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Changes in metabolite profiles in Norway spruce shoot tips during short-day induced winter bud development and long-day induced bud flush

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Abstract

The seasonal change in photoperiod is a primary environmental signal influencing tree growth. Long days (LD) sustain growth, whereas short days (SD) induce winter bud formation. In this respect, metabolomic responses have been studied to a limited extent only in conifers. Here we identified changes in metabolite profile in the conifer Norway spruce after transition to SD and following re-transfer to LDs inducing bud flush. After 1 week in SD initial changes in metabolite profile was visible but for the majority of compounds magnitudes of changes were small. However, the ascorbate content was strongly reduced and there were often temporary increases in several energy metabolism-related compounds, secondary metabolites, nucleosides, amino acids and lipids. After 8 weeks in SD substantial changes were observed; proper winter buds had high pools of ABA, antioxidants, flavonoids, terpenoids, phenylpropanoids, sugars, amino acids and lipids related to stress tolerance and hardening, and low levels of nucleosides and metabolites in energy metabolism. One week after re-transfer to LD the metabolome was generally relatively similar to under long-term SD, except e.g. increased urate and strongly decreased ABA and oxidized glutathione. Two weeks later, bud flush had occurred, and the metabolite profile resembled the situation before transfer to SD. This study thus revealed comprehensive modulation of the metabolome in Norway spruce in response to a day length shift, indicating substantially increased stress resistance under SD-induced bud set, and reversal upon bud flush in LD.

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References

  • Akpinar, N., Ali Akpinar, M., & Türkoğlu, Ş. (2001). Total lipid content and fatty acid composition of the seeds of some Vicia L. species. Food Chemistry, 74, 449–453.

    Article  CAS  Google Scholar 

  • Aronsson, A., Ingestad, T., & LööF, L. G. (1976). Carbohydrate metabolism and frost hardiness in pine and spruce seedlings grown at different photoperiods and thermoperiods. Physiologia Plantarum, 36, 127–132.

    Article  CAS  Google Scholar 

  • Asante, D. K. A., Yakovlev, I., Fossdal, C. G., Holefors, A., Opseth, L., Olsen, J. E., et al. (2011). Gene expression changes during short day induced terminal bud formation in Norway spruce. Plant, Cell and Environment, 34, 332–346.

    Article  CAS  PubMed  Google Scholar 

  • Bachmann, M., Matile, P., & Keller, F. (1994). Metabolism of the raffinose family oligosaccharides in leaves of Ajuga reptans L. (cold acclimation, translocation, and sink to source transition: Discovery of chain elongation enzyme). Plant Physiology, 105, 1335–1345.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baur, J. A., & Sinclair, D. A. (2006). Therapeutic potential of resveratrol: The in vivo evidence. Nature Reviews Drug Discovery, 5, 493–506.

    Article  CAS  PubMed  Google Scholar 

  • Bi, Y.-D., Wei, Z.-G., Shen, Z., Lu, T.-C., Cheng, Y.-X., Wang, B.-C., et al. (2011). Comparative, temporal analyses of the Pinus sylvestris L. var. mongolica litv. apical bud proteome from dormancy to growth. Molecular Biology Reports, 38, 721–729.

    Article  CAS  PubMed  Google Scholar 

  • Böhlenius, H., Huang, T., Charbonnel-Campaa, L., Brunner, A. M., Jansson, S., Strauss, S. H., et al. (2006). CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science, 312, 1040–1043.

    Article  PubMed  Google Scholar 

  • Callaway, J. C. (2004). Hempseed as a nutritional resource: An overview. Euphytica, 140, 65–72.

    Article  Google Scholar 

  • Canam, T., Unda, F., & Mansfield, S. (2008). Heterologous expression and functional characterization of two hybrid poplar cell-wall invertases. Planta, 228, 1011–1019.

    Article  CAS  PubMed  Google Scholar 

  • Codignola, A., Maffei, M., & Fieschi, M. (1988). Phenols and bud dormancy. I. Variations in total phenols and phenylalanine ammonia lyase activity in dormant buds of Fagus svlvatica L. New Phytologist, 108, 83–89.

    Article  CAS  Google Scholar 

  • Davies, H. V., Shepherd, L. V. T., Stewart, D., Frank, T., Röhlig, R. M., & Engel, K.-H. (2010). Metabolome variability in crop plant species: When, where, how much and so what? Regulatory Toxicology and Pharmacology, 58, S54–S61.

