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Only a matter of time: the impact of daily and seasonal rhythms on phytochemicals

  • Donna J. Liebelt
  • Juliette T. Jordan
  • Colleen J. DohertyEmail author
Article

Abstract

Plants regulate molecular bioactivity in response to daily and seasonal environmental fluctuations in temperature, light, humidity, and precipitation. These rhythms interconnect, overlap, and feedback both into each other and into the plant’s endogenous circadian clock. The resulting regulatory network tightly ensures that the overall phytochemical composition is highly adaptive to the plant’s needs at any point in time. Temporally coordinated control of primary and secondary metabolism ensures phytochemicals are in tune with the demands of the environment and the available resources. As a consequence, phytochemical composition varies throughout the day and year. This variation in phytochemical abundance and composition across time can affect experimental results and conclusions. Understanding how phytochemical composition varies across time is critical for uncovering the underlying regulatory connections and ultimately improving the quality of phytochemical products. Herein, we review the mechanisms underlying diel and seasonal variations in phytochemical composition and provide examples of temporal regulation of specific compounds within phenol, terpenoid, and alkaloid phytochemical classes.

Graphic abstract

Temporal regulation of phytochemical composition. The phytochemical composition of a plant is under complex control, affected by both external environmental factors and endogenous circadian rhythms. The environmental factors that directly affect phytochemical profiles and concentrations themselves vary across time of day and time of year. These cyclic environmental factors also entrain the endogenous circadian clock which imposes additional regulation on the production and processing of many phytochemicals. This concerted effort to ensure phytochemicals are exquisitely in tune with the demands of the environment results in fluctuating phytochemical composition. Variation in phytochemical abundance and composition across time can affect experimental results and conclusions. Failing to consider the factors of time of day and year can result in misleading or inconsistent estimations of the potency and composition of phytochemical extractions. Integrating temporal factors will improve our understanding of the underlying regulatory connections and ultimately improve the quality of phytochemical products.

Keywords

Diel Time of day Temporal regulation Circadian rhythms Photoperiod responses Environmental regulation Specialized metabolites Phenols Flavonoids Terpenoids Alkaloids 

Notes

References

  1. Adwan G, Mhanna M (2008) Synergistic effects of plant extracts and antibiotics on Staphylococcus aureus strains isolated from clinical specimens Middle-East. J Sci Res 3(3):134–139.  https://doi.org/10.1155/2015/520578 CrossRefGoogle Scholar
  2. Aftab T, Naeem M, Khan MMA et al (2018) Artemisia annua. Taylor & Francis, Boca Raton.  https://doi.org/10.1201/b22102 CrossRefGoogle Scholar
  3. Aharoni A et al (2003) Terpenoid metabolism in wild-type and transgenic arabidopsis plants. Plant Cell 15:2866–2884CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ahmed S, Stepp JR (2016) Beyond yields: climate change effects on specialty crop quality and agroecological management. Elem Sci Anthr 4:92.  https://doi.org/10.12952/journal.elementa.000092 CrossRefGoogle Scholar
  5. Ahmed S, Unachukwu U, Stepp JR et al (2010) Pu-erh tea tasting in Yunnan, China: correlation of drinkers’ perceptions to phytochemistry. J Ethnopharmacol 132:176–185.  https://doi.org/10.1016/j.jep.2010.08.016 CrossRefPubMedGoogle Scholar
  6. Ahmed S, Stepp JR, Orians C et al (2014) Effects of extreme climate events on tea (Camellia sinensis) functional quality validate indigenous farmer knowledge and sensory preferences in Tropical China. PLoS One.  https://doi.org/10.1371/journal.pone.0109126 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Akula R, Ravishankar GA (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav 6:1720–1731.  https://doi.org/10.4161/psb.6.11.17613 CrossRefGoogle Scholar
  8. Alabadí D, Yanovsky MJ, Más P et al (2002) Critical role for CCA1 and LHY in maintaining circadian rhythmicity in Arabidopsis. Curr Biol 12:757–761.  https://doi.org/10.1016/s0960-9822(02)00815-1 CrossRefPubMedGoogle Scholar
  9. Aninbon C, Jogloy S, Vorasoot N et al (2016) Effect of end of season water deficit on phenolic compounds in peanut genotypes with different levels of resistance to drought. Food Chem 196:123–129.  https://doi.org/10.1016/j.foodchem.2015.09.022 CrossRefPubMedGoogle Scholar
  10. Ariza MT, Martínez-Ferri E, Domínguez P et al (2015) Effects of harvest time on functional compounds and fruit antioxidant capacity in ten strawberry cultivars. J Berry Res 5:71–80.  https://doi.org/10.3233/jbr-150090 CrossRefGoogle Scholar
  11. Asghari G, Houshfar G, Mahmoudi Z, Asghari M (2014) Diurnal variation of essential of the oil components of Pycnocycla spinosa decne. ex boiss. Jundishapur J Nat Pharm Prod 9:35–38.  https://doi.org/10.17795/jjnpp-12229 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Augustijn D, Roy U, Van Schadewijk R et al (2016) Metabolic profiling of intact Arabidopsis thaliana leaves during circadian cycle using 1H high resolution magic angle spinning NMR. PLoS ONE 11:1–17.  https://doi.org/10.1371/journal.pone.0163258 CrossRefGoogle Scholar
  13. Bauer S, Störmer E, Graubaum HJ, Roots I (2001) Determination of hyperforin, hypericin, and pseudohypericin in human plasma using high-performance liquid chromatography analysis with fluorescence and ultraviolet detection. J Chromatogr B Biomed Sci Appl 765:29–35.  https://doi.org/10.1016/s0378-4347(01)00390-5 CrossRefPubMedGoogle Scholar
  14. Belesky DP, Malinowski DP (2016) Grassland communities in the USA and expected trends associated with climate change. Acta Agrobot 69:1–25.  https://doi.org/10.5586/aa.1673 CrossRefGoogle Scholar
  15. Bendix C, Marshall CM, Harmon FG (2015) Circadian clock genes universally control key agricultural traits. Mol Plant 8:1135–1152.  https://doi.org/10.1016/j.molp.2015.03.003 CrossRefPubMedGoogle Scholar
  16. Bernarth J, Tetenyi P (1979) Effect of environmental-factors on growth. Development and alkaloid production of poppy (Papaver somniferum L.): 1. Responses to day-length and light-intensity. Biochem Physiol Pflanz 174:468–478.  https://doi.org/10.1016/s0960-9822(02)00815-1 CrossRefGoogle Scholar
  17. Bhardwaj V, Meier S, Petersen LN et al (2011) Defence responses of Arabidopsis thaliana to infection by Pseudomonas syringae are regulated by the circadian clock. PLoS ONE 6:e26968.  https://doi.org/10.1371/journal.pone.0026968 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Bläsing OE, Gibon Y, Günther M et al (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell Online 17:3257–3281.  https://doi.org/10.1105/tpc.105.035261 CrossRefGoogle Scholar
