The relationship of leaf photosynthetic traits – Vcmax and Jmax – to leaf nitrogen, leaf phosphorus, and specific leaf area: a meta-analysis and modeling study

Great uncertainty exists in the global exchange of carbon between the atmosphere and the terrestrial biosphere. An important source of this uncertainty lies in the dependency of photosynthesis on the maximum rate of carboxylation (Vcmax) and the maximum rate of electron transport (Jmax). Understanding and making accurate prediction of C fluxes thus requires accurate characterization of these rates and their relationship with plant nutrient status over large geographic scales. Plant nutrient status is indicated by the traits: leaf nitrogen (N), leaf phosphorus (P), and specific leaf area (SLA). Correlations between Vcmax and Jmax and leaf nitrogen (N) are typically derived from local to global scales, while correlations with leaf phosphorus (P) and specific leaf area (SLA) have typically been derived at a local scale. Thus, there is no global-scale relationship between Vcmax and Jmax and P or SLA limiting the ability of global-scale carbon flux models do not account for P or SLA. We gathered published data from 24 studies to reveal global relationships of Vcmax and Jmax with leaf N, P, and SLA. Vcmax was strongly related to leaf N, and increasing leaf P substantially increased the sensitivity of Vcmax to leaf N. Jmax was strongly related to Vcmax, and neither leaf N, P, or SLA had a substantial impact on the relationship. Although more data are needed to expand the applicability of the relationship, we show leaf P is a globally important determinant of photosynthetic rates. In a model of photosynthesis, we showed that at high leaf N (3 gm−2), increasing leaf P from 0.05 to 0.22 gm−2 nearly doubled assimilation rates. Finally, we show that plants may employ a conservative strategy of Jmax to Vcmax coordination that restricts photoinhibition when carboxylation is limiting at the expense of maximizing photosynthetic rates when light is limiting.

[1]  J. A. Willis EFFECTS OF CARBON DIOXIDE EFFECTS OF DIFFERENT TENSIONS OF CARBON DIOXIDE ON CERTAIN ORTHOPTERA (GRASSHOPPERS) , 1925 .

[2]  Emil L. Smith THE INFLUENCE OF LIGHT AND CARBON DIOXIDE ON PHOTOSYNTHESIS , 1937, The Journal of general physiology.

[3]  A. Galston Plant Physiology , 1967, Nature.

[4]  H. Eyring,et al.  The nature of enzyme inhibitions in bacterial luminescence: Sulfanilamide, urethane, temperature and pressure† , 1942 .

[5]  J. Anderson,et al.  Light-dependent Assimilation of Nitrite by Isolated Pea Chloroplasts. , 1978, Plant Physiology.

[6]  Graham D. Farquhar,et al.  An Empirical Model of Stomatal Conductance , 1984 .

[7]  Stephen B. Powles,et al.  Photoinhibition of Photosynthesis Induced by Visible Light , 1984 .

[8]  H. Marschner Mineral Nutrition of Higher Plants , 1988 .

[9]  G. Collatz,et al.  Physiological and environmental regulation of stomatal conductance, photosynthesis and transpiration: a model that includes a laminar boundary layer , 1991 .

[10]  T. Sharkey,et al.  Theoretical Considerations when Estimating the Mesophyll Conductance to CO(2) Flux by Analysis of the Response of Photosynthesis to CO(2). , 1992, Plant physiology.

[11]  Stan D. Wullschleger,et al.  Biochemical Limitations to Carbon Assimilation in C3 Plants—A Retrospective Analysis of the A/Ci Curves from 109 Species , 1993 .

[12]  Thomas M. Smith,et al.  A global land primary productivity and phytogeography model , 1995 .

[13]  Dennis D. Baldocchi,et al.  Scaling carbon dioxide and water vapour exchange from leaf to canopy in a deciduous forest. II. Model testing and application , 1995 .

[14]  D. Beerling,et al.  A new technique for estimating rates of carboxylation and electron transport in leaves of C3 plants for use in dynamic global vegetation models , 1995 .

