Impact of growth temperature on scaling relationships linking photosynthetic metabolism to leaf functional traits

Summary 1. Scaling relationships linking photosynthesis (A) to leaf traits are important for predicting vegetation patterns and plant-atmosphere carbon fluxes. Here, we investigated the impact of growth temperature on such scaling relationships. 2. We assessed whether changes in growth temperature systematically altered the slope and/or intercepts of log–log plots of A vs leaf mass per unit leaf area (LMA), nitrogen and phosphorus concentrations for 19 contrasting plant species grown hydroponically at four temperatures (7, 14, 21 and 28 °C) in controlled environment cabinets. Responses of 21 °C-grown pre-existing (PE) leaves experiencing a 10 day growth temperature (7, 14, 21 and 28 °C) treatment, and newly-developed (ND) leaves formed at each of the four new growth temperatures, were quantified. Irrespective of the growth temperature treatment, rates of light-saturated photosynthesis (A) were measured at 21 °C. 3. Changes in growth temperature altered the scaling between A and leaf traits in pre-existing (PE) leaves, with thermal history accounting for up to 17% and 31% of the variation on a mass and area basis, respectively. However, growth temperature played almost no role in accounting for scatter when comparisons were made of newly-developed (ND) leaves that form at each growth temperature. 4. Photosynthetic nitrogen and phosphorus use efficiency (PNUE and PPUE, respectively) decreased with increasing LMA. No systematic differences in temperature-mediated reductions in PNUE or PPUE of PE leaves were found among species. 5. Overall, these results highlight the importance of leaf development in determining the effects of sustained changes in growth temperature on scaling relationships linking photosynthesis to other leaf traits.

[1]  E. Kruger,et al.  Thermal acclimation of photosynthesis: a comparison of boreal and temperate tree species along a latitudinal transect. , 2010, Plant, cell & environment.

[2]  O. Atkin,et al.  Temporal heterogeneity of cold acclimation phenotypes in Arabidopsis leaves. , 2010, Plant, cell & environment.

[3]  J. Peñuelas,et al.  The altitude-for-latitude disparity in the range retractions of woody species. , 2009, Trends in ecology & evolution.

[4]  K. Kitayama,et al.  Divergent patterns of photosynthetic phosphorus‐use efficiency versus nitrogen‐use efficiency of tree leaves along nutrient‐availability gradients , 2009 .

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

[6]  K. Hikosaka,et al.  The role of Rubisco and cell walls in the interspecific variation in photosynthetic capacity , 2009, Oecologia.

[7]  A. Nicotra,et al.  Nitrogen in cell walls of sclerophyllous leaves accounts for little of the variation in photosynthetic nitrogen-use efficiency. , 2009, Plant, cell & environment.

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

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

[10]  Inderjit,et al.  Evolutionary tradeoffs for nitrogen allocation to photosynthesis versus cell walls in an invasive plant , 2009, Proceedings of the National Academy of Sciences.

[11]  K. Hikosaka,et al.  Cold-tolerant crop species have greater temperature homeostasis of leaf respiration and photosynthesis than cold-sensitive species. , 2009, Plant & cell physiology.

[12]  F. Woodward,et al.  Using temperature‐dependent changes in leaf scaling relationships to quantitatively account for thermal acclimation of respiration in a coupled global climate–vegetation model , 2008 .

[13]  I. C. Prentice,et al.  Evaluation of the terrestrial carbon cycle, future plant geography and climate‐carbon cycle feedbacks using five Dynamic Global Vegetation Models (DGVMs) , 2008 .

[14]  Jingyun Fang,et al.  Leaf nitrogen:phosphorus stoichiometry across Chinese grassland biomes , 2008, Oecologia.

[15]  Maria Lundmark,et al.  Acclimation of photosynthesis and respiration is asynchronous in response to changes in temperature regardless of plant functional group. , 2007, The New phytologist.

[16]  Peter B Reich,et al.  Predicting leaf physiology from simple plant and climate attributes: a global GLOPNET analysis. , 2007, Ecological applications : a publication of the Ecological Society of America.

[17]  R. Sage,et al.  The temperature response of C(3) and C(4) photosynthesis. , 2007, Plant, cell & environment.

[18]  William F. Fagan,et al.  Phylogenetic and Growth Form Variation in the Scaling of Nitrogen and Phosphorus in the Seed Plants , 2006, The American Naturalist.

