Skip to main content
Log in

Restoration of secondary metabolism in birch seedlings relieved from PAL-inhibitor

  • Original Paper
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Phenylalanine ammonia lyase (PAL) plays a key role in phenylpropanoid metabolism, catalyzing the deamination of phenylalanine (Phe) to form trans-cinnamic acid. Inhibitors of PAL have been used to study the physiological role of the different compounds derived from trans-cinnamic acid, and to test theories about a trade-off between growth and defence in plants. In a previous study with birch (Betula pubescens Ehrh.) seedlings, the PAL inhibitor 2-aminoindane-2-phosphonic acid monohydrate (AIP) caused an accumulation of Phe and a strong decrease in the quantity of simple phenolics, soluble condensed tannins and growth, whereas flavonol glycosides were generally not affected. The present study demonstrates restoration of secondary metabolism in the previously AIP treated birch seedlings. Our results indicate that Phe accumulated during PAL inhibition could be partly used to increase the content of the phenolic acids, flavan-3-ols and to some extent the soluble condensed tannins. Seedling growth also increased when the supply of PAL inhibitor ceased. We thereby show that the inhibition of PAL by AIP in vivo is reversible, at least for moderate AIP concentrations and the rate of restoration is dependent on the inhibitor concentration.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Appert C, Zoń J, Amrhein N (2003) Kinetic analysis of the inhibition of phenylalanine ammonia-lyase by 2-aminoindan-2-phosphonic acid and other phenylalanine analogues. Phytochemistry 62:415–422

    Article  PubMed  CAS  Google Scholar 

  • Bryant JP, Chapin FS III, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368

    Article  CAS  Google Scholar 

  • Forkmann G, Heller W (1999) Biosynthesis of flavonoids. In: Barton D, Nakanishi K, Meth-Cohn O (eds) Comprehensive natural products chemistry. Elsevier, Amsterdam, 713–748

    Google Scholar 

  • Gitz DC, Liu L, McClure JW (1998) Phenolic metabolism, growth, and UV-B tolerance in phenylalanine ammonia-lyase-inhibited red cabbage seedlings. Phytochemistry 49:377–386

    Article  CAS  Google Scholar 

  • Hahlbrock K, Kuheln E, Lindl T (1971) Changes in enzyme activities during the growth of cell suspension cultures of Glycine max: phenylalanine ammonia-lyase and p-coumarate: coA ligase. Planta 99:311–318

    Article  CAS  Google Scholar 

  • Hanson KR, Havir EA (1981) Phenylalanine ammonia-lyase. In: Stumpf PK, Conn EE (eds) The biochemistry of plants, vol 7. Academic, New York, pp 577–625

  • Harborne JB, Baxter E (1999) The handbook of natural flavonoids, vol. 2 Wiley, Chichester

  • Haslam E (1989) Plant polyphenols. Cambridge University Press, Cambridge

    Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Ingestad T (1971) A definition of optimum nutrient requirements in birch seedlings. II. Physiol Plant 24:118–125

    Article  CAS  Google Scholar 

  • Janas KM, Osiecka R, Zoń J (1998) Growth-retarding effect of 2-aminoindan-2-phosphonic acid on Spirodela punctata. J Plant Growth Regul 17:169–172

    Article  CAS  Google Scholar 

  • Janas KM, Cvikrová M, Palagiewicz A, Szafranska K, Posmyk MM (2002) Constitutive elevated accumulation of phenylpropanoids in soybean roots at low temperature. Plant Sci 163:369–373

    Article  CAS  Google Scholar 

  • Julkunen-Tiitto R, Rousi M, Bryant JP, Sorsa S, Keinänen M, Sikanen H (1996) Chemical diversity of several Betulaceae species: comparison of phenolics and terpenoids in northern birch stems. Trees 11:16–22

    Article  Google Scholar 

  • Keski-Saari S, Falck M, Heinonen J, Zón J, Julkunen-Tiitto R (2007) Prioritization of flavonol glycosides over other phenolics during early development of Betula pubescens seedlings. Trees (in press)

  • Li J, Ou-Lee T-M, Raba R, Amundson RG, Last RL (1993) Arabidopsis flavonoid mutants are hypersensitive to UV-B radiation. Plant Cell 5: 171–179

    Article  PubMed  CAS  Google Scholar 

  • Lin Q, Northcote DH (1990) Expression of phenylalanine ammonia-lyase gene during tracheary-element differentiation from cultured mesophyll cells of Zinnia elegans L. Planta 182:591–598