    Article  CAS  PubMed  Google Scholar 

  • DeHaven, C. D., Evans, A. M., Dai, H., & Lawton, K. A. (2010). Organization of GC/MC and LC/MS metabolomics data into chemical libraries. Journal of Cheminformatics, 2, 1–12.

    Article  Google Scholar 

  • DeHaven, C. D., Evans, A. M., Dai H., & Lawton, K. A. (2012). Software techniques for enabling high throughput. In U. Roessner (Ed.), Metabolomics. InTech, Rijeka, pp 167–192. http://www.intechopen.com/books/metabolomics/software-techniques-for-enabling-high-throughput-analysis-on-metabolomic-datasets.

  • Druart, N., Johansson, A., Baba, K., Schrader, J., Sjödin, A., Bhalerao, R. R., et al. (2007). Environmental and hormonal regulation of the activity-dormancy cycle in the cambial meristem involves stage specific modulation of transcriptional and metabolic netwoerks. Plant Journal, 50, 557–573.

    Article  CAS  PubMed  Google Scholar 

  • Ekberg, I., Eriksson, G., & Weng, Y. (1985). Between- and within-population variation in growth rhythm and plant height in four Picea abies populations. Studia Forestalia Suecica, 167, 1–14.

    Google Scholar 

  • El Kayal, W., Allen, C. C. G., Ju, C. J. T., Adams, E. R. I., King-Jones, S., Zaharia, L. I., et al. (2011). Molecular events of apical bud formation in white spruce, Picea glauca. Plant, Cell and Environment, 34, 480–500.

    Article  PubMed  Google Scholar 

  • Erez, A., & Lavee, S. (1968). Naringenin and prunin-flavonoid mhibitors in resting peach buds. Israel Journal of Botany, 17, 35–42.

    Google Scholar 

  • Evans, A. M., DeHaven, C. D., Barrett, T., Mitchell, M., & Milgram, E. (2009). Integrated, nontargeted ultrahigh performance liquid chromatography/electrospray ionization tandem mass spectrometry platform for the identification and relative quantification of the small-molecule complement of biological systems. Analytical Chemistry, 81, 6656–6667.

    Article  CAS  PubMed  Google Scholar 

  • Fiehn, O. (2001). Combining genomics, metabolome analysis, and biochemical modelling to understand metabolic networks. Comparative and Functional Genomics, 2, 155–168.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fiehn, O. (2002). Metabolomics: The link between genotypes and phenotypes. Plant Molecular Biology, 48, 155–171.

    Article  CAS  PubMed  Google Scholar 

  • Gyllenstrand, N., Clapham, D., Källman, T., & Lagercrantz, U. (2007). A Norway spruce FLOWERING LOCUS T homolog is implicated in control of growth rhythm in conifers. Plant Physiology, 144, 248–257.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartigan, J. A., & Wong, M. A. (1979). Algorithm AS 136: A K-means clustering algorithm. Journal of the Royal Statistical Society Series C (Applied Statistics), 28, 100–108.

    Google Scholar 

  • Hoffman, D. E., Jonsson, P., Bylesjö, M. A. X., Trygg, J., Antti, H., Eriksson, M. E., et al. (2010). Changes in diurnal patterns within the Populus transcriptome and metabolome in response to photoperiod variation. Plant, Cell and Environment, 33, 1298–1313.

    CAS  PubMed  Google Scholar 

  • Holliday, J. A., Ralph, S. G., White, R., Bohlmann, J., & Aitken, S. N. (2008). Global monitoring of autumn gene expression within and among phenotypically divergent populations of Sitka spruce (Picea sitchensis). New Phytologist, 178, 103–122.

    Article  CAS  PubMed  Google Scholar 

  • Howe, G. T., Gardner, G., Hackett, W. P., & Furnier, G. R. (1996). Phytochrome control of short-day-induced bud set in black cottonwood. Physiologia Plantarum, 97, 95–103.

    Article  CAS  Google Scholar 

  • Jeandet, P., Douillet-Breuil, A. C., Bessis, R., Debord, S., Sbaghi, M., & Adrian, M. (2002). Phytoalexins from the Vitaceae: Biosynthesis, phytoalexin gene expression in transgenic plants, antifungal activity, and metabolism. Journal of Agricultural and Food Chemistry, 50, 2731–2741.