  19. Borges RM, Bessière JM, Ranganathan Y (2013) Diel variation in fig volatiles across syconium development: making sense of scents. J Chem Ecol 39:630–642.  https://doi.org/10.1007/s10886-013-0280-5 CrossRefPubMedGoogle Scholar
  20. Borges CV, Minatel IO, Gomez-Gomez HA, Lima GPP (2017) Medicinal plants: influence of environmental factors on the content of secondary metabolites. In: Ghorbanpour M, Varma A (eds) Medicinal plants and environmental challenges. Springer, Cham, pp 259–277.  https://doi.org/10.1007/978-3-319-68717-9 CrossRefGoogle Scholar
  21. Botha LE, Prinsloo G, Deutschländer MS (2018) Variations in the accumulation of three secondary metabolites in Euclea undulata Thunb. var. myrtina as a function of seasonal changes. S Afr J Bot 117:34–40.  https://doi.org/10.1016/j.sajb.2018.04.016 CrossRefGoogle Scholar
  22. Bottomley W, Smith H, Galston AW (1966) Flavonoid complexes in Pisum sativum—III.: the effect of light on the synthesis of kaempferol and quercetin complexes. Phytochemistry 5:117–123.  https://doi.org/10.1016/S0031-9422(00)85089-X CrossRefGoogle Scholar
  23. Buzby J, Farah-Wells H, Hyman J (2014) The estimated amount, value, and calories of postharvest food losses at the retail and consumer levels in the United States. USDA Economic Research Service Economic Information Bulletin 121. https://www.ers.usda.gov/webdocs/publications/43833/43680_eib121.pdf
  24. Caldwell MM, Björn LO, Bornman JF et al (1998) Effects of increased solar ultraviolet radiation on terrestrial ecosystems. J Photochem Photobiol B Biol 46:40–52.  https://doi.org/10.1016/s1011-1344(98)00184-5 CrossRefGoogle Scholar
  25. Charron CS, Saxton AM, Sams CE (2005) Relationship of climate and genotype to seasonal variation in the glucosinolate–myrosinase system. I. Glucosinolate content in ten cultivars of Brassica oleracea grown in fall and spring seasons. J Sci Food Agric 85:671–681.  https://doi.org/10.1002/jsfa.1880 CrossRefGoogle Scholar
  26. Chen L, Cao H, Xiao J (2018) 2-Polyphenols: absorption, bioavailability, and metabolomics. In: Galanakis C (ed) Recovery, and Applications CMBT-PP. Woodhead Publishing, Sawston, pp 45–67.  https://doi.org/10.1016/b978-0-12-813572-3.00002-6 CrossRefGoogle Scholar
  27. Cheruiyot EK, Mumera LM, Ng’etich WK et al (2007) Polyphenols as potential indicators for drought tolerance in tea (Camellia sinensis L.). Biosci Biotechnol Biochem 71:2190–2197.  https://doi.org/10.1271/bbb.70156 CrossRefPubMedGoogle Scholar
  28. Christie PJ, Alfenito MR, Walbot V (1994) Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta 194:541–549.  https://doi.org/10.1007/bf00714468 CrossRefGoogle Scholar
  29. Cook D, Fowler S, Fiehn O, Thomashow MF (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc Natl Acad Sci 101:15243–15248.  https://doi.org/10.1073/pnas.0406069101 CrossRefPubMedGoogle Scholar
  30. Copolovici L, Kännaste A, Pazouki L, Niinemets Ü (2012) Emissions of green leaf volatiles and terpenoids from Solanum lycopersicum are quantitatively related to the severity of cold and heat shock treatments. J Plant Physiol 169:664–672.  https://doi.org/10.1016/j.jplph.2011.12.019 CrossRefPubMedGoogle Scholar
  31. Counce PA, Bryant RJ, Bergman CJ et al (2005) Rice milling quality, grain dimensions, and starch branching as affected by high night temperatures. Cereal Chem 82:645–648.  https://doi.org/10.1094/cc-82-0645 CrossRefGoogle Scholar
  32. Covington MF, Maloof JN, Straume M et al (2008) Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol 9:15.  https://doi.org/10.1186/gb-2008-9-8-r130 CrossRefGoogle Scholar
  33. Cvejić JH, Krstonoŝić MA, Bursác M, Miljić U (2017) Polyphenols. Elsevier, Amsterdam.  https://doi.org/10.1016/B978-0-12-805257-0.00007-7 CrossRefGoogle Scholar
  34. Davies PJ (2010) The plant hormones: their nature, occurrence, and functions. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action!. Springer, Dordrecht, pp 1–15.  https://doi.org/10.1007/978-1-4020-2686-7_1 CrossRefGoogle Scholar
  35. Degu A, Hochberg U, Sikron N et al (2014) Metabolite and transcript profiling of berry skin during fruit development elucidates differential regulation between Cabernet Sauvignon and Shiraz cultivars at branching points in the polyphenol pathway. BMC Plant Biol 14:1–20.  https://doi.org/10.1186/s12870-014-0188-4 CrossRefGoogle Scholar
  36. Deharo E, Ginsburg H (2011) Analysis of additivity and synergism in the anti-plasmodial effect of purified compounds from plant extracts. Malar J 10:1–5.  https://doi.org/10.1186/1475-2875-10-s1-s5 CrossRefGoogle Scholar
  37. Desai JS, Sartor RC, Lawas LM et al (2017) Improving gene regulatory network inference by incorporating rates of transcriptional changes. Sci Rep 7:1–12.  https://doi.org/10.1038/s41598-017-17143-1 CrossRefGoogle Scholar
  38. Dodd AN, Toth R, Kevei E et al (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633.  https://doi.org/10.1126/science.1115581 CrossRefPubMedGoogle Scholar
  39. Dong MA, Farré EM, Thomashow MF (2011) Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. Proc Natl Acad Sci 108:7241–7246.  https://doi.org/10.1073/pnas.1103741108 CrossRefPubMedGoogle Scholar
  40. Dou H, Niu G, Gu M, Masabni J (2017) Effects of light quality on growth and phytonutrient accumulation of herbs under controlled environments. Horticulturae 3:36.  https://doi.org/10.3390/horticulturae3020036 CrossRefGoogle Scholar
  41. Dudareva N, Andersson S, Orlova I et al (2005) From the cover: the nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proc Natl Acad Sci 102:933–938.  https://doi.org/10.1073/pnas.0407360102 CrossRefPubMedGoogle Scholar
  42. Easterling DR, Kunkel KE, Arnold JR et al (2017) Precipitation change in the United States. In: Wuebbles DJ, Fahey DW, Hibbard KA et al (eds) Climate science special report: Fourth National Climate Assessment, vol I. Springer. U.S. Global Change Research Program, Washington, DC, pp 207–230.  https://doi.org/10.7930/j0h993cc CrossRefGoogle Scholar
  43. El Senousy AS, Farag MA, Al-Mahdy DA, Wessjohann LA (2014) Developmental changes in leaf phenolics composition from three artichoke cvs. (Cynara scolymus) as determined via UHPLC-MS and chemometrics. Phytochemistry 108:67–76.  https://doi.org/10.1016/j.phytochem.2014.09.004 CrossRefPubMedGoogle Scholar
  44. Elfawal MA, Towler MJ, Reich NG et al (2012) Dried whole plant Artemisia annua as an antimalarial therapy. PLoS ONE 7:e52746.  https://doi.org/10.1371/journal.pone.0052746 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Espinoza C, Degenkolbe T, Caldana C et al (2010) Interaction with diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in Arabidopsis. PLoS One.  https://doi.org/10.1371/journal.pone.0014101 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Fairbairn JW, Suwal PN (1961) The alkaloids of hemlock (Conium maculatum L.) evidence for a rapid turnover of the major alkaloids. Phytochemistry 1:38–46.  https://doi.org/10.1016/s0031-9422(00)82809-5 CrossRefGoogle Scholar
