The Influence of Biotic and Abiotic Factors on the Production of Secondary Metabolites in Medicinal Plants

Plant Bioactives and Drug Discovery: Principles, Practice, and Perspectives

Volumn , Issue , 2012, Pages 419-452

  Gouvea, Dayana R ^a   Gobbo Neto, Leonardo ^a   Lopes, Norberto P ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Biotic and abiotic, affecting biosynthesis, metabolite accumulation; Biotic, abiotic and secondary metabolites in medicinal plants; Eco physiologic variations on secondary metabolite content; Hydric stress, on secondary metabolite concentration; Rhythmical variations and ontogenesis

Indexed keywords

EID: 84886119525     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781118260005.ch12     Document Type: Chapter

References (200)

1. Lopes, N.P., Kato, M.J., Andrade, E.H.D.A., Maia, J.G.S., Yoshida, M. (1997). Circadian and seasonal variation in the essential oil from Virola surinamensis leaves. Phytochemistry, 46, 689-693.
2. Kuhlmann, F., Muller, C. (2009). Development-dependent effects of UV radiation exposure on broccoli plants and interactions with herbivorous insects. Environmental and Experimental Botany, 66, 61-68.
3. Bennett, R.N., Wallsgrove, R.M. (1994). Secondary metabolites in plant defence mechanisms. New Phytologist, 127, 617-633.
4. Jamieson, M.A., Bowers, M.D. (2010). Iridoid glycoside variation in the invasive plant dalmatian toadflax, Linaria dalmatica (Plantaginaceae), and sequestration by the biological control agent. Calophasia lunula. Journal of Chemical Ecology, 36, 70-79.
5. Gobbo-Neto, L., Lopes, N.P. (2007). Medicinal plants: Factors of influence on the content of secondary metabolites. Quimica Nova, 30, 374-381.
6. Darrow, K., Bowers, M.D. (1997). Phenological and population variation in iridoid glycosides of Plantago lanceolata (Plantaginaceae). Biochemical Systematics and Ecology, 25, 1-11.
7. Bowers, M.D., Stamp, N.E. (1993). Effects of plant-age, genotype, and herbivory on Plantago performance and chemistry. Ecology, 74, 1778-1791.
8. Lindroth, R.L., Hsia, M.T.S., Scriber, J.M. (1987). Seasonal patterns in the phytochemistry of 3 Populus species. Biochemical Systematics and Ecology, 15, 681-686.
9. Holopainen, J.K., Gershenzon, J. (2010). Multiple stress factors and the emission of plant VOCs. Trends in Plant Science, 15, 176-184.
10. Bidart-Bouzat, M.G., Imeh-Nathaniel, A. (2008). Global change effects on plant chemical defenses against insect herbivores. Journal of Integrative Plant Biology, 50, 1339-1354.
11. 3 on forests: Phytochemistry, trophic interactions, and ecosystem dynamics. Journal of Chemical Ecology, 36, 2-21.
12. Evans, W.C., Trease and Evans' Pharmacognosy, W B Saunders Company Ltd., London, 1996.
13. 2 environments on production of carbon-based allelochemicals in Plantago-a test of the carbon nutrient balance hypothesis. American Naturalist, 140, 707-723.
14. Sandermann, H., Ernst, D., Heller, W., Langebartels, C. (1998). Ozone: An abiotic elicitor of plant defence reactions. Trends in Plant Science, 3, 47-50.
15. Betz, G.A., Gerstner, E., Stich, S.,Winkler, B.,Welzl, G., Kremmer, E., Langebartels, C., Heller, W., Sandermann, H., Ernst, D. (2009). Ozone affects shikimate pathway genes and secondary metabolites in saplings of European beech (Fagus sylvatica L.) grown under greenhouse conditions. Trees-Structure and Function, 23, 539-553.
16. Riemer, J., Whittaker, J.B., Air pollution and insect herbivores: Observed interactions and possible mechanisms. In: Bernays, E.A. editor. Insect-Plant Interactions. CRC Press, Boca Raton, FL, 1989, pp. 73-105.
17. He, X.Y., Huang, W., Chen, W., Dong, T., Liu, C.B., Chen, Z.J., Xu, S., Ruan, Y.N. (2009). Changes of main secondary metabolites in leaves of Ginkgo biloba in response to ozone fumigation. Journal of Environmental Sciences-China, 21, 199-203.
18. Chen, F., Liu, C.J., Tschaplinski, T.J., Zhao, N. (2009). Genomics of secondary metabolism in Populus: Interactions with biotic and abiotic environments. Critical Reviews in Plant Sciences, 28, 375-392.
19. Keen, N.T., Taylor, O.C. (1975). Ozone injury in soybeans-isoflavonoid accumulation is related to necrosis. Plant Physiology, 55, 731-733.
20. Rosemann, D., Heller, W., Sandermann, H. (1991). Biochemical-plant responses to ozone: induction of stilbene biosynthesis in scots pine (Pinus sylvestris L) seedlings. Plant Physiology, 97, 1280-1286.
21. Heller, W., Rosemann, D., Osswald, W.F., Benz, B., Schonwitz, R., Lohwasser, K., Kloos, M., Sandermann, H. (1990). Biochemical response of norway spruce (Picea abies (L) Karst) towards 14-month exposure to ozone and acid mist: Effects on polyphenol and monoterpene metabolism. Environmental Pollution, 64, 353-366.
22. 3. Planta, 227, 427-437.
23. Vazquez-Flota, F., Carrillo-Pech, M., Minero-Garcia, Y., Miranda-Ham, M.D. (2004). Alkaloid metabolism in wounded Catharanthus roseus seedlings. Plant Physiology and Biochemistry, 42, 623-628.
