Abstract
Bilberry is a characteristic field layer species in the boreal forests and is an important forage plant for herbivores of the North European ecosystem. Bilberry leaves contain high levels of phenolic compounds, especially hydroxycinnamic acids, flavonols, catechins, and proanthocyanidins. We investigated the phenolic composition of bilberry leaves in two studies, one following foliar development in forest and open areas, and the other along a wide geographical gradient from south to north boreal forests in Finland. An analysis of bilberry leaves collected in open and forest areas showed that major phenolic changes appeared in the first stages of leaf development, but, most importantly, synthesis and accumulation of flavonoids was delayed in the forest compared to the high light sites. Sampling along a geographical gradient in the boreal zone indicated that leaves from higher latitudes and higher altitudes had greater soluble phenolic and flavonol levels, higher antioxidant capacity, and lower contents of chlorogenic acid derivatives. The ecological significance of the results is discussed.
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Burdulis, D., Ivanauskas, L., Dirsė, V., Kazlauskas, S., and Ražukas, A. 2007. Study of diversity of anthocyanin composition in bilberry (Vaccinium myrtillus L.) fruits. Medicina 43:971–977.
Burnham, K. P., and Anderson, D. R. 2002. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. 2nd edn, p. 488. Springer-Verlag, New York.
Close, D. C., and Mcarthur, C. 2002. Rethinking the role of many plant phenolics—protection from photodamage not herbivores? Oikos 99:166–172.
Coley, P. D., Bryant, J. P., and Chapin, R. S. 1985. Resource availability and plant anti-herbivore defence. Science 230:895–899.
Dixon, R. A., and Paiva, N. L. 1995. Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097.
Dombrowicz, E., Zadernowski, R., and Swiatek, L. 1991. Phenolic acids in leaves of Arctostaphylos uva ursi L., Vaccinium vitis idaea L. and Vaccinium myrtillus L. Pharmazie 46:680–681.
Duncan, A. J., and Poppi, D. P. 2008. Nutritional ecology of grazing and browsing ruminants, pp. 89–116, in I. J. Gordon and H. H. T. Prins (eds.). The Ecology of Browsing and Grazing. Springer-Verlag, Berlin Heidelberg.
Ehlenfeldt, M. K., and Prior, R. L. 2001. Oxygen radical absorbance capacity (ORAC) and phenolic and anthocyanin concentrations in fruit and leaf tissues of highbush blueberry. J. Agric. Food Chem. 49:2222–2227.
Fraisse, D., Carnat, A., and Lamaison, J.-L. 1996. Composition polyphénolique de la feuille de myrtille (Polyphenolic composition of the bilberry leaf). Ann. Pharm. Fr. 54:280–283.
Fritz, C., Palacios-Rojas, N., Feil, R., and Stitt, M. 2006. Regulation of secondary metabolism by the carbon–nitrogen status in tobacco: nitrate inhibits large sectors of phenylpropanoid metabolism. Plant J. 46:533–548.
Grotewold, E. 2006. The genetics and biochemistry of floral pigments. Annu. Rev. Plant Biol. 57:761–780.
Harris, C. S., Burt, A. J., Saleem, A., Le, P. M., Martineau, L. C., Haddad, P. S., Bennett, S. A. L., and Arnason, J. T. 2007. A single HPLC-PAD-APCI/MS method for the quantitative comparison of phenolic compounds found in leaf, stem, root and fruit extracts of Vaccinium angustifolium. Phytochem. Anal. 18:161–169.
Hartmann, U., Sagasser, M., Mehrtens, F., Stracke, R., and Weisshaar, B. 2005. Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Mol. Biol. 57:155–171.
Huang, D., Ou, B., and Prior, R. L. 2005. The chemistry behind antioxidant capacity assays. J. Agric. Food Chem. 53:1841–1856.
Ice, C. H., and Wender, S. H. 1953. Quercetin and its glycosides in leaves of Vaccinium myrtillus. J. Am. Chem. Soc. 75:50–52.