  47. Farré EM, Weise SE (2012) The interactions between the circadian clock and primary metabolism. Curr Opin Plant Biol 15:293–300.  https://doi.org/10.1016/j.pbi.2012.01.013 CrossRefPubMedGoogle Scholar
  48. Fenske MP, Imaizumi T (2016) Circadian rhythms in floral scent emission. Front Plant Sci 7:1–6.  https://doi.org/10.3389/fpls.2016.00462 CrossRefGoogle Scholar
  49. Ferreira JFS, Benedito VA, Sandhu D et al (2018) Seasonal and differential sesquiterpene accumulation in Artemisia annua suggest selection based on both artemisinin and dihydroartemisinic acid may increase artemisinin in planta. Front Plant Sci 9:1–12.  https://doi.org/10.3389/fpls.2018.01096 CrossRefGoogle Scholar
  50. Filichkin SA, Breton G, Priest HD et al (2011) Global profiling of rice and poplar transcriptomes highlights key conserved circadian-controlled pathways and cis-regulatory modules. PLoS One.  https://doi.org/10.1371/journal.pone.0016907 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Flis A, Sulpice R, Seaton DD et al (2016) Photoperiod-dependent changes in the phase of core clock transcripts and global transcriptional outputs at dawn and dusk in Arabidopsis. Plant Cell Environ 39:1955–1981.  https://doi.org/10.1111/pce.12754 CrossRefPubMedGoogle Scholar
  52. Footitt S, Douterelo-Soler I, Clay H, Finch-Savage WE (2011) Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways.  https://doi.org/10.1073/pnas.1116325108 CrossRefGoogle Scholar
  53. Fowler SG, Cook D, Thomashow MF (2005) Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol 137:961–968.  https://doi.org/10.1104/pp.104.058354 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Fujiuchi N, Matoba N, Matsuda R (2016) Environment control to improve recombinant protein yields in plants based on agrobacterium-mediated transient gene expression. Front Bioeng Biotechnol 4:1–6.  https://doi.org/10.3389/fbioe.2016.00023 CrossRefGoogle Scholar
  55. Fukushima A, Kusano M, Nakamichi N et al (2009) Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination. Proc Natl Acad Sci 106:7251–7256.  https://doi.org/10.1073/pnas.0900952106 CrossRefPubMedGoogle Scholar
  56. Ganguli P, Ganguly AR (2016) Space-time trends in U.S. meteorological droughts. J Hydrol Reg Stud 8:235–259.  https://doi.org/10.1016/j.ejrh.2016.09.004 CrossRefGoogle Scholar
  57. Gibon Y, Usadel B, Blaesing OE et al (2006) Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes. Genome Biol 7:R76.  https://doi.org/10.1186/gb-2006-7-8-r76 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Gitau M (2016) Long-term seasonality of rainfall in the southwest Florida Gulf coastal zone. Clim Res 69:93–105.  https://doi.org/10.3354/cr01399 CrossRefGoogle Scholar
  59. Glaubitz U, Erban A, Kopka J et al (2015) High night temperature strongly impacts TCA cycle, amino acid and polyamine biosynthetic pathways in rice in a sensitivity-dependent manner. J Exp Bot 66:6385–6397.  https://doi.org/10.1093/jxb/erv352 CrossRefPubMedPubMedCentralGoogle Scholar
  60. González-Zeas D, Erazo B, Lloret P et al (2019) Linking global climate change to local water availability: limitations and prospects for a tropical mountain watershed. Sci Total Environ 650:2577–2586.  https://doi.org/10.1016/j.scitotenv.2018.09.309 CrossRefPubMedGoogle Scholar
  61. Goodspeed D, Chehab EW, Min-Venditti A et al (2012) Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior. Proc Natl Acad Sci 109:4674–4677.  https://doi.org/10.1073/pnas.1116368109 CrossRefPubMedGoogle Scholar
  62. Goodspeed D, Liu JD, Chehab EW et al (2013) Postharvest circadian entrainment enhances crop pest resistance and phytochemical cycling. Curr Biol 23:1235–1241.  https://doi.org/10.1016/j.cub.2013.05.034 CrossRefPubMedGoogle Scholar
  63. Gouinguene SP, Turlings TCJ (2002) The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol 129:1296–1307.  https://doi.org/10.1104/pp.001941 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Graf A, Schlereth A, Stitt M, Smith AM (2010) Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc Natl Acad Sci 107:9458–9463.  https://doi.org/10.1073/pnas.0914299107 CrossRefPubMedGoogle Scholar
  65. Green RM, Tingay S, Wang Z-Y, Tobin EM (2002) Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant Physiol 129:576–584.  https://doi.org/10.1104/pp.004374 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Greenham K, Guadagno CR, Gehan MA et al (2017) Temporal network analysis identifies early physiological and transcriptomic indicators of mild drought in Brassica rapa. Elife.  https://doi.org/10.7554/elife.29655.001 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Greenway H, Hughes PG, Klepper B (1969) Effects of water deficit on phosphorus nutrition of tomato plants. Physiol Plant 22:199–207.  https://doi.org/10.1111/j.1399-3054.1969.tb07856.x CrossRefGoogle Scholar
  68. Grinevich DO, Desai JS, Stroup KP et al (2019) Novel transcriptional responses to heat revealed by turning up the heat at night. Plant Mol Biol.  https://doi.org/10.1007/s11103-019-00873-3 CrossRefPubMedGoogle Scholar
  69. Guo R, Li W, Wang X et al (2019) Effect of photoperiod on the formation of cherry radish root. Sci Hortic (Amsterdam) 244:193–199.  https://doi.org/10.1016/j.scienta.2018.09.044 CrossRefGoogle Scholar
  70. Gyllenstrand N, Karlgren A, Clapham D et al (2014) No time for spruce: rapid dampening of circadian rhythms in Picea abies (L. Karst). Plant Cell Physiol 55:535–550.  https://doi.org/10.1093/pcp/pct199 CrossRefPubMedGoogle Scholar
  71. Hannah MA, Caldana C, Steinhauser D et al (2010) Combined transcript and metabolite profiling of Arabidopsis grown under widely variant growth conditions facilitates the identification of novel metabolite-mediated regulation of gene expression. Plant Physiol 152:2120–2129.  https://doi.org/10.1104/pp.109.147306 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Harmer S (2010) Plant biology in the fourth dimension. Plant Physiol 154:467–470.  https://doi.org/10.1104/pp.110.161448 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Hasperué JH, Chaves AR, Martínez GA (2011) End of day harvest delays postharvest senescence of broccoli florets. Postharvest Biol Technol 59:64–70.  https://doi.org/10.1016/j.postharvbio.2010.08.005 CrossRefGoogle Scholar
  74. Helmig D, Ortega J, Duhl T et al (2007) Sesquiterpene emissions from pine trees—identifications, emission rates and flux estimates for the contiguous United States. Environ Sci Technol 41:1545–1553.  https://doi.org/10.1021/es0618907 CrossRefPubMedGoogle Scholar
  75. Hernández I, Alegre L, Munné-Bosch S (2004) Drought-induced changes in flavonoids and other low molecular weight antioxidants in Cistus clusii grown under Mediterranean field conditions. Tree Physiol 24:1303–1311.  https://doi.org/10.7554/elife.29655.001 CrossRefPubMedGoogle Scholar
