Skip to main content
SpringerLink
Log in

Allelopathic effects of exogenous phenylalanine: a comparison of four monocot species

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Exogenous phenylalanine stunted annual ryegrass but not switchgrass or winter grain rye, with deuterium incorporation up to 3% from phenyalanine-d 8 . Toxicity to duckweed varied with illumination intensity and glucose uptake.

Isotopic labeling of biomolecules through biosynthesis from deuterated precursors has successfully been employed for both structural studies and metabolic analysis. Phenylalanine is the precursor of many products synthesized by plants, including the monolignols used for synthesis of lignin. Possible allelochemical effects of phenylalanine have not been reported, although its deamination product cinnamic acid is known to have deleterious effects on root elongation and growth of several plant species. The effects of phenylalanine and its deuterated analog phenylalanine-d 8 added to growth media were studied for annual ryegrass (Lolium multiflorum), winter grain rye (Secale cereale), and switchgrass (Panicum virgatum) cultivated under hydroponic conditions. Growth of annual ryegrass was inhibited by phenylalanine while switchgrass and rye were not significantly affected. Growth was less affected by deuterated phenylalanine-d 8 than by its protiated counterpart, which may be a typical deuterium kinetic isotope effect resulting in slower enzymatic reaction rates. Deuterium incorporation levels of 2–3% were achieved in biomass of switchgrass and annual ryegrass. Both protiated and deuterated phenylalanine were moderately toxic (IC25 values 0.6 and 0.8 mM, respectively) to duckweed (Lemna minor) grown using a 12 h diurnal cycle under photoautotrophic conditions. A significant increase in toxicity, greater for the deuterated form, was noted when duckweed was grown under higher intensity, full spectrum illumination with a metal halide lamp compared to fluorescent plant growth lamps emitting in the blue and red spectral regions. Supplementation with glucose increased toxicity of phenylalanine consistent with synergy between hexose and amino acid uptake that has been reported for duckweed.

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
Fig. 7

Similar content being viewed by others

References

  • Carlsen SC, Kudsk P, Laursen B, Mathiassen SK, Mortensen AG, Fomsgaard IS (2009) Allelochemicals in rye (Secale cereale L.): cultivar and tissue differences in the production of benzoxazinoids and phenolic acids. Nat Prod Commun 4:199–208

    CAS  PubMed  Google Scholar 

  • Cass CL, Peraldi A, Dowd PF, Mottiar Y, Santoro N, Karlen SD, Bukhman YV, Foster CE, Thrower N, Bruno LC, Moskvin OV, Johnson ET, Willhoit ME, Phutane M, Ralph J, Mansfield SD, Nicholson P, Sedbrook JC (2015) Effects of phenylalanine ammonia lyase (PAL) knockdown on cell wall composition, biomass digestibility, and biotic and abiotic stress responses in Brachypodium. J Exp Bot 66:4317–4335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cope BT, Bose S, Crespi HL, Katz JJ (1965) Growth of Lemna in H2O–D2O mixtures: enhancement by kinetin. Bot Gaz 126:214–221

    Article  CAS  Google Scholar 

  • Datko AH, Mudd SH (1985) Uptake of amino acids and other organic compounds by Lemna paucicostata Hegelm. 6746. Plant Physiol 77:770–778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans BR, Shah R (2015) Development of approaches for deuterium incorporation in plants. In: Kelman Z (ed) Isotope labeling of biomolecules-labeling methods, Vol 565, Chapter 10, Methods in Enzymology. Academic Press, UK, pp 213–243

  • Evans B, Bali G, Reeves D, O’Neill H, Sun Q, Shah R, Ragauskas A (2014) Effect of D2O on growth properties and chemical structure of annual ryegrass (Lolium multiflorum). J Agric Food Chem 62:2592–2604

    Article  Google Scholar 

  • Evans BR, Bali G, Foston M, Ragauskas AJ, O’Neill H, Shah R, McGaughey J, Reeves D, Rempe CS, Davison BH (2015) Production of deuterated switchgrass by hydroponic cultivation. Planta 242:215–222

    Article  CAS  PubMed  Google Scholar 

  • Foston MB, McGaughey J, O’Neill H, Evans BR, Ragauskas AJ (2012) Deuterium Incorporation in biomass cell wall components by NMR analysis. Analyst 137:1090–1093

    Article  CAS  PubMed  Google Scholar 

  • Geiger HH, Miedaner T (2009) Rye breeding. In: Mj Carena (ed) Cereals. Springer, New York, pp 157–181

