Glutathione Enhances Auxin Sensitivity in Arabidopsis Roots

Root development is regulated by the tripeptide glutathione (GSH), a strong non-enzymatic antioxidant found in plants but with a poorly understood function in roots. Here, Arabidopsis mutants deficient in GSH biosynthesis (<i>cad2</i>, <i>rax1</i>, and <i>rml1</i>...

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Main Authors: Taras Pasternak, Klaus Palme, Ivan A. Paponov
Format: Article
Language:English
Published: MDPI AG 2020-11-01
Series:Biomolecules
Subjects:
Online Access:https://www.mdpi.com/2218-273X/10/11/1550
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spelling doaj-51afdc27e4c24927b65a898fd87ab5172020-11-25T04:03:32ZengMDPI AGBiomolecules2218-273X2020-11-01101550155010.3390/biom10111550Glutathione Enhances Auxin Sensitivity in Arabidopsis RootsTaras Pasternak0Klaus Palme1Ivan A. Paponov2Institute of Biology II/Molecular Plant Physiology, Centre for BioSystems Analysis, BIOSS Centre for Biological Signalling Studies University of Freiburg, 79104 Freiburg, GermanyInstitute of Biology II/Molecular Plant Physiology, Centre for BioSystems Analysis, BIOSS Centre for Biological Signalling Studies University of Freiburg, 79104 Freiburg, GermanyDepartment of Food Science, Aarhus University, 8200 Aarhus N, DenmarkRoot development is regulated by the tripeptide glutathione (GSH), a strong non-enzymatic antioxidant found in plants but with a poorly understood function in roots. Here, Arabidopsis mutants deficient in GSH biosynthesis (<i>cad2</i>, <i>rax1</i>, and <i>rml1</i>) and plants treated with the GSH biosynthesis inhibitor buthionine sulfoximine (BSO) showed root growth inhibition, significant alterations in the root apical meristem (RAM) structure (length and cell division), and defects in lateral root formation. Investigation of the molecular mechanisms of GSH action showed that GSH deficiency modulated total ubiquitination of proteins and inhibited the auxin-related, ubiquitination-dependent degradation of Aux/IAA proteins and the transcriptional activation of early auxin-responsive genes. However, the DR5 auxin transcriptional response differed in root apical meristem (RAM) and pericycle cells. The RAM DR5 signal was increased due to the up-regulation of the auxin biosynthesis TAA1 protein and down-regulation of PIN4 and PIN2, which can act as auxin sinks in the root tip. The transcription auxin response (the DR5 signal and expression of auxin responsive genes) in isolated roots, induced by a low (0.1 µM) auxin concentration, was blocked following GSH depletion of the roots by BSO treatment. A higher auxin concentration (0.5 µM) offset this GSH deficiency effect on DR5 expression, indicating that GSH deficiency does not completely block the transcriptional auxin response, but decreases its sensitivity. The ROS regulation of GSH, the active GSH role in cell proliferation, and GSH cross-talk with auxin assume a potential role for GSH in the modulation of root architecture under stress conditions.https://www.mdpi.com/2218-273X/10/11/1550auxinauxin responseglutathne (GSH)auxin transportroot apical meristemlateral root formation
collection DOAJ
language English
format Article
sources DOAJ
author Taras Pasternak
Klaus Palme
Ivan A. Paponov
spellingShingle Taras Pasternak
Klaus Palme
Ivan A. Paponov
Glutathione Enhances Auxin Sensitivity in Arabidopsis Roots
Biomolecules
auxin
auxin response
glutathne (GSH)
auxin transport
root apical meristem
lateral root formation
author_facet Taras Pasternak
Klaus Palme
Ivan A. Paponov
author_sort Taras Pasternak
title Glutathione Enhances Auxin Sensitivity in Arabidopsis Roots
title_short Glutathione Enhances Auxin Sensitivity in Arabidopsis Roots
title_full Glutathione Enhances Auxin Sensitivity in Arabidopsis Roots
title_fullStr Glutathione Enhances Auxin Sensitivity in Arabidopsis Roots
title_full_unstemmed Glutathione Enhances Auxin Sensitivity in Arabidopsis Roots
title_sort glutathione enhances auxin sensitivity in arabidopsis roots
publisher MDPI AG
series Biomolecules
issn 2218-273X
publishDate 2020-11-01
description Root development is regulated by the tripeptide glutathione (GSH), a strong non-enzymatic antioxidant found in plants but with a poorly understood function in roots. Here, Arabidopsis mutants deficient in GSH biosynthesis (<i>cad2</i>, <i>rax1</i>, and <i>rml1</i>) and plants treated with the GSH biosynthesis inhibitor buthionine sulfoximine (BSO) showed root growth inhibition, significant alterations in the root apical meristem (RAM) structure (length and cell division), and defects in lateral root formation. Investigation of the molecular mechanisms of GSH action showed that GSH deficiency modulated total ubiquitination of proteins and inhibited the auxin-related, ubiquitination-dependent degradation of Aux/IAA proteins and the transcriptional activation of early auxin-responsive genes. However, the DR5 auxin transcriptional response differed in root apical meristem (RAM) and pericycle cells. The RAM DR5 signal was increased due to the up-regulation of the auxin biosynthesis TAA1 protein and down-regulation of PIN4 and PIN2, which can act as auxin sinks in the root tip. The transcription auxin response (the DR5 signal and expression of auxin responsive genes) in isolated roots, induced by a low (0.1 µM) auxin concentration, was blocked following GSH depletion of the roots by BSO treatment. A higher auxin concentration (0.5 µM) offset this GSH deficiency effect on DR5 expression, indicating that GSH deficiency does not completely block the transcriptional auxin response, but decreases its sensitivity. The ROS regulation of GSH, the active GSH role in cell proliferation, and GSH cross-talk with auxin assume a potential role for GSH in the modulation of root architecture under stress conditions.
topic auxin
auxin response
glutathne (GSH)
auxin transport
root apical meristem
lateral root formation
url https://www.mdpi.com/2218-273X/10/11/1550
work_keys_str_mv AT taraspasternak glutathioneenhancesauxinsensitivityinarabidopsisroots
AT klauspalme glutathioneenhancesauxinsensitivityinarabidopsisroots
AT ivanapaponov glutathioneenhancesauxinsensitivityinarabidopsisroots
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