Temporal heterogeneity of cold acclimation phenotypes in Arabidopsis leaves.

To predict the effects of temperature changes on plant growth and performance, it is crucial to understand the impact of thermal history on leaf morphology, anatomy and physiology. Here, we document a comprehensive range of leaf phenotypes in 25/20 degrees C-grown Arabidopsis thaliana plants that were shifted to 5 degrees C for up to 2 months. When warm-grown, pre-existing (PE) leaves were exposed to cold, leaf thickness increased due to an increase in mesophyll cell size. Leaves that were entirely cold-developed (CD) were twice as thick (eight cell layers) as their warm-developed (WD) counterparts (six layers), and also had higher epidermal and stomatal cell densities. After 4 d of cold, PE leaves accumulated high levels of total non-structural carbohydrates (TNC). However, glucose and starch levels declined thereafter, and after 45 d in the cold, PE leaves exhibited similar TNC to CD leaves. A similar phenomenon was observed in delta(13)C and a range of photosynthetic parameters. In cold-treated PE leaves, an increase in respiration (R(dark)) with cold exposure time was evident when measured at 25 degrees C but not 5 degrees C. Cold acclimation was associated with a large increase in the ratio of leaf R(dark) to photosynthesis. The data highlight the importance of understanding developmental thermal history in determining individual phenotypic traits.

[1]  M. Werger,et al.  The leaf anatomy of a broad-leaved evergreen allows an increase in leaf nitrogen content in winter. , 2009, Physiologia plantarum.

[2]  S. Yazawa,et al.  Dramatic changes in leaf development of the native Capsicum chinense from the Seychelles at temperatures below 24°C , 2009, Journal of Plant Research.

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

[4]  A. Millar,et al.  Dynamic changes in the mitochondrial electron transport chain underpinning cold acclimation of leaf respiration. , 2008, Plant, cell & environment.

[5]  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.

[6]  J. Flexas,et al.  Mesophyll conductance to CO2 in Arabidopsis thaliana. , 2007, The New phytologist.

[7]  F. Valladares,et al.  Does growth irradiance affect temperature dependence and thermal acclimation of leaf respiration? Insights from a Mediterranean tree with long-lived leaves. , 2007, Plant, cell & environment.

[8]  J. Flexas,et al.  Mesophyll conductance to CO 2 in Arabidopsis thaliana , 2007 .

[9]  D. Logan,et al.  On the developmental dependence of leaf respiration: responses to short- and long-term changes in growth temperature. , 2006, American journal of botany.

[10]  K. Noguchi,et al.  Effects of internal conductance on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. , 2006, Plant & cell physiology.

[11]  David C Logan,et al.  Heterogeneity of plant mitochondrial responses underpinning respiratory acclimation to the cold in Arabidopsis thaliana leaves. , 2006, Plant, cell & environment.

[12]  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 .

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

[14]  Doug Heath,et al.  A global reorganization of the metabolome in Arabidopsis during cold acclimation is revealed by metabolic fingerprinting , 2005 .

[15]  Z. Ristić,et al.  Changes in leaf ultrastructure and carbohydrates inArabidopsis thaliana L. (Heyn) cv. Columbia during rapid cold acclimation , 1993, Protoplasma.

[16]  Charles L. Guy,et al.  Exploring the Temperature-Stress Metabolome of Arabidopsis1[w] , 2004, Plant Physiology.

[17]  Oliver Fiehn,et al.  A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[18]  C. Körner,et al.  Carbon isotope discrimination by plants follows latitudinal and altitudinal trends , 1991, Oecologia.

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

[20]  P. Reich,et al.  Rapid temperature acclimation of leaf respiration rates in Quercus alba and Quercus rubra. , 2003, Tree physiology.

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

[22]  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 .

[23]  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.

[24]  M. A. Equiza,et al.  Morphological plasticity of spring and winter wheats in response to changing temperatures. , 2002, Functional plant biology : FPB.

[25]  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.

[26]  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.

[27]  D. Royer,et al.  Stomatal density and stomatal index as indicators of paleoatmospheric CO(2) concentration. , 2001, Review of palaeobotany and palynology.

[28]  M. A. Equiza,et al.  Morphological, Anatomical and Physiological Responses Related to Differential Shoot vs. Root Growth Inhibition at Low Temperature in Spring and Winter Wheat , 2001 .

[29]  K. Ichimura,et al.  Sucrose synthase and sucrose phosphate synthase, but not acid invertase, are regulated by cold acclimation and deacclimation in cabbage seedlings , 2001 .

[30]  M. Thomashow.  So what's new in the field of plant cold acclimation? Lots! , 2001, Plant physiology.

[31]  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.

[32]  U. Sonnewald,et al.  High CO2‐mediated down‐regulation of photosynthetic gene transcripts is caused by accelerated leaf senescence rather than sugar accumulation , 2000, FEBS letters.

