Skip to main content
SpringerLink
Log in

Seasonal variation of natural products in European trees

  • Published:
Phytochemistry Reviews Aims and scope Submit manuscript

Abstract

The present review gives an overview about the status of research on seasonal variation of natural products in European trees. Due to their different life forms, gymnosperms, deciduous angiosperms, and evergreen angiosperms are reviewed separately. Besides trying to give an overview about the existing newer literature, the review tries to define some repetitively found trends and discusses some possible explanations for these trends. Moreover, open research questions are highlighted and some suggestions for future studies are given. These suggestions encompass both subjects and desirable quality standards with regards to experimental designs. The reviewed publications are mainly focused on leaves, some on fruits, and some on barks and twigs. Phenolics, including phenolic acids and flavonoids of different types as well as tannins, are the most often studied compound class; additionally, some papers assess seasonal variation of alkaloids, diterpenes, essential oils, lignans, simple organic acid, secoiridoids, and stilbenoids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Albert A, Sareedenchai V, Heller W, Seidlitz HK, Zidorn C (2009) Temperature is the key to altitudinal variation of phenolics in Arnica montana L cv. ARBO. Oecologia 160:1–8

    Article  PubMed  Google Scholar 

  • Amaral JS, Valentão P, Andrade PB, Martins RC, Seabra RM (2010) Phenolic composition of hazelnut leaves: influence of cultivar, geographical origin and ripening stage. Sci Hortic 126:306–313

    Article  CAS  Google Scholar 

  • Awad MA, de Jager A, van der Plas LHW, van der Krol AR (2001) Flavonoid and chlorogenic acid changes in skin of ‘Elstar’ and ‘Jonagold’ apples during development and ripening. Sci Hortic 90:69–83

    Article  CAS  Google Scholar 

  • Beltrán G, Aguilera MP, Del Rio C, Sanchez S, Martinez L (2005) Influence of fruit ripening process on the natural antioxidant content of Hojiblanca virgin olive oils. Food Chem 89:207–215

    Article  CAS  Google Scholar 

  • Bernal M, Llorens L, Julkunen-Tiitto R, Badosa J, Verdaguer D (2013) Altitudinal and seasonal changes of phenolic compounds in Buxus sempervirens leaves and cuticles. Plant Physiol Biochem 70:471–482

    Article  PubMed  CAS  Google Scholar 

  • Blasi F, Urbani E, Simonetti MS, Chiesi C, Cossignani L (2016) Seasonal variation in antioxidant compounds of Olea europaea leaves collected from different Italian cultivars. J Appl Bot Food Qual 89:202–207

    CAS  Google Scholar 

  • Brossa R, Casals I, Pintó-Marijuan Fleck I (2009) Leaf flavonoid content in Quercus ilex L. resprouts and its seasonal variation. Trees 23:401–408

    Article  CAS  Google Scholar 

  • Carey DB, Wink M (1994) Elevational variation of quinolizidine alkaloid contents in a lupine (Lupinus argenteus) of the Rocky Mountains. J Chem Ecol 20:849–857

    Article  PubMed  CAS  Google Scholar 

  • Chaves N, Escudero JC, Guitérrez-Merino C (1993) Seasonal variation of exudate of Cistus ladanifer. J Chem Ecol 19:2577–2591

    Article  PubMed  CAS  Google Scholar 

  • Cosmulescu S, Trandafir I, Nour V (2014) Seasonal variation of the main individual phenolics and juglone in walnut (Juglans regia) leaves. Pharm Biol 52:575–580

    Article  PubMed  CAS  Google Scholar 

  • Evergetis E, Michaelakis A, Papachristos DP, Badieritakis E, Kapsaski-Kanelli VN, Haroutounian SA (2016) Seasonal variation and bioactivity of the essential oils of two Juniperus species against Aedes (Stegomya) albopictus (Skuse, 1894). Parasitol Res 115:2175–2183

    Article  PubMed  CAS  Google Scholar 

  • Falasca A, Melck D, Paris D, Saviano G, Motta A, Iorizzi M (2014) Seasonal changes in the metabolomic fingerprint of Juniperus communis L. berry extract by 1H NMR-based metabolomics. Metabolomics 10:165–174

    Article  CAS  Google Scholar 

  • Fischbach RJ, Staudt M, Zimmer I, Rambal S, Schnitzler J-P (2002) Seasonal pattern of monoterpene synthase activities in leaves of the evergreen tree Quercus ilex. Physiol Plant 114:354–360

    Article  PubMed  CAS  Google Scholar 

  • Förster N, Ulrichs C, Zander M, Kätzel R, Mewis I (2010) Factors influencing the variability of antioxidative phenolic glycosides in Salix species. J Agric Food Chem 58:8205–8210

    Article  PubMed  CAS  Google Scholar 

  • Frédérich M, Marcowycz A, Cieckiewicz E, Mégalizzi V, Angenot L, Kiss LR (2009) In vitro anticancer potential of tree extracts from the Walloon Region forest. Planta Med 75:1634–1637

