Skip to main content
SpringerLink
Log in

Variation in Birch (Betula pendula) Shoot Secondary Chemistry due to Genotype, Environment, and Ontogeny

  • Original Article
  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Plant secondary chemistry is determined by both genetic and environmental factors, and large intraspecific variation in secondary chemistry has frequently been reported. The heritability of specific tree secondary metabolites is, however, mostly unknown. We tested the effect of plant genotype, environment, and ontogeny on the variation in shoot secondary chemistry of juvenile and mature European white birches (Betula pendula). Phenolic compounds and triterpenoids were analyzed in 30 naturally regenerated 20-year-old parental trees and micropropagated plantlets that originated from 14 of those same parental trees, planted at four growing sites. Most of the variation for phenolic compounds was explained by differences between parental trees, whereas triterpenoids had a high variation both between parental trees and within the canopy of individual tree. The effect of ontogeny was strong for some individual compounds. In mature trees, the amount of triterpenoids was less than 1 mg/g (DW), whereas the concentration in juvenile plantlets was up to 64 mg/g (DW). Clonal plantlets and parental trees were generally quite similar in their phenolic contents, but there were significant differences for all analyzed compounds among clones. Environment had no significant effect on the accumulation of some compounds, whereas for others, a significant environmental effect and/or significant genotype by environment interaction was found. These results suggest that birch shoot secondary chemistry is under strong genetic control and that the environmental effects depend on the studied chemical trait.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • J. P. Bryant R. Julkunen-Tiitto (1995) ArticleTitleOntogenic development of chemical defence by seedling resin birch: Energy cost of defence production J. Chem. Ecol. 21 883–896 Occurrence Handle1:CAS:528:DyaK2MXnvV2jsLs%3D

    CAS  Google Scholar 

  • J. P. Bryant F. S. Chapin SuffixIII D. R. Klein (1983) ArticleTitleCarbon/nutrient balance of boreal plants in relation to vertebrate herbivory Oikos 40 357–368 Occurrence Handle1:CAS:528:DyaL3sXltVahsr0%3D

    CAS  Google Scholar 

  • Dickerson, G. 1969. Techniques for research in quantitative animal genetics, pp. 138–147, in Techniques and Procedures in Animal Science Research. Am. Soc. Anim. Sci., Albany, NY.

  • J. R. Dugle (1966) ArticleTitleA taxonomic study of western Canadian species in the genus Betula Can. J. Bot. 44 929–1006

    Google Scholar 

  • D. S. FALCONER (1989) Introduction to Quantitative Genetics EditionNumber3 Longman Group Ltd New York

    Google Scholar 

  • A. E. Hagerman M. E. Rice N. T. Ritchard (1998) ArticleTitleMechanisms of protein precipitation for two tannins, pentagalloyl glucose and epicatechin16 (4→8) catechin (procyanidin) J. Agric. Food Chem. 46 2590–2595 Occurrence Handle10.1021/jf971097k Occurrence Handle1:CAS:528:DyaK1cXkt1Wgsr0%3D

    Article  CAS  Google Scholar 

  • J. Hakulinen (1998) ArticleTitleNitrogen-induced reduction in leaf phenolic level is not accompanied by increased rust frequency in a compatible willow (Salix myrcinifolia)–Melampora rust interaction Physiol. Plant. 102 101–110 Occurrence Handle10.1034/j.1399-3054.1998.1020114.x Occurrence Handle1:CAS:528:DyaK1cXhslOrsbY%3D

    Article  CAS  Google Scholar 

  • J. HAKULINEN R. JULKUNEN-TIITTO J. TAHVANAINEN (1995) ArticleTitleDoes nitrogen fertilization have an impact on the trade-off between willow growth and defensive secondary metabolism? Trees 9 235–240 Occurrence Handle10.1007/BF00195278

    Article  Google Scholar 

  • J. G. HAMILTON A. R. ZANGERL E. H. DELUCIA M. R. BERENBAUM (2001) ArticleTitleThe carbon–nutrient balance hypothesis: its rise and fall Ecol. Lett. 4 86–95 Occurrence Handle10.1046/j.1461-0248.2001.00192.x

    Article  Google Scholar 

  • J. W. HANOVER (1966) ArticleTitleGenetics of terpenes. I. Gene control of monoterpene levels in Pinus monticola Dougl. Heredity 21 73–84 Occurrence Handle1:CAS:528:DyaF28XkvVCisbc%3D

    CAS  Google Scholar 

  • D. A. HERMS W. J. MATTSON (1992) ArticleTitleThe dilemma of plants: to grow or defend Q. Rev. Biol. 67 283–335 Occurrence Handle10.1086/417659