[33]  M. Ball,et al.  Acclimation of snow gum (Eucalyptus pauciflora) leaf respiration to seasonal and diurnal variations in temperature: the importance of changes in the capacity and temperature sensitivity of respiration , 2000 .

[34]  A. Kacperska,et al.  Low temperature-induced modifications of cell wall content and polysaccharide composition in leaves of winter oilseed rape (Brassica napus L. var. oleifera L.) , 1999 .

[35]  Roderick C. Dewar,et al.  Acclimation of the respiration/photosynthesis ratio to temperature: insights from a model , 1999 .

[36]  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.

[37]  R. Leegood,et al.  Regulation of Leaf Senescence by Cytokinin, Sugars, and Light: Effects on NADH-Dependent Hydroxypyruvate Reductase , 1998 .

[38]  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.

[39]  Roger M. Gifford,et al.  Whole plant respiration and photosynthesis of wheat under increased CO2 concentration and temperature: long‐term vs. short‐term distinctions for modelling , 1995 .

[40]  J. McElwain,et al.  Stomatal Density and Index of Fossil Plants Track Atmospheric Carbon Dioxide in the Palaeozoic , 1995 .

[41]  L. J. Kok,et al.  HOW INDICATIVE ARE CHANGES IN MAJOR METABOLITES FOR FREEZING TOLERANCE OF WHEAT , 1995 .

[42]  D. Beerling,et al.  The Impact of Atmospheric CO2 and Temperature Changes on Stomatal Density: Observation from Quercus robur Lammas Leaves , 1993 .

[43]  C. Guy,et al.  Sucrose phosphate synthase and sucrose accumulation at low temperature. , 1992, Plant physiology.

[44]  M. L. Kagan,et al.  Variable Cell Lineages form the Functional Pea Epidermis , 1992 .

[45]  D. Sims,et al.  Response of leaf anatomy and photosynthetic capacity in Alocasia macrorrhiza (Araceae) to a transfer from low to high light. , 1992 .

[46]  A. Holaday,et al.  Changes in Activities of Enzymes of Carbon Metabolism in Leaves during Exposure of Plants to Low Temperature. , 1992, Plant physiology.

[47]  D. V. Lynch,et al.  Solute Accumulation and Compartmentation during the Cold Acclimation of Puma Rye. , 1992, Plant physiology.

[48]  V. Hurry,et al.  Low growth temperature effects a differential inhibition of photosynthesis in spring and winter wheat. , 1991, Plant physiology.

[49]  N. Huner,et al.  Effect of growth temperature and temperature shifts on spinach leaf morphology and photosynthesis. , 1990, Plant physiology.

[50]  Christian Körner,et al.  Functional Morphology of Mountain Plants) , 1989 .

[51]  J. Ehleringer,et al.  Carbon Isotope Discrimination and Photosynthesis , 1989 .

[52]  G. Farquhar,et al.  Isotopic Composition of Plant Carbon Correlates With Water-Use Efficiency of Wheat Genotypes , 1984 .

[53]  J. Palta,et al.  Anatomical Changes in Leaves of Puma Rye in Response to Growth at Cold-Hardening Temperatures , 1981, Botanical Gazette.

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

[55]  R. Slatyer,et al.  Altitudinal Variation in the Photosynthetic Characteristics of Snow Gum, Eucalyptus pauciflora Sieb. Ex Spreng. II. Effects of Growth Temperature Under Controlled Conditions , 1977 .

[56]  P. Ferrar,et al.  Altitudinal Variation in the Photosynthetic Characteristics of Snow Gum, Eucalyptus pauciflora Sieb. ex Spreng. V. Rate of Acclimation to an Altered Growth Environment , 1977 .

[57]  Bruce N. Smith,et al.  Influence of Carbon Source, Oxygen Concentration, Light Intensity, and Temperature on 13C/12C Ratios in Plant Tissues , 1976, Botanical Gazette.

[58]  Bruce N. Smith,et al.  Effect of growth temperature on carbon isotopic ratios in barley, pea and rape , 1973 .

[59]  W. D. Billings,et al.  Metabolic Acclimation to Temperature in Arctic and Alpine Ecotypes of Oxyr1A Digyna , 1971 .

[60]  D. Rasmusson,et al.  Frrequency and Distribution of Stomata in Barley 1 , 1970 .

[61]  L. Romberg,et al.  A METHOD FOR THE TREATMENT OF CUTTINGS AND ROOTS OF THE PECAN WITH ROOT-INDUCING CHEMICALS. , 1939, Plant physiology.

[62]  Gabrielle L. C. Matthaei,et al.  Experimental Researches in Vegetable Assimilation and Respiration. IV.--A Quantitative Study of Carbon-Dioxide Assimilation and Leaf-Temperature in Natural Illumination , 1905 .

[63]  Gabrielle L. C. Matthaei.  Experimental Researches on Vegetable Assimilation and Respiration. III. On the Effect of Temperature on Carbon-Dioxide Assimilation , 1905 .