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Mol Plant. 2014 Jul;7(7):1191-210. doi: 10.1093/mp/ssu070. Epub 2014 Jun 7.

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

Author information

  • 1Institut of Developmental and Molecular Biology of Plants, Plant Molecular Physiology and Biotechnology Group, Heinrich-Heine-Universität, Universitätsstraße 1, 40225 Düsseldorf, Germany Botany Department, Faculty of Science, Tanta University, 31527, Tanta, Egypt.
  • 2Institut of Developmental and Molecular Biology of Plants, Plant Molecular Physiology and Biotechnology Group, Heinrich-Heine-Universität, Universitätsstraße 1, 40225 Düsseldorf, Germany.
  • 3Department of Plant Systems Biology, VIB, and Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 927, B-9052, Gent, Belgium.
  • 4Department of Plant Systems Biology, VIB, and Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 927, B-9052, Gent, Belgium Present address: Mendel Centre for Plant Genomics and Proteomics, CEITEC-Central European Institute of Technology, Masaryk University, Kamenice 5, CZ-62500 Brno, Czech Republic.
  • 5Botanical Institute, Cologne Biocenter, University of Cologne, 50674 Cologne, Germany Cluster of Excellence on Plant Sciences (CEPLAS), 40225 Düsseldorf and 50674 Cologne, Germany.
  • 6Molecular Ecophysiology of Plants, Heinrich-Heine-Universität, Universitätsstraße 1, 40225 Düsseldorf, Germany.
  • 7Cluster of Excellence on Plant Sciences (CEPLAS), 40225 Düsseldorf and 50674 Cologne, Germany Molecular Ecophysiology of Plants, Heinrich-Heine-Universität, Universitätsstraße 1, 40225 Düsseldorf, Germany.
  • 8Institut of Developmental and Molecular Biology of Plants, Plant Molecular Physiology and Biotechnology Group, Heinrich-Heine-Universität, Universitätsstraße 1, 40225 Düsseldorf, Germany Cluster of Excellence on Plant Sciences (CEPLAS), 40225 Düsseldorf and 50674 Cologne, Germany veronica.maurino@uni-duesseldorf.de.

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; Inzé 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 responses were accompanied by the accumulation of 4-methoxy-indol-3-ylmethyl glucosinolate and stigmasterol.

KEYWORDS:

catalase; glycolate oxidase; hydrogen peroxide; oxidative signaling.; photorespiration; reactive oxygen species

PMID:
24908268
DOI:
10.1093/mp/ssu070
[PubMed - indexed for MEDLINE]
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