Daily Changes in Temperature, Not the Circadian Clock, Regulate Growth Rate in Brachypodium distachyon

Plant growth is commonly regulated by external cues such as light, temperature, water availability, and internal cues generated by the circadian clock. Changes in the rate of growth within the course of a day have been observed in the leaves, stems, and roots of numerous species. However, the relative impact of the circadian clock on the growth of grasses has not been thoroughly characterized. We examined the influence of diurnal temperature and light changes, and that of the circadian clock on leaf length growth patterns in Brachypodium distachyon using high-resolution time-lapse imaging. Pronounced changes in growth rate were observed under combined photocyles and thermocycles or with thermocycles alone. A considerably more rapid growth rate was observed at 28°C than 12°C, irrespective of the presence or absence of light. In spite of clear circadian clock regulated gene expression, plants exhibited no change in growth rate under conditions of constant light and temperature, and little or no effect under photocycles alone. Therefore, temperature appears to be the primary cue influencing observed oscillations in growth rate and not the circadian clock or photoreceptor activity. Furthermore, the size of the leaf meristem and final cell length did not change in response to changes in temperature. Therefore, the nearly five-fold difference in growth rate observed across thermocycles can be attributed to proportionate changes in the rate of cell division and expansion. A better understanding of the growth cues in B. distachyon will further our ability to model metabolism and biomass accumulation in grasses.

[1]  Henry D. Priest,et al.  Functional characterization of cinnamyl alcohol dehydrogenase and caffeic acid O-methyltransferase in Brachypodium distachyon , 2013, BMC Biotechnology.

[2]  B. Drosse,et al.  HvLUX1 is a candidate gene underlying the early maturity 10 locus in barley: phylogeny, diversity, and interactions with the circadian clock and photoperiodic pathways , 2013, The New phytologist.

[3]  Xianghua Li,et al.  OsELF3 is involved in circadian clock regulation for promoting flowering under long-day conditions in rice. , 2013, Molecular plant.

[4]  A. Walter,et al.  REVIEW: PART OF A HIGHLIGHT ON BREEDING STRATEGIES FOR FORAGE AND GRASS IMPROVEMENT Advanced phenotyping offers opportunities for improved breeding of forage and turf species , 2012 .

[5]  D. Inzé,et al.  A Local Maximum in Gibberellin Levels Regulates Maize Leaf Growth by Spatial Control of Cell Division , 2012, Current Biology.

[6]  D. Laurie,et al.  Mutation at the circadian clock gene EARLY MATURITY 8 adapts domesticated barley (Hordeum vulgare) to short growing seasons , 2012, Proceedings of the National Academy of Sciences.

[7]  E. M. Farré,et al.  The regulation of plant growth by the circadian clock. , 2012, Plant biology.

[8]  Kaworu Ebana,et al.  Natural variation in Hd17, a homolog of Arabidopsis ELF3 that is involved in rice photoperiodic flowering. , 2012, Plant & cell physiology.

[9]  A. Graner,et al.  Induced mutations in circadian clock regulator Mat-a facilitated short-season adaptation and range extension in cultivated barley , 2012, Proceedings of the National Academy of Sciences.

[10]  S. Davis,et al.  Expression conservation within the circadian clock of a monocot: natural variation at barley Ppd-H1 affects circadian expression of flowering time genes, but not clock orthologs , 2012, BMC Plant Biology.

[11]  Morio Iijima,et al.  A circadian and an ultradian rhythm are both evident in root growth of rice. , 2011, Journal of plant physiology.

[12]  Diana V. Dugas,et al.  Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum , 2011, Proceedings of the National Academy of Sciences.

[13]  E. Grotewold,et al.  Brachypodium as a Model for the Grasses: Today and the Future1[W] , 2011, Plant Physiology.

[14]  Steve A. Kay,et al.  The ELF4-ELF3-LUX Complex Links the Circadian Clock to Diurnal Control of Hypocotyl Growth , 2011, Nature.