    Article  PubMed  Google Scholar 

  • Ganthaler A, Stöggl W, Kranner I, Mayr S (2017) Foliar phenolic compounds in Norway spruce with varying susceptibility to Chrysomyxa rhododendri: analyses of seasonal and infection-induced accumulation patterns. Front Plant Sci 8:1173

    Article  PubMed  PubMed Central  Google Scholar 

  • Gobbo-Neto L, Lopes NP (2007) Plantas medicinais: fatores de influência no conteúdo de metabólitos secundários. Quim Nova 30:374–381

    Article  CAS  Google Scholar 

  • Haukioja E (2003) Putting the insect into the birch–insect interaction. Oecologia 136:161–168

    Article  PubMed  Google Scholar 

  • Hofmann T, Nebehaj E, Levente A (2016) Antioxidant properties and detailed polyphenol profiling of European hornbeam (Carpinus betulus L.) leaves by multiple antioxidant capacity assays and high-performance liquid chromatography/multistage electrospray mass spectrometry. Ind Crops Prod 87:340–349

    Article  CAS  Google Scholar 

  • Holubová P, Šmejkal K (2011) Changes in the level of bioactive compounds in Paulownia tomentosa fruits. J Liq Chromatogr 34:276–288

    Article  CAS  Google Scholar 

  • Holzke C, Hoffmann T, Jaeger L, Koppmann R, Zimmer W (2006) Diurnal and seasonal variation of monoterpene and sesquiterpene emissions from Scots pine (Pinus sylvestris L.). Atmos Environ 40:3174–3185

    Article  CAS  Google Scholar 

  • Hook I, Poupat C, Ahond A, Guénard D, Guéritte 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

    Article  CAS  Google Scholar 

  • Knutti R, Rogelj J, Sedláček J, Fischer EM (2016) A scientific critique of the two-degree climate change target. Nat Geosci 9:13–18

    Article  CAS  Google Scholar 

  • Laitinen M-L, Julkunen-Tiitto R, Rousi M (2002) Foliar phenolic composition of European white birch during bud unfolding and leaf development. Physiol Plant 114:450–460

    Article  PubMed  CAS  Google Scholar 

  • Lang KJ (1989) Die Zusammensetzung der Monoterpen-Fraktion in Zweigen von Larix decidua und L. kaempferi in Abhängigkeit von Jahreszeit und Provenienz. Phyton 29:23–32

    CAS  Google Scholar 

  • Liimatainen J, Karonen M, Sinkkonen J, Helander M, Salminen J-P (2012) Phenolic compounds of the inner bark of Betula pendula: seasonal and genetic variation and induction by wounding. J Chem Ecol 38:1410–1418

    Article  PubMed  CAS  Google Scholar 

  • Martins ANC, Simeonov SP, Frija LMT, Viveiros R, Lourenço A, da Silva MS, Casimiro T, Afonso CAM (2014) Isolation, analytical quantification and seasonal variation of labdanolic acid from the Portuguese-grown Cistus ladaniferus. Ind Crop Prod 60:226–232

    Article  CAS  Google Scholar 

  • Mert C, Barut E, İpek A (2013) Qualitative seasonal changes in the leaf phenolic content related to the alternate-bearing patterns of olive (Olea europaea L. cv. Gemlik). J Agric Sci Tech 15:995–1006

    CAS  Google Scholar 

  • Nenadis N, Llorens L, Koufogianni A, Diaz L, Font J, Gonzalez JA, Verdaguer D (2015) Interactive effects of UV radiation and reduced precipitation on the seasonal leaf phenolic content/composition and the antioxidant activity of naturally growing Arbutus unedo plants. J Photochem Photobiol B 153:435–444

    Article  PubMed  CAS  Google Scholar 

  • Nerg A, Kainulainen P, Vuorinen M, Hanso M, Holopainen JK, Kurkela T (1994) Seasonal and geographical variation of terpenes, resin acids and total phenolics in nursery grown seedlings of Scots pine (Pinus sylvestris L.). New Phytol 128:703–713

    Article  CAS  Google Scholar 

  • Oliveira AP, Pereira JA, Andrade PA, Valentão P, Seabra RM, Silva BM (2008) Organic acids composition of Cydonia oblonga Miller leaf. Food Chem 111:393–399

    Article  PubMed  CAS  Google Scholar 

  • Ossipov V, Loponen J, Ossipova S, Haukioja E, Pihlaja K (1997) Gallotannins of birch Betula pubescens leaves: HPLC separation and quantification. Biochem Syst Ecol 25:493–504

    Article  CAS  Google Scholar 

  • Raal A, Boikova T, Püssa T (2015) Content and dynamics of polyphenols in Betula spp. leaves naturally growing in Estonia. Rec Nat Prod 9:41–48

    Google Scholar 

  • Rehwald A, Meier B, Sticher O (1994) Qualitative and quantitative reversed-phase high-performance liquid chromatography of flavonoids in Crataegus leaves and flowers. J Chromatogr A 677:25–33