    Article  CAS  PubMed  Google Scholar 

  • Jones, W. W., Coggins, C. W., & Embleton, T. W. (1976). Endogenous abscisic acid in relation to bud growth in alternate bearing `Valencia’ orange. Plant Physiology, 58, 681–682.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jovanovic, S. V., Steenken, S., Tosic, M., Marjanovic, B., & Simic, M. G. (1994). Flavonoids as antioxidants. Journal of the American Chemical Society, 116, 4846–4851.

    Article  CAS  Google Scholar 

  • Junttila, O. (1976). Apical growth cessation and shoot tip abscission in Salix. Physiologia Plantarum, 38, 278–286.

    Article  CAS  Google Scholar 

  • Karlberg, A., Englund, M., Petterle, A., Molnar, G., Sjodin, A., et al. (2010). Analysis of global changes in gene expression during activity-dormancy cycle in hybrid aspen apex. Plant Biotechnology, 27, 1–16.

    Article  CAS  Google Scholar 

  • Kasuga, J., Arakawa, K., & Fujikawa, S. (2007). High accumulation of soluble sugars in deep supercooling Japanese white birch xylem parenchyma cells. New Phytologist, 174, 569–579.

    Article  CAS  PubMed  Google Scholar 

  • Keeling, C. I., & Bohlmann, J. (2006). Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytologist, 170, 657–675.

    Article  CAS  PubMed  Google Scholar 

  • Khandelwal, A., Cho, S. H., Marella, H., Sakata, Y., Perroud, P.-F., Pan, A., et al. (2010). Role of ABA and ABI3 in desiccation tolerance. Science, 327, 546.

    Article  CAS  PubMed  Google Scholar 

  • Kusano, M., Jonsson, P., Fukushima, A., Gullberg, J., Sjöström, M., Trygg, J., et al. (2011). Metabolite signature during short-day induced growth cessation in Populus. Frontiers in Plant Science, 2, 29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwon, S. H., Kim, J. A., Hong, S. I., Jung, Y. H., Kim, H. C., Lee, S. Y., et al. (2011). Loganin protects against hydrogen peroxide-induced apoptosis by inhibiting phosphorylation of JNK, p38, and ERK 1/2 MAPKs in SH-SY5Y cells. Neurochemistry International, 58, 533–541.

    Article  CAS  PubMed  Google Scholar 

  • Lang, G. A. (1987). Dormancy: A new universal terminology. Horticultural Science, 22, 817–820.

    Google Scholar 

  • MacDonald, J. E., & Owens, J. N. (1993). Bud development in coastal Douglas-fir seedlings under controlled-environment conditions. Canadian Journal of Forest Research, 23, 1203–1212.

    Article  Google Scholar 

  • Martinelli, T., Whittaker, A., Bochicchio, A., Vazzana, C., Suzuki, A., & Masclaux-Daubresse, C. (2007). Amino acid pattern and glutamate metabolism during dehydration stress in the ‘resurrection’ plant Sporobolus stapfianus: A comparison between desiccationsensitive and desiccation-tolerant leaves. Journal of Experimental Botany, 58, 3037–3046.

    Article  CAS  PubMed  Google Scholar 

  • Mølmann, J. A., Asante, D. K., Jensen, J. B., Krane, M. N., Ernstsen, A., Junttila, O., et al. (2005). Low night temperature and inhibition of GA biosynthesis overrides phytochrome action and induce bud set and cold acclimation, but not dormancy in PHYA overexpressors and wild-type of hybrid aspen. Plant, Cell and Environment, 28, 1579–1588.

    Article  Google Scholar 

  • Mølmann, J. A., Junttila, O., Johnsen, Ø., & Olsen, J. E. (2006). Effects of red, far-red and blue light in maintaining growth in latitudinal populations of Norway spruce (Picea abies). Plant, Cell and Environment, 29, 166–172.

    Article  PubMed  Google Scholar 

  • Moritz, T. (1995). Biological activity, identification and quantification of gibberellins in seedlings in Norway spruce (Picea abies) grown under different photoperiods. Physiologia Plantarum, 95, 67–72.

    Article  CAS  Google Scholar 

  • Munné-Bosch, S. (2005). The role of alpha-tocopherol in plant stress tolerance. Journal of Plant Physiology, 162, 743–748.

    Article  PubMed  Google Scholar 

  • Nienstaedt, H. (1967). Chilling requirements in seven Picea species. Silvae Genetica, 16, 65–68.

    Google Scholar 

  • Nishizawa, A., Yabuta, Y., & Shigeoka, S. (2008). Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiology, 147, 1251–1263.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noctor, G., & Foyer, C. H. (1998). Ascorbate and glutathione: Keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology, 49, 249–279.

