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

(2014) MOLECULAR PLANT. 7(7). p.1191-1210
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Biotechnology for a sustainable economy (Bio-Economy)
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.
Keywords
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

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Citation

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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.
@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},
}

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