  76. Herranz-López M, Losada-Echeberría M, Barrajón-Catalán E (2018) The multitarget activity of natural extracts on cancer: synergy and xenohormesis. Medicines 6:6.  https://doi.org/10.3390/medicines6010006 CrossRefPubMedCentralGoogle Scholar
  77. Hevia MA, Canessa P, Müller-Esparza H, Larrondo LF (2015) A circadian oscillator in the fungus Botrytis cinerea regulates virulence when infecting Arabidopsis thaliana. Proc Natl Acad Sci 112:8744–8749.  https://doi.org/10.1073/pnas.1508432112 CrossRefPubMedGoogle Scholar
  78. Hirai MY, Klein M, Yano M et al (2005) Elucidation of gene-to-gene and metabolite-to-gene networks in Arabidopsis by integration of metabolomics and transcriptomics. J Biol Chem.  https://doi.org/10.1074/jbc.m502332200 CrossRefPubMedGoogle Scholar
  79. Hirai MY, Yano M, Goodenowe DB et al (2006) Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana. Proc Natl Acad Sci.  https://doi.org/10.1073/pnas.0403218101 CrossRefPubMedGoogle Scholar
  80. Hochberg U, Degu A, Toubiana D et al (2013) Metabolite profiling and network analysis reveal coordinated changes in grapevine water stress response. BMC Plant Biol.  https://doi.org/10.1186/1471-2229-13-184 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Holopainen JK, Virjamo V, Ghimire RP et al (2018) Climate change effects on secondary compounds of forest trees in the northern hemisphere. Front Plant Sci 9:1–10.  https://doi.org/10.3389/fpls.2018.01445 CrossRefGoogle Scholar
  82. Horak E, Farré EM (2015) The regulation of UV-B responses by the circadian clock. Plant Signal Behav 10:1–4.  https://doi.org/10.1080/15592324.2014.1000164 CrossRefGoogle Scholar
  83. Huang ZA, Zhao T, Fan HJ et al (2012) The upregulation of NtAN2 expression at low temperature is required for anthocyanin accumulation in juvenile leaves of Lc-transgenic tobacco (Nicotiana tabacum L.). J Genet Genom 39:149–156.  https://doi.org/10.1016/j.jgg.2012.01.007 CrossRefGoogle Scholar
  84. Huang X, Yao J, Zhao Y et al (2016) Efficient rutin and quercetin biosynthesis through flavonoids-related gene expression in fagopyrum tataricum gaertn. Hairy root cultures with uV-B irradiation. Front Plant Sci 7:1–11.  https://doi.org/10.3389/fpls.2016.00063 CrossRefGoogle Scholar
  85. Hura T, Hura K, Grzesiak S (2008) Contents of total phenolics and ferulic acid, and PAL activity during water potential changes in leaves of maize single-cross hybrids of different drought tolerance. J Agron Crop Sci 194:104–112.  https://doi.org/10.1111/j.1439-037x.2008.00297.x CrossRefGoogle Scholar
  86. Hwang H, Cho M-H, Hahn B-S et al (2011) Proteomic identification of rhythmic proteins in rice seedlings. Biochim Biophys Acta Proteins Proteom 1814:470–479.  https://doi.org/10.1016/j.bbapap.2011.01.010 CrossRefGoogle Scholar
  87. Hykkerud AL, Uleberg E, Hansen E et al (2018) Seasonal and yearly variation of total polyphenols, total anthocyanins and ellagic acid in different clones of cloudberry (Rubus chamaemorus L.). J Appl Bot Food Qual 91:96–102.  https://doi.org/10.5073/jabfq.2018.091.013 CrossRefGoogle Scholar
  88. Ibrahim MA, Mäenpää M, Hassinen V et al (2010) Elevation of night-time temperature increases terpenoid emissions from Betula pendula and Populus tremula. J Exp Bot 61:1583–1595.  https://doi.org/10.1093/jxb/erq034 CrossRefPubMedPubMedCentralGoogle Scholar
  89. Impa SM, Sunoj VSJ, Krassovskaya I et al (2018) Carbon balance and source-sink metabolic changes in winter wheat exposed to high night-time temperature. Plant Cell Environ.  https://doi.org/10.1111/pce.13488 CrossRefGoogle Scholar
  90. Ingle RA, Stoker C, Stone W et al (2015) Jasmonate signalling drives time-of-day differences in susceptibility of Arabidopsis to the fungal pathogen Botrytis cinerea. Plant J 84:937–948.  https://doi.org/10.1111/tpj.13050 CrossRefPubMedPubMedCentralGoogle Scholar
  91. IPCC (2018) Summary for policymakers. In: Masson-Delmotte V, Zhai P, Pörtner HO, Roberts D, Skea J, Shukla PR, Pirani A, Moufouma-Okia W, Péan C, Pidcock R, Connors S, Matthews JBR, Chen Y, Zhou X, Gomis MI, Lonnoy E, Maycock T, Tignor M, Waterfield T (eds) Global warming of 1.5°C. An IPCC special report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. World Meteorological Organization, Geneva, Switzerland. http://ipcc.ch/report/sr15/
  92. Itenov K, Mølgaard P, Nyman U (1999) Diurnal fluctuations of the alkaloid concentration in latex of poppy Papaver somniferum is due to day-night fluctuations of the latex water content. Phytochemistry 52:1229–1234.  https://doi.org/10.1016/s0031-9422(99)00420-3 CrossRefGoogle Scholar
  93. Jaafar HZE, Ibrahim MH, Fakri NFM (2012) Impact of soil field water capacity on secondary metabolites, phenylalanine ammonia-lyase (PAL), maliondialdehyde (MDA) and photosynthetic responses of Malaysian Kacip Fatimah (Labisia pumila Benth). Molecules 17:7305–7322.  https://doi.org/10.3390/molecules17067305 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Jaleel CA, Sankar B, Murali PV et al (2008) Water deficit stress effects on reactive oxygen metabolism in Catharanthus roseus; impacts on ajmalicine accumulation. Colloids Surf B Biointerfaces 62:105–111.  https://doi.org/10.1016/j.colsurfb.2007.09.026 CrossRefPubMedGoogle Scholar
  95. Kanno K, Mae T, Makino A (2009) High night temperature stimulates photosynthesis, biomass production and growth during the vegetative stage of rice plants. Soil Sci Plant Nutr 55:124–131.  https://doi.org/10.1111/j.1747-0765.2008.00343.x CrossRefGoogle Scholar
  96. Kaplan F, Kopka J, Sung DY et al (2007) Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J 50:967–981.  https://doi.org/10.1111/j.1365-313x.2007.03100.x CrossRefPubMedGoogle Scholar
  97. Keggenhoff I, Elizbarashvili M, Amiri-Farahani A, King L (2014) Trends in daily temperature and precipitation extremes over Georgia, 1971–2010. Weather Clim Extrem 4:75–85.  https://doi.org/10.1016/j.wace.2014.05.001 CrossRefGoogle Scholar
  98. Kim SG, Yon F, Gaquerel E et al (2011) Tissue specific diurnal rhythms of metabolites and their regulation during herbivore attack in a native Tobacco, Nicotiana attenuata. PLoS One.  https://doi.org/10.1371/journal.pone.0026214 CrossRefPubMedPubMedCentralGoogle Scholar
  99. Klepper B (1968) Diurnal pattern of water potential in woody plants. Plant Physiol 43:1931.  https://doi.org/10.1104/pp.43.12.1931 CrossRefPubMedPubMedCentralGoogle Scholar
  100. Koda S, Onda Y, Matsui H et al (2017) Diurnal transcriptome and gene network represented through sparse modeling in Brachypodium distachyon. Front Plant Sci 8:1–11.  https://doi.org/10.3389/fpls.2017.02055 CrossRefGoogle Scholar
  101. Kreslavski VD, Los DA, Schmitt FJ et al (2018) The impact of the phytochromes on photosynthetic processes. Biochim Biophys Acta Bioenerg 1859:400–408.  https://doi.org/10.1016/j.bbabio.2018.03.003 CrossRefPubMedGoogle Scholar