    Article  CAS  PubMed  Google Scholar 

  • Nystedt, B., Street, N. R., Wetterbom, A., Zuccolo, A., Lin, Y.-C., Scofield, D. G., et al. (2013). The Norway spruce genome sequence and conifer genome evolution. Nature, 497, 579–584.

    Article  CAS  PubMed  Google Scholar 

  • Ögren, E. (1997). Relationship between temperature, respiratory loss of sugar and premature dehardening in dormant Scots pine seedlings. Tree Physiology, 17, 47–51.

    Article  PubMed  Google Scholar 

  • Ohta, T., Masutomi, N., Tsutsui, N., Sakairi, T., Mitchell, M., & Milburn, M. V. (2009). Untargeted metabolomic profiling as an evaluative tool of fenofibrate-induced toxicology in Fischer 344 male rats. Toxicological Pathology, 37, 521–535.

    Article  CAS  Google Scholar 

  • Oliver, M. J., Guo, L., Alexander, D. C., Ryals, J. A., Wone, B. W. M., & Cushman, J. C. (2011). A sister group contrast using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. Plant Cell, 23, 1231–1248.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olsen, J. E. (2010). Light and temperature sensing and signaling in induction of bud dormancy in woody plants. Plant Molecular Biology, 73, 37–47.

    Article  CAS  PubMed  Google Scholar 

  • Olsen, J. E., Jensen, E., Junttila, O., & Moritz, T. (1995a). Photoperiodic control of endogenous gibberellins in seedlings of Salix pentandra. Physiologia Plantarum, 93, 639–644.

    Article  CAS  Google Scholar 

  • Olsen, J. E., Junttila, O., & Moritz, T. (1995b). A localised decrease of GA1 in shoot tips of Salix pentandra seedings precedes cessation of shoot elongation under short photoperiod. Physiologia Plantarum, 95, 627–632.

    Article  CAS  Google Scholar 

  • Olsen, J. E., Junttila, O., & Moritz, T. (1997a). Long-day induced bud break in Salix pentandra is associated with transiently elevated levels of GA1 and gradual increase in indole-3-acetic acid. Plant and Cell Physiology, 38, 536–540.

    Article  CAS  Google Scholar 

  • Olsen, J. E., Junttila, O., Nilsen, J., Eriksson, M. E., Martinussen, I., Olsson, O., et al. (1997b). Ectopic expression of oat phytochrome A in hybrid aspen changes critical daylength for growth and prevents cold acclimatization. The Plant Journal, 12, 1339–1350.

    Article  CAS  Google Scholar 

  • Ophir, R., Pang, X., Halaly, T., Venkateswari, J., Lavee, S., Galbraith, D., et al. (2009). Gene-expression profiling of grape bud response to alternative dormancy-release stimuli expose possible links between impaired mitochondrial activity, hypoxia, ethylene-ABA interplay and cell enlargement. Plant Molecular Biology, 71, 403–423.

    Article  CAS  PubMed  Google Scholar 

  • Owens, J. H., & Molder, M. (1975). Bud development in Sitka spruce. I. Annual growth cycle of vegetative buds and shoots. Canadian Journal of Botany, 54, 313–325.

    Article  Google Scholar 

  • Peñuelas, J., & Sardans, J. (2009). Ecological metabolomics. Chemical Ecology, 25, 305–309.

    Article  Google Scholar 

  • Proctor, P. (1970). Similar functions of yric acid and ascorbate in man? Nature, 228, 868.

    Article  CAS  PubMed  Google Scholar 

  • Punyasiria, P. A. N., Abeysinghea, I. S. B., Kumarb, V., Treutterc, D., Duyd, D., Goschd, C., et al. (2004). Flavonoid biosynthesis in the tea plant Camellia sinensis: Properties of enzymes of the prominent epicatechin and catechin pathways. Archives of Biochemistry and Biophysics, 431, 22–30.

    Article  Google Scholar 

  • Qamaruddin, M., Dormling, I., Ekberg, I., Erikason, G., & Tillberg, E. (1993). Abscisic acid content at defined levels of bud dormancy and frost tolerance in two contrasting populations of Picea abies grown in a phytotron. Physiologia Plantarum, 87, 203–210.

    Article  CAS  Google Scholar 

  • Regier, N., Streb, S., Zeeman, S. C., & Frey, B. (2010). Seasonal changes in starch and sugar content of poplar (Populus deltoides × nigra cv. Dorskamp) and the impact of stem girdling on carbohydrate allocation to roots. Tree Physiology, 30, 979–987.