[15]  M. Hirai,et al.  Os-GIGANTEA Confers Robust Diurnal Rhythms on the Global Transcriptome of Rice in the Field[C][W][OA] , 2011, Plant Cell.

[16]  S. Kay,et al.  Automated analysis of hypocotyl growth dynamics during shade avoidance in Arabidopsis. , 2011, The Plant journal : for cell and molecular biology.

[17]  Young Hun Song,et al.  Similarities in the circadian clock and photoperiodism in plants. , 2010, Current opinion in plant biology.

[18]  M. Stitt,et al.  Modelling temperature-compensated physiological rates, based on the co-ordination of responses to temperature of developmental processes. , 2010, Journal of experimental botany.

[19]  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.

[20]  Sai Guna Ranjan Gurazada,et al.  Genome sequencing and analysis of the model grass Brachypodium distachyon , 2010, Nature.

[21]  T. Imaizumi,et al.  Arabidopsis circadian clock and photoperiodism: time to think about location. , 2010, Current opinion in plant biology.

[22]  Chung-Mo Park,et al.  Identification and molecular characterization of a Brachypodium distachyonGIGANTEA gene: functional conservation in monocot and dicot plants , 2010, Plant Molecular Biology.

[23]  H. Scharr,et al.  Simultaneous phenotyping of leaf growth and chlorophyll fluorescence via GROWSCREEN FLUORO allows detection of stress tolerance in Arabidopsis thaliana and other rosette plants. , 2009, Functional plant biology : FPB.

[24]  Stephen P. Long,et al.  More Productive Than Maize in the Midwest: How Does Miscanthus Do It?1[W][OA] , 2009, Plant Physiology.

[25]  U. Schurr,et al.  Environmental effects on spatial and temporal patterns of leaf and root growth. , 2009, Annual review of plant biology.

[26]  S. Harmer,et al.  The circadian system in higher plants. , 2009, Annual review of plant biology.

[27]  Chung-Mo Park,et al.  Exploring valid reference genes for gene expression studies in Brachypodium distachyon by real-time PCR , 2008, BMC Plant Biology.

[28]  Joanne Chory,et al.  A Morning-Specific Phytohormone Gene Expression Program underlying Rhythmic Plant Growth , 2008, PLoS biology.

[29]  R. Perrin,et al.  Net energy of cellulosic ethanol from switchgrass , 2008, Proceedings of the National Academy of Sciences.

[30]  Kanwarpal S. Dhugga,et al.  Maize Biomass Yield and Composition for Biofuels , 2007 .

[31]  Jürg M. Blumenthal,et al.  Designing sorghum as a dedicated bioenergy feedstock , 2007 .

[32]  Nathan D. Miller,et al.  Computer-vision analysis of seedling responses to light and gravity. , 2007, The Plant journal : for cell and molecular biology.

[33]  Stacey L. Harmer,et al.  Rhythmic growth explained by coincidence between internal and external cues , 2007, Nature.

[34]  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.

[35]  Francois Tardieu,et al.  Leaf growth rate per unit thermal time follows QTL-dependent daily patterns in hundreds of maize lines under naturally fluctuating conditions. , 2007, Plant, cell & environment.

[36]  D. Inzé,et al.  Cold Nights Impair Leaf Growth and Cell Cycle Progression in Maize through Transcriptional Changes of Cell Cycle Genes1[W][OA] , 2007, Plant Physiology.

[37]  D. Tilman,et al.  Carbon-Negative Biofuels from Low-Input High-Diversity Grassland Biomass , 2006, Science.

[38]  K. Chenu,et al.  PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit. , 2006, The New phytologist.

[39]  D. Laurie,et al.  The Pseudo-Response Regulator Ppd-H1 Provides Adaptation to Photoperiod in Barley , 2005, Science.

[40]  U. Schurr,et al.  Glycine max leaflets lack a base-tip gradient in growth rate , 2005, Journal of Plant Research.