24. Cipollini, D.F. (1997).Wind-induced mechanical stimulation increases pest resistance in common bean. Oecologia, 111, 84-90.
25. Wurst, S., Van Dam, N.M., Monroy, F., Biere, A., Van der Putten, W.H. (2008). Intraspecific variation in plant defense alters effects of root herbivores on leaf chemistry and aboveground herbivore damage. Journal of Chemical Ecology, 34, 1360-1367.
26. Zheng, Z.U., Wu, M. (2004). Cadmium treatment enhances the production of alkaloid secondary metabolites in Catharanthus roseus. Plant Science, 166, 507-514.
27. Reymond, P.,Weber, H., Damond, M., Farmer, E.E. (2000). Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell, 12, 707-719.
28. Korth, K.L., Dixon, R.A. (1997). Evidence for chewing insect-specific molecular events distinct from a general wound response in leaves. Plant Physiology, 115, 1299-1305.
29. Neuvonen, S., Haukioja, E., Molarius, A. (1987). Delayed inducible resistance against a leaf-chewing insect in 4 deciduous tree species. Oecologia, 74, 363-369.
30. Waterman, P.G., Mole, S., Extrinsic factors influencing production of secondary metabolites in plants. In: Bernays, E.A. editor. Insect-Plant Interactions. CRS Press, Boca Raton, 1989, pp. 107-134.
31. Baldwin, I.T., Zhang, Z.P., Diab, N., Ohnmeiss, T.E., McCloud, E.S., Lynds, G.Y., Schmelz, E.A. (1997). Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris. Planta, 201, 397-404.
32. Johnson, N.D., Brain, S.A. (1985). The Response of Leaf Resin to Artificial Herbivory in Eriodictyon-Californicum. Biochemical Systematics and Ecology, 13, 5-9.
33. Harborne, J.B., The coevolutionary arms race: Plant defense and animal response. In: Harborne, J.B. editor. Introduction to Ecological Biochemistry. Academic Press Limited, London, 1989, pp. 214-239.
34. Graham, J.S., Hall, G., Pearce, G., Ryan, C.A. (1986). Regulation of synthesis of proteinase inhibitor-I and inhibitor-II messenger-RNAs in leaves of wounded tomato plants. Planta, 169, 399-405.
35. Salisbury, F.B., Ross, C.W., Plant Physiology, Wadsworth Publishing, Belmont, 1991.
36. Hilder, V.A., Gatehouse, A.M.R., Sheerman, S.E., Barker, R.F., Boulter, D. (1987). A novel mechanism of insect resistance engineered into tobacco. Nature, 330, 160-163.
37. Harborne, J.B., Higher plant-lower plant interactions: phytoalexins and phytotoxins. In: Harborne, J.B. editor. Introduction to Ecological Biochemistry. Academic Press Limited, London, 1989, pp. 302-340.
38. Heil, M., Bostock, R.M. (2002). Induced systemic resistance (ISR) against pathogens in the context of induced plant defences. Annals of Botany, 89, 503-512.
39. Opitz, S., Kunert, G., Gershenzon, J. (2008). Increased terpenoid accumulation in cotton (Gossypium hirsutum) foliage is a general wound response. Journal of Chemical Ecology, 34, 508-522.
40. Malcolm, S.B., Zalucki, M.P. (1996). Milkweed latex and cardenolide induction may resolve the lethal plant defence paradox. Entomologia Experimentalis Et Applicata, 80, 193-196.
41. Mccloud, E.S., Tallamy, D.W., Halaweish, F.T. (1995). Squash beetle trenching behavior-Avoidance of cucurbitacin induction or mucilaginous plant sap. Ecological Entomology, 20, 51-59.
42. Schultz, J.C., Baldwin, I.T. (1982). Oak leaf quality declines in response to defoliation by gypsy-moth larvae. Science, 217, 149-150.
43. Osier, T.L., Lindroth, R.L. (2001). Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. Journal of Chemical Ecology, 27, 1289-1313.
44. Yuan, J.S., Kollner, T.G., Wiggins, G., Grant, J., Degenhardt, J., Chen, F. (2008). Molecular and genomic basis of volatile-mediated indirect defense against insects in rice. Plant Journal, 55, 491-503.
45. Evans, W.C., Trease and Evans' Pharmacognosy, WB Saunders Company, London, 1996.
46. Albert, A., Sareedenchai,V., Heller,W., Seidlitz, H.K., Zidorn, C. (2009).Temperature is the key to altitudinal variation of phenolics in Arnica montana L. cv. ARBO. Oecologia, 160, 1-8.
47. Bilger,W., Rolland, M., Nybakken, L. (2007). UV screening in higher plants induced by low temperature in the absence of UV-B radiation. Photochemical & Photobiological Sciences, 6, 190-195.
48. Christie, P.J., Alfenito, M.R., 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.
49. Koeppe, D.E., Rohrbaug, L.M., Rice, E.L., Wender, S.H. (1970). Effect of age and chilling temperatures on concentration of scopolin and caffeoylquinic acids in tobacco. Physiologia Plantarum, 23, 258-266.
50. Grace, S.C., Logan, B.A., Adams,W.W. (1998). Seasonal differences in foliar content of chlorogenic acid, a phenylpropanoid antioxidant, in Mahonia repens. Plant Cell and Environment, 21, 513-521.
51. Wallaart, T.E., Pras, N., Beekman, A.C., Quax, W.J. (2000). Seasonal variation of artemisinin and its biosynthetic precursors in plants of Artemisia annua of different geographical origin: Proof for the existence of chemotypes. Planta Medica, 66, 57-62.
52. Pala-Paul, J., Perez-Alonso, M.J., Velasco-Negueruela, A., Pala-Paul, R., Sanz, J., Conejero, F. (2001). Seasonal variation in chemical constituents of Santolina rosmarinifolia L. ssp rosmarinifolia. Biochemical Systematics and Ecology, 29, 663-672.