    Article  Google Scholar 

  • C. G. JONES S. E. HARTLEY (1999) ArticleTitleA protein competition model of phenolic allocation Oikos 86 27–44 Occurrence Handle1:CAS:528:DyaK1MXkslOgu7c%3D

    CAS  Google Scholar 

  • R. JULKUNEN-TIITTO M. ROUSI J. BRYANT S. SORSA M. KEINÄNEN H. SIKANEN (1996) ArticleTitleChemical diversity of several Betulaceae species: comparison of phenolics and terpenoids in northern birch stems Trees 11 16–22

    Google Scholar 

  • M. KEINÄNEN R. JULKUNEN-TIITTO (1998) ArticleTitleHigh-performance liquid chromatographic determination of flavonoids in Betula pendula and Betula pubescens leaves J. Chromatogr. A 793 370–377

    Google Scholar 

  • M. KEINÄNEN R. JULKUNEN-TIITTO P. MUTIKAINEN M. WALLS J. OVASKA E. VAPAAVUORI (1999) ArticleTitleTrade-offs in secondary metabolism: effects of fertilization, defoliation, and genotype on birch leaf phenolics Ecology 80 1970–1986

    Google Scholar 

  • M. KEINÄNEN R. JULKUNEN-TIITTO M. ROUSI J. TAHVANAINEN (1999) ArticleTitleTaxonomic implications of phenolic variation in leaves of birch (Betula L.) species Biochem. Syst. Ecol. 27 243–254

    Google Scholar 

  • J. N. KING A. D. YANCHUK G. K. KISS R. I. ALFARO (1997) ArticleTitleGenetic and phenotypic relationships between weevil (Pissodes strobi) resistance and height growth in spruce populations of British Columbia Can. J. For. Res. 27 732–739

    Google Scholar 

  • T. E. C. KRAUS Z. YU C. M. PRESTON R. A. DHALGREN R. J. ZASOSKI (2003) ArticleTitleLinking chemical reactivity and protein precipitation to structural characteristics of foliar tannins J. Chem. Ecol. 29 703–729 Occurrence Handle1:CAS:528:DC%2BD3sXitFarsb0%3D Occurrence Handle12757329

    CAS  PubMed  Google Scholar 

  • K. KUOKKANEN R. JULKUNEN-TIITTO M. KEINÄNEN P. NIEMELÄ J. TAHVANAINEN (2001) ArticleTitleThe effect of elevated CO2 and temperature on the secondary chemistry of Betula bendula seedlings Trees 15 378–384 Occurrence Handle1:CAS:528:DC%2BD3MXotlyqt7w%3D

    CAS  Google Scholar 

  • K. KUOKKANEN Y. SHANCHUN P. NIEMELÄ (2003) ArticleTitleEffects of elevated CO2 and temperature on the leaf chemistry of birch Betula pendula (Roth) and the feeding behaviour of the weevil Phyllobius maculicornis Agric. For. Entomol. 5 1–9

    Google Scholar 

  • M. L. LAITINEN R. JULKUNEN-TIITTO M. ROUSI (2000) ArticleTitleVariation in phenolic compounds within a birch (Betula pendula) population J. Chem. Ecol. 26 1609–1622 Occurrence Handle1:CAS:528:DC%2BD3cXltFGisbw%3D

    CAS  Google Scholar 

  • M. L. LAITINEN R. JULKUNEN-TIITTO M. ROUSI (2002) ArticleTitleFoliar phenolic composition of European white birch during bud unfolding and leaf development Physiol. Plant. 114 450–460 Occurrence Handle1:CAS:528:DC%2BD38Xjt1alt7k%3D Occurrence Handle12060268

    CAS  PubMed  Google Scholar 

  • M.-L. LAITINEN R. JULKUNEN-TIITTO K. YAMAJI J. HEINONEN M. ROUSI (2004) ArticleTitleVariation in birch bark secondary chemistry between and within clones: implications for herbivory Oikos 104 316–326 Occurrence Handle1:CAS:528:DC%2BD2cXhslGgurg%3D

    CAS  Google Scholar 

  • C. M. NICHOLS-ORIANS R. S. FRITZ T. P. CLAUSEN (1993) ArticleTitleThe genetic basis for variation in the concentration of phenolic glycosides in Salix sericea: clonal variation and sex-based differences Biochem. Syst. Ecol. 21 535–542 Occurrence Handle1:CAS:528:DyaK3sXmt1Wksr4%3D