  102. Kumar KN, Molini A, Ouarda TBMJ, Rajeevan MN (2017) North Atlantic controls on wintertime warm extremes and aridification trends in the Middle East. Sci Rep 7:1–11.  https://doi.org/10.1038/s41598-017-12430-3 CrossRefGoogle Scholar
  103. Lai AG, Doherty CJ, Mueller-Roeber B et al (2012) Circadian clock-associated 1 regulates ROS homeostasis and oxidative stress responses. Proc Natl Acad Sci 109:17129–17134.  https://doi.org/10.1073/pnas.1209148109 CrossRefPubMedGoogle Scholar
  104. Lavoir AV, Staudt M, Schnitzler JP et al (2009) Drought reduced monoterpene emissions from the evergreen Mediterranean oak Quercus ilex: results from a throughfall displacement experiment. Biogeosciences 6:1167–1180.  https://doi.org/10.5194/bg-6-1167-2009 CrossRefGoogle Scholar
  105. Laza MRC, Sakai H, Cheng W et al (2015) Differential response of rice plants to high night temperatures imposed at varying developmental phases. Agric For Meteorol 209–210:69–77.  https://doi.org/10.1016/j.agrformet.2015.04.029 CrossRefGoogle Scholar
  106. Lee H, Oh IN, Kim J et al (2018) Phenolic compound profiles and their seasonal variations in new red-phenotype head-forming Chinese cabbages. LWT Food Sci Technol 90:433–439.  https://doi.org/10.1016/j.lwt.2017.12.056 CrossRefGoogle Scholar
  107. Leyva A, Jarillo JA, Salinas J, Martinez-Zapater JM (1995) Low temperature induces the accumulation of phenylalanine ammonia-lyase and chalcone synthase mRNAs of Arabidopsis thaliana in a light-dependent manner. Plant Physiol 108:39–46.  https://doi.org/10.1104/pp.108.1.39 CrossRefPubMedPubMedCentralGoogle Scholar
  108. Li H, Chen Z, Hu M et al (2011) Different effects of night versus day high temperature on rice quality and accumulation profiling of rice grain proteins during grain filling. Plant Cell Rep 30:1641–1659.  https://doi.org/10.1007/s00299-011-1074-2 CrossRefPubMedGoogle Scholar
  109. Li H, Lin Y, Chen X et al (2018) Effects of blue light on flavonoid accumulation linked to the expression of miR393, miR394 and miR395 in longan embryogenic calli. PLoS ONE 13:1–22.  https://doi.org/10.1371/journal.pone.0191444 CrossRefGoogle Scholar
  110. Liao K-L, Jones RD, McCarter P et al (2017) A shadow detector for photosynthesis efficiency. J Theor Biol 414:231–244.  https://doi.org/10.1016/j.jtbi.2016.11.027 CrossRefPubMedGoogle Scholar
  111. Linkosalo T, Lechowicz MJ (2006) Twilight far-red treatment advances leaf bud burst of silver birch (Betula pendula). Tree Physiol 26:1249–1256.  https://doi.org/10.1093/treephys/26.10.1249 CrossRefPubMedGoogle Scholar
  112. Liu Y, Fang S, Yang W et al (2018) Light quality affects flavonoid production and related gene expression in Cyclocarya paliurus. J Photochem Photobiol B Biol 179:66–73.  https://doi.org/10.1016/j.jphotobiol.2018.01.002 CrossRefGoogle Scholar
  113. Lobell DB, Ortiz-Monasterio JI (2007) Impacts of day versus night temperatures on spring wheat yields: a comparison of empirical and CERES model predictions in three locations. Agron J 99:469–477.  https://doi.org/10.2134/agronj2006.0209 CrossRefGoogle Scholar
  114. Lombardo S, Pandino G, Mauromicale G et al (2010) Influence of genotype, harvest time and plant part on polyphenolic composition of globe artichoke [Cynara cardunculus L. var. scolymus (L.) Fiori]. Food Chem 119:1175–1181.  https://doi.org/10.1016/j.foodchem.2009.08.033 CrossRefGoogle Scholar
  115. Lu S, Xu R, Jia J et al (2002) Cloning and functional characterization of a β-pinene synthase from Artemisia annua that shows a circadian pattern of expression 1. Plant Physiol 130:477–486.  https://doi.org/10.1104/pp.006544.the CrossRefPubMedPubMedCentralGoogle Scholar
  116. Ma D, Sun D, Wang C et al (2014) Expression of flavonoid biosynthesis genes and accumulation of flavonoid in wheat leaves in response to drought stress. Plant Physiol Biochem 80:60–66.  https://doi.org/10.1016/j.plaphy.2014.03.024 CrossRefPubMedGoogle Scholar
  117. Madar A, Greenfield A, Ostrer H et al (2009) The inferelator 2.0: a scalable framework for reconstruction of dynamic regulatory network models. In: Proceedings of the 31st annual international conference on IEEE engineering in medicine and biology society engineering the future of biomedicine EMBC 2009, pp 5448–5451.  https://doi.org/10.1109/iembs.2009.5334018
  118. Maffei M, Scannerini S (1999) Photomorphogenic and chemical responses to blue light in Mentha piperia. J Essent Oil Res 11:730–738.  https://doi.org/10.1080/10412905.1999.9712007 CrossRefGoogle Scholar
  119. Mallakpour I, Villarini G (2017) Analysis of changes in the magnitude, frequency, and seasonality of heavy precipitation over the contiguous USA. Theor Appl Climatol 130:345–363.  https://doi.org/10.1007/s00704-016-1881-z CrossRefGoogle Scholar
  120. Manivannan A, Soundararajan P, Halimah N et al (2015) Blue LED light enhances growth, phytochemical contents, and antioxidant enzyme activities of Rehmannia glutinosa cultured in vitro. Hortic Environ Biotechnol 56:105–113.  https://doi.org/10.1007/s13580-015-0114-1 CrossRefGoogle Scholar
  121. Mazur SP, Nes A, Wold AB et al (2014) Quality and chemical composition of ten red raspberry (Rubus idaeus L.) genotypes during three harvest seasons. Food Chem 160:233–240.  https://doi.org/10.1016/j.foodchem.2014.02.174 CrossRefPubMedGoogle Scholar
  122. McClung CR (2006) Plant circadian rhythms. Plant Cell 18:792–803.  https://doi.org/10.1105/tpc.106.040980 CrossRefPubMedPubMedCentralGoogle Scholar
  123. McClung CR (2008) Comes a time. Curr Opin Plant Biol 11:514–520.  https://doi.org/10.1016/j.pbi.2008.06.010 CrossRefPubMedGoogle Scholar
  124. McClung CR (2014) Wheels within wheels: new transcriptional feedback loops in the Arabidopsis circadian clock. F1000Prime Rep 6:1–6.  https://doi.org/10.12703/p6-2 CrossRefGoogle Scholar
  125. Michael TP, Mockler TC, Breton G et al (2008) Network discovery pipeline elucidates conserved time-of-day-specific cis-regulatory modules. PLoS Genet.  https://doi.org/10.1371/journal.pgen.0040014 CrossRefPubMedPubMedCentralGoogle Scholar
  126. Mithöfer A, Boland W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450.  https://doi.org/10.1146/annurev-arplant-042110-103854 CrossRefPubMedGoogle Scholar
  127. Mohammed AR, Tarpley L (2009) High nighttime temperatures affect rice productivity through altered pollen germination and spikelet fertility. Agric For Meteorol 149:999–1008.  https://doi.org/10.1016/j.agrformet.2008.12.003 CrossRefGoogle Scholar
  128. Mølmann JAB, Steindal ALH, Bengtsson GB et al (2015) Effects of temperature and photoperiod on sensory quality and contents of glucosinolates, flavonols and vitamin C in broccoli florets. Food Chem 172:47–55.  https://doi.org/10.1016/j.foodchem.2014.09.015 CrossRefPubMedGoogle Scholar
  129. Mouradov A, Spangenberg G (2014) Flavonoids: a metabolic network mediating plants adaptation to their real estate. Front Plant Sci 5:1–16.  https://doi.org/10.3389/fpls.2014.00620 CrossRefGoogle Scholar