53. Spring, O., Bienert, U. (1987). Capitate glandular hairs from sunflower leaves-development, distribution and sesquiterpene lactone content. Journal of Plant Physiology, 130, 441-448.
54. Yamaura, T., Tanaka, S., Tabata, M. (1989). Light-dependent formation of glandular trichomes and monoterpenes in Thyme seedlings. Phytochemistry, 28, 741-744.
55. Briske, D.D., Camp, B.J. (1982). Water-stress increases alkaloid concentrations in threadleaf groundsel (Senecio longilobus). Weed Science, 30, 106-108.
56. Dustin, C.D., Cooperdriver, G.A. (1992). Changes in phenolic production in the hayscented Fern (Dennstaedtia punctilobula) in relation to resource availability. Biochemical Systematics and Ecology, 20, 99-106.
57. Hirata, K., Asada, M., Yatani, E., Miyamoto, K., Miura, Y. (1993). Effects of nearultraviolet light on alkaloid production in Catharanthus roseus plants. Planta Medica, 59, 46-50.
58. Burns, A.E., Gleadow, R.M., Woodrow, I.E. (2002). Light alters the allocation of nitrogen to cyanogenic glycosides in Eucalyptus cladocalyx. Oecologia, 133, 288-294.
59. Morales, L.O., Tegelberg, R., Brosche, M., Keinanen, M., Lindfors, A., Aphalo, P.J. (2010). Effects of solar UV-A and UV-B radiation on gene expression and phenolic accumulation in Betula pendula leaves. Tree Physiology, 30, 923-934.
60. Markham, K.R., Ryan, K.G., Bloor, S.J., Mitchell, K.A. (1998). An increase in the luteolin: apigenin ratio in Marchantia polymorpha on UV-B enhancement. Phytochemistry, 48, 791-794.
61. Dudt, J.F., Shure, D.J. (1994). The influence of light and nutrients on foliar phenolics and insect herbivory. Ecology, 75, 86-98.
62. Jeong, S.T., Goto-Yamamoto, N., Kobayashi, S., Esaka, A. (2004). Effects of plant hormones and shading on the accumulation of anthocyanins and the expression of anthocyanin biosynthetic genes in grape berry skins. Plant Science, 167, 247-252.
63. Pare, P.W., Tumlinson, J.H. (1997). De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiology, 114, 1161-1167.
64. Demkura, P.V., Abdala, G., Baldwin, I.T., Ballare, C.L. (2010). Jasmonate-dependent and -independent pathways mediate specific effects of solar ultraviolet B radiation on leaf phenolics and antiherbivore defense. Plant Physiology, 152, 1084-1095.
65. Waterman, P.G., Mole, S., Why are phenolic compounds so important? In: Waterman, P.G., Mole, S. editors. Analysis of Phenolic Plant Metabolites, Blackwell Scientific Publications, Oxford, UK, 1994, pp. 44-55.
66. Tattini, M., Galardi, C., Pinelli, P., Massai, R., Remorini, D., Agati, G. (2004). Differential accumulation of flavonoids and hydroxycinnamates in leaves of Ligustrum vulgare under excess light and drought stress. New Phytologist, 163, 547-561.
67. Cuadra, P., Harborne, J.B., Waterman, P.G. (1997). Increases in surface flavonols and photosynthetic pigments in Gnaphalium luteo-album in response to UV-B radiation. Phytochemistry, 45, 1377-1383.
68. Markham, K.R., Tanner, G.J., Caasi-Lit, M., Whitecross, M.I., Nayudu, M., Mitchell, K.-A. (1998). Possible protective role for 30, 40-dihydroxyflavones induced by enhanced UV-B in a UV-tolenant rice cultivar. Phytochemistry, 49, 1913-1919.
69. Grace, S.C., Logan, B.A. (2000). Energy dissipation and radical scavenging by the plant phenylpropanoid pathway. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 355, 1499-1510.
70. Delucia, E.H., Day, T.A., Vogelman, T.C. (1992). Ultraviolet-B and visible-light penetration into needles of 2 species of sub-alpine conifers during foliar development. Plant Cell and Environment, 15, 921-929.
71. Alenius, C.M., Vogelmann, T.C., Bornman, J.F. (1995). A 3-dimensional representation of the relationship between penetration ofUV-B radiation andUV-screening pigments in leaves of Brassica napus. New Phytologist, 131, 297-302.
72. Bieza, K., Lois, R. (2001). An Arabidopsis mutant tolerant to lethal ultraviolet-B levels shows constitutively elevated accumulation of flavonoids and other phenolics. Plant Physiology, 126, 1105-1115.
73. Martyn M. Caldwell, R.R., Stephan D. Flint. (1983). Internal filters: Prospects for UV-acclimation in higher plants. Physiologia Plantarum, 58, 445-450.
74. Larson, R.A. (1995). Plant defenses against oxidative stress. Archives of Insect Biochemistry and Physiology, 29, 175-186.
75. Zhang,W.J., Bjorn, L.O. (2009). The effect of ultraviolet radiation on the accumulation of medicinal compounds in plants. Fitoterapia, 80, 207-218.
76. Chappell, J., Hahlbrock, K. (1984). Transcription of plant defense genes in response to UV-light or fungal elicitor. Nature, 311, 76-78.
77. Chappell, J., Hahlbrock, K., Boller, T. (1984). Rapid induction of ethylene biosynthesis in cultured parsley cells by fungal elicitor and its relationship to the induction of phenylalanine ammonia-lyase. Planta, 161, 475-480.
