Acquisition and assimilation of nitrogen as peptide-bound and D-enantiomers of amino acids by wheat

Paul W Hill*, Richard S Quilliam, Thomas H DeLuca, John Farrar, Mark Farrell, Paula Roberts, Kevin K Newsham, David W Hopkins, Richard D Bardgett, David L Jones

*Corresponding author for this work

Research output: Contribution to journalArticleResearchpeer-review

75 Citations (Scopus)

Abstract

Nitrogen is a key regulator of primary productivity in many terrestrial ecosystems. Historically, only inorganic N (NH(4)(+) and NO(3)(-)) and L-amino acids have been considered to be important to the N nutrition of terrestrial plants. However, amino acids are also present in soil as small peptides and in D-enantiomeric form. We compared the uptake and assimilation of N as free amino acid and short homopeptide in both L- and D-enantiomeric forms. Sterile roots of wheat (Triticum aestivum L.) plants were exposed to solutions containing either (14)C-labelled L-alanine, D-alanine, L-trialanine or D-trialanine at a concentration likely to be found in soil solution (10 µM). Over 5 h, plants took up L-alanine, D-alanine and L-trialanine at rates of 0.9±0.3, 0.3±0.06 and 0.3±0.04 µmol g(-1) root DW h(-1), respectively. The rate of N uptake as L-trialanine was the same as that as L-alanine. Plants lost ca.60% of amino acid C taken up in respiration, regardless of the enantiomeric form, but more (ca.80%) of the L-trialanine C than amino acid C was respired. When supplied in solutions of mixed N form, N uptake as D-alanine was ca.5-fold faster than as NO(3)(-), but slower than as L-alanine, L-trialanine and NH(4)(+). Plants showed a limited capacity to take up D-trialanine (0.04±0.03 µmol g(-1) root DW h(-1)), but did not appear to be able to metabolise it. We conclude that wheat is able to utilise L-peptide and D-amino acid N at rates comparable to those of N forms of acknowledged importance, namely L-amino acids and inorganic N. This is true even when solutes are supplied at realistic soil concentrations and when other forms of N are available. We suggest that it may be necessary to reconsider which forms of soil N are important in the terrestrial N cycle.

Original languageEnglish
Article numbere19220
JournalPLoS ONE
Volume6
Issue number4
DOIs
Publication statusPrint publication - 26 Apr 2011
Externally publishedYes

Fingerprint

Enantiomers
enantiomers
Alanine
alanine
Triticum
assimilation (physiology)
Nitrogen
peptides
Amino Acids
Peptides
wheat
amino acids
nitrogen
Soil
Soils
uptake mechanisms
soil
Nutrition
alanyl-alanyl-alanine
soil solution

Keywords

  • Amino acids
  • Nitrogen
  • Peptides
  • Plant roots
  • Soil chemistry
  • Solutions
  • Stereoisomerism
  • Triticum metabolism
  • United Kingdom