  130. Mwimba M, Karapetyan S, Liu L et al (2018) Daily humidity oscillation regulates the circadian clock to influence plant physiology. Nat Commun 9:1–10.  https://doi.org/10.1038/s41467-018-06692-2 CrossRefGoogle Scholar
  131. Naeem M, Aftab T, Masroor M, Khan A (2017) Strategies for enhancing artemisinin production in Artemisia annua under changing environment. In: Ghorbanpour M, Varma A (eds) Medicinal plants and environmental challenges. Springer, Berlin, pp 227–246.  https://doi.org/10.1007/978-3-319-68717-9 CrossRefGoogle Scholar
  132. Ncube B, Finnie JF, Van Staden J (2012) Quality from the field: the impact of environmental factors as quality determinants in medicinal plants. S Afr J Bot 82:11–20.  https://doi.org/10.1016/j.sajb.2012.05.009 CrossRefGoogle Scholar
  133. Nishioka N, Nishimura T, Ohyama K et al (2008) Light quality affected growth and contents of essential oil components of Japanese mint plants. Acta Hortic 797:431–436CrossRefGoogle Scholar
  134. Niu J, Zhang G, Zhang W et al (2017) Anthocyanin concentration depends on the counterbalance between its synthesis and degradation in plum fruit at high temperature. Sci Rep 7:1–16.  https://doi.org/10.1038/s41598-017-07896-0 CrossRefGoogle Scholar
  135. Nozue K, Maloof JN (2006) Diurnal regulation of plant growth. Plant Cell Environ 29:396–408.  https://doi.org/10.1111/j.1365-3040.2005.01489.x CrossRefPubMedGoogle Scholar
  136. Pal I, Anderson BT, Salvucci GD, Gianotti DJ (2013) Shifting seasonality and increasing frequency of precipitation in wet and dry seasons across the U.S. Geophys Res Lett 40:4030–4035.  https://doi.org/10.1002/grl.50760 CrossRefGoogle Scholar
  137. Papadopoulos AP, Hao X (2000) Effects of day and night air temperature on growth, productivity and energy use of long English cucumber. Can J Plant Sci 80:143–150.  https://doi.org/10.4141/P99-021 CrossRefGoogle Scholar
  138. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669.  https://doi.org/10.1146/annurev.ecolsys.37.091305.110100 CrossRefGoogle Scholar
  139. Pavarini DP, Pavarini SP, Niehues M, Lopes NP (2012) Exogenous influences on plant secondary metabolite levels. Anim Feed Sci Technol 176:5–16.  https://doi.org/10.1016/j.anifeedsci.2012.07.002 CrossRefGoogle Scholar
  140. Peng S, Huang J, Sheehy JE et al (2004) Rice yields decline with higher night temperature from global warming. PNAS 101:9971–9975.  https://doi.org/10.1073/pnas.0403720101 CrossRefPubMedGoogle Scholar
  141. Pérez-Schindler J, Kanhere A, Edwards L et al (2017) Exercise and high-fat feeding remodel transcript-metabolite interactive networks in mouse skeletal muscle. Sci Rep 7:1–11.  https://doi.org/10.1038/s41598-017-14081-w CrossRefGoogle Scholar
  142. Piazzolla F, Pati S, Amodio ML, Colelli G (2016) Effect of harvest time on table grape quality during on-vine storage. J Sci Food Agric 96:131–139.  https://doi.org/10.1002/jsfa.7072 CrossRefPubMedGoogle Scholar
  143. Pincemail J, Kevers C, Tabart J et al (2012) Cultivars, culture conditions, and harvest time influence phenolic and ascorbic acid contents and antioxidant capacity of strawberry (Fragaria x ananassa). J Food Sci 77(2):C205–C210.  https://doi.org/10.1111/j.1750-3841.2011.02539.x CrossRefPubMedGoogle Scholar
  144. Plaut Z, Reinhold L (1965) Effect of water stress on 14C sucrose transport in bean plant. Aust J Biol Sci 18:1143–1155.  https://doi.org/10.1071/BI965114 CrossRefGoogle Scholar
  145. Porqueddu C, Ates S, Louhaichi M et al (2016) Grasslands in “Old World” and “New World” Mediterranean-climate zones: past trends, current status and future research priorities. Grass Forage Sci 71:1–35.  https://doi.org/10.1111/gfs.12212 CrossRefGoogle Scholar
  146. Pulice G, Pelaz S, Matías-Hernández L (2016) Molecular farming in Artemisia annua, a promising approach to improve anti-malarial drug production. Front Plant Sci 7:329.  https://doi.org/10.3389/fpls.2016.00329 CrossRefPubMedPubMedCentralGoogle Scholar
  147. Ragusa L, Picchi V, Tribulato A et al (2017) The effect of the germination temperature on the phytochemical content of broccoli and rocket sprouts. Int J Food Sci Nutr 68:411–420.  https://doi.org/10.1080/09637486.2016.1248907 CrossRefPubMedGoogle Scholar
  148. Rahimpour V, Zeng Y, Mannaerts CM, Su Z (2016) Attributing seasonal variation of daily extreme precipitation events across the Netherlands. Weather Clim Extrem 14:56–66.  https://doi.org/10.1016/j.wace.2016.11.003 CrossRefGoogle Scholar
  149. Rai R, Meena RP, Smita SS et al (2011) UV-B and UV-C pre-treatments induce physiological changes and artemisinin biosynthesis in Artemisia annua L.: an antimalarial plant. J Photochem Photobiol B Biol 105:216–225.  https://doi.org/10.1016/j.jphotobiol.2011.09.004 CrossRefGoogle Scholar
  150. Ramakrishna A, Ravishankar GA (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav 6:1720–1731.  https://doi.org/10.4161/psb.6.11.17613 CrossRefPubMedPubMedCentralGoogle Scholar
  151. Rasoanaivo P, Wright CW, Willcox ML, Gilbert B (2011) Whole plant extracts versus single compounds for the treatment of malaria: synergy and positive interactions. Malar J 10:S4.  https://doi.org/10.1186/1475-2875-10-S1-S4 CrossRefPubMedPubMedCentralGoogle Scholar
  152. Reshef N, Agam N, Fait A (2018) Grape berry acclimation to excessive solar irradiance leads to repartitioning between major flavonoid groups. J Agric Food Chem 66:3624–3636CrossRefPubMedGoogle Scholar
  153. Reshef N, Fait A, Agam N (2019) Grape berry position affects the diurnal dynamics of its metabolic profile. Plant Cell Environ.  https://doi.org/10.1111/pce.13522 CrossRefPubMedGoogle Scholar
  154. Ribeiro AF, Andrade EHA, Salimena FRG, Maia JGS (2014) Circadian and seasonal study of the cinnamate chemotype from Lippia origanoides Kunth. Biochem Syst Ecol 55:249–259.  https://doi.org/10.1016/j.bse.2014.03.014 CrossRefGoogle Scholar
  155. Richards JH, Caldwell MM (1987) Hydraulic lift: substantial nocturnal water transport between soil layers by Artemisia tridentata roots. Oecologia 73:486–489.  https://doi.org/10.1007/BF00379405 CrossRefPubMedGoogle Scholar
  156. Robinson T (1974) Metabolism and function of alkaloids in plants. Science 184:430–435.  https://doi.org/10.1126/science.184.4135.430 CrossRefPubMedGoogle Scholar
  157. Roque-Malo S, Kumar P (2017) Patterns of change in high frequency precipitation variability over North America. Sci Rep 7:10853.  https://doi.org/10.1038/s41598-017-10827-8 CrossRefPubMedPubMedCentralGoogle Scholar
  158. Rowan DD, Cao M, Lin-Wang K et al (2009) Environmental regulation of leaf colour in red 35S:PAP1 Arabidopsis thaliana. New Phytol 182:102–115.  https://doi.org/10.1111/j.1469-8137.2008.02737.x CrossRefPubMedGoogle Scholar
  159. Rufty TW, MacKown CT, Volk RJ (1989) Effects of altered carbohydrate availability on whole-plant assimilation of 15NO3 . Plant Physiol 89:457–463.  https://doi.org/10.1104/pp.89.2.457 CrossRefPubMedPubMedCentralGoogle Scholar
