Ozone-induced gene expression occurs via ethylene-dependent and -independent signalling

Bernhard Grimmig, Maria N. Gonzalez-Perez, Gerhard Leubner-Metzger, Regina Vögeli-Lange, Fred Meins, Rüdiger Hain, Josep Penuelas, Bernd Heidenreich, Christian Langebartels, Dieter Ernst, Heinrich Sandermann

    Research output: Contribution to journalArticleResearchpeer-review

    32 Citations (Scopus)

    Abstract

    Recent studies suggest that ethylene is involved in signalling ozone-induced gene expression. We show here that application of ozone increased glucuronidase (GUS) expression of chimeric reporter genes regulated by the promoters of the tobacco class I β-1,3-glucanases (GLB and Gln2) and the grapevine resveratrol synthase (Vst1) genes in transgenic tobacco leaves. 5′-deletion analysis of the class I β-1,3-glucanase promoter revealed that ozone-induced gene regulation is mainly mediated by the distal enhancer region containing the positively acting ethylene-responsive element (ERE). In addition, application of 1-methylcyclopropene (1-MCP), an inhibitor of ethylene action, blocked ozone-induced class I β-1,3-glucanase promoter activity. Enhancer activity and ethylene-responsiveness depended on the integrity of the GCC boxes, cis-acting elements present in the ERE of the class I β-1,3-glucanase and the basic-type pathogenesis-related PR-1 protein (PRB-1b) gene promoters. The minimal PRB-1b promoter containing only the ERE with intact GCC boxes, was sufficient to confer 10-fold ozone inducibility to a GUS-reporter gene, while a substitution mutation in the GCC box abolished ozone responsiveness. The ERE region of the class I β-1,3-glucanase promoter containing two intact GCC boxes confered strong ozone inducibility to a minimal cauliflower mosaic virus (CaMV) 35S RNA promoter, whereas two single-base substitution in the GCC boxes resulted in a complete loss of ozone inducibility. Taken together, these data strongly suggest that ethylene is signalling ozone-induced expression of class I β-1,3-glucanase and PRB-1b genes. Promoter analysis of the stilbene synthase Vst1 gene unravelled different regions for ozone and ethylene-responsiveness. Application of 1-MCP blocked ethylene-induced Vst1 induction, but ozone induction was not affected. This shows that ozone-induced gene expression occurs via at least two different signalling mechanisms and suggests an additional ethylene independent signalling pathway for ozone-induced expression of genes involved in phytoalexin biosynthesis.
    Original languageEnglish
    Pages (from-to)599-607
    JournalPlant Molecular Biology
    Volume51
    Issue number4
    DOIs
    Publication statusPublished - 1 Mar 2003

    Keywords

    • Ethylene
    • Gene regulation
    • Ozone
    • Pathogenesis-related
    • Promoter
    • Resveratrol
    • Stilbene

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