Cite this

Hill, P. W., Quilliam, R. S., DeLuca, T. H., Farrar, J., Farrell, M., Roberts, P., ... Jones, D. L. (2011). Acquisition and assimilation of nitrogen as peptide-bound and D-enantiomers of amino acids by wheat. PLoS ONE, 6(4), [e19220]. https://doi.org/10.1371/journal.pone.0019220
Hill, Paul W ; Quilliam, Richard S ; DeLuca, Thomas H ; Farrar, John ; Farrell, Mark ; Roberts, Paula ; Newsham, Kevin K ; Hopkins, David W ; Bardgett, Richard D ; Jones, David L. / Acquisition and assimilation of nitrogen as peptide-bound and D-enantiomers of amino acids by wheat. In: PLoS ONE. 2011 ; Vol. 6, No. 4.
@article{0b2e82c294544916a0de0089ba105686,
title = "Acquisition and assimilation of nitrogen as peptide-bound and D-enantiomers of amino acids by wheat",
abstract = "Nitrogen is a key regulator of primary productivity in many terrestrial ecosystems. Historically, only inorganic N (NH(4)(+) and NO(3)(-)) and L-amino acids have been considered to be important to the N nutrition of terrestrial plants. However, amino acids are also present in soil as small peptides and in D-enantiomeric form. We compared the uptake and assimilation of N as free amino acid and short homopeptide in both L- and D-enantiomeric forms. Sterile roots of wheat (Triticum aestivum L.) plants were exposed to solutions containing either (14)C-labelled L-alanine, D-alanine, L-trialanine or D-trialanine at a concentration likely to be found in soil solution (10 µM). Over 5 h, plants took up L-alanine, D-alanine and L-trialanine at rates of 0.9±0.3, 0.3±0.06 and 0.3±0.04 µmol g(-1) root DW h(-1), respectively. The rate of N uptake as L-trialanine was the same as that as L-alanine. Plants lost ca.60{\%} of amino acid C taken up in respiration, regardless of the enantiomeric form, but more (ca.80{\%}) of the L-trialanine C than amino acid C was respired. When supplied in solutions of mixed N form, N uptake as D-alanine was ca.5-fold faster than as NO(3)(-), but slower than as L-alanine, L-trialanine and NH(4)(+). Plants showed a limited capacity to take up D-trialanine (0.04±0.03 µmol g(-1) root DW h(-1)), but did not appear to be able to metabolise it. We conclude that wheat is able to utilise L-peptide and D-amino acid N at rates comparable to those of N forms of acknowledged importance, namely L-amino acids and inorganic N. This is true even when solutes are supplied at realistic soil concentrations and when other forms of N are available. We suggest that it may be necessary to reconsider which forms of soil N are important in the terrestrial N cycle.",
keywords = "Amino acids, Nitrogen, Peptides, Plant roots, Soil chemistry, Solutions, Stereoisomerism, Triticum metabolism, United Kingdom",
author = "Hill, {Paul W} and Quilliam, {Richard S} and DeLuca, {Thomas H} and John Farrar and Mark Farrell and Paula Roberts and Newsham, {Kevin K} and Hopkins, {David W} and Bardgett, {Richard D} and Jones, {David L}",
year = "2011",
month = "4",
day = "26",
doi = "10.1371/journal.pone.0019220",
language = "English",
volume = "6",
journal = "PLoS ONE",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "4",

}

Hill, PW, Quilliam, RS, DeLuca, TH, Farrar, J, Farrell, M, Roberts, P, Newsham, KK, Hopkins, DW, Bardgett, RD & Jones, DL 2011, 'Acquisition and assimilation of nitrogen as peptide-bound and D-enantiomers of amino acids by wheat', PLoS ONE, vol. 6, no. 4, e19220. https://doi.org/10.1371/journal.pone.0019220

Acquisition and assimilation of nitrogen as peptide-bound and D-enantiomers of amino acids by wheat. / Hill, Paul W; Quilliam, Richard S; DeLuca, Thomas H; Farrar, John; Farrell, Mark; Roberts, Paula; Newsham, Kevin K; Hopkins, David W; Bardgett, Richard D; Jones, David L.

In: PLoS ONE, Vol. 6, No. 4, e19220, 26.04.2011.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Acquisition and assimilation of nitrogen as peptide-bound and D-enantiomers of amino acids by wheat

