Auxin increases the hydrogen peroxide (H 2 O 2 ) concentration in tomato (Solanum lycopersicum) root tips while inhibiting root growth

Maria G. Ivanchenko, Désirée Den Os, Gabriele Brigitte Monshausen, Joseph G. Dubrovsky, Andrea Bednářová, Natraj Krishnan

Research output: Contribution to journalArticle

43 Citations (Scopus)

Abstract

Background and AimsThe hormone auxin and reactive oxygen species (ROS) regulate root elongation, but the interactions between the two pathways are not well understood. The aim of this study was to investigate how auxin interacts with ROS in regulating root elongation in tomato, Solanum lycopersicum. MethodsWild-type and auxin-resistant mutant, diageotropica (dgt), of tomato (S. lycopersicum 'Ailsa Craig') were characterized in terms of root apical meristem and elongation zone histology, expression of the cell-cycle marker gene Sl-CycB1;1, accumulation of ROS, response to auxin and hydrogen peroxide (H 2 O 2 ), and expression of ROS-related mRNAs.Key ResultsThe dgt mutant exhibited histological defects in the root apical meristem and elongation zone and displayed a constitutively increased level of hydrogen peroxide (H 2 O 2 ) in the root tip, part of which was detected in the apoplast. Treatments of wild-type with auxin increased the H 2 O 2 concentration in the root tip in a dose-dependent manner. Auxin and H 2 O 2 elicited similar inhibition of cell elongation while bringing forth differential responses in terms of meristem length and number of cells in the elongation zone. Auxin treatments affected the expression of mRNAs of ROS-scavenging enzymes and less significantly mRNAs related to antioxidant level. The dgt mutation resulted in resistance to both auxin and H 2 O 2 and affected profoundly the expression of mRNAs related to antioxidant level. Conclusions The results indicate that auxin regulates the level of H 2 O 2 in the root tip, so increasing the auxin level triggers accumulation of H 2 O 2 leading to inhibition of root cell elongation and root growth. The dgt mutation affects this pathway by reducing the auxin responsiveness of tissues and by disrupting the H 2 O 2 homeostasis in the root tip.

Original languageEnglish (US)
Pages (from-to)1107-1116
Number of pages10
JournalAnnals of botany
Volume112
Issue number6
DOIs
StatePublished - Oct 1 2013

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Solanum lycopersicum
root tips
hydrogen peroxide
auxins
root growth
tomatoes
reactive oxygen species
cell growth
root meristems
apical meristems
mutation
antioxidants
mutants
apoplast
meristems
histology
cell cycle
homeostasis
hormones
genetic markers

All Science Journal Classification (ASJC) codes

  • Plant Science

Cite this

Ivanchenko, Maria G. ; Den Os, Désirée ; Monshausen, Gabriele Brigitte ; Dubrovsky, Joseph G. ; Bednářová, Andrea ; Krishnan, Natraj. / Auxin increases the hydrogen peroxide (H 2 O 2 ) concentration in tomato (Solanum lycopersicum) root tips while inhibiting root growth In: Annals of botany. 2013 ; Vol. 112, No. 6. pp. 1107-1116.
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abstract = "Background and AimsThe hormone auxin and reactive oxygen species (ROS) regulate root elongation, but the interactions between the two pathways are not well understood. The aim of this study was to investigate how auxin interacts with ROS in regulating root elongation in tomato, Solanum lycopersicum. MethodsWild-type and auxin-resistant mutant, diageotropica (dgt), of tomato (S. lycopersicum 'Ailsa Craig') were characterized in terms of root apical meristem and elongation zone histology, expression of the cell-cycle marker gene Sl-CycB1;1, accumulation of ROS, response to auxin and hydrogen peroxide (H 2 O 2 ), and expression of ROS-related mRNAs.Key ResultsThe dgt mutant exhibited histological defects in the root apical meristem and elongation zone and displayed a constitutively increased level of hydrogen peroxide (H 2 O 2 ) in the root tip, part of which was detected in the apoplast. Treatments of wild-type with auxin increased the H 2 O 2 concentration in the root tip in a dose-dependent manner. Auxin and H 2 O 2 elicited similar inhibition of cell elongation while bringing forth differential responses in terms of meristem length and number of cells in the elongation zone. Auxin treatments affected the expression of mRNAs of ROS-scavenging enzymes and less significantly mRNAs related to antioxidant level. The dgt mutation resulted in resistance to both auxin and H 2 O 2 and affected profoundly the expression of mRNAs related to antioxidant level. Conclusions The results indicate that auxin regulates the level of H 2 O 2 in the root tip, so increasing the auxin level triggers accumulation of H 2 O 2 leading to inhibition of root cell elongation and root growth. The dgt mutation affects this pathway by reducing the auxin responsiveness of tissues and by disrupting the H 2 O 2 homeostasis in the root tip.",
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Auxin increases the hydrogen peroxide (H 2 O 2 ) concentration in tomato (Solanum lycopersicum) root tips while inhibiting root growth . / Ivanchenko, Maria G.; Den Os, Désirée; Monshausen, Gabriele Brigitte; Dubrovsky, Joseph G.; Bednářová, Andrea; Krishnan, Natraj.