Jaakola, L., Pirttilä, A. M., Halonen, M., and Hohtola, A. 2001. Isolation of high quality RNA from bilberry (Vaccinium myrtillus L.) fruit. Mol. Biotechnol. 19:201–203.
Jaakola, L., Määttä, K., Pirttilä, A. M., Törrönen, R., Kärenlampi, S., and Hohtola, A. 2002. Expression of genes involved in anthocyanin biosynthesis in relation to anthocyanin, proanthocyanidin, and flavonol levels during bilberry fruit development. Plant Physiol. 130:729–739.
Jaakola, L., Määttä-Riihinen, K., Kärenlampi, S., and Hohtola, A. 2004. Activation of flavonoid biosynthesis by solar radiation in bilberry (Vaccinium myrtillus L.) leaves. Planta 218:721–728.
Jäderlund, A., Zackrisson, O., and Nilsson, M.C. 1996. Effects of bilberry (Vaccinium myrtillus L.) litter on seed germination and early seedling growth of four boreal tree species. J. Chem. Ecol. 22:973–986.
Jones, C. G., and Hartley, S. E. 1999. A protein competition model of phenolic allocation. Oikos 86:27–44.
Keski-Saari, S., and Julkunen-Tiitto, R. 2003. Resource allocation in different parts of juvenile mountain birch plants: effect of nitrogen supply on seedling phenolics and growth. Physiol. Plant. 118:114–117.
Koes, R., Verweij, W., and Quattrocchio, F. 2005. Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci. 10:236–242.
Lätti, A. K., Riihinen, K. R., and Kainulainen, P. S. 2008. Analysis of anthocyanin variation in wild populations of bilberry (Vaccinium myrtillus L.) in Finland. J. Agric. Food Chem. 56:190–196.
Lee, J., Durst, R. W., and Wrolstad, R. E. 2005. Determination of total monomeric anthocyanin pigment content of fruit juices, beverages, natural colorants, and wines by the pH differential method: Collaborative study. J. AOAC Int. 88:1269–1278.
Lillo, C., Lea, U. S., and Ruoff, P. 2008. Nutrient depletion as a key factor for manipulating gene expression and product formation in different branches of the flavonoid pathway. Plant Cell Environ. 31:587–601.
Määttä-Riihinen, K. R., Kähkönen, M. P., Törrönen, A. R., and Heinonen, I. M. 2005. Catechins and procyanidins in berries of Vaccinium species and their antioxidant activity. J. Agric. Food Chem. 53:8485–8491.
Mäkitalo, I., Siivari, J., and Hannukkala, A. 2006. Luonnosta teolliseen tuotantoon : Kuvaus luonnontuotealan kehittämishankkeesta Lapissa 2000–2006. Maa- ja elintarviketalous, Jokioinen, 109 p.
Mallik, A. U., and Pelissier, F. 2000. Effects of Vaccinium myrtillus in spruce regeneration: testing the notion of coevoluationary significance of allelopathy. J. Chem. Ecol. 26: 2197–2209.
Martz, F., Peltola, R., Fontanay, S., Duval, R. E., Julkunen-Tiitto, R., and Stark, S. 2009. Effect of latitude and altitude on the terpenoid and soluble phenolic composition of juniper (Juniperus communis) needles and evaluation of their antibacterial activity in the boreal zone. J. Agric. Food Chem. 57:9575–9584.
Matt, P., Krapp, A., Haake, V., Mock, H. P., and Stitt, M. 2002. Decreased Rubisco activity leads to dramatic changes of nitrate metabolism, amino acid metabolism and the levels of phenylpropanoids and nicotine in tobacco antisense RBCS transformants. Plant J. 30:663–677.
Matus, J. T., Loyola, R., Vega, A., Peña-Neira, A., Bordeu, E., Arce-Johnson, P., and Alcalde, J. A. 2009. Post-veraison sunlight exposure induces MYB-mediated transcriptional regulation of anthocyanin and flavonol synthesis in berry skins of Vitis vinifera. J. Exp. Bot. 60:853–867.
