Metabolism and Growth in Arabidopsis Depend on the Daytime Temperature but Are Temperature-Compensated against Cool Nights[W][OA]

This study investigated the response of metabolism and growth to fluctuating temperatures under carbon-limiting conditions (short days, low light). It is shown that biomass production is determined largely by the daytime temperature via its effect on photosynthesis. By contrast, the mobilization of starch and use of carbon for growth is compensated against changes in the night temperature. Diurnal cycles provide a tractable system to study the response of metabolism and growth to fluctuating temperatures. We reasoned that the response to daytime and night temperature may vary; while daytime temperature affects photosynthesis, night temperature affects use of carbon that was accumulated in the light. Three Arabidopsis thaliana accessions were grown in thermocycles under carbon-limiting conditions with different daytime or night temperatures (12 to 24°C) and analyzed for biomass, photosynthesis, respiration, enzyme activities, protein levels, and metabolite levels. The data were used to model carbon allocation and growth rates in the light and dark. Low daytime temperature led to an inhibition of photosynthesis and an even larger inhibition of growth. The inhibition of photosynthesis was partly ameliorated by a general increase in protein content. Low night temperature had no effect on protein content, starch turnover, or growth. In a warm night, there is excess capacity for carbon use. We propose that use of this capacity is restricted by feedback inhibition, which is relaxed at lower night temperature, thus buffering growth against fluctuations in night temperature. As examples, the rate of starch degradation is completely temperature compensated against even sudden changes in temperature, and polysome loading increases when the night temperature is decreased.

[1]  C. Osmond,et al.  Physiological Plant Ecology I , 1981, Encyclopedia of Plant Physiology.

[2]  Martijn Gough Climate change , 2009, Canadian Medical Association Journal.

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

[4]  V. Hurry,et al.  Impact of growth temperature on scaling relationships linking photosynthetic metabolism to leaf functional traits , 2010 .

[5]  T. Mitchell-Olds,et al.  Establishment of a high-efficiency SNP-based framework marker set for Arabidopsis. , 2003, The Plant journal : for cell and molecular biology.

[6]  K. Halliday,et al.  Edinburgh Research Explorer Beta-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active beta-amylases in Arabidopsis chloroplasts , 2008 .

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

[8]  G. E. Blackman,et al.  Interacting Effects of Light and Day and Night Temperatures on the Growth of Four Species in the Vegetative Phase , 1975 .

[9]  Alison M. Smith,et al.  Starch: its metabolism, evolution, and biotechnological modification in plants. , 2010, Annual review of plant biology.

[10]  Yves Gibon,et al.  Global Transcript Levels Respond to Small Changes of the Carbon Status during Progressive Exhaustion of Carbohydrates in Arabidopsis Rosettes1[W][OA] , 2008, Plant Physiology.

[11]  Hendrik Poorter,et al.  Avoiding bias in calculations of relative growth rate. , 2002, Annals of botany.

[12]  M. Mann,et al.  Exponentially Modified Protein Abundance Index (emPAI) for Estimation of Absolute Protein Amount in Proteomics by the Number of Sequenced Peptides per Protein*S , 2005, Molecular & Cellular Proteomics.

[13]  S. Seneviratne,et al.  Global Convergence in the Temperature Sensitivity of Respiration at Ecosystem Level , 2010, Science.

[14]  M. Thomashow,et al.  Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. , 2004, The Plant journal : for cell and molecular biology.

[15]  D. Geiger,et al.  Role of starch in carbon translocation and partitioning at the plant level , 2000 .

[16]  Thomas Altmann,et al.  Variation of Enzyme Activities and Metabolite Levels in 24 Arabidopsis Accessions Growing in Carbon-Limited Conditions1[W] , 2006, Plant Physiology.

[17]  Frank Schleifenbaum,et al.  Analysis of Arabidopsis with Highly Reduced Levels of Malate and Fumarate Sheds Light on the Role of These Organic Acids as Storage Carbon Molecules1[W] , 2010, Plant Physiology.

[18]  U. Flügge,et al.  An Arabidopsis thaliana knock-out mutant of the chloroplast triose phosphate/phosphate translocator is severely compromised only when starch synthesis, but not starch mobilisation is abolished. , 2002, The Plant journal : for cell and molecular biology.

[19]  S. Zeeman,et al.  A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolysing enzyme. , 1998, The Plant journal : for cell and molecular biology.

[20]  G. Berntson,et al.  Plant responses to carbon dioxide , 1993, Nature.

[21]  D. Manahan,et al.  Cost of Protein Synthesis and Energy Allocation During Development of Antarctic Sea Urchin Embryos and Larvae , 2007, The Biological Bulletin.