    Article  CAS  Google Scholar 

  • Loomis WE (1932) Growth-differentiation balance versus carbohydrate-nitrogen ratio. Proc Am Soc Hort Sci 29:240–245

    CAS  Google Scholar 

  • Loomis WE (1953) Growth and differentiation—an introduction and summary. In: Loomis WE (ed) Growth and differentiation in plants. Iowa State College Press, pp 1–17

  • Maher EA, Bate NJ, Ni W, Elkind Y, Dixon RA, Lamb CJ (1994) Increased disease susceptibility of transgenic tobacco plants with suppressed levels of preformed phenylpropanoid products. Proc Natl Acad Sci USA 91:7802–7806

    Article  PubMed  CAS  Google Scholar 

  • Neumann G, El-Aschker A, Schwemmle B (1991) L-phenylalanine ammonia-lyase and chalcone synthase in seedlings of Oenothera: plasmotype dependent regulation and tissue specific distribution. J Plant Physiol 138:263–269

    CAS  Google Scholar 

  • Porter LJ, Hrstich LN, Chan BG (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230

    Article  CAS  Google Scholar 

  • Reuber S, Leitsch J, Krause GH, Weissenböck G (1993) Metabolic reduction of phenylpropanoid compounds in primary leaves of rye (Secale cereale L.) leads to increased UV-B sensitivity of photosynthesis. Z Naturforsch 48c:749–756

    Google Scholar 

  • Rice-Evans CA, Miller NJ, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci 2: 152–159

    Article  Google Scholar 

  • Ruuhola T, Julkunen-Tiitto R (2003) Trade-off between synthesis of salicylates and growth of micropropagated Salix pentandra. J Chem Ecol 29:1565–1588

    Article  PubMed  CAS  Google Scholar 

  • Ruuhola TM, Julkunen-Tiitto M-RK (2000) Salicylates of intact Salix myrsinifolia plantlets do not undergo rapid metabolic turnover. Plant Physiol 122:895–905

    Article  PubMed  CAS  Google Scholar 

  • Scoch G, Goepfert S, Morant M, Hehn A, Meyer D, Ullmann P, Werck-Reichardt D (2001) CYP98A3 from Arabidopsis thaliana is a 3′-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J Prioritization Bio Prioritization l Chem 276:36566–36574

    Google Scholar 

  • Shadle GL, Wesley SV, Korth KL, Chen F, Lamb C, Dixon RA (2003) Phenylpropanoid compounds and disease resistance in transgenic tobacco with altered expression of-phenylalanine ammonia-lyase. Phytochemistry 64:153–161

    Article  PubMed  CAS  Google Scholar 

  • Siegler DS (1998) Plant secondary metabolism. Kluwer, Boston

    Google Scholar 

  • Treutter D (2005) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol 7:581–591

    Article  PubMed  CAS  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis. A colourful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493

    Article  PubMed  CAS  Google Scholar 

  • Zoń J, Szefczyk B, Sawka-Dobrowolska W, Gancarz R, Kucharska- Zoń M, Latajka R, Amrhein N, Miziak P, Szczepanik W (2004) Experimental and ab initio calculated structures of 2-aminoindane-2-phosphonic acid, a potent inhibitor of phenylalanine ammonia-lyase, and theoretical studies of its binding to the model enzyme structure. New J Chem 28:1048–1055

    Article  Google Scholar 

  • Zoń J, Amrhein N (1992) Inhibitors of phenylalanine ammonia-lyase: 2-aminoindan-2-phosphonic acid and related compounds. Liebigs Ann Chem 625–628

Download references

Acknowledgments

We thank Outi Nousiainen for help in the laboratory. We also thank Matti Rousi at METLA for the seeds, and two anonymous reviewers for valuable comments to the manuscript. Finnish Cultural Foundation, The Academy of Finland (Finnish Centre of Excellence Program 2000–2005, project no. 64308) and The Norwegian Research council (Project 159778/V40) provided financial support for the research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Line Nybakken.

Additional information

Communicated by D. Treutter.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nybakken, L., Keski-Saari, S., Falck, M.A. et al. Restoration of secondary metabolism in birch seedlings relieved from PAL-inhibitor. Trees 21, 273–281 (2007). https://doi.org/10.1007/s00468-006-0120-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-006-0120-0

Keywords

Navigation