Photoperiodic variations induce shifts in the leaf metabolic profile of Chrysanthemum morifolium.

Plants have a high ability to adjust their metabolism, growth and development to changes in the light environment and to photoperiodic variation, but the current knowledge on how changes in metabolite contents are associated with growth and development is limited. We investigated the effect of three different photoperiodic treatments with similar daily light integral (DLI) on the growth responses and diurnal patterns in detected leaf metabolites in the short day plant Chrysanthemum×morifolium Ramat. Treatments were long day (LD, 18h light/6h dark), short day (SD, 12h light/12h dark) and short day with irregular night interruptions (NI-SD,12h light/12h dark, applied in a weekly pattern, shifting from day-to-day). Photoperiodic variation resulted in changes in the phenotypic development of the plants. The plants grown in the SD treatment started to initiate reproductive development of the meristems and a decrease in leaf expansion resulted in lower leaf area of expanding leaves. In contrast, plants in the NI-SD and LD treatments did not show reproductive development at any stage and final leaf area of the expanding leaves was intermediate for the NI-SD plants and largest for the LD plants. Photoperiodic variation also resulted in changes in the leaf metabolic profile for most of the analysed metabolites, but only carbohydrates, citrate and some amino acids displayed a shift in their diurnal pattern. Further, our results illustrated that short days (SD) increased the diurnal turnover of 1-kestose after 2 weeks, and decreased the overall contents of leaf hexoses after 3 weeks. In the two other treatments a diurnal turnover of 1-kestose was not stimulated before after 3 weeks, and hexoses together with the hexose:sucrose ratio steadily increased during the experiment. Our results enlighten the plasticity of leaf growth and metabolism to environmental changes, and demonstrate that diurnally regulated metabolites not always respond to photoperiodic variation.

[1]  F. A. Langton Interrupted lighting of chrysanthemums: monitoring of average daily light integral as an aid to timing , 1992 .

[2]  A. Walter,et al.  Aberrant temporal growth pattern and morphology of root and shoot caused by a defective circadian clock in Arabidopsis thaliana. , 2012, The Plant journal : for cell and molecular biology.

[3]  K. Nishida Effects of Internal and External Factors on Photosynthetic 14CO2 Fixation in General and on Formation of 14C-Maltose in Acer Leaf in Particular , 1962 .

[4]  J. Trygg,et al.  Changes in diurnal patterns within the Populus transcriptome and metabolome in response to photoperiod variation. , 2010, Plant, cell & environment.

[5]  N. J. Chatterton,et al.  Photosynthate partitioning into leaf starch as affected by daily photosynthetic period duration in six species , 1980 .

[6]  Michael J. Haydon,et al.  Interactions between plant circadian clocks and solute transport. , 2011, Journal of experimental botany.

[7]  D. Livingston,et al.  Carbohydrate partitioning between upper and lower regions of the crown in oat and rye during cold acclimation and freezing. , 2006, Cryobiology.

[8]  K. H. Kjaer,et al.  Growth of Chrysanthemum in Response to Supplemental Light Provided by Irregular Light Breaks during the Night , 2011 .

[9]  T. Sharkey,et al.  Daylength and Circadian Effects on Starch Degradation and Maltose Metabolism1 , 2005, Plant Physiology.

[10]  Karine Chenu,et al.  Day length affects the dynamics of leaf expansion and cellular development in Arabidopsis thaliana partially through floral transition timing. , 2007, Annals of botany.

[11]  U. Wobus,et al.  Seed coat-associated invertases of fava bean control both unloading and storage functions: cloning of cDNAs and cell type-specific expression. , 1995, The Plant cell.

[12]  Ying Zhang,et al.  HMDB: the Human Metabolome Database , 2007, Nucleic Acids Res..

[13]  E. Heuvelink,et al.  Influence of greenhouse climate and plant density on external quality of chrysanthemum (Dendranthema grandiflorum (Ramat.) Kitamura): First steps towards a quality model , 2001 .

[14]  F Savorani,et al.  icoshift: A versatile tool for the rapid alignment of 1D NMR spectra. , 2010, Journal of magnetic resonance.

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

[16]  A. Oda,et al.  CsFTL3, a chrysanthemum FLOWERING LOCUS T-like gene, is a key regulator of photoperiodic flowering in chrysanthemums , 2011, Journal of experimental botany.

[17]  W. Van den Ende,et al.  The role of fructan in flowering of Campanula rapunculoides. , 2000, Journal of experimental botany.

[18]  Wim Van den Ende Multifunctional fructans and raffinose family oligosaccharides , 2013, Front. Plant Sci..

[19]  N. Hoffman,et al.  A light‐entrained circadian clock controls transcription of several plant genes. , 1988, The EMBO journal.

