Plant Molecular Biology 51: 597-605 (2003)
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Ozone-induced gene expression occurs via ethylene-dependent and -independent
signalling
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Grimmig B (1,5), Gonzalez-Perez M N (1,2),
Leubner-Metzger G (3,6), Vögeli-Lange R (3,7), Meins F (3), Hain R
(4), Penuelas J (2), Heidenreich B (1), Langebartels C (1), Ernst D (1),
Sanderman H Jr (1)
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(1) GSF - National Research Center for Environment
and Health, Institute of Biochemical, Plant Pathology, D-85764 Neuherberg,
Germany
(2) CREAF, Facultat di Ciencies, Universitat Autonoma, E-08193 Barcelona,
Spain
(3) Friedrich Miescher - lnstitute for Biomedical Research, A branch of
the Novartis Research Foundation, Maulbeerstr. 33, CH-4058 Basel, Switzerland
(4) Bayer AG, Landwirtschaftszentrum Monheim, Molecular Target Research
and Biotechnology, D-51368 Leverkusen, Germany; Present address: (5) Bayer
AG, BG Pflanzenschutz, Forschung/MW, D-51368 Leverkusen, Germany
(6) Universität Freiburg, Institut für Biologie II, Botanik, Schänzlestr.
1, D-79104 Freiburg, Germany
(7) Syngenta Crop Protection AG, Schwarzwaldallee 215, CH-4058 Basel, Switzerland
Received: 9 January 2002 / Accepted: 31 July 2002
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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
1 ß-1,3-glucanases (GLB and Gln2) and the grapevine resveratrol synthase
(Vstl) genes in transgenic tobacco leaves. 5'-Deletion analysis of the class
I ß-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
ß-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 ß-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 ß-1,3-glucanase
promoter containing two intact GCC boxes confered strong ozone-inducibility
to a minimal cauliflower mosaic virus (CaMV) 35S RNA promoter, wheras 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 ß-1,3-glucanase
genes. Promoter analysis of the stilbene synthase Vst1 gene unraveled 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.
Key words: ethylene, gene regulation, ozone, pathogenesis-related,
promoter, resveratrol, stilbene
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