  160. Ruts T, Matsubara S, Wiese-Klinkenberg A, Walter A (2012) Diel patterns of leaf and root growth: endogenous rhythmicity or environmental response? J Exp Bot 63:3339–3351.  https://doi.org/10.1093/jxb/err334 CrossRefPubMedGoogle Scholar
  161. Sabzalian MR, Heydarizadeh P, Zahedi M et al (2014) High performance of vegetables, flowers, and medicinal plants in a red-blue LED incubator for indoor plant production. Agron Sustain Dev 34:879–886.  https://doi.org/10.1007/s13593-014-0209-6 CrossRefGoogle Scholar
  162. Sanchez-Castillo M, Blanco D, Tienda-Luna IM et al (2018) A Bayesian framework for the inference of gene regulatory networks from time and pseudo-time series data. Bioinformatics 34:964–970.  https://doi.org/10.1093/bioinformatics/btx605 CrossRefPubMedGoogle Scholar
  163. Sánchez-Rodríguez E, Ruiz JM, Ferreres F, Moreno DA (2011) Phenolic metabolism in grafted versus nongrafted cherry tomatoes under the influence of water stress. J Agric Food Chem 59:8839–8846.  https://doi.org/10.1021/jf201754t CrossRefPubMedGoogle Scholar
  164. Sarker U, Oba S (2018) Drought stress enhances nutritional and bioactive compounds, phenolic acids and antioxidant capacity of Amaranthus leafy vegetable. BMC Plant Biol.  https://doi.org/10.1186/s12870-018-1484-1 CrossRefPubMedPubMedCentralGoogle Scholar
  165. Scheel GL, Daiane E, Rakocevic M et al (2016) Environmental stress evaluation of Coffea arabica L. leaves from spectrophotometric fingerprints by PCA and OSC-PLS-DA. Arab J Chem.  https://doi.org/10.1016/j.arabjc.2016.05.014 CrossRefGoogle Scholar
  166. Selmar D, Kleinwächter M (2013) Influencing the product quality by deliberately applying drought stress during the cultivation of medicinal plants. Ind Crops Prod 42:558–566.  https://doi.org/10.1016/j.indcrop.2012.06.020 CrossRefGoogle Scholar
  167. Sethe BE, Bussell AN, Lye SH et al (2017) Photosensing and thermosensing by phytochrome B require both proximal and distal allosteric features within the dimeric photoreceptor. Sci Rep 7:13648.  https://doi.org/10.1038/s41598-017-14037-0 CrossRefGoogle Scholar
  168. Shah AR, Khan TM, Sadaqat HA, Chatha AA (2011) Alterations in leaf pigments in cotton (Gossypium hirsutum) genotypes subjected to drought stress conditions. Int J Agric Biol 13:902–908Google Scholar
  169. Shallan MA, Hassan HMM, Namich AAM, Ibrahim AA (2012) Effect of sodium niroprusside, putrescine and glycine betaine on alleviation of drought stress in cotton plant. J Agric Environ Sci 12:1252–1265.  https://doi.org/10.5829/idosi.aejaes.2012.12.09.1902 CrossRefGoogle Scholar
  170. Shamloo M, Babawale EA, Furtado A et al (2017) Effects of genotype and temperature on accumulation of plant secondary metabolites in Canadian and Australian wheat grown under controlled environments. Sci Rep 7:1–13.  https://doi.org/10.1038/s41598-017-09681-5 CrossRefGoogle Scholar
  171. Sharam GJ, Turkington R (2005) Diurnal cycle of sparteine production in Lupinus arcticus. Can J Bot.  https://doi.org/10.1139/b05-104 CrossRefGoogle Scholar
  172. Sharkey TD, Wiberley AE, Donohue AR (2008) Isoprene emission from plants: why and how. Ann Bot 101:5–18.  https://doi.org/10.1093/aob/mcm240 CrossRefPubMedGoogle Scholar
  173. Shi W, Yin X, Struik PC et al (2017) High day- and night-time temperatures affect grain growth dynamics in contrasting rice genotypes. J Exp Bot 68:5233–5245.  https://doi.org/10.1093/jxb/erx344 CrossRefPubMedPubMedCentralGoogle Scholar
  174. Shojaie B, Mostajeran A, Ghannadian M (2016) Flavonoid dynamic responses to different drought conditions: amount, type, and localization of flavonols in roots and shoots of Arabidopsis thaliana L. Turk J Biol 40:612–622.  https://doi.org/10.3906/biy-1505-2 CrossRefGoogle Scholar
  175. Singh M, Mas P (2018) A functional connection between the circadian clock and hormonal timing in Arabidopsis. Genes (Basel) 9:567.  https://doi.org/10.3390/genes9120567 CrossRefGoogle Scholar
  176. Singh-Sangwan N, Farooqi AHA, Sangwan RS (1994) Effect of drought stress on growth and essential oil metabolism in lemongrasses. New Phytol 128:173–179.  https://doi.org/10.1111/j.1469-8137.1994.tb04000.x CrossRefGoogle Scholar
  177. Snyder KA, Tartowski SL (2006) Multi-scale temporal variation in water availability: implications for vegetation dynamics in arid and semi-arid ecosystems. J Arid Environ 65:219–234.  https://doi.org/10.1016/j.jaridenv.2005.06.023 CrossRefGoogle Scholar
  178. Soengas P, Cartea ME, Velasco P, Francisco M (2018) Endogenous circadian rhythms in polyphenolic composition induce changes in antioxidant properties in Brassica cultivars. J Agric Food Chem 66:5984–5991.  https://doi.org/10.1021/acs.jafc.8b01732 CrossRefPubMedGoogle Scholar
  179. Soni U, Brar S, Gauttam VK (2015) Effect of seasonal variation on secondary metabolites of medicinal plants. Int J Pharm Sci Res 6:3654–3662.  https://doi.org/10.13040/IJPSR.0975-8232.6(9).3654-62 CrossRefGoogle Scholar
  180. Steindal ALH, Rdven R, Hansen E, Mlmann J (2015) Effects of photoperiod, growth temperature and cold acclimatisation on glucosinolates, sugars and fatty acids in kale. Food Chem 174:44–51.  https://doi.org/10.1016/j.foodchem.2014.10.129 CrossRefPubMedGoogle Scholar
  181. Stitt M, Gibon Y, Lunn JE, Piques M (2007) Multilevel genomics analysis of carbon signalling during low carbon availability: coordinating the supply and utilisation of carbon in a fluctuating environment. Funct Plant Biol 34:526–549.  https://doi.org/10.1071/FP06249 CrossRefGoogle Scholar
  182. Takeuchi T, Newton L, Burkhardt A et al (2014) Light and the circadian clock mediate time-specific changes in sensitivity to UV-B stress under light/dark cycles. J Exp Bot 65:6003–6012.  https://doi.org/10.1093/jxb/eru339 CrossRefPubMedPubMedCentralGoogle Scholar
  183. Tarvainen V, Hakola H, Hellén H et al (2005) Temperature and light dependence of the VOC emissions of Scots pine. Atmos Chem Phys 5:989–998.  https://doi.org/10.5194/acp-5-989-2005 CrossRefGoogle Scholar
  184. Taulavuori K, Hyöky V, Oksanen J et al (2016) Species-specific differences in synthesis of flavonoids and phenolic acids under increasing periods of enhanced blue light. Environ Exp Bot 121:145–150.  https://doi.org/10.1016/j.envexpbot.2015.04.002 CrossRefGoogle Scholar
  185. Taxak AK, Murumkar AR, Arya DS (2014) Long term spatial and temporal rainfall trends and homogeneity analysis in Wainganga basin, Central India. Weather Clim Extrem 4:50–61.  https://doi.org/10.1016/j.wace.2014.04.005 CrossRefGoogle Scholar
  186. Tegelberg R, Julkunen-Tiitto R, Aphalo PJ (2004) Red: far-red light ratio and UV-B radiation: their effects on leaf phenolics and growth of silver birch seedlings. Plant Cell Environ 27:1005–1013.  https://doi.org/10.1111/j.1365-3040.2004.01205.x CrossRefGoogle Scholar