[22]  B. Bugbee,et al.  Night temperature has a minimal effect on respiration and growth in rapidly growing plants. , 2004, Annals of botany.

[23]  G. Soldatini,et al.  The influence of chilling on photosynthesis and activities of some enzymes of sucrose metabolism in Lycopersicon esculentum Mill , 2000, Acta Physiologiae Plantarum.

[24]  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.

[25]  K. Lagerspetz What is thermal acclimation , 2006 .

[26]  F. D. Vries,et al.  The cost of maintenance processes in plant cells , 1975 .

[27]  S. Zeeman,et al.  The Laforin-Like Dual-Specificity Phosphatase SEX4 from Arabidopsis Hydrolyzes Both C6- and C3-Phosphate Esters Introduced by Starch-Related Dikinases and Thereby Affects Phase Transition of α-Glucans1[W] , 2009, Plant Physiology.

[28]  N. Weeden,et al.  Dissociation, reassociation, and purification of plastid and cytosolic phosphoglucose isomerase isozymes. , 1982, Plant physiology.

[29]  N. Kruger,et al.  A Mutant of Arabidopsis Lacking the Triose-Phosphate/Phosphate Translocator Reveals Metabolic Regulation of Starch Breakdown in the Light1[w] , 2004, Plant Physiology.

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

[31]  D. MacLean,et al.  A Putative Phosphatase, LSF1, Is Required for Normal Starch Turnover in Arabidopsis Leaves1[W][OA] , 2009, Plant Physiology.

[32]  B. Usadel,et al.  Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis , 2009, Molecular systems biology.

[33]  H. Enoch,et al.  Temperature dependence of vegetative growth and dark respiration: a mathematical model. , 1983, Plant physiology.

[34]  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.

[35]  M. Burrell,et al.  Effects of low temperature on the respiratory metabolism of carbohydrates by plants. , 1988, Symposia of the Society for Experimental Biology.

[36]  Thomas Altmann,et al.  Description and applications of a rapid and sensitive non-radioactive microplate-based assay for maximum and initial activity of D-ribulose-1,5-bisphosphate carboxylase/oxygenase. , 2007, Plant, cell & environment.

[37]  David Thorneycroft,et al.  Diurnal Changes in the Transcriptome Encoding Enzymes of Starch Metabolism Provide Evidence for Both Transcriptional and Posttranscriptional Regulation of Starch Metabolism in Arabidopsis Leaves1 , 2004, Plant Physiology.

[38]  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 .

[39]  Mark Stitt,et al.  Circadian control of root elongation and C partitioning in Arabidopsis thaliana. , 2011, Plant, cell & environment.

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

[41]  M. Stitt,et al.  Coordination of carbon supply and plant growth. , 2007, Plant, cell & environment.

[42]  Jingyuan Fu,et al.  Integrative analyses of genetic variation in enzyme activities of primary carbohydrate metabolism reveal distinct modes of regulation in Arabidopsis thaliana , 2008, Genome Biology.

[43]  M. Stitt,et al.  Interactions between Sucrose Synthesis and CO2 Fixation IV. Temperature-dependent adjustment of the relation between sucrose synthesis and CO2 fixation , 1988 .

[44]  Yves Gibon,et al.  Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes , 2006, Genome Biology.

[45]  W. Driedzic,et al.  Tissue-specific changes in protein synthesis associated with seasonal metabolic depression and recovery in the north temperate labrid, Tautogolabrus adspersus. , 2007, American journal of physiology. Regulatory, integrative and comparative physiology.

[46]  Joachim Selbig,et al.  Extension of the Visualization Tool MapMan to Allow Statistical Analysis of Arrays, Display of Coresponding Genes, and Comparison with Known Responses1 , 2005, Plant Physiology.

[47]  M. Thomashow,et al.  Cold Induction of Arabidopsis CBF Genes Involves Multiple ICE (Inducer of CBF Expression) Promoter Elements and a Cold-Regulatory Circuit That Is Desensitized by Low Temperature1 , 2003, Plant Physiology.

[48]  J. Warner,et al.  The economics of ribosome biosynthesis in yeast. , 1999, Trends in biochemical sciences.

[49]  G. Evans,et al.  The quantitative analysis of plant growth , 1972 .

[50]  M. Stitt,et al.  Adjustment of growth and central metabolism to a mild but sustained nitrogen-limitation in Arabidopsis. , 2009, Plant, cell & environment.

[51]  J. Fisahn,et al.  Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. , 2004, The Plant journal : for cell and molecular biology.

[52]  S. Holm A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[53]  Mark G Tjoelker,et al.  The hot and the cold: unravelling the variable response of plant respiration to temperature. , 2005, Functional plant biology : FPB.