    CAS  Google Scholar 

  • C. M. ORIANS B. M. ROCHE R. S. FRITZ (1996) ArticleTitleThe genetic basis for variation in the concentration of phenolic glycosides in Salix sericea: an analysis of heritability Biochem. Syst. Ecol. 24 719–724 Occurrence Handle1:CAS:528:DyaK2sXoslSitQ%3D%3D

    CAS  Google Scholar 

  • L. J. PORTER L. N. HRSTICH B. G. CHAN (1986) ArticleTitleThe conversion of procyanidins and prodelphidins to cyanidin and delphinidin Phytochemistry 25 223–230 Occurrence Handle1:CAS:528:DyaL28XlsFaktLw%3D

    CAS  Google Scholar 

  • P. B. REICHARDT (1981) ArticleTitlePapyriferic acid: a triterpenoid from Alaskan paper birch J. Org. Chem. 46 4576–4578 Occurrence Handle1:CAS:528:DyaL3MXls12msbg%3D

    CAS  Google Scholar 

  • P. B. REICHARDT J. P. BRYANT T. P. CLAUSEN G. D. WIELAND (1984) ArticleTitleDefence of winter-dormant Alaska paper birch against snowshoe hares Oecologia 65 58–69

    Google Scholar 

  • W. M. RICE (1989) ArticleTitleAnalyzing tables of statistical tests Evolution 43 223–225

    Google Scholar 

  • K. L. RISENHOOVER L. A. RENECKER L. E. MORGANTINI (1985) ArticleTitleEffects of secondary metabolites from balsam poplar and paper birch on cellulose digestion J. Range Manag. 38 370–371

    Google Scholar 

  • M. ROUSI J. TAHVANAINEN I. UOTILA (1991) ArticleTitleA mechanism of resistance to hare browsing in winter-dormant European white birch (Betula pendula) Am. Nat. 137 64–82

    Google Scholar 

  • J. P. SALMINEN V. OSSIPOV K. PIHLAJA (2002) ArticleTitleDistribution of hydrolysable tannins in the foliage of Finnish birch species Z. Naturforch. 57c 248–256

    Google Scholar 

  • S. R. SEARLE (1997) NoChapterTitle Linear Models Wiley New York 414

    Google Scholar 

  • D. S. SEIGLER (1998) Plant Secondary Metabolism Kluwer Academic Publishers Boston

    Google Scholar 

  • D. STRACK (1997) Phenolic metabolism P. M. DAY J. B. HARBORNE (Eds) Plant Biochemistry Academic Press London 387–416

    Google Scholar 

  • J. TAHVANAINEN R. JULKUNEN-TIITTO M. ROUSI P. B. REICHARDT (1991) ArticleTitleChemical determinants of resistance in winter-dormant seedlings of European white birch (Betula pendula) to browsing by the mountain hare Chemoecology 2 49–54 Occurrence Handle1:CAS:528:DyaK3sXjsFyksA%3D%3D

    CAS  Google Scholar 

  • H. T. TAIPALE J. VEPSÄLÄINEN R. LAATIKAINEN P. B. REICHARDT S. P. LAPINJOKI (1993) ArticleTitleIsolation and structure determination of three triterpenes from bark resin of juvenile European white birch Phytochemistry 34 755–758 Occurrence Handle1:CAS:528:DyaK2cXntleqsQ%3D%3D

    CAS  Google Scholar 

  • H. T. TAIPALE L. HÄRMÄLÄ M. ROUSI S. P. LAPINJOKI (1994) ArticleTitleHistological and chemical comparison of triterpene and phenolic deterrent contents of juvenile shoots of Betula species Trees 8 232–236

    Google Scholar 

  • R. TEGELBERG R. JULKUNEN-TIITTO P. J. APHALO (2001) ArticleTitleThe effects of long-term elevated UV-B on the growth and phenolics of field-grown silver birch (Betula pendula) Glob. Chang. Biol. 7 839–848

    Google Scholar 

  • R. TEGELBERG P. J. APHALO R. JULKUNEN-TIITTO (2002) ArticleTitleEffects of long-term-elevated ultraviolet-B radiation on phytochemicals in the bark of silver birch (Betula pendula) Tree Physiol. 22 1257–1263 Occurrence Handle1:CAS:528:DC%2BD38XpsV2ktr8%3D Occurrence Handle12464579

    CAS  PubMed  Google Scholar 

  • P. VAINIOTALO R. JULKUNEN-TIITTO M.-R. JUNTHEIKKI P. REICHARDT S. AURIOLA (1991) ArticleTitleChemical characteristics of herbivore defenses in Betula pendula winter-dormant young stems J. Chromatogr. 547 367–376 Occurrence Handle1:CAS:528:DyaK3MXkvV2iu7c%3D

