Rice acclimation to soil flooding: Low concentrations of organic acids can trigger a barrier to radial oxygen loss in roots

Research output: Contribution to journalArticle

Abstract

Waterlogged soils contain monocarboxylic acids produced by anaerobic microorganisms. These “organic acids” can accumulate to phytotoxic levels and promote development of a barrier to radial O2 loss (ROL) in roots of some wetland species. Environmental cues triggering root ROL barrier induction, a feature that together with tissue gas-filled porosity facilitates internal aeration, are important to elucidate for knowledge of plant stress physiology. We tested the hypothesis that comparatively low, non-toxic, concentrations of acetic, propionic, butyric, and/or hexanoic acids might induce root ROL barrier formation in rice. Each organic acid, individually, triggered the ROL barrier in roots but with no effect (acetic or butyric acids) or with only slight effects (propionic or hexanoic acids) on root extension. Transcripts of four genes related to suberin biosynthesis were increased by some of the organic acid treatments. Respiration in root tissues was not, or moderately, inhibited. Beyond a narrow concentration range, however, respiration declined exponentially and the order (least to greatest) for EC50 (effective concentration for 50% inhibition) was butyric, propionic, acetic, then hexanoic acid. An understanding of the environmental cue for root ROL barrier induction should enhance future work to elucidate the molecular regulation of this root trait contributing to plant flooding tolerance.

Original languageEnglish
Pages (from-to)2183-2197
Number of pages15
JournalPlant Cell and Environment
Volume42
Issue number7
DOIs
Publication statusPublished - 1 Jul 2019

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hexanoic acid
Acclimatization
organic acids and salts
acclimation
Caproates
Soil
Oxygen
oxygen
rice
Acids
breathing
Propionates
monocarboxylic acids
Acetic Acid
flooding tolerance
Cues
suberin
soil
Respiration
plant stress

Cite this

@article{566235f93c474151bed3eb1861b190c9,
title = "Rice acclimation to soil flooding: Low concentrations of organic acids can trigger a barrier to radial oxygen loss in roots",
abstract = "Waterlogged soils contain monocarboxylic acids produced by anaerobic microorganisms. These “organic acids” can accumulate to phytotoxic levels and promote development of a barrier to radial O2 loss (ROL) in roots of some wetland species. Environmental cues triggering root ROL barrier induction, a feature that together with tissue gas-filled porosity facilitates internal aeration, are important to elucidate for knowledge of plant stress physiology. We tested the hypothesis that comparatively low, non-toxic, concentrations of acetic, propionic, butyric, and/or hexanoic acids might induce root ROL barrier formation in rice. Each organic acid, individually, triggered the ROL barrier in roots but with no effect (acetic or butyric acids) or with only slight effects (propionic or hexanoic acids) on root extension. Transcripts of four genes related to suberin biosynthesis were increased by some of the organic acid treatments. Respiration in root tissues was not, or moderately, inhibited. Beyond a narrow concentration range, however, respiration declined exponentially and the order (least to greatest) for EC50 (effective concentration for 50{\%} inhibition) was butyric, propionic, acetic, then hexanoic acid. An understanding of the environmental cue for root ROL barrier induction should enhance future work to elucidate the molecular regulation of this root trait contributing to plant flooding tolerance.",
keywords = "aerenchyma, lignin, Oryza sativa, ROL, root internal aeration, root respiration, soil phytotoxins, soil waterlogging, suberin, transcripts",
author = "Colmer, {Timothy David} and Lukasz Kotula and Malik, {Al Imran} and Hirokazu Takahashi and Dennis Konnerup and Mikio Nakazono and Ole Pedersen",
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T1 - Rice acclimation to soil flooding

T2 - Low concentrations of organic acids can trigger a barrier to radial oxygen loss in roots

AU - Colmer, Timothy David

AU - Kotula, Lukasz

AU - Malik, Al Imran

AU - Takahashi, Hirokazu

AU - Konnerup, Dennis

AU - Nakazono, Mikio

AU - Pedersen, Ole

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N2 - Waterlogged soils contain monocarboxylic acids produced by anaerobic microorganisms. These “organic acids” can accumulate to phytotoxic levels and promote development of a barrier to radial O2 loss (ROL) in roots of some wetland species. Environmental cues triggering root ROL barrier induction, a feature that together with tissue gas-filled porosity facilitates internal aeration, are important to elucidate for knowledge of plant stress physiology. We tested the hypothesis that comparatively low, non-toxic, concentrations of acetic, propionic, butyric, and/or hexanoic acids might induce root ROL barrier formation in rice. Each organic acid, individually, triggered the ROL barrier in roots but with no effect (acetic or butyric acids) or with only slight effects (propionic or hexanoic acids) on root extension. Transcripts of four genes related to suberin biosynthesis were increased by some of the organic acid treatments. Respiration in root tissues was not, or moderately, inhibited. Beyond a narrow concentration range, however, respiration declined exponentially and the order (least to greatest) for EC50 (effective concentration for 50% inhibition) was butyric, propionic, acetic, then hexanoic acid. An understanding of the environmental cue for root ROL barrier induction should enhance future work to elucidate the molecular regulation of this root trait contributing to plant flooding tolerance.

AB - Waterlogged soils contain monocarboxylic acids produced by anaerobic microorganisms. These “organic acids” can accumulate to phytotoxic levels and promote development of a barrier to radial O2 loss (ROL) in roots of some wetland species. Environmental cues triggering root ROL barrier induction, a feature that together with tissue gas-filled porosity facilitates internal aeration, are important to elucidate for knowledge of plant stress physiology. We tested the hypothesis that comparatively low, non-toxic, concentrations of acetic, propionic, butyric, and/or hexanoic acids might induce root ROL barrier formation in rice. Each organic acid, individually, triggered the ROL barrier in roots but with no effect (acetic or butyric acids) or with only slight effects (propionic or hexanoic acids) on root extension. Transcripts of four genes related to suberin biosynthesis were increased by some of the organic acid treatments. Respiration in root tissues was not, or moderately, inhibited. Beyond a narrow concentration range, however, respiration declined exponentially and the order (least to greatest) for EC50 (effective concentration for 50% inhibition) was butyric, propionic, acetic, then hexanoic acid. An understanding of the environmental cue for root ROL barrier induction should enhance future work to elucidate the molecular regulation of this root trait contributing to plant flooding tolerance.

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KW - root internal aeration

KW - root respiration

KW - soil phytotoxins

KW - soil waterlogging

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KW - transcripts

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