78. Logemann, E., Tavernaro, A., Schulz, W.G., Somssich, I.E., Hahlbrock, K. (2000). UV light selectively coinduces supply pathways from primary metabolism and flavonoid secondary product formation in parsley. Proceedings of the National Academy of Sciences of the United States of America, 97, 1903-1907.
79. Jones, D.H. (1984). Phenylalanine ammonia-lyase-regulation of its induction and its role in plant development. Phytochemistry, 23, 1349-1359.
80. Zucker, M. (1972). Light and Enzymes. Annual Reviewof Plant Physiology, 23, 133-156.
81. Schmelzer, E., Jahnen, W., Hahlbrock, K. (1988). In situ localization of light-induced chalcone synthase messenger-RNA, chalcone synthase, and flavonoid end products in epidermal-cells of Parsley leaves. Proceedings of the National Academy of Sciences of the United States of America, 85, 2989-2993.
82. Bharti, A.K., Khurana, J.P. (1997). Mutants of Arabidopsis as tools to understand the regulation of phenylpropanoid pathway and UVB protection mechanisms. Photochemistry and Photobiology, 65, 765-776.
83. Ioannidis, D., Bonner, L., Johnson, C.B. (2002). UV-B is required for normal development of oil glands in Ocimum basilicum L. (sweet basil). Annals of Botany, 90, 453-460.
84. Voirin, B., Brun, N., Bayet, C. (1990). Effects of daylength on the monoterpene composition of leaves of Mentha x piperita. Phytochemistry, 29, 749-755.
85. Hoft, M., Verpoorte, R., Beck, E. (1996). Growth and alkaloid contents in leaves of Tabernaemontana pachysiphon Stapf (Apocynaceae) as influenced by light intensity, water and nutrient supply. Oecologia, 107, 160-169.
86. Germ, M., Stibilj, V., Kreft, S., Gaberscik, A., Kreft, I. (2010). Flavonoid, tannin and hypericin concentrations in the leaves of St. John's wort (Hypericum perforatum L.) are affected by UV-B radiation levels. Food Chemistry, 122, 471-474.
87. Bazzaz, F.A., Chiariello, N.R., Coley, P.D., Pitelka, L.F. (1987). Allocating resources to reproduction and defense. Bioscience, 37, 58-67.
88. Langebartels C., Schraudner M., Heller W., Ernst D.H.S., Oxidative stress and defense reactions in plants exposed to air pollutants and UV-B radiation. Oxidative Stress in Plants. Taylor & Francis, London, 2002.
89. Gershenzon, J., Maffei, M., Croteau, R. (1989). Biochemical and histochemical-localization of monoterpene biosynthesis in the glandular trichomes of spearmint (Mentha spicata). Plant Physiology, 89, 1351-1357.
90. Blua, M.J., Hanscom, Z., Collier, B.D. (1988). Glucocapparin variability among 4 populations of Isomeris arborea Nutt. Journal of Chemical Ecology, 14, 623-633.
91. Lokar, L.C., Maurich, V., Mellerio, G., Moneghini, M., Poldini, L. (1987). Variation in terpene composition of Artemisia alba in relation to environmental conditions. Biochemical Systematics and Ecology, 15, 327-333.
92. Jung, V., Olsson, E., Caspersen, S., Asp, H., Jensen, P., Alsanius, B.W. (2004). Response of young hydroponically grown tomato plants to phenolic acids. Scientia Horticulturae, 100, 23-37.
93. Ndamba, J., Lemmich, E., Molgaard, P. (1994). Investigation of the diurnal, ontogenic and seasonal variation in the molluscicidal saponin content of Phytolacca dodecandra aqueous berry extracts. Phytochemistry, 35, 95-99.
94. Gray, D.E., Pallardy, S.G., Garrett, H.E., Rottinghaus, G.E. (2003). Acute drought stress and plant age effects on alkamide and phenolic acid content in purple coneflower roots. Planta Medica, 69, 50-55.
95. Zobayed, S.M.A., Afreen, F., Kozai, T. (2007). Phytochemical and physiological changes in the leaves of St. John's wort plants under a water stress condition. Environmental and Experimental Botany, 59, 109-116.
96. Lavoir, A.V., Staudt, M., Schnitzler, J.P., Landais, D., Massol, F., Rocheteau, A., Rodriguez, R., Zimmer, I., Rambal, S. (2009). Drought reduced monoterpene emissions from the evergreen Mediterranean oak Quercus ilex: Results from a throughfall displacement experiment. Biogeosciences, 6, 1167-1180.
97. Gershenzon, J. (1984). Changes in the levels of plant secondary metabolites under water and nutrient stress. Recent Advances in Phytochemistry, 18, 273-320.
98. Cooperdriver, G., Finch, S., Swain, T., Bernays, E. (1977). Seasonal-variation in secondary plant compounds in relation to palatability of Pteridium aquilinum. Biochemical Systematics and Ecology, 5, 177-183.
99. Horner, J.D. (1990). Nonlinear effects of water deficits on foliar tannin concentration. Biochemical Systematics and Ecology, 18, 211-213.
100. Dement, W.A., Mooney, H.A. (1974). Seasonal-variation in production of tannins and cyanogenic glucosides in chaparral shrub, Heteromeles arbutifolia. Oecologia, 15, 65-76.
101. Guinn, G., Eidenbock, M.P. (1982). Catechin and condensed tannin contents of leaves and bolls of cotton in relation to irrigation and boll load. Crop Science, 22, 614-616.
102. Mattson, W.J., Haack, R.A. (1987). The role of drought in outbreaks of plant-eating insects. Bioscience, 37, 110-118.
103. Frischknecht, P.M., Battig, M., Baumann, T.W. (1987). Effect of drought and wounding stress on indole alkaloid formation in Catharanthus roseus. Phytochemistry, 26, 707-710.