    Article  CAS  PubMed  Google Scholar 

  • Riedelsheimer, C., Czedik-Eysenberg, A., Grieder, C., Lisec, J., Technow, F., Sulpice, R., et al. (2012a). Genomic and metabolic prediction of complex heterotic traits in hybrid maize. Nature Genetics, 44, 217–220.

    Article  CAS  PubMed  Google Scholar 

  • Riedelsheimer, C., Lisec, J., Czedik-Eysenberg, A., Sulpice, R., Flis, A., Grieder, C., et al. (2012b). Genome-wide association mapping of leaf metabolic profiles for dissecting complex traits in maize. Proceedings of the National Academy of Sciences of the United States of America, 109, 8872–8877.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rohde, A., & Bhalerao, R. P. (2007). Plant dormancy in the perennial context. Trends in Plant Science, 12, 217–223.

    Article  CAS  PubMed  Google Scholar 

  • Rohde, A., Prinsen, E., De Rycke, R., Engler, G., Van Montagu, M., & Boerjan, W. (2002). PtABI3 impinges on the growth and differentiation of embryonic leaves during bud set in poplar. Plant Cell, 14, 1885–1901.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rohde, A., Ruttink, T., Hostyn, V., Sterck, L., Van Driessche, K., & Boerjan, W. (2007). Gene expression during the induction, maintenance, and release of dormancy in apical buds of poplar. Journal of Experimental Botany, 58, 4047–4060.

    Article  CAS  PubMed  Google Scholar 

  • Rutherford, R. S., Meyer, H., Smith, G. S., & Van Staden, J. (1993). Resistance to Eldana saccharina (Lepidoptera:Pyralidea) in sugarcane and some phytochemical correlations. Proceedings of South African Sugar Technologist’s Association, 67, 82–87.

    CAS  Google Scholar 

  • Ruttink, T., Arend, M., Morreel, K., Storme, V., Rombauts, S., Fromm, J., et al. (2007). A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell, 19, 2370–2390.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santarius, K. (1973). The protective effect of sugars on chloroplast membranes during temperature and water stress and its relationship to frost, desiccation and heat resistance. Planta, 113, 105–114.

    Article  CAS  PubMed  Google Scholar 

  • Sardans, J., Peñuelas, J., & Rivas-Ubach, A. (2011). Ecological metabolomics: Overview of current developments and future challenges. Chemoecology, 21, 191–225.

    Article  CAS  Google Scholar 

  • Schaberg, P. G., Snyder, M. C., Shane, J. B., & Donnelly, J. R. (2000). Seasonal patterns of carbohydrate reserves in red spruce seedlings. Tree Physiology, 20(8), 549–555.

    Article  CAS  PubMed  Google Scholar 

  • Shulaev, V., Cortes, D., Miller, G., & Mittler, R. (2008). Metabolomics for plant stress response. Physiologia Plantarum, 132, 199–208.

    Article  CAS  PubMed  Google Scholar 

  • Skrøppa, T. (1982). Genetic variation in growth rhythm characteristics within and between natural populations of Norway spruce. A preliminary report. Silva Fennica, 16, 160–167.

    Google Scholar 

  • Skrøppa, T. (1991). Within-population variation in autumn frost hardiness and its relationship to bud-set and height growth in Picea abies. Scandinavian Journal of Forest Research, 6, 353–363.

    Article  Google Scholar 

  • Smirnoff, N., & Cumbers, Q. J. (1989). Hydroxyl radical scavenging activities of compatible solutes. Phytochemistry, 28, 1057–1060.

    Article  CAS  Google Scholar 

  • Søgaard, G., Johnsen, Ø., Nilsen, J., & Junttila, O. (2008). Climatic control of bud burst in young seedlings of nine provenances of Norway spruce. Tree Physiology, 28, 311–320.

    Article  PubMed  Google Scholar 

  • Steele, C. L., Lewinsohn, E., & Croteau, R. (1995). Induced oleoresin biosynthesis in grand fir as a defense against bark beetles. Proceedings of the National Academy of Sciences of the United States of America, 92, 4164–4168.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Storey, J. D., & Tibshirani, R. (2003). Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences, 100, 9440–9445.

    Article  CAS  Google Scholar 

  • Strimbeck, G. R., Kjellsen, T. D., Schaberg, P. G., & Murakami, P. F. (2008). Dynamics of low-temperature acclimation in temperate and boreal conifer foliage in a mild winter climate. Tree Physiology, 28, 1365–1374.

