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

Barbara R. Evans; Garima Bali; Art Ragauskas; Riddhi Shah; Hugh O’Neill; Cory Howard; Fayola Lavenhouse; Dawn Ramirez; Kelly Weston; Kelly Ramey; Valerie Cangemi; Brian Kinney; Claudia Partee; Teresa Ware; Brian Davison

doi:10.1007/s00425-017-2720-x

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

Barbara R. Evans, Garima Bali, Art Ragauskas, Riddhi Shah, Hugh O’Neill, Cory Howard, Fayola Lavenhouse, Dawn Ramirez, Kelly Weston, Kelly Ramey, Valerie Cangemi, Brian Kinney, Claudia Partee, Teresa Ware, Brian Davison

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3 Scopus citations

Abstract

Main conclusion: Exogenous phenylalanine stunted annual ryegrass but not switchgrass or winter grain rye, with deuterium incorporation up to 3% from phenyalanine-d₈. 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-d₈ 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-d₈ 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.

Original language	English
Pages (from-to)	673-685
Number of pages	13
Journal	Planta
Volume	246
Issue number	4
DOIs	https://doi.org/10.1007/s00425-017-2720-x
State	Published - Oct 1 2017

Funding

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 ). 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.

Keywords

Allelopathy
Deuterium
Lemna
Phenylalanine
Ryegrass
Switchgrass

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10.1007/s00425-017-2720-x

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title = "Allelopathic effects of exogenous phenylalanine: a comparison of four monocot species",

abstract = "Main conclusion: Exogenous phenylalanine stunted annual ryegrass but not switchgrass or winter grain rye, with deuterium incorporation up to 3% from phenyalanine-d8. 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-d8 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-d8 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.",

keywords = "Allelopathy, Deuterium, Lemna, Phenylalanine, Ryegrass, Switchgrass",

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AU - Ragauskas, Art

AU - Shah, Riddhi

AU - O’Neill, Hugh

AU - Howard, Cory

AU - Lavenhouse, Fayola

AU - Ramirez, Dawn

AU - Weston, Kelly

AU - Ramey, Kelly

AU - Cangemi, Valerie

AU - Kinney, Brian

AU - Partee, Claudia

AU - Ware, Teresa

AU - Davison, Brian

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AB - Main conclusion: Exogenous phenylalanine stunted annual ryegrass but not switchgrass or winter grain rye, with deuterium incorporation up to 3% from phenyalanine-d8. 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-d8 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-d8 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.

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

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