    Chapter  Google Scholar 

  • Gordon WR, Koukkari WL (1978) Circadian rhythmicity in the activities of phenylalanine ammonia-lyase from Lemna perpusilla and Spirodela polyrhiza. Plant Physiol 62:612–615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He J, Pingali SV, Chundawat SPS, Pack A, Jones AD, Langan P, Davison BH, Urban V, Evans BR, O’Neill H (2014) Controlled incorporation of deuterium into bacterial cellulose. Cellulose 21:927–936

    Article  CAS  Google Scholar 

  • Houben D, Evrard L, Sonnet P (2013) Mobility, bioavailability and pH-dependent leaching of cadmium, zinc and lead in a contaminated soil amended with biochar. Chemosphere 92:1450–1457

    Article  CAS  PubMed  Google Scholar 

  • Humphreys M, Feuerstein U, Vandewalle M, Baert J (2010) Ryegrasses. In: Boller B, Posselt UK, Veronesi F (eds) Fodder crops and amenity grasses. Springer, New York, pp 211–260

    Chapter  Google Scholar 

  • Hussain MI, Reigosa MJ (2011) Allelechemical stress inhibits growth, leaf water relations, PSII photochemistry, non-photochemcial fluorescence quenching, and heat energy dissipation in three C3 perennial species. J Exp Botan 62:4533–4545

    Article  CAS  Google Scholar 

  • Jansen MAK, van der Noort RE, Tan MYA, Prinsen E, Lagrimini LM, Thormeley RNF (2001) Phenol-oxidizing peroxidases contribute to the protection of plants from ultraviolet radiation stress. Plant Physiol 126:1012–1023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ji X, Huh B, Kim S (2008) Determination of biosynthetic pathway of decursin in hairy root culture of Angelica gigas. J Korean Soc Appl Biol Chem 51:1738–2203

    Article  Google Scholar 

  • Kaspar TC, Jaynes DB, Parkin TB, Moorman TB (2007) Rye cover crop and gamagrass strip effects on NO3 concentration and load in tile drainage. J Environ Qual 36:1503–1511

    Article  CAS  PubMed  Google Scholar 

  • Katz JJ, Crespi H (1966) Deuterated organisms: cultivation and uses. Science 151:1187–1194

    Article  CAS  PubMed  Google Scholar 

  • King-Díaz B, Montes-Ayala J, Escartín-Guzmán C, Castillo-Blum SE, Iglesias-Prieto T, Lotina-Hennsen B, Barba-Behrens N (2005) Cobalt (II) coordination compounds of ethyl 4-methyl-5-imidazolecarboxylate: chemical and biochemical characterization on photosynthesis and seed germination. Bioinorg Chem Appl 3:93–108

    Article  PubMed Central  Google Scholar 

  • Laloy E, Bielders CL (2010) Effect of intercropping period management on runoff and erosion in a maize cropping system. J Environ Qual 39:1001–1008

    Article  CAS  PubMed  Google Scholar 

  • Langan P, Evans BR, Foston M, Heller WT, O’Neill HM, Petridis L, Pingali SV, Ragauskas AJ, Smith JC, Davison B (2012) Neutron technologies for bioenergy research. Indus Biotechnol 8:209–216

    Article  CAS  Google Scholar 

  • Les DH, Landolt E, Crawford DJ (1997) Systematics of the Lemnaceae (duckweeds): inferences from micromolecular and morphological data. Pl Syst Evol 204:161–171

    Article  Google Scholar 

  • Lima RB, Salvador VH, dos Santos WD, Bubna GA, Finger-Teixeira A, Soares AR, Marchiosi R, de Ferrarese Maria LL, Ferrarese-Filho O, (2013) Enhanced lignin monomer production caused by cinnamic acid and its hydroxylated derivatives inhibits soybean root growth. PLoS ONE 8(12):e80542

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Z, He X, Chen W, Zhao M (2013) Ecotoxicological responses of three ornamental herb species to cadmium. Environ Toxicol Chem 32:1746–1751

    Article  CAS  PubMed  Google Scholar 

  • Moody M, Miller J (2005) Lemna minor Growth Inhibition Test. In: Blaise C, Férard J-F (eds) Small scale freshwater toxicity investigations. Springer Netherlands, Amsterdam, pp 271–298

  • Novacky A, Ullrich-Eberius CI, Lüttge U (1978) Membrane potential changes during transport of hexoses in Lemna gibba G1. Planta 138:263–270