104. Medina, E., Olivares, E., Diaz, M. (1986). Water-stress and light-intensity effects on growth and nocturnal acid accumulation in a terrestrial cam bromeliad (Bromelia humilis Jacq) under natural conditions. Oecologia, 70, 441-446.
105. Rivoal, A., Fernandez, C., Lavoir, A.V., Olivier, R., Lecareux, C., Greff, S., Roche, P., Vila, B. (2010). Environmental control of terpene emissions from Cistus monspeliensis L. in natural Mediterranean shrublands. Chemosphere, 78, 942-949.
106. Gavidia, I., PerezBermudez, P. (1997). Cardenolides of Digitalis obscura: The effect of phosphate and manganese on growth and productivity of shoot-tip cultures. Phytochemistry, 45, 81-85.
107. Hagimori, M., Matsumoto, T., Obi, Y. (1983). Studies on the production of Digitalis cardenolides by plant-tissue culture: Effects of mineral salts, initial pH and precursors on digitoxin formation by shoot-forming cultures of Digitalis purpurea L grown in liquidmedia. Agricultural and Biological Chemistry, 47, 565-571.
108. Ohlsson, A.B., Berglund, T. (1989). Effects of high MnSO4 levels on cardenolide accumulation by Digitalis lanata tissue-cultures in light and darkness. Journal of Plant Physiology, 135, 505-507.
109. Roca-Perez, L., Boluda, R., Perez-Bermudez, P. (2004). Soil-plant relationships, micronutrient contents, and cardenolide production in natural populations of Digitalis obscura. Journal of Plant Nutrition and Soil Science-Zeitschrift Fur Pflanzenernahrung Und Bodenkunde, 167, 79-84.
110. Letchamo, W. (1986). Effect of trace-elements on cardiac-glycosides accumulation in Digitalis grandiflora. Planta Medica, 5, 421-421.
111. Costa, D.P., Santos, S.C., Seraphin, J.C., Ferri, P.H. (2009). Seasonal variability of essential oils of Eugenia uniflora leaves. Journal of the Brazilian Chemical Society, 20, 1287-1293.
112. Koricheva, J., Larsson, S., Haukioja, E.,Keinanen, M. (1998). Regulation of woody plant secondary metabolism by resource availability: Hypothesis testing by means of metaanalysis. Oikos, 83, 212-226.
113. Bryant, J.P., Chapin, F.S., Klein, D.R. (1983). Carbon Nutrient Balance of boreal plants in relation to vertebrate herbivory. Oikos, 40, 357-368.
114. Jones, C.G., Hartley, S.E. (1999). A protein competition model of phenolic allocation. Oikos, 86, 27-44.
115. Koricheva, J. (2002). The Carbon-Nutrient Balance Hypothesis is dead; long live the carbon-nutrient balance hypothesis? Oikos, 98, 537-539.
116. Coley, P.D., Bryant, J.P., Chapin, F.S. (1985). Resource availability and plant antiherbivore defense. Science, 230, 895-899.
117. Said-Al Ahl, H.A.H., Meawad, A.A., Abou-Zeid, E.N., Ali, M. (2010). Response of different basil varieties to soil salinity. International Agrophysics, 24, 183-188.
118. Lee, K.T., Yamakawa, T., Kodama, T., Igarashi, Y., Shimomura, K. (1998). Effects of aeration on tropane alkaloid production by transformed root of Atropa belladonna in flask cultures. Journal of Fermentation and Bioengineering, 86, 614-616.
119. Rajaratnam, J.A., Hock, L.I. (1975). Effect of boron nutrition on intensity of red spidermite attack on oil palm seedlings. Experimental Agriculture, 11, 59-63.
120. Laitinen, M.L., Julkunen-Tiitto, R., Rousi, M. (2000). Variation in phenolic compounds within a birch (Betula pendula) population. Journal ofChemical Ecology, 26, 1609-1622.
121. Mabry, T.J. (1973). The chemistry of geographical races. Pure and Applied Chemistry, 34, 377-400.
122. Wilt, F.M., Geddes, J.D., Tamma, R.V., Miller, G.C., Everett, R.L. (1992). Interspecific variation of phenolic concentrations in persistent leaves among 6 taxa from subgenus Tridentatae of Artemisia (Asteraceae). Biochemical Systematics and Ecology, 20, 41-52.
123. Bruni, R., Sacchetti, G. (2009). Factors affecting polyphenol biosynthesis in wild and field grown St. John's wort (Hypericum perforatum L. Hypericaceae/Guttiferae). Molecules, 14, 682-725.
124. Gobbo-Neto, L., Guaratini, T., Pessoa, C., de Moraes, M.O., Costa-Lotufo, L.V., Vieira, R.F., Colepicolo, P., Lopes, N.P. (2010). Differential metabolic and biological profiles of Lychnophora ericoides Mart. (Asteraceae) from different localities in the Brazilian "campos rupestres". Journal of the Brazilian Chemical Society, 21, 750-759.
125. Sobrinho, T.J.S.P., Cardoso, K.C.M., Gomes, T.L.B., Albuquerque, U.P., Amorim, E.L.C. (2009). Analysis of rainfall and edge-effects on flavonoid levels in Bauhinia cheilantha (Bong.) Steud., Fabaceae. Revista Brasileira de Farmacognosia, 19, 740-745.
126. Seemann, A.,Wallner, T., Poschlod, P., Heilmann, J. (2010). Variation of sesquiterpene lactone contents in different Arnica montana populations: Influence of ecological parameters. Planta Medica, 76, 837-842.
127. Carey, D.B.,Wink, M. (1994). Elevational variation of quinolizidine alkaloid contents in a lupine (Lupinus argenteus) of the rocky-mountains. Journal of Chemical Ecology, 20, 849-857.