[15]  Dennis D. Baldocchi,et al.  Scaling carbon dioxide and water vapour exchange from leaf to canopy in a deciduous forest. I. Leaf model parametrization , 1995 .

[16]  H. Lambers,et al.  Leaf Respiration in Light and Darkness (A Comparison of Slow- and Fast-Growing Poa Species) , 1997, Plant physiology.

[17]  R. Leuning Scaling to a common temperature improves the correlation between the photosynthesis parameters Jmax and Vcmax , 1997 .

[18]  D. Loustau,et al.  Variability of the photosynthetic characteristics of mature needles within the crown of a 25-year-old Pinus pinaster. , 1998, Tree physiology.

[19]  Michael Bahn,et al.  Inter‐specific variation of the biochemical limitation to photosynthesis and related leaf traits of 30 species from mountain grassland ecosystems under different land use , 1999 .

[20]  Jessica Gurevitch,et al.  STATISTICAL ISSUES IN ECOLOGICAL META‐ANALYSES , 1999 .

[21]  S. Wand,et al.  Nutrient and genotypic effects on CO2-responsiveness: photosynthetic regulation in Leucadendron species of a nutrient-poor environment , 1999 .

[22]  Bahn,et al.  The use of the ratio between the photosynthesis parameters p(ml)and v(cmax)for scaling up photosynthesis of C(3)Plants from leaves to canopies: A critical examination of different modelling approaches , 1999, Journal of theoretical biology.

[23]  Ülo Niinemets,et al.  Research review. Components of leaf dry mass per area – thickness and density – alter leaf photosynthetic capacity in reverse directions in woody plants , 1999 .

[24]  Peter M. Cox,et al.  Description of the "TRIFFID" Dynamic Global Vegetation Model , 2001 .

[25]  Carl J. Bernacchi,et al.  Improved temperature response functions for models of Rubisco‐limited photosynthesis , 2001 .

[26]  G. Berntson,et al.  Regenerating temperate forests under elevated CO2 and nitrogen deposition: comparing biochemical and stomatal limitation of photosynthesis , 2001 .

[27]  David R. Anderson,et al.  Bayesian Methods in Cosmology: Model selection and multi-model inference , 2009 .

[28]  P. Meir,et al.  Photosynthetic parameters in seedlings of Eucalyptus grandis as affected by rate of nitrogen supply , 2002 .

[29]  Denis Loustau,et al.  Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data , 2002 .

[30]  B. Medlyn,et al.  Temperature response of parameters of a biochemically based model of photosynthesis. I. Seasonal changes in mature maritime pine (Pinus pinaster Ait.) , 2002 .

[31]  K. Pregitzer,et al.  Photosynthetic acclimation of overstory Populus tremuloides and understory Acer saccharum to elevated atmospheric CO2 concentration: interactions with shade and soil nitrogen. , 2002, Tree physiology.

[32]  A. Bloom,et al.  Nitrate photo-assimilation in tomato leaves under short-term exposure to elevated carbon dioxide and low oxygen , 2003 .

[33]  R. Xu Measuring explained variation in linear mixed effects models , 2003, Statistics in medicine.

[34]  Christina Gloeckner,et al.  Modern Applied Statistics With S , 2003 .

[35]  G. Farquhar,et al.  Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves , 1981, Planta.

[36]  R. Norby,et al.  Persistent stimulation of photosynthesis by elevated CO2 in a sweetgum (Liquidambar styraciflua) forest stand , 2004 .

[37]  Sean C. Thomas,et al.  The worldwide leaf economics spectrum , 2004, Nature.

[38]  C. Warren The photosynthetic limitation posed by internal conductance to CO2 movement is increased by nutrient supply. , 2004, Journal of experimental botany.

[39]  W. Ye,et al.  Gas Exchange Characteristics of the Invasive Species Mikania Micrantha and its Indigenous Congener M. Cordata (Asteraceae) in South China , 2004 .

[40]  James F. Reynolds,et al.  Coordination theory of leaf nitrogen distribution in a canopy , 1993, Oecologia.

