martre P, Kattge J, Gastal F, Esser G, Fontaine S, Soussana JF. 2012. The coordination of leaf photosynthesis links C and N fluxes in C3 plant species. PLoS ONE 7: e38345.
Maire V, Wright IJ, Prentice IC, Batjes NH, Bhaskar R, van Bodegom PM, Santiago LS. 2015. Global effects of soil and climate on leaf photosynthetic traits and rates. Global Ecology and Biogeography 24: 706-717.
Medlyn BE, Duursma R, Eamus D, Ellsworth DS, Prentice C, Barton CVM, Wingate L. 2011. Reconciling the optimal and empirical approaches to modelling stomatal conductance. Global Change Biology 17: 2134-2144.
Minocha R, Minocha SC. 2005. Effects of soil pH and aluminium on plant respiration. In: Lambers H, Ribas-Carbo M, eds. Plant respiration: from cell to ecosystem. Dordrecht, the Netherlands: Springer, 85-94.
Neina D. 2019. The role of soil pH in plant nutrition and soil remediation. Applied and Environmental Soil Science 2019: 5794869.
Niinemets U, Tenhunen JD, Canta NR, Chaves MM, Faria T, Pereira JS, Reynolds JF. 1999. Interactive effects of nitrogen and phosphorus on the acclimation potential of foliage photosynthetic properties of cork oak, Quercus suber, to elevated atmospheric CO2 concentrations. Global Change Biology 5: 455-470.
New M, Lister D, Hulme M, Makin I. 2002. A high-resolution data set of surface climate over global land areas. Climate research 21: 1-25.
Onoda Y, Wright IJ, Evans JR, Hikosaka K, Kitajima K, Niinemets Ü, Poorter H, Tosens T, Westoby M. 2017. Physiological and structural tradeoffs underlying the leaf economics spectrum. New Phytologist 214: 1447-1463.
Perveen N, Barot S, Maire V, Cotrufo MF, Shahzad T, Blagodatskaya E, Stewart CE, Ding W, Siddiq MR, Dimassi B et al. 2019. Universality of priming effect: an analysis using thirty five soils with contrasted properties sampled from five continents. Soil Biology and Biochemistry 134: 162-171.
Prentice IC, Dong N, Gleason SM, Maire V, Wright IJ. 2014. Balancing the costs of carbon gain and water transport: testing a new theoretical framework for plant functional ecology. Ecology Letters 17: 82-91.
Prentice IC, Meng T, Wang H, Harrison SP, Ni J, Wang G. 2011. Evidence of a universal scaling relationship for leaf CO2 drawdown along an aridity gradient. New Phytologist 190: 169-180.
Raupach MR. 2000. Equilibrium evaporation and the convective boundary layer. Boundary-Layer Meterology 96: 107-141.
Raven JA. 1985. Tansley review no. 2. Regulation of pH and generation of osmolarity in vascular plants: a cost-benefit analysis in relation to efficiency of use of energy, nitrogen and water. New Phytologist 101: 25-77.
Reich PB, Sendall KM, Stefanski A, Rich RL, Hobbie SE, Montgomery RA. 2018. Effects of climate warming on photosynthesis in boreal tree species depend on soil moisture. Nature 562: 263-267.
Reid JS, Koppmann R, Eck TF, Eleuterio DP. 2005. A review of biomass burning emissions part II: intensive physical properties of biomass burning particles. Atmospheric Chemistry and Physics 5: 799-825.
Rowland L, Zaragoza-Castells J, Bloomfield KJ, Turnbull MH, Bonal D, Burban B, Meir P. 2017. Scaling leaf respiration with nitrogen and phosphorus in tropical forests across two continents. New Phytologist 214: 1064-1077.
Schimel JP, Bennett J. 2004. Nitrogen mineralization: challenges of a changing paradigm. Ecology 85: 591-602.
Shangguan W, Dai Y, Duan Q, Liu B, Yuan H. 2014. A global soil data set for earth system modeling. Journal of Advances in Modeling Earth Systems 6: 249-263.
Shangguan W, Hengl T, de Jesus JM, Yuan H, Dai Y. 2017. Mapping the global depth to bedrock for land surface modeling. Journal of Advances in Modeling Earth Systems 9: 65-88.
Sinclair TR. 2005. Theoretical analysis of soil and plant traits influencing daily plant water flux on drying soils. Agronomy Journal 97: 1148-1152.
Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Zeglin LH. 2008. Stoichiometry of soil enzyme activity at global scale. Ecology Letters 11: 1252-1264.
Slessarev EW, Lin Y, Bingham NL, Johnson JE, Dai Y, Schimel JP, Chadwick OA. 2016. Water balance creates a threshold in soil pH at the global scale. Nature 540: 567-569.
Smith NG, Dukes JS. 2018. Drivers of leaf carbon exchange capacity across biomes at the continental scale. Ecology 99: 1610-1620.
Smith NG, Keenan TF, Prentice IC, Wang H, Wright IJ, Niinemets Ü, Zhou SX. 2019. Global photosynthetic capacity is optimized to the environment. Ecology Letters 22: 506-517.
Sperry JS, Venturas MD, Anderegg WRL, Mencuccini M, Mackay DS, Wang Y, Love DM. 2017. Predicting stomatal responses to the environment from the optimization of photosynthetic gain and hydraulic cost. Plant, Cell & Environment 40: 816-830.
Stocker B, Wang H, Smith N, Harrison S, Keenan T, David S, Tyler D, Prentice IC. 2020. P-Model v1.0: an optimality-based light use efficiency model for simulating ecosystem gross primary production. Geoscientific Model Development Discussions, no. August: 1-59. doi: 10.5194/gmd-2019-200.
Tuzet A, Perrier A, Leuning R. 2003. A coupled model of stomatal conductance, photosynthesis and transpiration. Plant, Cell & Environment 26: 1097-1117.
Ubierna N, Farquhar GD. 2014. Advances in measurements and models of photosynthetic carbon isotope discrimination in C3 plants. Plant, Cell & Environment 37: 1494-1498.
Viet HD, Kwak JH, Lee KHKS, Lim SS, Matsushima M, Chang SX, Choi WJ. 2013. Foliar chemistry and tree ring δ13C of Pinus densiflora in relation to tree growth along a soil pH gradient. Plant and Soil 363: 101-112.
Vitousek PM, Porder S, Houlton BZ, Chadwick OA. 2010. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen - phosphorus interactions. Ecological Applications 20: 5-15.
Wang H, Atkin OK, Keenan TF, Smith NG, Wright IJ, Bloomfield KJ, Prentice IC. 2020. Acclimation of leaf respiration consistent with optimal photosynthetic capacity. Global Change Biology 26: 2573-2583.
Wang H, Prentice IC, Davis TW. 2014. Biophysical constraints on gross primary production by the terrestrial biosphere. Biogeosciences 11: 5987-6001.
Wang H, Prentice IC, Davis TW, Keenan TF, Wright IJ, Peng C. 2017a. Photosynthetic responses to altitude: an explanation based on optimality principles. New Phytologist 213: 976-982.
Wang H, Prentice IC, Keenan TF, Davis TW, Wright IJ, Cornwell WK, Peng C. 2017b. Towards a universal model for carbon dioxide uptake by plants. Nature Plants 3: 734-741.
Wang J, Wen X, Zhang X, Li S, Zhang DY. 2018. Co-regulation of photosynthetic capacity by nitrogen, phosphorus and magnesium in a subtropical Karst forest in China. Scientific Reports 8: 1-9.
Warren CR. 2004. The photosynthetic limitation posed by internal conductance to CO2 movement is increased by nutrient supply. Journal of Experimental Botany 55: 2313-2321.
Warren CR, Adams MA. 2002. Phosphorus affects growth and partitioning of N to Rubisco in Pinus pinaster. Tree Physiology 22: 11-19.
Warton DI, Duursma RA, Falster DS, Taskinen S. 2012. smatr 3 - an R package for estimation and inference about allometric lines. Methods in Ecology and Evolution 3: 257-259.
Warton DI, Wright IJ, Falster DS, Westoby M. 2005. Bivariate line-fitting methods for allometry. Biological Reviews 81: 259.
Weitner A, Dupouey JL, Lefèvre Y, Bréda N, Badeau V, Ferhi A, Thimonier A. 2007. Roles of soil chemistry and water availability in site-related delta(13)C variations in French beech forests. Tree Physiology 27: 1043-1051.
Wolf A, Anderegg WR, Pacala SW. 2016. Optimal stomatal behavior with competition for water and risk of hydraulic impairment. Proceedings of the National Academy of Sciences, USA 113: E7222-E7230.
Wright IJ, Reich PB, Westoby M. 2003. Least-cost input mixtures of water and nitrogen for photosynthesis. The American Naturalist 161: 98-111.