  187. Tye MR, Blenkinsop S, Fowler HJ et al (2016) Simulating multimodal seasonality in extreme daily precipitation occurrence. J Hydrol 537:117–129.  https://doi.org/10.1016/j.jhydrol.2016.03.038 CrossRefGoogle Scholar
  188. Ubi BE, Honda C, Bessho H et al (2006) Expression analysis of anthocyanin biosynthetic genes in apple skin: effect of UV-B and temperature. Plant Sci 170:571–578.  https://doi.org/10.1016/j.plantsci.2005.10.009 CrossRefGoogle Scholar
  189. Ulijasz AT, Vierstra RD (2011) Phytochrome structure and photochemistry: recent advances toward a complete molecular picture. Curr Opin Plant Biol 14:498–506.  https://doi.org/10.1016/j.pbi.2011.06.002 CrossRefPubMedGoogle Scholar
  190. Unal YS, Deniz A, Toros H, Incecik S (2012) Temporal and spatial patterns of precipitation variability for annual, wet, and dry seasons in Turkey. Int J Climatol 32:392–405.  https://doi.org/10.1002/joc.2274 CrossRefGoogle Scholar
  191. Uriu DM, de Almeida Godoy BS, Battirola LD et al (2018) Temporal variation of the total phenolic compounds concentration in Vochysia divergens Pohl. (Vochysiaceae) leaves in the Brazilian pantana L. Rev Árvore.  https://doi.org/10.1590/1806-90882017000300016 CrossRefGoogle Scholar
  192. Ushijima T, Hanada K, Gotoh E et al (2017) Light controls protein localization through phytochrome-mediated alternative promoter selection. Cell 171:1316–1325.e12.  https://doi.org/10.1016/j.cell.2017.10.018 CrossRefPubMedGoogle Scholar
  193. Vallejo F, Toma FA (2003) Total and individual glucosinolate contents in inflorescences of eight broccoli cultivars grown under various climatic and fertilisation. J Sci Food Agric 83:307–313.  https://doi.org/10.1002/jsfa.1320 CrossRefGoogle Scholar
  194. Veit M, Bilger W, Mühlbauer T et al (1996) Diurnal changes in flavonoids. J Plant Physiol 148:478–482.  https://doi.org/10.1016/S0176-1617(96)80282-3 CrossRefGoogle Scholar
  195. Verma N, Shukla S (2015) Impact of various factors responsible for fluctuation in plant secondary metabolites. J Appl Res Med Aromat Planta 2:105–113.  https://doi.org/10.1016/j.jarmap.2015.09.002 CrossRefGoogle Scholar
  196. Vose RS, Easterling DR, Gleason B (2004) Maximum and minimum temperature trends for the Globe: an update through 2004. Geophys Res Lett 32:15.  https://doi.org/10.1029/2005gl024379 CrossRefGoogle Scholar
  197. Wang GY, Shi JL, Ng G et al (2011) Circadian clock-regulated phosphate transporter PHT4; 1 Plays an important role in Arabidopsis defense. Mol Plant 4:516–526.  https://doi.org/10.1093/mp/ssr016 CrossRefPubMedPubMedCentralGoogle Scholar
  198. Weiss J, Terry MI, Martos-Fuentes M et al (2018) Diel pattern of circadian clock and storage protein gene expression in leaves and during seed filling in cowpea (Vigna unguiculata). BMC Plant Biol 18:1–20.  https://doi.org/10.1186/s12870-018-1244-2 CrossRefGoogle Scholar
  199. Welch JR, Vincent JR, Auffhammer M et al (2010) Rice yields in tropical/subtropical Asia exhibit large but opposing sensitivities to minimum and maximum temperatures. PNAS 107:14562–14567.  https://doi.org/10.1073/pnas.1001222107 CrossRefPubMedGoogle Scholar
  200. Wink M, Witte L (1984) Turnover and transport of quinolizidine alkaloids. Diurnal fluctuations of lupanine in the phloem sap, leaves and fruits of Lupinus albus L. Planta 161:519–524.  https://doi.org/10.1007/BF00407083 CrossRefPubMedGoogle Scholar
  201. World Health Organization (2015) Guidelines for the treatment of malaria, 3rd edn. World Health Organization, GenevaGoogle Scholar
  202. Xia J, Chen J, Piao S et al (2014) Terrestrial carbon cycle affected by non-uniform climate warming. Nat Geosci 7:173–180.  https://doi.org/10.1038/ngeo2093 CrossRefGoogle Scholar
  203. Xu C, Zhang Y, Zhu L et al (2011) Influence of growing season on phenolic compounds and antioxidant properties of grape berries from vines grown in subtropical climate. J Agric Food Chem 59:1078–1086.  https://doi.org/10.1021/jf104157z CrossRefPubMedGoogle Scholar
  204. Yang Y, He F, Yu L et al (2007) Influence of drought on oxidative stress and flavonoid production in cell suspension culture of Glycyrrhiza inflata Batal. Yunnan Zhiwu Yanjiu. Z Naturforschung C.  https://doi.org/10.1515/znc-2007-5-615 CrossRefGoogle Scholar
  205. Yang Z, Wang X, Peng X et al (2014) Effect of difference between day and night temperature on nutrients and dry mass partitioning of tomato in climate chamber. Trans Chin Soc Agric Eng 30:138–147.  https://doi.org/10.3969/j.issn.1002-6819.2014.05.018 CrossRefGoogle Scholar
  206. Yang D, Seaton D, Krahmer J et al (2016a) Photoreceptor effects on plant biomass, resource allocation, and metabolic state. PNAS 113:7667–7672.  https://doi.org/10.1073/pnas.1601309113 CrossRefPubMedGoogle Scholar
  207. Yang Z, Li Y, Li P et al (2016b) Effect of difference between day and night temperature on tomato (Lycopersicon esculentum Mill.) root activity and low molecular weight organic acid secretion. Soil Sci Plant Nutr 62:423–431.  https://doi.org/10.1080/00380768.2016.1224449 CrossRefGoogle Scholar
  208. Yang L, Wen KS, Ruan X et al (2018) Response of plant secondary metabolites to environmental factors. Molecules 23:1–26.  https://doi.org/10.3390/molecules23040762 CrossRefGoogle Scholar
  209. Yerushalmi S, Yakir E, Green RM (2011) Circadian clocks and adaptation in Arabidopsis. Mol Ecol 20:1155–1165.  https://doi.org/10.1111/j.1365-294X.2010.04962.x CrossRefPubMedGoogle Scholar
  210. Yin H, Guo HB, Weston DJ et al (2018) Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave. BMC Genom 19:1–16.  https://doi.org/10.1186/s12864-018-4964-7 CrossRefGoogle Scholar
  211. Yoshida K, Oyama-okubo N (2018) An R2R3-MYB transcription factor ODORANT1 regulates fragrance biosynthesis in lilies (Lilium spp.). Mol Breed 28:1–14.  https://doi.org/10.1007/s11032-018-0902-2 CrossRefGoogle Scholar
  212. Zeng L, Wang X, Kang M et al (2017) Regulation of the rhythmic emission of plant volatiles by the circadian clock. Int J Mol Sci 18:1–10.  https://doi.org/10.3390/ijms18112408 CrossRefGoogle Scholar
  213. Ziska LH, Manalo PA (1996) Increasing night temperature can reduce seed set and potential yield of tropical rice. Aust J Plant Physiol 23:791–794.  https://doi.org/10.1071/PP9960791 CrossRefGoogle Scholar
  214. Zobayed SMA, Afreen F, Kozai T (2005) Temperature stress can alter the photosynthetic efficiency and secondary metabolite concentrations in St. John’s wort. Plant Physiol Biochem 43:977–984.  https://doi.org/10.1016/j.plaphy.2005.07.013 CrossRefPubMedGoogle Scholar
  215. Zobayed SMA, Afreen F, Kozai T (2007) Phytochemical and physiological changes in the leaves of St. John’s wort plants under a water stress condition. Environ Exp Bot 59:109–116.  https://doi.org/10.1016/j.envexpbot.2005.10.002 CrossRefGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Molecular and Structural BiochemistryNorth Carolina State UniversityRaleighUSA

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