    Article  CAS  PubMed  Google Scholar 

  • Parrish DJ, Casler MD, Monti A (2012) The evolution of switchgrass as an energy crop. In: Monti A (ed) Switchgrass: a valuable biomass crop for energy. Springer, London, pp 1–26

    Google Scholar 

  • Pavon JA, Fitzpatrick PF (2006) Insights into the catalytic mechanisms of phenylalanine and tryptophan hydroxylase from kinetic isotope effects on aromatic hydroxylation. Biochemistry 45:11030–11037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramirez Toro G, Leather GR, Einhellig FA (1988) Effects of three phenolic compounds on Lemna gibba G3. J Chem Ecology 14:845–853

    Article  CAS  Google Scholar 

  • Rohde A, Morreel K, Ralph J, Goeminne G, Hostyn V, De Rycke R, Kushnir S, Van Doorsselaere J, Joseleau JP, Vuylsteke M, Van Driessche G, Van Beeumen J, Messens E, Boerjan W (2004) Molecular phenotyping of the pal1 and pal2 mutants of Arabidopsis thaliana reveals far-reaching consequences on phenylpropanoid, amino acid, and carbohydrate metabolism. Plant Cell 16:2749–2771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rolando C, Daubresse N, Pollet B, Jouanin L, Lapierre C (2004) Lignification in Poplar Plantlets Fed with Deuterium-Labelled Lignin Precursors. C R Biologies 327:799–807

    Article  CAS  PubMed  Google Scholar 

  • Rossmann M, Matos AT, Abreu EC, Silva FF, Borges AC (2013) Effect of influent aeration on removal of organic matter from coffee processing wastewater in constructed wetlands. J Environ Manage 128:912–919

    Article  CAS  PubMed  Google Scholar 

  • Salvador VH, Lima RB, dos Santos WB, Soares AR, Böhm PAF, Marchiosi R, Ferrarese MdLL, Ferrarese-Filho O (2013) Cinnamic acid increases lignin production and inhibits soybean root growth. PLOS-One 8:e69105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samuel R, Pu Y, Raman B, Ragauskas AJ (2010) Structural characterization and comparison of switchgrass ball-milled lignin before and after dilute acid pretreatment. Appl Biochem Biotechnol 162:62–74

    Article  CAS  PubMed  Google Scholar 

  • Sandrin CZ, de Figueiredo-Ribeiro RC, Delitti WB, Domingos M (2013) Short-term changes of fructans in ryegrass (Lolium multiflorum ‘Lema’) in response to urban air pollutants and meteorological conditions. Ecotoxicol Environ Saf 96:80–85

    Article  CAS  PubMed  Google Scholar 

  • Schenk RM, Hildebrandt AC (1972) Medium and techniques for induction and growth of monocotyledonous and dicotyledonous plant cell cultures. Can J Bot 50:199–204

    Article  CAS  Google Scholar 

  • Schulz M, Marocco A, Tabaglio V, Macias FA, Molinillo JMG (2013) Benzoxazinoids in rye allelopathy - from discovery to application in sustainable weed control and organic farming. J Chem Ecology 39:154–174

    Article  CAS  Google Scholar 

  • Siegel SM, Halpern LA, Giumarro C (1964) Germination and seedling growth of winter rye in deuterium oxide. Nature 201:1244–1245

    Article  CAS  Google Scholar 

  • Shao X, DiMarco K, Richard TL, Lynd LR (2015) Winter rye as a bioenergy feedstock: impact of crop maturity on composition, biological solubilization and potential revenue. Biotechnol Biofuels 8:35

    Article  PubMed  PubMed Central  Google Scholar 

  • Shibabe S, Yoda K (1985) Water and potassium ion absorption by deuterium oxide resistant winter rye seedlings. Radioisotopes 34:266–269

    Article  CAS  PubMed  Google Scholar 

  • Shui J, An Y, Ma Y, Ichizen N (2010) Allelopathic potential of switchgrass (Panicum virgatum L.) on perennial ryegrass (Lolium perenne L.) and alfalfa (Medicago sativa L.). Environ Manage 46:590–598

    Article  PubMed  Google Scholar 

  • Stomp AM (2005) The duckweeds: a valuable plant for biomanufacturing. Biotechnol Ann Rev 11:69–99

    Article  CAS  Google Scholar 

  • Strock JS, Porter PM, Russelle MP (2004) Cover cropping to reduce nitrate loss through subsurface drainage in the Northern U.S. Corn Belt. J Environ Qual 33:1010–1016