AU - Hill, Paul W

AU - Quilliam, Richard S

AU - DeLuca, Thomas H

AU - Farrar, John

AU - Farrell, Mark

AU - Roberts, Paula

AU - Newsham, Kevin K

AU - Hopkins, David W

AU - Bardgett, Richard D

AU - Jones, David L

PY - 2011/4/26

Y1 - 2011/4/26

N2 - Nitrogen is a key regulator of primary productivity in many terrestrial ecosystems. Historically, only inorganic N (NH(4)(+) and NO(3)(-)) and L-amino acids have been considered to be important to the N nutrition of terrestrial plants. However, amino acids are also present in soil as small peptides and in D-enantiomeric form. We compared the uptake and assimilation of N as free amino acid and short homopeptide in both L- and D-enantiomeric forms. Sterile roots of wheat (Triticum aestivum L.) plants were exposed to solutions containing either (14)C-labelled L-alanine, D-alanine, L-trialanine or D-trialanine at a concentration likely to be found in soil solution (10 µM). Over 5 h, plants took up L-alanine, D-alanine and L-trialanine at rates of 0.9±0.3, 0.3±0.06 and 0.3±0.04 µmol g(-1) root DW h(-1), respectively. The rate of N uptake as L-trialanine was the same as that as L-alanine. Plants lost ca.60% of amino acid C taken up in respiration, regardless of the enantiomeric form, but more (ca.80%) of the L-trialanine C than amino acid C was respired. When supplied in solutions of mixed N form, N uptake as D-alanine was ca.5-fold faster than as NO(3)(-), but slower than as L-alanine, L-trialanine and NH(4)(+). Plants showed a limited capacity to take up D-trialanine (0.04±0.03 µmol g(-1) root DW h(-1)), but did not appear to be able to metabolise it. We conclude that wheat is able to utilise L-peptide and D-amino acid N at rates comparable to those of N forms of acknowledged importance, namely L-amino acids and inorganic N. This is true even when solutes are supplied at realistic soil concentrations and when other forms of N are available. We suggest that it may be necessary to reconsider which forms of soil N are important in the terrestrial N cycle.

AB - Nitrogen is a key regulator of primary productivity in many terrestrial ecosystems. Historically, only inorganic N (NH(4)(+) and NO(3)(-)) and L-amino acids have been considered to be important to the N nutrition of terrestrial plants. However, amino acids are also present in soil as small peptides and in D-enantiomeric form. We compared the uptake and assimilation of N as free amino acid and short homopeptide in both L- and D-enantiomeric forms. Sterile roots of wheat (Triticum aestivum L.) plants were exposed to solutions containing either (14)C-labelled L-alanine, D-alanine, L-trialanine or D-trialanine at a concentration likely to be found in soil solution (10 µM). Over 5 h, plants took up L-alanine, D-alanine and L-trialanine at rates of 0.9±0.3, 0.3±0.06 and 0.3±0.04 µmol g(-1) root DW h(-1), respectively. The rate of N uptake as L-trialanine was the same as that as L-alanine. Plants lost ca.60% of amino acid C taken up in respiration, regardless of the enantiomeric form, but more (ca.80%) of the L-trialanine C than amino acid C was respired. When supplied in solutions of mixed N form, N uptake as D-alanine was ca.5-fold faster than as NO(3)(-), but slower than as L-alanine, L-trialanine and NH(4)(+). Plants showed a limited capacity to take up D-trialanine (0.04±0.03 µmol g(-1) root DW h(-1)), but did not appear to be able to metabolise it. We conclude that wheat is able to utilise L-peptide and D-amino acid N at rates comparable to those of N forms of acknowledged importance, namely L-amino acids and inorganic N. This is true even when solutes are supplied at realistic soil concentrations and when other forms of N are available. We suggest that it may be necessary to reconsider which forms of soil N are important in the terrestrial N cycle.

KW - Amino acids

KW - Nitrogen

KW - Peptides

KW - Plant roots

KW - Soil chemistry

KW - Solutions

KW - Stereoisomerism

KW - Triticum metabolism

KW - United Kingdom

U2 - 10.1371/journal.pone.0019220

DO - 10.1371/journal.pone.0019220

M3 - Article

VL - 6

JO - PLoS ONE

JF - PLoS ONE

SN - 1932-6203

IS - 4

M1 - e19220

ER -

Hill PW, Quilliam RS, DeLuca TH, Farrar J, Farrell M, Roberts P et al. Acquisition and assimilation of nitrogen as peptide-bound and D-enantiomers of amino acids by wheat. PLoS ONE. 2011 Apr 26;6(4). e19220. https://doi.org/10.1371/journal.pone.0019220