[41]  J. Berry,et al.  A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species , 1980, Planta.

[42]  D. Manter,et al.  Growth response of Douglas-fir seedlings to nitrogen fertilization: importance of Rubisco activation state and respiration rates. , 2005, Tree physiology.

[43]  K. Heinsoo,et al.  Leaf photosynthetic properties in a willow (Salix viminalis and Salix dasyclados) plantation in response to fertilization , 2006, European Journal of Forest Research.

[44]  Carlo Calfapietra,et al.  Canopy profiles of photosynthetic parameters under elevated CO2 and N fertilization in a poplar plantation. , 2005, Environmental pollution.

[45]  D. Whitehead,et al.  Stomatal and non-stomatal limitations to photosynthesis in four tree species in a temperate rainforest dominated by Dacrydium cupressinum in New Zealand. , 2005, Tree physiology.

[46]  Stephen Sitch,et al.  Effects of parameter uncertainties on the modeling of terrestrial biosphere dynamics , 2005 .

[47]  D. Whitehead,et al.  Plasticity in photosynthetic response to nutrient supply of seedlings from a mixed conifer‐angiosperm forest , 2005 .

[48]  Shiwei Guo,et al.  Influence of N form on growth photosynthesis of Phaseolus vulgaris L. plants , 2006 .

[49]  R. Joffre,et al.  Photosynthesis, growth and structural characteristics of holm oak resprouts originated from plants grown under elevated CO2 , 2006 .

[50]  Q. Dang,et al.  Effects of carbon dioxide concentration and nutrition on photosynthetic functions of white birch seedlings. , 2006, Tree physiology.

[51]  Helmut Hillebrand,et al.  Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. , 2007, Ecology letters.

[52]  M. Naramoto,et al.  Photosynthetic capacity and nitrogen partitioning in foliage of the evergreen shrub Daphniphyllum humile along a natural light gradient. , 2007, Tree physiology.

[53]  Corinne Le Quéré,et al.  Contributions to accelerating atmospheric CO2 growth from economic activity, carbon intensity, and efficiency of natural sinks , 2007, Proceedings of the National Academy of Sciences.

[54]  B. Richardson,et al.  Partititioning concurrent influences of nitrogen and phosphorus supply on photosynthetic model parameters of Pinus radiata. , 2007, Tree physiology.

[55]  Jens Kattge,et al.  Temperature acclimation in a biochemical model of photosynthesis: a reanalysis of data from 36 species. , 2007, Plant, cell & environment.

[56]  T. Sharkey,et al.  Fitting photosynthetic carbon dioxide response curves for C(3) leaves. , 2007, Plant, cell & environment.

[57]  P. Palange,et al.  From the authors , 2007, European Respiratory Journal.

[58]  M. Adams,et al.  Increased photosynthesis following partial defoliation of field-grown Eucalyptus globulus seedlings is not caused by increased leaf nitrogen. , 2007, Tree physiology.

[59]  T. Kawasaki,et al.  Leaf-age effects on seasonal variability in photosynthetic parameters and its relationships with leaf mass per area and leaf nitrogen concentration within a Pinus densiflora crown. , 2008, Tree physiology.

[60]  P. Reich,et al.  Leaf physiological versus morphological acclimation to high-light exposure at different stages of foliar development in oak. , 2008, Tree physiology.

[61]  J. Flexas,et al.  Mesophyll conductance to CO 2 : current knowledge and future prospects , 2008 .

[62]  Jaume Flexas,et al.  Mesophyll conductance to CO2: current knowledge and future prospects. , 2008, Plant, cell & environment.

[63]  Ian J. Wright,et al.  Leaf phosphorus influences the photosynthesis–nitrogen relation: a cross-biome analysis of 314 species , 2009, Oecologia.

[64]  L. Poorter,et al.  Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. , 2009, The New phytologist.

[65]  Rachel M. Law,et al.  A global model of carbon, nitrogen and phosphorus cycles for the terrestrial biosphere , 2009 .