128. Spitaler, R., Schlorhaufer, P.D., Ellmerer, E.P., Merfort, I., Bortenschlager, S., Stuppner, H., Zidorn, C. (2006). Altitudinal variation of secondary metabolite profiles in flowering heads of Arnica montana cv. ARBO. Phytochemistry, 67, 409-417.
129. Spitaler, R.,Winkler, A., Lins, I., Yanar, S., Stuppner, H., Zidorn, C. (2008). Altitudinal variation of phenolic contents in flowering heads of Arnica montana cv. ARBO:A3-year comparison. Journal of Chemical Ecology, 34, 369-375.
130. Ganzera, M., Guggenberger, M., Stuppner, H., Zidorn, C. (2008). Altitudinal variation of secondary metabolite profiles in flowering heads of Matricaria chamomilla cv. BONA. Planta Medica, 74, 453-457.
131. Zidorn, C. (2010). Altitudinal variation of secondary metabolites in flowering heads of the Asteraceae: Trends and causes. Phytochemistry Reviews, 9, 197-203.
132. Alonso-Amelot, M.E., Oliveros-Bastidas, A., Calcagno-Pisarelli, M.P. (2007). Phenolics and condensed tannins of high altitude Pteridium arachnoideum in relation to sunlight exposure, elevation, and rain regime. Biochemical Systematics and Ecology, 35, 1-10.
133. Zidorn, C., Stuppner, H. (2001). Chemosystematics of taxa from the Leontodon section Oporinia. Biochemical Systematics and Ecology, 29, 827-837.
134. Bachereau, F., Marigo, G., Asta, J. (1998). Effect of solar radiation (UVand visible) at high altitude on CAM-cycling and phenolic compound biosynthesis in Sedum album. Physiologia Plantarum, 104, 203-210.
135. Yang, H.L., Duan, Y.W., Hu, F.Z., Liu, J.Q. (2004). Lack of altitudinal trends in phytochemical constituents of Swertia franchetiana (Gentianaceae). Biochemical Systematics and Ecology, 32, 861-866.
136. Robinson, T. (1974). Metabolism and function of alkaloids in plants. Science, 184, 430-435.
137. Fairbairn, J.W., Suwal, P.N. (1961). The alkaloids of hemlock (Conium maculatum L): Evidence for a rapid turnover of the major alkaloids. Phytochemistry, 1, 38-46.
138. Angelopoulou, D., Demetzos, C., Perdetzoglou, D. (2002). Diurnal and seasonal variation of the essential oil labdanes and clerodanes from Cistus monspeliensis L. leaves. Biochemical Systematics and Ecology, 30, 189-203.
139. Pitarevic, I., Kuftinec, J., Blazevic, N., Kustrak, D. (1984). Seasonal-variation of essential oil yield and composition of Dalmatian sage, Salvia officinalis. Journal of Natural Products, 47, 409-412.
140. Schmidt, T.J., Bomme, U., Alfermann, A.W. (1998). Sesquiterpene lactone content in leaves of in vitro and field cultivated Arnica montana. Planta Medica, 64, 268-270.
141. Yao, L.H., Caffin, N., D'Arcy, B., Jiang,Y.M., Shi, J., Singanusong, R., Liu, X., Datta, N., Kakuda, Y., Xu, Y. (2005). Seasonal variations of phenolic compounds in Australiagrown tea (Camellia sinensis). Journal of Agricultural and Food Chemistry, 53, 6477-6483.
142. Brooks, J.S., Feeny, P. (2004). Seasonal variation in Daucus carota leaf-surface and leaftissue chemical profiles. Biochemical Systematics and Ecology, 32, 769-782.
143. Atkinson, P., Blakeman, J.P. (1982). Seasonal occurrence of an antimicrobial flavanone, sakuranetin, associated with glands on leaves of Ribes nigrum. New Phytologist, 92, 63-74.
144. Wilt, F.M., Miller, G.C. (1992). Seasonal-variation of coumarin and flavonoid concentrations in persistent leaves of Wyoming Big Sagebrush (Artemisia tridentata ssp wyomingensis, Asteraceae). Biochemical Systematics and Ecology, 20, 53-67.
145. Menkovic, N., Savikin-Fodulovic, K., Savin, K. (2000). Chemical composition and seasonal variations in the amount of secondary compounds in Gentiana lutea leaves and flowers. Planta Medica, 66, 178-180.
146. Lobstein, A., Rietschjako, L., Haagberrurier, M., Anton, R. (1991). Seasonal-variations of the flavonoid content from Ginkgo biloba leaves. Planta Medica, 57, 430-433.
147. Clark, L.E., Clark, W.D. (1990). Flavonoid aglycones of the tribe Astereae: Seasonalvariation in leaf exudate flavonoids of Isocoma acradenia (Asteraceae). Biochemical Systematics and Ecology, 18, 145-148.
148. Jalal, M.A.F., Read, D.J., Haslam, E. (1982). Phenolic composition and its seasonalvariation in Calluna vulgaris. Phytochemistry, 21, 1397-1401.
149. Kim, S.K., Sakamoto, I., Morimoto, K., Sakata, M., Yamasaki, K., Tanaka, O. (1981). Seasonal-variation of saponins, sucrose and monosaccharides in cultivated Ginseng roots. Planta Medica, 42, 181-186.
150. Elgorashi, E.E., Drewes, S.E., Van Staden, J. (2002). Organ-to-organ and seasonal variation in alkaloids from Crinum macowanii. Fitoterapia, 73, 490-495.
151. Wu, T.S., Wang, M.L., Wu, P.L. (1996). Seasonal variations of carbazole alkaloids in Murraya euchrestifolia. Phytochemistry, 43, 785-789.