[54]  Michael F. Thomashow,et al.  PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms. , 1999, Annual review of plant physiology and plant molecular biology.

[55]  Ichiro Terashima,et al.  Increase in respiratory cost at high growth temperature is attributed to high protein turnover cost in Petunia x hybrida petals. , 2007, Plant, cell & environment.

[56]  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 .

[57]  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 .

[58]  Thomas Altmann,et al.  Network Analysis of Enzyme Activities and Metabolite Levels and Their Relationship to Biomass in a Large Panel of Arabidopsis Accessions[C][W][OA] , 2010, Plant Cell.

[59]  Yves Gibon,et al.  Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. , 2007, The Plant journal : for cell and molecular biology.

[60]  K. Espelie,et al.  Lipid polymers accumulate in the epidermis and mestome sheath cell walls during low temperature development of winter rye leaves , 1985, Protoplasma.

[61]  Norio Murata,et al.  A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. , 2006, Biochimica et biophysica acta.

[62]  Michael F. Thomashow,et al.  Low Temperature Induction of Arabidopsis CBF1, 2, and 3 Is Gated by the Circadian Clock1 , 2005, Plant Physiology.

[63]  A. Millar,et al.  NAD malic enzyme and the control of carbohydrate metabolism in potato tubers. , 2001, Plant physiology.

[64]  M. M. Christ,et al.  Spatio-temporal leaf growth patterns of Arabidopsis thaliana and evidence for sugar control of the diel leaf growth cycle. , 2007, The New phytologist.

[65]  T. Sharkey,et al.  Sucrose Synthesis, Temperature, and Plant Yield , 1995 .

[66]  S. Gibson,et al.  Fumaric acid: an overlooked form of fixed carbon in Arabidopsis and other plant species , 2000, Planta.

[67]  K. Niyogi,et al.  PHOTOPROTECTION REVISITED: Genetic and Molecular Approaches. , 1999, Annual review of plant physiology and plant molecular biology.

[68]  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.

[69]  J. Amthor The McCree-de Wit-Penning de Vries-Thornley Respiration Paradigms: 30 Years Later , 2000 .

[70]  A. Haschemeyer,et al.  Effect of temperature on protein synthesis in fish of the Galapagos and Perlas Islands. , 1979, Comparative biochemistry and physiology. B, Comparative biochemistry.

[71]  Robert W. Pearcy,et al.  Plant Physiological Ecology , 1989, Springer Netherlands.

[72]  Ulrich Schurr,et al.  Diel time-courses of leaf growth in monocot and dicot species: endogenous rhythms and temperature effects , 2010, Journal of experimental botany.

[73]  Joachim Selbig,et al.  A Robot-Based Platform to Measure Multiple Enzyme Activities in Arabidopsis Using a Set of Cycling Assays: Comparison of Changes of Enzyme Activities and Transcript Levels during Diurnal Cycles and in Prolonged Darknessw⃞ , 2004, The Plant Cell Online.

[74]  B. Muller,et al.  Control of Leaf Expansion: A Developmental Switch from Metabolics to Hydraulics1[W][OA] , 2011, Plant Physiology.

[75]  D. Lawlor Plant responses to climate change: impacts and adaptation , 2005 .

[76]  A. Rogers,et al.  Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. , 2009, Journal of experimental botany.

[77]  B. Usadel,et al.  Multilevel genomic analysis of the response of transcripts, enzyme activities and metabolites in Arabidopsis rosettes to a progressive decrease of temperature in the non-freezing range. , 2008, Plant, cell & environment.

[78]  T. Mcnelley,et al.  Temperature dependence of , 1993, Metallurgical and Materials Transactions A.

[79]  Joachim Selbig,et al.  Starch as a major integrator in the regulation of plant growth , 2009, Proceedings of the National Academy of Sciences.

[80]  S. Zeeman,et al.  Arabidopsis mutants Atisa1 and Atisa2 have identical phenotypes and lack the same multimeric isoamylase, which influences the branch point distribution of amylopectin during starch synthesis. , 2005, The Plant journal : for cell and molecular biology.

[81]  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 .

[82]  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.

[83]  D. Lawlor,et al.  Causes of Decreased Photosynthetic Rate and Metabolic Capacity in Water-deficient Leaf Cells: a Critical Evaluation of Mechanisms and Integration of Processes , 1996 .

[84]  A. Masoni,et al.  Growth responses of sorghum plants to chilling temperature and duration of exposure , 2004 .