In: Annals of botany, Vol. 112, No. 6, 01.10.2013, p. 1107-1116.

Research output: Contribution to journalArticle

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T1 - Auxin increases the hydrogen peroxide (H 2 O 2 ) concentration in tomato (Solanum lycopersicum) root tips while inhibiting root growth

AU - Ivanchenko, Maria G.

AU - Den Os, Désirée

AU - Monshausen, Gabriele Brigitte

AU - Dubrovsky, Joseph G.

AU - Bednářová, Andrea

AU - Krishnan, Natraj

PY - 2013/10/1

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N2 - Background and AimsThe hormone auxin and reactive oxygen species (ROS) regulate root elongation, but the interactions between the two pathways are not well understood. The aim of this study was to investigate how auxin interacts with ROS in regulating root elongation in tomato, Solanum lycopersicum. MethodsWild-type and auxin-resistant mutant, diageotropica (dgt), of tomato (S. lycopersicum 'Ailsa Craig') were characterized in terms of root apical meristem and elongation zone histology, expression of the cell-cycle marker gene Sl-CycB1;1, accumulation of ROS, response to auxin and hydrogen peroxide (H 2 O 2 ), and expression of ROS-related mRNAs.Key ResultsThe dgt mutant exhibited histological defects in the root apical meristem and elongation zone and displayed a constitutively increased level of hydrogen peroxide (H 2 O 2 ) in the root tip, part of which was detected in the apoplast. Treatments of wild-type with auxin increased the H 2 O 2 concentration in the root tip in a dose-dependent manner. Auxin and H 2 O 2 elicited similar inhibition of cell elongation while bringing forth differential responses in terms of meristem length and number of cells in the elongation zone. Auxin treatments affected the expression of mRNAs of ROS-scavenging enzymes and less significantly mRNAs related to antioxidant level. The dgt mutation resulted in resistance to both auxin and H 2 O 2 and affected profoundly the expression of mRNAs related to antioxidant level. Conclusions The results indicate that auxin regulates the level of H 2 O 2 in the root tip, so increasing the auxin level triggers accumulation of H 2 O 2 leading to inhibition of root cell elongation and root growth. The dgt mutation affects this pathway by reducing the auxin responsiveness of tissues and by disrupting the H 2 O 2 homeostasis in the root tip.

AB - Background and AimsThe hormone auxin and reactive oxygen species (ROS) regulate root elongation, but the interactions between the two pathways are not well understood. The aim of this study was to investigate how auxin interacts with ROS in regulating root elongation in tomato, Solanum lycopersicum. MethodsWild-type and auxin-resistant mutant, diageotropica (dgt), of tomato (S. lycopersicum 'Ailsa Craig') were characterized in terms of root apical meristem and elongation zone histology, expression of the cell-cycle marker gene Sl-CycB1;1, accumulation of ROS, response to auxin and hydrogen peroxide (H 2 O 2 ), and expression of ROS-related mRNAs.Key ResultsThe dgt mutant exhibited histological defects in the root apical meristem and elongation zone and displayed a constitutively increased level of hydrogen peroxide (H 2 O 2 ) in the root tip, part of which was detected in the apoplast. Treatments of wild-type with auxin increased the H 2 O 2 concentration in the root tip in a dose-dependent manner. Auxin and H 2 O 2 elicited similar inhibition of cell elongation while bringing forth differential responses in terms of meristem length and number of cells in the elongation zone. Auxin treatments affected the expression of mRNAs of ROS-scavenging enzymes and less significantly mRNAs related to antioxidant level. The dgt mutation resulted in resistance to both auxin and H 2 O 2 and affected profoundly the expression of mRNAs related to antioxidant level. Conclusions The results indicate that auxin regulates the level of H 2 O 2 in the root tip, so increasing the auxin level triggers accumulation of H 2 O 2 leading to inhibition of root cell elongation and root growth. The dgt mutation affects this pathway by reducing the auxin responsiveness of tissues and by disrupting the H 2 O 2 homeostasis in the root tip.

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