Palviainen, M., Finér, L., Mannerkoski, H., Piirainen, S., and Starr, M. 2005. Changes in the above- and below-ground biomass and nutrient pools of ground vegetation after clear-cutting of a mixed boreal forest. Plant Soil 275:157–167.
Rieger, G., Muller, M., Guttenberger, H., and Bucar, F. 2008. Influence of altitudinal variation on the content of phenolic compounds in wild populations of Calluna vulgaris, Sambucus nigra, and Vaccinium myrtillus. J. Agric. Food Chem. 56:9080–9086.
Riihinen, K., Jaakola, L., Kärenlampi, S., and Hohtola, A. 2008. Organ-specific distribution of phenolic compounds in bilberry (Vaccinium myrtillus) and ‘northblue’ blueberry (Vaccinium corymbosum x V. angustifolium). Food Chem. 110:156–160.
Salemaa, M., Derome, J., and Nöjd, P. 2008. Response of boreal forest vegetation to the fertility status of the organic layer along a climatic gradient. Boreal Environ. Res. 13: 48–66.
Stark, S., Julkunen-Tiitto, R., Holappa, E., Mikkola, K., and Nikula, A. 2008. Concentrations of foliar quercetin in natural populations of white birch (Betula pubescens) increase with latitude. J. Chem. Ecol. 34:1382–1391.
Thiel, A. L., and Perakis, S. S. 2009. Nitrogen dynamics across silvicultural canopy gaps in young forests of western Oregon. For. Ecol. Manag. 258:273–287.
Tuomi, J., Niemelä, P., and Siren, S. 1990. The Panglossian paradigm and delayed inducible accumulation of foliar phenolics in mountain birch. Oikos 59: 399–410.
Usadel, B., Bläsing, O. E., Gibon, Y., Poree, F., Höhne, M., Günter, M., Trethewey, R., Kamlage, B., Poorter, H., and Stitt, M. 2008. Multilevel genomic analysis of the response of transcripts, enzyme activities and metabolites in Arabidopsis rosettes to a progressive decrease of temperature in the non-freezing range. Plant Cell Environ. 31:518–547.
Witzell, J., and Shevtsova, A. 2004. Nitrogen-induced changes in phenolics of Vaccinium myrtillus—Implications for interaction with a parasitic fungus. J. Chem. Ecol. 30:1937–1956.
Witzell, J., Gref, R., and Näsholm, T. 2003. Plant-part specific and temporal variation in phenolic compounds of boreal bilberry (Vaccinium myrtillus) plants. Biochem. Syst. Ecol. 31:115–127.
Zhang, Z., Kou, X., Fugal, K., and Mclaughlin J. 2004. Comparison of HPLC methods for determination of anthocyanins and anthocyanidins in bilberry extracts. J. Agric. Food Chem. 52: 688–691.
Acknowledgments
The authors thank K. Mikkola for providing background information for site selection, R. Nielsen and M. Weissman for technical help, and J. Hyvönen for statistical advices. We are indebted to everyone involved in the sampling that was done in connection with the BioSoil project (Finnish Forest Research Institute). This work was supported by the European Commission, Regional Development Fund (project “Mette” number 70025/05), the Lapland Regional Fund of the Finnish Cultural Foundation (to F. M.), the Kone Foundation, Finland (to F. M.), and the Academy of Finland (grant no 09141 to L. J.).
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Martz, F., Jaakola, L., Julkunen-Tiitto, R. et al. Phenolic Composition and Antioxidant Capacity of Bilberry (Vaccinium myrtillus) Leaves in Northern Europe Following Foliar Development and Along Environmental Gradients. J Chem Ecol 36, 1017–1028 (2010). https://doi.org/10.1007/s10886-010-9836-9
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DOI: https://doi.org/10.1007/s10886-010-9836-9