[19]  Wenyun Zuo,et al.  A test of the generality of leaf trait relationships on the Tibetan Plateau. , 2006, The New phytologist.

[20]  T. Pons,et al.  High thermal acclimation potential of both photosynthesis and respiration in two lowland Plantago species in contrast to an alpine congeneric , 2006 .

[21]  T. Pons,et al.  Phenotypic plasticity and growth temperature: understanding interspecific variability. , 2006, Journal of experimental botany.

[22]  K. Hikosaka,et al.  The balance between RuBP carboxylation and RuBP regeneration: a mechanism underlying the interspecific variation in acclimation of photosynthesis to seasonal change in temperature. , 2005, Functional plant biology : FPB.

[23]  William G. Lee,et al.  Modulation of leaf economic traits and trait relationships by climate , 2005 .

[24]  P. Reich,et al.  Assessing the generality of global leaf trait relationships. , 2005, The New phytologist.

[25]  K. Noguchi,et al.  Temperature acclimation of photosynthesis in spinach leaves: analyses of photosynthetic components and temperature dependencies of photosynthetic partial reactions , 2005 .

[26]  K. Hikosaka,et al.  Seasonal change in the balance between capacities of RuBP carboxylation and RuBP regeneration affects CO2 response of photosynthesis in Polygonum cuspidatum. , 2005, Journal of experimental botany.

[27]  S. Güsewell.  N : P ratios in terrestrial plants: variation and functional significance. , 2004, The New phytologist.

[28]  K. Hikosaka.  Interspecific difference in the photosynthesis–nitrogen relationship: patterns, physiological causes, and ecological importance , 2004, Journal of Plant Research.

[29]  T. Pons,et al.  Analysis of differences in photosynthetic nitrogen‐use efficiency between four contrasting species , 2004 .

[30]  Tadaki Hirose,et al.  Allocation of nitrogen to cell walls decreases photosynthetic nitrogen‐use efficiency , 2004 .

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

[32]  A. Mead,et al.  Phylogenetic variation in the shoot mineral concentration of angiosperms. , 2004, Journal of experimental botany.

[33]  V. Hurry,et al.  Cold-hardening results in increased activity of enzymes involved in carbon metabolism in leaves of winter rye (Secale cereale L.) , 1995, Planta.

[34]  V. Hurry,et al.  Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants , 1993, Photosynthesis Research.

[35]  V. Hurry,et al.  Reduced sensitivity to photoinhibition following frost-hardening of winter rye is due to increased phosphate availability , 1993, Planta.

[36]  Hendrik Poorter,et al.  Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate , 1990, Oecologia.

[37]  Z. Teklehaimanot.  Review: Physiological Plant Ecology: Ecophysiology and Stress Physiology of Functional Groups, 4th edn , 2004 .

[38]  H. Lambers,et al.  Contrasting effects of N and P deprivation on the regulation of photosynthesis in tomato plants in relation to feedback limitation. , 2003, Journal of experimental botany.

[39]  Alastair Fitter,et al.  Thermal acclimation of leaf and root respiration: An investigation comparing inherently fast- and slow-growing plant species , 2003 .

[40]  C. Foyer,et al.  Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance , 2003 .

[41]  A. Fitter,et al.  Growth temperature influences the underlying components of relative growth rate: an investigation using inherently fast‐ and slow‐growing plant species , 2002 .

[42]  Mark Stitt,et al.  A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. , 2002, Current opinion in plant biology.

[43]  T. Mikkelsen,et al.  Does the direct effect of atmospheric CO2 concentration on leaf respiration vary with temperature? Responses in two species of Plantago that differ in relative growth rate. , 2002, Physiologia plantarum.

[44]  V. Hurry,et al.  Cold acclimation of Arabidopsis thaliana results in incomplete recovery of photosynthetic capacity, associated with an increased reduction of the chloroplast stroma , 2001, Planta.

[45]  P. Reich,et al.  Strategy shifts in leaf physiology, structure and nutrient content between species of high‐ and low‐rainfall and high‐ and low‐nutrient habitats , 2001 .

[46]  M. Stitt,et al.  The role of inorganic phosphate in the development of freezing tolerance and the acclimatization of photosynthesis to low temperature is revealed by the pho mutants of Arabidopsis thaliana. , 2000, The Plant journal : for cell and molecular biology.