[66]  W. Knorr,et al.  Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global‐scale terrestrial biosphere models , 2009 .

[67]  D. Parkinson,et al.  Bayesian Methods in Cosmology: Model selection and multi-model inference , 2009 .

[68]  P. Reich,et al.  A global study of relationships between leaf traits, climate and soil measures of nutrient fertility , 2009 .

[69]  Lianhong Gu,et al.  Reliable estimation of biochemical parameters from C₃ leaf photosynthesis-intercellular carbon dioxide response curves. , 2010, Plant, cell & environment.

[70]  Andrew D. Friend,et al.  Carbon and nitrogen cycle dynamics in the O‐CN land surface model: 1. Model description, site‐scale evaluation, and sensitivity to parameter estimates , 2010 .

[71]  P. Ciais,et al.  Benchmarking coupled climate‐carbon models against long‐term atmospheric CO2 measurements , 2010 .

[72]  T. Feldpausch,et al.  Co-limitation of photosynthetic capacity by nitrogen and phosphorus in West Africa woodlands. , 2010, Plant, cell & environment.

[73]  R. Leuningb,et al.  Assessing parameter variability in a photosynthesis model within and between plant functional types using global Fluxnet eddy covariance data , 2010 .

[74]  M. Adams,et al.  An analytical model of non-photorespiratory CO₂release in the light and dark in leaves of C₃species based on stoichiometric flux balance. , 2011, Plant, cell & environment.

[75]  Benjamin L Turner,et al.  Photosynthetic physiology of eucalypts along a sub-continental rainfall gradient in northern Australia , 2011 .

[76]  S. Higgins,et al.  TRY – a global database of plant traits , 2011, Global Change Biology.

[77]  Markus Reichstein,et al.  Improving canopy processes in the Community Land Model version 4 (CLM4) using global flux fields empirically inferred from FLUXNET data , 2011 .

[78]  H. Utsugi,et al.  Growth and photosynthetic traits of hybrid larch F1 (Larix gmelinii var. japonica x L. kaempferi) under elevated CO2 concentration with low nutrient availability. , 2011, Tree physiology.

[79]  Stephen Sitch,et al.  Variations in Amazon forest productivity correlated with foliar nutrients and modelled rates of photosynthetic carbon supply , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[80]  I. J. Wright,et al.  Impacts of trait variation through observed trait-climate relationships on performance of a representative Earth System model : a conceptual analysis , 2012 .

[81]  Pierre Martre,et al.  The Coordination of Leaf Photosynthesis Links C and N Fluxes in C3 Plant Species , 2012, PloS one.

[82]  Daniel S. Goll,et al.  Nutrient limitation reduces land carbon uptake in simulations with a model of combined carbon, nitrogen and phosphorus cycling , 2012 .

[83]  K. Winter,et al.  Photosynthesis, photoprotection, and growth of shade-tolerant tropical tree seedlings under full sunlight , 2012, Photosynthesis Research.

[84]  Josep Peñuelas,et al.  The human‐induced imbalance between C, N and P in Earth's life system , 2012 .

[85]  Ian J. Wright,et al.  Impacts of trait variation through observed trait–climate relationships on performance of an Earth system model: a conceptual analysis , 2012 .

[86]  P. Friedlingstein,et al.  A unifying conceptual model for the environmental responses of isoprene emissions from plants , 2013, Annals of botany.

[87]  Alistair Rogers,et al.  The use and misuse of Vc,max in Earth System Models , 2014, Photosynthesis Research.

[88]  W. Post,et al.  The role of phosphorus dynamics in tropical forests – a modeling study using CLM-CNP , 2013 .

[89]  R. Dickinson,et al.  Asymmetrical effects of mesophyll conductance on fundamental photosynthetic parameters and their relationships estimated from leaf gas exchange measurements. , 2014, Plant, cell & environment.

[90]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[91]  S S I T C H,et al.  Evaluation of Ecosystem Dynamics, Plant Geography and Terrestrial Carbon Cycling in the Lpj Dynamic Global Vegetation Model , 2022 .