    Article  CAS  Google Scholar 

  • Salminen J-P, Roslin T, Karonen M, Sinkkonen J, Pihlaja K, Pulkkinen P (2004) Seasonal variation in the content of hydrolyzable tannins, flavonoid glycosides, and proanthocyanidins in oak leaves. J Chem Ecol 30:1693–1711

    Article  PubMed  CAS  Google Scholar 

  • Slimestad R (1998) Amount of flavonols and stilbenes during needle development of Picea abies; variations between provenances. Biochem Syst Ecol 26:225–238

    Article  CAS  Google Scholar 

  • Solar A, Colarič M, Usenik V, Stampar F (2006) Seasonal variations of selected flavonoids, phenolic acids and quinones in annual shoots of common walnut (Juglans regia L.). Plant Sci 170:453–461

    Article  CAS  Google Scholar 

  • Sommavilla V, Haidacher-Gasser D, Sgarbossa M, Zidorn C (2012) Seasonal variation in phenolics in leaves of Celtis australis (Cannabaceae). Biochem Syst Ecol 41:110–114

    Article  CAS  Google Scholar 

  • Stermitz FR, Tawara JN, Boeckl M, Pomeroy M, Foderaro TA, Todd FG (1994) Pteridine alkaloid content of Picea (Spruce) and Pinus (Pine). Phytochemistry 35:951–953

    Article  CAS  Google Scholar 

  • Szentesi Á, Wink M (1991) Fate of quinolizidine alkaloids through three trophic levels: Laburnum anagyroides (Leguminosae) and associated organisms. J Chem Ecol 17:1557–1573

    Article  PubMed  CAS  Google Scholar 

  • ThePlantList (2018) The plant list. A working list of all plant species. www.theplantlist.org. Accessed on 22 Feb 2018

  • Vagiri M, Conner S, Stewart D, Andersson SC, Verral S, Johansson E, Rumpunen K (2015a) Phenolic compounds in black currant (Ribes nigrum L.) leaves relative to leaf position and harvest date. Food Chem 172:135–142

    Article  PubMed  CAS  Google Scholar 

  • Vagiri M, Ekholm A, Johansson E, Andersson SC, Rumpunen K (2015b) Major phenolic compounds in black currant (Ribes nigrum L.) buds: variation due to genotype, ontogenetic stage and location. LWT Food Sci Tech 63:1274–1280

    Article  CAS  Google Scholar 

  • Valkama E, Salminen J-P, Koricheva J, Pihlaja K (2003) Comparative analysis of leaf trichome structure and composition of epicuticular flavonoids in Finnish birch species. Ann Bot 91:643–655

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Valkama E, Salminen J-P, Koricheva J, Pihlaja K (2004) Changes in leaf trichomes and epicuticular flavonoids during leaf development in three birch taxa. Ann Bot 94:233–242

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Veselá D, Šaman D, Valterová I, Vaněk T (1999) Seasonal variations in the content of taxanes in the bark of Taxus baccata L. Phytochem Anal 10:319–321

    Article  Google Scholar 

  • Virjamo V, Julkunen-Tiitto R (2014) Shoot development of Norway spruce (Picea abies) involves changes in piperidine alkaloids and condensed tannins. Trees 28:427–437

    Article  CAS  Google Scholar 

  • Wam HK, Stolter C, Nybakken L (2017) Compositional changes in foliage phenolics with plant age, a natural experiment in boreal forests. J Chem Ecol 43:920–928

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wiesneth S, Aas G, Heilmann J, Jürgenliemk G (2018) Investigation of the flavan-3-ol patterns in willow species during one growing season. Phytochemistry 145:26–39

    Article  PubMed  CAS  Google Scholar 

  • Yang W, Alanne A-L, Liu P, Kallio H, Yang B (2015) Flavonol glycosides in currant leaves and variation with growth season, growth location, and leaf position. J Agric Food Chem 63:9269–9276

    Article  PubMed  CAS  Google Scholar 

  • Zidorn C (2010) Altitudinal variation of phenolics contents in flowering heads of the Asteraceae family. Phytochem Rev 9:197–203

    Article  CAS  Google Scholar 

  • Zidorn C, Schubert B, Stuppner H (2005) Altitudinal differences in the contents of phenolics in flowering heads of three members of the tribe Lactuceae (Asteraceae) occurring as introduced species in New Zealand. Biochem Syst Ecol 33:855–872

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Thanks are due to Britta von der Heydt (Kiel) for logistic support. Special thanks go to Dr Serhat Sezai Çiçek (Kiel) and Dr Moira Madeo (Kiel and Malonno) for critical feedback on earlier versions of this manuscript.

Author information

Authors and Affiliations

  1. Pharmazeutisches Institut, Abteilung Pharmazeutische Biologie, Christian-Albrechts-Universität zu Kiel, Gutenbergstraße 76, 24118, Kiel, Germany

    Christian Zidorn

Authors
  1. Christian Zidorn
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christian Zidorn.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zidorn, C. Seasonal variation of natural products in European trees. Phytochem Rev 17, 923–935 (2018). https://doi.org/10.1007/s11101-018-9570-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11101-018-9570-4

Keywords

Search

Navigation