[85]  O. Atkin,et al.  Assessing the relationship between respiratory acclimation to the cold and photosystem II redox poise in Arabidopsis thaliana. , 2007, Plant, cell & environment.

[86]  Alison M. Smith,et al.  STARCH-EXCESS4 Is a Laforin-Like Phosphoglucan Phosphatase Required for Starch Degradation in Arabidopsis thaliana[W][OA] , 2009, The Plant Cell Online.

[87]  K. Halliday,et al.  Edinburgh Research Explorer Beta-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active beta-amylases in Arabidopsis chloroplasts , 2008 .

[88]  Alison M. Smith,et al.  Starch and the clock: the dark side of plant productivity. , 2011, Trends in plant science.

[89]  A. Fitter,et al.  Impact of temperature on the relationship between respiration and nitrogen concentration in roots: an analysis of scaling relationships, Q10 values and thermal acclimation ratios. , 2007, The New phytologist.

[90]  M. Stitt,et al.  Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. , 2009, Plant, cell & environment.

[91]  B. Usadel,et al.  Arabidopsis and primary photosynthetic metabolism - more than the icing on the cake. , 2010, The Plant journal : for cell and molecular biology.

[92]  Mark G Tjoelker,et al.  Thermal acclimation and the dynamic response of plant respiration to temperature. , 2003, Trends in plant science.

[93]  H. H. Laar,et al.  Products, requirements and efficiency of biosynthesis: a quantitative approach. , 1974, Journal of theoretical biology.

[94]  P. Reich,et al.  Coupling of respiration, nitrogen, and sugars underlies convergent temperature acclimation in Pinus banksiana across wide‐ranging sites and populations , 2008 .

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

[96]  F. D. Vries,et al.  Rates of Respiration and of Increase in Structural Dry Matter in Young Wheat, Ryegrass and Maize Plants in Relation to Temperature, to Water Stress and to Their Sugar Content , 1979 .

[97]  M. M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[98]  J. Amthor Terrestrial higher‐plant response to increasing atmospheric [CO2] in relation to the global carbon cycle , 1995 .

[99]  J. Botto,et al.  The plant cell , 2007, Plant Molecular Biology Reporter.

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

[101]  Wenxu Zhou,et al.  Arabidopsis has a cytosolic fumarase required for the massive allocation of photosynthate into fumaric acid and for rapid plant growth on high nitrogen. , 2010, The Plant journal : for cell and molecular biology.

[102]  S. Rhee,et al.  MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. , 2004, The Plant journal : for cell and molecular biology.

[103]  J. Dale Leaf Growth in Phaseolus vulgaris 2. Temperature Effects and the Light Factor , 1965 .

[104]  V. Planchot,et al.  Further Evidence for the Mandatory Nature of Polysaccharide Debranching for the Aggregation of Semicrystalline Starch and for Overlapping Functions of Debranching Enzymes in Arabidopsis Leaves1[W] , 2008, Plant Physiology.

[105]  J. Smith MOLECULAR EQUIVALENCE OF CARBOHYDRATES TO CARBON DIOXIDE IN PHOTOSYNTHESIS. , 1943, Plant physiology.

[106]  R. G. Hurd,et al.  Effect of Night Temperature on Photosynthesis, Transpiration, and Growth of Spray Carnations , 1976 .

[107]  S. Zeeman,et al.  Starch breakdown: recent discoveries suggest distinct pathways and novel mechanisms. , 2007, Functional plant biology : FPB.

[108]  J. Dale Leaf Growth in Phaseolus vulgarisI. Growth of the first pair of leaves under constant conditions , 1964 .

[109]  Eva M Farré,et al.  CIRCADIAN CLOCK-ASSOCIATED 1 and LATE ELONGATED HYPOCOTYL regulate expression of the C-REPEAT BINDING FACTOR (CBF) pathway in Arabidopsis , 2011, Proceedings of the National Academy of Sciences.

[110]  D. King Climate change: the science and the policy , 2005 .

[111]  Mark Stitt,et al.  Circadian control of carbohydrate availability for growth in Arabidopsis plants at night , 2010, Proceedings of the National Academy of Sciences.

[112]  G. Hussey Growth and Development in the Young Tomato III. THE EFFECT OF NIGHT AND DAY TEMPERATURES ON VEGETATIVE GROWTH , 1965 .

[113]  P. Reich The Carbon Dioxide Exchange , 2010, Science.

[114]  Donald R. Geiger,et al.  Diurnal Regulation of Photosynthetic Carbon Metabolism in C3 Plants , 1994 .

[115]  Philippe Ciais,et al.  Update on CO2 emissions , 2010 .

[116]  C. Vance,et al.  Glutamate synthase and nitrogen assimilation , 1998 .