152. Bandopadhyay, J., De, B. (1997). Seasonal variation of strychnine and brucine in vegetative parts of Strychnos nux-vomica. International Journal of Pharmacognosy, 35, 349-353.
153. Roca-Perez, L., Boluda, R., Gavidia, I., Perez-Bermudez, P. (2004). Seasonal cardenolide production and Dop5Br gene expression in natural populations of Digitalis obscura. Phytochemistry, 65, 1869-1878.
154. Salminen, J.P., Ossipov, V., Haukioja, E., Pihlaja, K. (2001). Seasonal variation in the content of hydrolysable tannins in leaves of Betula pubescens. Phytochemistry, 57, 15-22.
155. Osier, T.L., Hwang, S.Y., Lindroth, R.L. (2000). Within-and between-year variation in early season phytochemistry of quaking aspen (Populus tremuloides Michx.) clones. Biochemical Systematics and Ecology, 28, 197-208.
156. Jonasson, S., Bryant, J.P., Chapin, F.S., Andersson, M. (1986). Plant phenols and nutrients in relation to variations in climate and rodent grazing. American Naturalist, 128, 394-408.
157. Feeny, P.P., Bostock, H. (1968). Seasonal changes in tannin content of Oak leaves. Phytochemistry, 7, 871-880.
158. Faini, F., Labbe, C., Coll, J. (1999). Seasonal changes in chemical composition of epicuticular waxes from the leaves of Baccharis linearis. Biochemical Systematics and Ecology, 27, 673-679.
159. Bowers, M.D., Collinge, S.K., Gamble, S.E., Schmitt, J. (1992). Effects of genotype, habitat, and seasonal-variation on iridoid glycoside content of Plantago lanceolata (Plantaginaceae) and the implications for insect herbivores. Oecologia, 91, 201-207.
160. Hogedal, B.D., Molgaard, P. (2000). HPLC analysis of the seasonal and diurnal variation of iridoids in cultivars of Antirrhinum majus. Biochemical Systematics and Ecology, 28, 949-962.
161. Kaplan, M.A.C., Figueiredo, M.R., Gottlieb, O.R. (1983). Variation on cyanogenesis in plants with season and insect pressure. Biochemical Systematics and Ecology, 11, 367.
162. Agerbirk, N., Olsen, C.E., Nielsen, J.K. (2001). Seasonal variation in leaf glucosinolates and insect resistance in two types of Barbarea vulgaris ssp arcuata. Phytochemistry, 58, 91-100.
163. Rodman, J.E., Louda, S.M. (1985). Seasonal flux of isothiocyanate-yielding glucosinolates in roots, stems and leaves of Cardamine cordifolia. Biochemical Systematics and Ecology, 13, 405-412.
164. Pio, C.A., Silva, P.A., Cerqueira, M.A., Nunes, T.V. (2005). Diurnal and seasonal emissions of volatile organic compounds from cork oak (Quercus suber) trees. Atmospheric Environment, 39, 1817-1827.
165. Staudt, M., Mandl, N., Joffre, R., Rambal, S. (2001). Intraspecific variability of monoterpene composition emitted by Quercus ilex leaves. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere, 31, 174-180.
166. Curado, M.A., Oliveira, C.B.A., Jesus, J.G., Santos, S.C., Seraphin, J.C., Ferri, P.H. (2006). Environmental factors influence on chemical polymorphism of the essential oils of Lychnophora ericoides. Phytochemistry, 67, 2363-2369.
167. Southwell, I.A., Bourke, C.A. (2001). Seasonal variation in hypericin content of Hypericum perforatum L. (St. John's wort). Phytochemistry, 56, 437-441.
168. Beek, T.A., Bombardelli, E., Morazzoni, P., Peterlongo, F. (1998). Ginkgo biloba L. Fitoterapia, 59, 195.
169. Beppu, H., Kawai, K., Shimpo, K., Chihara, T., Tamai, I., Ida, C., Ueda, M., Kuzuya, H. (2004). Studies on the components of Aloe arborescens from Japan-monthly variation and differences due to part and position of the leaf. Biochemical Systematics and Ecology, 32, 783-795.
170. Park, M.K., Park, J.H., Kim, N.Y., Shin,Y.G., Choi, Y.S., Lee, J.G., Kim, K.H., Lee, S.K. (1998). Analysis of 13 phenolic compounds in aloe species by high performance liquid chromatography. Phytochemical Analysis, 9, 186-191.
171. Bos, R., Woerdenbag, H.J., van Putten, F.M.S., Hendriks, H., Scheffer, J.C. (1998). Seasonal variation of the essential oil, valerenic acid and derivatives, and valepotriates in Valeriana officinalis roots and rhizomes, and the selection of plants suitable for phytomedicines. Planta Medica, 64, 143-147.
172. Hook, I., Poupat, C., Ahond, A., Guenard, D., Gueritte, F., Adeline, M.T., Wang, X.P., Dempsey, D., Breuillet, S., Potier, P. (1999). Seasonal variation of neutral and basic taxoid contents in shoots of European Yew (Taxus baccata). Phytochemistry, 52, 1041-1045.
173. Vesela, D., Saman, D., Valterova, I., Vanek, T. (1999). Seasonal variations in the content of taxanes in the bark of Taxus baccata L. Phytochemical Analysis, 10, 319-321.
174. Vance, N.C., Kelsey, R.G., Sabin, T.E. (1994). Seasonal and tissue variation in taxane concentrations of Taxus brevifolia. Phytochemistry, 36, 1241-1244.
175. ElSohly, H.N., Croom, E.M., Kopycki, W.J., Joshi, A.S., McChesney, J.D. (1997). Diurnal and seasonal effects on the taxane content of the clippings of certain Taxus cultivars. Phytochemical Analysis, 8, 124-129.