    Article  CAS  PubMed  Google Scholar 

  • Yamauchi K, Fukushima K (2004) The regulation from guaiacyl to syringyl lignin in the differentiating xylem of Robinia pseudoacacia. CR Biol 327:791–797

    Article  CAS  Google Scholar 

  • Yin L, Cheng Y, Espinasse B, Colman BP, Auffan M, Wiesner M, Rose J, Liu J, Bernhardt ES (2011) More than the ions: the effects of silver nanoparticles on Lolium multiflorum. Environ Sci Technol 45:2360–2367

    Article  CAS  PubMed  Google Scholar 

  • Yin L, Colman BP, McGill BM, Wright JP, Bernhardt ES, Rozhkova EA (2012) Effects of silver nanoparticle exposure on germination and early growth of eleven wetland plants. PLoS ONE 7:e47674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported by the U. S. Department of Energy, Office of Science, through the Genomic Science Program, Office of Biological and Environmental Research, under Contract FWP ERKP752. The research at Oak Ridge National Laboratory’s Center for Structural Molecular Biology (CSMB) was supported by the U. S. Department of Energy, Office of Science, through the Office of Biological and Environmental Research under Contract FWP ERKP291, using facilities supported by the Office of Basic Energy Sciences, U. S. Department of Energy. R. Shah was partly supported by the graduate fellowship program of the Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee, Knoxville. C. Howard, F. Lavenhouse, and D. Ramirez, with K. Ramey as teacher-mentor, were supported by the Siemens Foundation through the Siemens Teachers As Research Scientists (STARS) summer 2014 program administered by Oak Ridge Institute of Science and Education, Oak Ridge Associated Universities. V. Cangemi, B. Kinney, C. Partee, and T. Ware were participants in the Appalachian Regional Commission/Oak Ridge National Laboratory Summer Math Science Technology Institute 2015 summer program. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the U. S. Department of Energy under Contract DE-AC05-00OR22725.

Author information

Authors and Affiliations

  1. Chemical Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA

    Barbara R. Evans

  2. Institute of Paper Science and Technology, School of Chemistry and Biochemistry, Georgia Institute of Technology, Atlanta, GA, 30332, USA

    Garima Bali & Art Ragauskas

  3. Department of Chemical and Biomolecular Engineering, University of Tennessee, Knoxville, TN, 37996, USA

    Art Ragauskas

  4. Department of Forestry, Wildlife, and Fisheries, Center for Renewable Carbon, University of Tennessee Institute of Agriculture, Knoxville, TN, 37996, USA

    Art Ragauskas

  5. Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA

    Art Ragauskas & Brian Davison

  6. Biology and Soft Matter Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA

    Riddhi Shah & Hugh O’Neill

  7. Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee, Knoxville, TN, 37996, USA

    Riddhi Shah

  8. Siemens Teachers As Research Scientists (STARS) High School Science Teacher Summer Research Experience Program, Oak Ridge Institute of Science and Education, Oak Ridge Associated Universities, Oak Ridge, USA

    Cory Howard, Fayola Lavenhouse, Dawn Ramirez, Kelly Weston & Kelly Ramey

  9. Participants in Appalachian Regional Commission (ARC) High School Science Teacher Summer Research Experience Program, Oak Ridge National Laboratory, Oak Ridge, USA

    Valerie Cangemi, Brian Kinney, Claudia Partee & Teresa Ware

Authors
  1. Barbara R. Evans
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Garima Bali
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Art Ragauskas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Riddhi Shah
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hugh O’Neill
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cory Howard
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Fayola Lavenhouse
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Dawn Ramirez
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Kelly Weston
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Kelly Ramey
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Valerie Cangemi
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Brian Kinney
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Claudia Partee
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Teresa Ware
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Brian Davison
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Barbara R. Evans.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

This manuscript has been authored by UT-Battelle, LLC, under Contract No. DE-AC05-00OR22725 with the U.S. Department of Energy. The United States Government retains and the publisher, by accepting the article for publication, acknowledges that the United States Government retains a non-exclusive, paid-up, irrevocable, world-wide license to publish or reproduce the published form of this manuscript, or allow others to do so, for United States Government purposes. The Department of Energy will provide public access to these results of federally sponsored research in accordance with the DOE Public Access Plan (http://energy.gov/downloads/doe-public-access-plan).

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1435 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Evans, B.R., Bali, G., Ragauskas, A. et al. Allelopathic effects of exogenous phenylalanine: a comparison of four monocot species. Planta 246, 673–685 (2017). https://doi.org/10.1007/s00425-017-2720-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-017-2720-x

Keywords

Search

Navigation