[20]  Anthony Hall,et al.  Plant Circadian Clocks Increase Photosynthesis, Growth, Survival, and Competitive Advantage , 2005, Science.

[21]  Alison M. Smith,et al.  The breakdown of starch in leaves. , 2004, The New phytologist.

[22]  J. Lorenzen,et al.  Starch Accumulation in Leaves of Potato (Solanum tuberosum L.) during the First 18 Days of Photoperiod Treatment , 1992 .

[23]  N. Schilling Characterization of maltose biosynthesis from α-d-glucose-1-phosphate in Spinacia oleracea. L. , 1982, Planta.

[24]  G. Bernier,et al.  The role of carbohydrates in the induction of flowering in Arabidopsis thaliana: comparison between the wild type and a starchless mutant , 1998, Planta.

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

[26]  A. Pessoa,et al.  Inulin-type fructans: a review on different aspects of biochemical and pharmaceutical technology. , 2014, Carbohydrate polymers.

[27]  Y. Ruan,et al.  Evidence That High Activity of Vacuolar Invertase Is Required for Cotton Fiber and Arabidopsis Root Elongation through Osmotic Dependent and Independent Pathways, Respectively1[C][W][OA] , 2010, Plant Physiology.

[28]  F. Cejudo,et al.  Circadian and developmental regulation of vacuolar invertase expression in petioles of sugar beet plants , 2005, Planta.

[29]  C. Granier,et al.  A dynamic analysis of the shade-induced plasticity in Arabidopsis thaliana rosette leaf development reveals new components of the shade-adaptative response. , 2006, Annals of botany.

[30]  Kazuki Saito,et al.  Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination , 2009, Proceedings of the National Academy of Sciences.

[31]  K. H. Kjaer,et al.  Rapid adjustment in chrysanthemum carbohydrate turnover and growth activity to a change in time-of-day application of light and daylength. , 2012, Functional plant biology : FPB.

[32]  E. Goldschmidt,et al.  The nature of floral signals in Arabidopsis. I. Photosynthesis and a far-red photoresponse independently regulate flowering by increasing expression of FLOWERING LOCUS T (FT) , 2008, Journal of experimental botany.

[33]  M. Ernst,et al.  Relation between Nitrogen Status, Carbohydrate Distribution and Subsequent Rooting of Chrysanthemum Cuttings as Affected by Pre-harvest Nitrogen Supply and Cold-storage , 2000 .

[34]  K. Cockshull Flower and Leaf Initiation by Chrysanthemum Morifolium Ramat in Long Days , 1976 .

[35]  M. Adachi,et al.  Changes in Carbohydrate Content in Cut Chrysanthemum [Dendranthema×grandiflorum (Ramat.) Kitamura] 'Shuho-no-chikara' Stems Kept at Different Temperatures during Anthesis and Senescence , 1999 .

[36]  Midori Yoshida,et al.  Fructan 1-exohydrolase is associated with flower opening in Campanula rapunculoides. , 2007, Functional plant biology : FPB.

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

[38]  T. Tonon,et al.  Diurnal oscillations of metabolite abundances and gene analysis provide new insights into central metabolic processes of the brown alga Ectocarpus siliculosus. , 2010, The New phytologist.

[39]  Mohammad R. Bolouri Moghaddam,et al.  Sugars, the clock and transition to flowering , 2013, Front. Plant Sci..

[40]  J. Lockhart An analysis of irreversible plant cell elongation. , 1965, Journal of theoretical biology.

[41]  R. L. Bieleski,et al.  Fructan Hydrolysis Drives Petal Expansion in the Ephemeral Daylily Flower , 1993, Plant physiology.

[42]  N. Mattson,et al.  The impact of photoperiod and irradiance on flowering of several herbaceous ornamentals , 2005 .

[43]  Paul E. Brown,et al.  Quantitative analysis of regulatory flexibility under changing environmental conditions , 2010, Molecular systems biology.

[44]  R. Sicher Effects of CO2 enrichment on soluble amino acids and organic acids in barley primary leaves as a function of age, photoperiod and chlorosis , 2008 .

[45]  F. Rolland,et al.  Exploring the neutral invertase–oxidative stress defence connection in Arabidopsis thaliana , 2011, Journal of experimental botany.

[46]  Carl Troein,et al.  Multiple light inputs to a simple clock circuit allow complex biological rhythms , 2011, The Plant journal : for cell and molecular biology.

[47]  W. Miller,et al.  Postproduction Carbohydrate Levels in Pot Chrysanthemums , 1991 .

[48]  S. Adams,et al.  Photoperiod and plant growth: a review , 2005 .

[49]  T. Roitsch,et al.  Function and regulation of plant invertases: sweet sensations. , 2004, Trends in plant science.