[47]  S. V. Caemmerer,et al.  Plants in Action: Adaptation in Nature, Performance in Cultivation , 2000 .

[48]  P. Reich,et al.  Generality of leaf trait relationships: a test across six biomes: Ecology , 1999 .

[49]  P. Reich,et al.  Acclimation of respiration to temperature and CO2 in seedlings of boreal tree species in relation to plant size and relative growth rate , 1999 .

[50]  P. Reich,et al.  Changes in leaf nitrogen and carbohydrates underlie temperature and CO2 acclimation of dark respiration in five boreal tree species , 1999 .

[51]  K. Hikosaka,et al.  Balancing carboxylation and regeneration of ribulose‐1,5‐ bisphosphate in leaf photosynthesis: temperature acclimation of an evergreen tree, Quercus myrsinaefolia , 1999 .

[52]  M. Cambridge,et al.  Analysis of differences in photosynthetic nitrogen use efficiency of alpine and lowland Poa species , 1999, Oecologia.

[53]  M. Stitt,et al.  Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway. , 1999, Plant physiology.

[54]  Colin G. N. Turnbull,et al.  Plants in Action: adaption in nature, performance in cultivation , 1999 .

[55]  J. R. Evans,et al.  Variation in the components of relative growth rate in 10 Acacia species from contrasting environments , 1998 .

[56]  John R. Evans,et al.  Photosynthetic nitrogen-use efficiency of species that differ inherently in specific leaf area , 1998, Oecologia.

[57]  P. Reich,et al.  From tropics to tundra: global convergence in plant functioning. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[58]  P. Gustafsson,et al.  Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. , 1997, The Plant journal : for cell and molecular biology.

[59]  I. Nishida,et al.  CHILLING SENSITIVITY IN PLANTS AND CYANOBACTERIA: The Crucial Contribution of Membrane Lipids. , 1996, Annual review of plant physiology and plant molecular biology.

[60]  V. Hurry,et al.  Cold Hardening of Spring and Winter Wheat and Rape Results in Differential Effects on Growth, Carbon Metabolism, and Carbohydrate Content , 1995, Plant physiology.

[61]  T. Pons,et al.  Nitrogen reallocation and photosynthetic acclimation in response to partial shading in soybean plants , 1994 .

[62]  V. Hurry,et al.  Effects of a Short-Term Shift to Low Temperature and of Long-Term Cold Hardening on Photosynthesis and Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase and Sucrose Phosphate Synthase Activity in Leaves of Winter Rye (Secale cereale L.) , 1994, Plant physiology.

[63]  H. Lambers,et al.  Carbon and nitrogen economy of 24 wild species differing in relative growth rate. , 1990, Plant physiology.

[64]  T. Sharkey,et al.  The Effect of Temperature on the Occurrence of O(2) and CO(2) Insensitive Photosynthesis in Field Grown Plants. , 1987, Plant physiology.

[65]  T. Sharkey,et al.  Limitation of Photosynthesis by Carbon Metabolism : II. O(2)-Insensitive CO(2) Uptake Results from Limitation Of Triose Phosphate Utilization. , 1986, Plant physiology.

[66]  R. A. Kedrowski.  Extraction and analysis of nitrogen, phosphorus and carbon fractions in plant material , 1983 .

[67]  J. Berry,et al.  Interaction between light and chilling temperature on the inhibition of photosynthesis in chilling-sensitive plants† , 1983 .

[68]  K. Grossmann.  Why does DNA-dependent RNA polymerase I from higher plants possess a more complex subunit structure than the enzyme from Escherichia colil? A hypothesis , 1983 .

[69]  Joseph A. Berry,et al.  Correlations between the thermal stability of chloroplast (thylakoid) membranes and the composition and fluidity of their polar lipids upon acclimation of the higher plant, Nerium oleander, to growth temperature. , 1982 .

[70]  M. Badger,et al.  An analysis of photosynthetic response and adaptation to temperature in higher plants: temperature acclimation in the desert evergreen Nerium oleander L , 1982 .

[71]  J. Berry,et al.  Photosynthetic Response and Adaptation to Temperature in Higher Plants , 1980 .

[72]  J. B. Kenworthy,et al.  Chemical Analysis of Ecological Materials. , 1976 .

[73]  B. Juniper.  Plants in action , 1974, Nature.