    Article  PubMed  Google Scholar 

  • Swain, S. M., & Singh, D. P. (2005). Tall tales from sly dwarves: Novel functions of gibberellins in plant development. Trends in Plant Scence, 10, 123–129.

    Article  CAS  Google Scholar 

  • Taji, T., Ohsumi, C., Iuchi, S., Seki, M., Kasuga, M., Kobayashi, M., et al. (2002). Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant Journal, 29, 417–426.

    Article  CAS  PubMed  Google Scholar 

  • Tanino, K., Kalcsits, L., Silim, S., Kendall, E., & Gray, G. (2010). Temperature-driven plasticity in growth cessation and dormancy development in deciduous woody plants: A working hypothesis suggesting how molecular and cellular function is affected by temperature during dormancy induction. Plant Molcular Biology, 73, 49–65.

    Article  CAS  Google Scholar 

  • Turtola, S., Manninen, A.-M., Rikala, R., & Kainulainen, P. (2003). Drought stress alters the concentration of wood terpenoids in Scots Pine and Norway Spruce seedlings. Journal of Chemical Ecology, 29, 1981–1995.

    Article  CAS  PubMed  Google Scholar 

  • Verbruggen, N., & Hermans, C. (2008). Proline accumulation in plants: A review. Amino Acids, 35, 753–759.

    Article  CAS  PubMed  Google Scholar 

  • Walton, E. F., Clark, C. J., & Boldingh, H. L. (1991). Effect of hydrogen cyanamide on amino acid profiles in kiwifruit buds during budbreak. Plant Physiology, 97, 1256–1259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, S. Y., & Faust, M. (1994). Changes in antioxidant system associated with budbreak in ‘Anna’ apple (Malus domestica Borkh.) buds. Journal of the American Soceity of Horticultural Science, 119, 735–741.

    CAS  Google Scholar 

  • Welling, A., Moritz, T., Palva, E. T., & Junttila, O. (2002). Independent activation of cold acclimation by low temperature and short photoperiod in hybrid aspen. Plant Physiology, 129, 1633–1641.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whittaker, A., Martinelli, T., Farrant, J. M., Bochicchio, A., & Vazzana, C. (2007). Sucrose phosphate synthase activity and the co-ordination of carbon partitioning during sucrose and amino acid accumulation in desiccation-tolerant leaf material of the C4 resurrection plant Sporobolus stapfianus during dehydration. Journal of Experimental Botany, 58, 3775–3787.

    Article  CAS  PubMed  Google Scholar 

  • Wiemken, V., & Ineichen, K. (1993). Effect of temperature and photoperiod on the raffinose content of spruce roots. Planta, 190, 387–392.

    Article  CAS  Google Scholar 

  • Wink, M. (2003). Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry, 64, 3–19.

    Article  CAS  PubMed  Google Scholar 

  • Witt, S., Galicia, L., Lisec, J., Cairns, J., Tiessen, A., Araus, J. L., et al. (2012). Metabolic and phenotypic responses of greenhouse-grown maize hybrids to experimentally controlled drought stress. Molecular Plant, 5, 401–417.

    Article  CAS  PubMed  Google Scholar 

  • Wollenweber, E., & Dietz, V. H. (1981). Occurrence and distribution of free flavonoid aglycones in plants. Phytochemistry, 20, 869–932.

    Article  CAS  Google Scholar 

  • Worrall, J., & Mergen, F. (1967). Environmental and genetic control of dormancy in Picea abies. Physiologia Plantarum, 20, 733–745.

    Article  Google Scholar 

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Acknowledgments

The Norwegian Research Council (Grant 191455/V40) and the Norwegian University of Life Sciences are acknowledged for financial support. Thanks to Marit Siira for excellent technical assistance and to Dr. Lars Snipen for advices on cluster analysis.

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  1. Department of Plant Sciences, CERAD, Norwegian University of Life Sciences, P.O. Box 5003, 1432, Aas, Norway

    Yeon Kyeong Lee & Jorunn Elisabeth Olsen

  2. Metabolon, Inc, 617 Davis Dr. Suite 400, Durham, NC, 27713, USA

    Danny Alexander & Jacob Wulff

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Lee, Y.K., Alexander, D., Wulff, J. et al. Changes in metabolite profiles in Norway spruce shoot tips during short-day induced winter bud development and long-day induced bud flush. Metabolomics 10, 842–858 (2014). https://doi.org/10.1007/s11306-014-0646-x

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