    CAS  Google Scholar 

  • E. VALKAMA J. P. SALMINEN J. KORICHEVA K. PIHLAJA (2003) ArticleTitleComparative analysis of leaf trichome structure and composition of epicuticular flavonoids in Finnish birch species Ann. Bot. 91 643–655 Occurrence Handle1:CAS:528:DC%2BD3sXksFOmu7o%3D Occurrence Handle12714363

    CAS  PubMed  Google Scholar 

  • J. P. BUIJTENEN ParticleVAN (1992) Fundamental genetic principles L. FINS S. T. FRIEDMAN J. V. BROTSCHOL (Eds) Handbook of Quantitative Forest Genetics Kluwer Academic Publishers The Netherlands 29–68

    Google Scholar 

  • P. G. WATERMAN (1988) Tannins and plant–animal interactions V. CODY E. MIDDLETON J. B. HARBORNE A. BERETZ (Eds) Plant Flavonoids in Biology and Medicine II: Biochemical, Cellular, and Medicinal Properties Alan R. Liss, Inc. New York 77–91

    Google Scholar 

  • P. G. WATERMAN (1992) Roles for secondary metabolites in plants Secondary Metabolites: Their Function and Evolution SeriesTitleCiba Found. Symp. Wiley Chichester 255–275

    Google Scholar 

  • T. O. VETELI K. KUOKKANEN R. JULKUNEN-TIITTO H. ROININEN J. TANHVANAINEN (2002) ArticleTitleEffects of elevated CO2 and temperature on plant growth and herbivore defensive chemistry Glob. Chang. Biol. 8 1240–1252

    Google Scholar 

  • S. VIA (1984) ArticleTitleThe quantitative genetics of polyphagy in an insect herbivore. I. Genotype-environment interaction in larval performance on different host plant species Evolution 38 881–895

    Google Scholar 

  • K. YAMAJI R. JULKUNEN-TIITTO M. ROUSI V. FREIWALD E. OKSANEN (2003) ArticleTitleOzone exposure over two growing seasons alters root to shoot ratio and chemical composition of birch (Betula pendula Roth) Glob. Chang. Biol. 9 1–15

    Google Scholar 

Download references

Acknowledgments

We thank Anna-Maija Niskanen for the micropropagation; Anneli Kurkkio for help with the laboratory work; Hanni Sikanen, Susanne Heiska, Päivi Immonen, Heikki Kinnunen, Kalevi Silvennoinen, Jussi Tiainen, Mari Tuominen, and Satu Turtola for their help with fieldwork and technical assistance; and Seppo Ruotsalainen, Markku Keinänen, and Sarita Keski-Saari for valuable comments on the manuscript. James Callaway and Ewen Macdonald kindly helped to revise the English text. This study was part of the Finnish Biodiversity Research Programme, was mainly funded by the Academy of Finland, and was partly funded by the Finnish Centre of Excellence Program 2000–2005, Centre for Excellence for Forest Ecology and management, project no. 64308.

Author information

Authors and Affiliations

  1. Department of Pharmaceutical Chemistry, University of Kuopio, P.O. Box 1627, 70211, Kuopio, Finland

    Marja-Leena Laitinen

  2. Department of Biology, University of Joensuu, Natural Product Research Laboratories, P.O. Box 111, 80101, Joensuu, Finland

    Riitta Julkunen-Tiitto

  3. Department of Biology, University of Joensuu, P.O. Box 111, 80101, Joensuu, Finland

    Jorma Tahvanainen

  4. Finnish Forest Research Institute, Joensuu Research Centre, Yliopistokatu 7, 80101, Joensuu, Finland

    Jaakko Heinonen

  5. Finnish Forest Research Institute, Punkaharju Research Station, Finlandiantie 18, 58450, Punkaharju, Finland

    Matti Rousi

Authors
  1. Marja-Leena Laitinen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Riitta Julkunen-Tiitto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jorma Tahvanainen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jaakko Heinonen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Matti Rousi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marja-Leena Laitinen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Laitinen, ML., Julkunen-Tiitto, R., Tahvanainen, J. et al. Variation in Birch (Betula pendula) Shoot Secondary Chemistry due to Genotype, Environment, and Ontogeny. J Chem Ecol 31, 697–717 (2005). https://doi.org/10.1007/s10886-005-3539-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-005-3539-7

Key Words

Search

Navigation