176. Glowniak, K., Mroczek, T., Zobel, A.M. (1999). Seasonal changes in the concentrations of four taxoids in Taxus baccata L. during the autumn-spring period. Phytomedicine, 6, 135-140.
177. Wheeler, N.C., Jech, K., Masters, S., Brobst, S.W., Alvarado, A.B., Hoover, A.J., Snader, K.M. (1992). Effects of genetic, epigenetic, and environmental factors on taxol content in Taxus brevifolia and related species. Journal of Natural Products, 55, 432-440.
178. Silva, M.G.D., Craveiro, A.A., Matos, F.J.A., Machado, M.I.L., Alencar, J.W. (1999). Chemical variation during daytime of constituents of the essential oil of Ocimum gratissimum leaves. Fitoterapia, 70, 32-34.
179. Itenov, K., Molgaard, 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.
180. Fairbairn, J.W., Wassel, G. (1964). The alkaloids of Papaver somniferum L.: Evidence for a rapid turnover of the major alkaloids. Phytochemistry, 3, 253-258.
181. Hendriks, H., AndersonWildeboer, Y., Engels, G., Bos, R., Woerdenbag, H.J. (1997). The content of parthenolide and its yield per plant during the growth of Tanacetum parthenium. Planta Medica, 63, 356-359.
182. Jenks, M.A., Tuttle, H.A., Feldmann, K.A. (1996). Changes in epicuticular waxes on wildtype and Eceriferum mutants in Arabidopsis during development. Phytochemistry, 42, 29-34.
183. Buta, J.G., Spaulding, D.W. (1997). Endogenous levels of phenolics in tomato fruit during growth and maturation. Journal of Plant Growth Regulation, 16, 43-46.
184. Doan, A.T., Ervin, G., Felton, G. (2004). Temporal effects on jasmonate induction of anti-herbivore defense in Physalis angulata: Seasonal and ontogenetic gradients. Biochemical Systematics and Ecology, 32, 117-126.
185. Vogt, T., Gulz, P.G. (1994). Accumulation of flavonoids during leaf development in Cistus laurifolius. Phytochemistry, 36, 591-597.
186. Scora, R.W., Kumamoto, J., Horner, P.F., Hollenberg, J.L. (1984). Ontogenetic variation and diurnal study in the composition of essential oil in Artemisia douglasiana. Journal of Natural Products, 47, 279-284.
187. Wisdom, C.S., Rodriguez, E. (1983). Seasonal age-specific measurements of the sesquiterpene lactones and chromenes of Encelia farinosa. Biochemical Systematics and Ecology, 11, 345-352.
188. Goralka, R.J.L., Schumaker, M.A., Langenheim, J.H. (1996). Variation in chemical and physical properties during leaf development in California Bay Tree (Umbellularia californica): Predictions regarding palatability for deer. Biochemical Systematics and Ecology, 24, 93-103.
189. Slimestad, R. (1998). Amount of flavonols and stilbenes during needle development of Picea abies; variations between provenances. Biochemical Systematics and Ecology, 26, 225-238.
190. Williams, R.D., Ellis, B.E. (1989). Age and tissue distribution of alkaloids in Papaver somniferum. Phytochemistry, 28, 2085-2088.
191. Hoft, M., Verpoorte, R., Beck, E. (1998). Leaf alkaloid contents of Tabernaemontana pachysiphon as influenced by endogenous and environmental factors in the natural habitat. Planta Medica, 64, 148-152.
192. Crankshaw, D.R., Langenheim, J.H. (1981). Variation in terpenes and phenolics through leaf development in Hymenaea and its possible significance to herbivory. Biochemical Systematics and Ecology, 9, 115-124.
193. Palo, R.T., Sunnerheim, K., Theander, O. (1985). Seasonal-variation of phenols, crude protein and cell-wall content of Birch (Betula pendula Roth) in relation to ruminant in vitro digestibility. Oecologia, 65, 314-318.
194. Lilov, D., Angelova, Y. (1987). Changes in the content of some phenolic compounds in connection with flower-formation and fruit-formation of vine. Biologia Plantarum, 29, 34-37.
195. Hartmann, T. (1996). Diversity and variability of plant secondary metabolism: A mechanistic view. Entomologia Experimentalis Et Applicata, 80, 177-188.
196. Hall, G.D., Langenheim, J.H. (1986). Temporal changes in the leaf monoterpenes of Sequoia sempervirens. Biochemical Systematics and Ecology, 14, 61-69.
197. Xenophontos, M., Stavropoulos, E., Avramakis, E., Navakoudis, E., Dornemann, D., Kotzabasis, K. (2007). Influence of the developmental stage on the (proto)hypericin and (proto)pseudohypericin levels of Hypericum plants from Crete. Planta Medica, 73, 1309-1315.
198. Schwob, I., Bessiere, J.M., Masotti, W., Viano, J. (2004). Changes in essential oil composition in Saint John's wort (Hypericum perforatum L.) aerial parts during its phenological cycle. Biochemical Systematics and Ecology, 32, 735-745.
199. Neffati, A., Hennequin, D., Basset, B., Chekir-Ghedira, L., Ghedira, K., Barillier, D., Ledauphin, J. (2009). Influence of growth phase and geographic origin on the essential oil composition of Pituranthos chloranthus from Tunisia. Natural Product Communications, 4, 1585-1594.
200. Maldonado-Lopez, Y., Linares-Mazari, E., Bye, R., Espinosa-Garcia, F.J., Delgado, G. (2008). Mexican arnica anti-inflammatory action: Plant age is correlated with the concentration of anti-inflammatory sesquiterpenes in the medicinal plant Heterotheca inuloides Cass. (Asteraceae). Economic Botany, 62, 161-170.