[41]  M. M. Christ,et al.  The effect of elevated CO2 on diel leaf growth cycle, leaf carbohydrate content and canopy growth performance of Populus deltoides , 2005 .

[42]  Ulrich Schurr,et al.  Dynamics of leaf and root growth: endogenous control versus environmental impact. , 2005, Annals of botany.

[43]  Mao-sen Liu,et al.  The wheat TaGI1, involved in photoperiodic flowering, encodesan Arabidopsis GI ortholog , 2005, Plant Molecular Biology.

[44]  Michael D. Abràmoff,et al.  Image processing with ImageJ , 2004 .

[45]  T. Mizuno,et al.  The evolutionarily conserved OsPRR quintet: rice pseudo-response regulators implicated in circadian rhythm. , 2003, Plant & cell physiology.

[46]  S. Kay,et al.  Circadian photoperception. , 2001, Annual review of physiology.

[47]  A. Millar,et al.  Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. , 1999, The Plant journal : for cell and molecular biology.

[48]  B. Jähne,et al.  Quantitative analysis of the local rates of growth of dicot leaves at a high temporal and spatial resolution, using image sequence analysis , 1998 .

[49]  B. Lercari,et al.  Kinetics of Stem Elongation in Light‐Grown Tomato Plants. Responses to Different Photosynthetically Active Radiation Levels by Wild‐Type and aurea Mutant Plants , 1997 .

[50]  F. Tardieu,et al.  Temperature Affects Expansion Rate of Maize Leaves without Change in Spatial Distribution of Cell Length (Analysis of the Coordination between Cell Division and Cell Expansion) , 1995, Plant physiology.

[51]  I. Rademacher,et al.  Drought effects on cellular and spatial parameters of leaf growth in tall fescue , 1995 .

[52]  P. Karlsen,et al.  Patterns in stem elongation rate in chrysanthemum and tomato plants in relation to irradiance and day/night temperature , 1994 .

[53]  P. Hicklenton,et al.  The Influence of Photoperiod and Temperature on the Kinetics of Stem Elongation in Dendranthema grandiflorum , 1994 .

[54]  J. Richards,et al.  Diurnal variation in the temperature response of leaf extension of two bunchgrass species in the field , 1992 .

[55]  R. Sands,et al.  Diurnal variation in extension growth of leaves of Salix viminalis. , 1992, Tree physiology.

[56]  P. Lancashire,et al.  A uniform decimal code for growth stages of crops and weeds , 1991 .

[57]  M. Matthews,et al.  Dynamic Relation between Expansion and Cellular Turgor in Growing Grape (Vitis vinifera L.) Leaves. , 1987, Plant physiology.

[58]  W. Davies,et al.  YIELD TURGOR OF GROWING LEAVES OF BETULA AND ACER , 1986 .

[59]  W. Davies,et al.  The Influence of Water Deficit on the Factors Controlling the Daily Pattern of Growth of Phaseolus Trifoliates , 1983 .

[60]  J. M. Cutler,et al.  Dynamic aspects and enhancement of leaf elongation in rice. , 1980, Plant physiology.

[61]  D. Kemp,et al.  Diurnal Extension Rates of Wheat Leaves in Relation to Temperatures and Carbohydrate Concentrations of the Extension Zone , 1980 .

[62]  E. Fereres,et al.  Diurnal growth trends, water potential, and osmotic adjustment of maize and sorghum leaves in the field. , 1979, Plant physiology.

[63]  P. Biscoe,et al.  Radiation absorption, growth and yield of cereals , 1978, The Journal of Agricultural Science.

[64]  W. R. Watts,et al.  Role of Temperature in the Regulation of Leaf Extension in Zea mays , 1971, Nature.

[65]  G. Meijer.  RAPID GROWTH INHIBITION OF GHERKIN HYPOCOTYLS IN BLUE LIGHT1 , 1968 .

[66]  W. C. Johnson.  Diurnal Variation in Growth Rate of Grain Sorghum 1 , 1967 .