Auteurs

Jennifer Paillassa (J)

Département des Sciences de l'environnement, Université du Québec à Trois-Rivières, CP 500, Trois-Rivières, QC, G9A 5H7, Canada.
Département des sols et de Génie Agroalimentaire, Université Laval, 2480 boul. Hochelaga, Québec, QC, G1V 0A6, Canada.

Ian J Wright (IJ)

Department of Biological Sciences, Macquarie University, North Ryde, NSW, 2109, Australia.

I Colin Prentice (IC)

Department of Biological Sciences, Macquarie University, North Ryde, NSW, 2109, Australia.
Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, SL5 7PY, UK.
Department of Earth System Science, Tsinghua University, Haidian District, Beijing, 100084, China.

Steeve Pepin (S)

Département des sols et de Génie Agroalimentaire, Université Laval, 2480 boul. Hochelaga, Québec, QC, G1V 0A6, Canada.

Nicholas G Smith (NG)

Department of Biological Sciences, Texas Tech University, 2901 Main Street, Lubbock, TX, 79409, USA.

Gilbert Ethier (G)

Département de phytologie, Université Laval, Québec, QC, G1V 0A6, Canada.

Andrea C Westerband (AC)

Département des sols et de Génie Agroalimentaire, Université Laval, 2480 boul. Hochelaga, Québec, QC, G1V 0A6, Canada.

Laurent J Lamarque (LJ)

Département des Sciences de l'environnement, Université du Québec à Trois-Rivières, CP 500, Trois-Rivières, QC, G9A 5H7, Canada.

Han Wang (H)

Department of Earth System Science, Tsinghua University, Haidian District, Beijing, 100084, China.

Will K Cornwell (WK)

School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, 2052, Australia.

Vincent Maire (V)

Département des Sciences de l'environnement, Université du Québec à Trois-Rivières, CP 500, Trois-Rivières, QC, G9A 5H7, Canada.

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