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Spatial H2O2 signaling specificity: H2O2 from chloroplasts and peroxisomes modulates the plant transcriptome differentially

Nasser Sewelam, Nils Jaspert, Katrien Van Der Kelen, Vanesa Tognetti UGent, Jessica Schmitz, Henning Frerigmann, Elia Stahl, Jürgen Zeier, Frank Van Breusegem UGent and Veronica G Maurino (2014) MOLECULAR PLANT. 7(7). p.1191-1210
abstract
Hydrogen peroxide (H2O2) operates as a signaling molecule in eukaryotes, but the specificity of its signaling capacities remains largely unrevealed. Here, we analyzed whether a moderate production of H2O2 from two different plant cellular compartments has divergent effects on the plant transcriptome. Arabidopsis thaliana overexpressing glycolate oxidase in the chloroplast (Fahnenstich et al., 2008; Balazadeh et al., 2012) and plants deficient in peroxisomal catalase (Queval et al., 2007; Inze et al., 2012) were grown under non-photorespiratory conditions and then transferred to photorespiratory conditions to foster the production of H2O2 in both organelles. We show that H2O2 originating in a specific organelle induces two types of responses: one that integrates signals independently from the subcellular site of H2O2 production and another that is dependent on the H2O2 production site. H2O2 produced in peroxisomes induces transcripts involved in protein repair responses, while H2O2 produced in chloroplasts induces early signaling responses, including transcription factors and biosynthetic genes involved in production of secondary signaling messengers. There is a significant bias towards the induction of genes involved in responses to wounding and pathogen attack by chloroplastic-produced H2O2, including indolic glucosinolates-, camalexin-, and stigmasterol-biosynthetic genes. These transcriptional (r)esponses were accompanied by the accumulation of 4-methoxy-indol-3-ylmethyl glucosinolate and stigmasterol.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
OXIDATIVE STRESS-RESPONSE, INTRACELLULAR HYDROGEN-PEROXIDE, SUBCELLULAR-LOCALIZATION, INDUCED GENE-EXPRESSION, GUARD-CELLS, HIGH LIGHT, PROTEIN, oxidative signaling, OXYGEN, photorespiration, CELL-DEATH, ARABIDOPSIS-THALIANA, catalase, glycolate oxidase, hydrogen peroxide, reactive oxygen species
journal title
MOLECULAR PLANT
Mol. Plant.
volume
7
issue
7
pages
1191 - 1210
Web of Science type
Article
Web of Science id
000339947600009
JCR category
PLANT SCIENCES
JCR impact factor
6.337 (2014)
JCR rank
9/204 (2014)
JCR quartile
1 (2014)
ISSN
1674-2052
DOI
10.1093/mp/ssu070
project
Biotechnology for a sustainable economy (Bio-Economy)
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
5709853
handle
http://hdl.handle.net/1854/LU-5709853
date created
2014-09-24 16:50:09
date last changed
2016-12-19 15:47:32
@article{5709853,
  abstract     = {Hydrogen peroxide (H2O2) operates as a signaling molecule in eukaryotes, but the specificity of its signaling capacities remains largely unrevealed. Here, we analyzed whether a moderate production of H2O2 from two different plant cellular compartments has divergent effects on the plant transcriptome. Arabidopsis thaliana overexpressing glycolate oxidase in the chloroplast (Fahnenstich et al., 2008; Balazadeh et al., 2012) and plants deficient in peroxisomal catalase (Queval et al., 2007; Inze et al., 2012) were grown under non-photorespiratory conditions and then transferred to photorespiratory conditions to foster the production of H2O2 in both organelles. We show that H2O2 originating in a specific organelle induces two types of responses: one that integrates signals independently from the subcellular site of H2O2 production and another that is dependent on the H2O2 production site. H2O2 produced in peroxisomes induces transcripts involved in protein repair responses, while H2O2 produced in chloroplasts induces early signaling responses, including transcription factors and biosynthetic genes involved in production of secondary signaling messengers. There is a significant bias towards the induction of genes involved in responses to wounding and pathogen attack by chloroplastic-produced H2O2, including indolic glucosinolates-, camalexin-, and stigmasterol-biosynthetic genes. These transcriptional (r)esponses were accompanied by the accumulation of 4-methoxy-indol-3-ylmethyl glucosinolate and stigmasterol.},
  author       = {Sewelam, Nasser and Jaspert, Nils and Van Der Kelen, Katrien and Tognetti, Vanesa and Schmitz, Jessica and Frerigmann, Henning and Stahl, Elia and Zeier, J{\"u}rgen and Van Breusegem, Frank and Maurino, Veronica G},
  issn         = {1674-2052},
  journal      = {MOLECULAR PLANT},
  keyword      = {OXIDATIVE STRESS-RESPONSE,INTRACELLULAR HYDROGEN-PEROXIDE,SUBCELLULAR-LOCALIZATION,INDUCED GENE-EXPRESSION,GUARD-CELLS,HIGH LIGHT,PROTEIN,oxidative signaling,OXYGEN,photorespiration,CELL-DEATH,ARABIDOPSIS-THALIANA,catalase,glycolate oxidase,hydrogen peroxide,reactive oxygen species},
  language     = {eng},
  number       = {7},
  pages        = {1191--1210},
  title        = {Spatial H2O2 signaling specificity: H2O2 from chloroplasts and peroxisomes modulates the plant transcriptome differentially},
  url          = {http://dx.doi.org/10.1093/mp/ssu070},
  volume       = {7},
  year         = {2014},
}

Chicago
Sewelam, Nasser, Nils Jaspert, Katrien Van Der Kelen, Vanesa Tognetti, Jessica Schmitz, Henning Frerigmann, Elia Stahl, Jürgen Zeier, Frank Van Breusegem, and Veronica G Maurino. 2014. “Spatial H2O2 Signaling Specificity: H2O2 from Chloroplasts and Peroxisomes Modulates the Plant Transcriptome Differentially.” Molecular Plant 7 (7): 1191–1210.
APA
Sewelam, N., Jaspert, N., Van Der Kelen, K., Tognetti, V., Schmitz, J., Frerigmann, H., Stahl, E., et al. (2014). Spatial H2O2 signaling specificity: H2O2 from chloroplasts and peroxisomes modulates the plant transcriptome differentially. MOLECULAR PLANT, 7(7), 1191–1210.
Vancouver
1.
Sewelam N, Jaspert N, Van Der Kelen K, Tognetti V, Schmitz J, Frerigmann H, et al. Spatial H2O2 signaling specificity: H2O2 from chloroplasts and peroxisomes modulates the plant transcriptome differentially. MOLECULAR PLANT. 2014;7(7):1191–210.
MLA
Sewelam, Nasser, Nils Jaspert, Katrien Van Der Kelen, et al. “Spatial H2O2 Signaling Specificity: H2O2 from Chloroplasts and Peroxisomes Modulates the Plant Transcriptome Differentially.” MOLECULAR PLANT 7.7 (2014): 1191–1210. Print.