Plant Physiol. Illumina
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First published online November 7, 2002; 10.1104/pp.009712

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Plant Physiol, December 2002, Vol. 130, pp. 1918-1926

Ethylene Synthesis Regulated by Biphasic Induction of 1-Aminocyclopropane-1-Carboxylic Acid Synthase and 1-Aminocyclopropane-1-Carboxylic Acid Oxidase Genes Is Required for Hydrogen Peroxide Accumulation and Cell Death in Ozone-Exposed Tomato1

Wolfgang Moeder,2 Cornelius S. Barry,2 Airi A. Tauriainen, Christian Betz,3 Jaana Tuomainen,4 Merja Utriainen,5 Donald Grierson, Heinrich Sandermann, Christian Langebartels, and Jaakko Kangasjärvi*

Institute of Biochemical Plant Pathology, GSF-National Research Center for Environment and Health, D-85764 Oberschleissheim, Germany (W.M., C.B., H.S., C.L.); Plant Science Division, School of Biosciences, The University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD, United Kingdom (C.S.B., D.G.); Institute of Biotechnology and Division of Genetics, Department of Biosciences, University of Helsinki, FIN-00014 Helsinki, Finland (A.A.T., M.U., J.K.); Department of Ecology and Environmental Science, University of Kuopio, FIN-70211 Kuopio, Finland (J.T.); and Plant Physiology and Molecular Biology, Department of Biology, University of Turku, FIN-20014 Turku, Finland (J.K.)

We show that above a certain threshold concentration, ozone leads to leaf injury in tomato (Lycopersicon esculentum). Ozone-induced leaf damage was preceded by a rapid increase in 1-aminocyclopropane-1-carboxylic acid (ACC) synthase activity, ACC content, and ethylene emission. Changes in mRNA levels of specific ACC synthase, ACC oxidase, and ethylene receptor genes occurred within 1 to 5 h. Expression of the genes encoding components of ethylene biosynthesis and perception, and biochemistry of ethylene synthesis suggested that ozone-induced ethylene synthesis in tomato is under biphasic control. In transgenic plants containing an LE-ACO1 promoter-beta -glucuronidase fusion construct, beta -glucuronidase activity increased rapidly at the beginning of the O3 exposure and had a spatial distribution resembling the pattern of extracellular H2O2 production at 7 h, which coincided with the cell death pattern after 24 h. Ethylene synthesis and perception were required for active H2O2 production and cell death resulting in visible tissue damage. The results demonstrate a selective ozone response of ethylene biosynthetic genes and suggest a role for ethylene, in combination with the burst of H2O2 production, in regulating the spread of cell death.

1 This work was supported by the Scientific Council of Research of Environment and Natural Resources in Finland (grant nos. 33200 and 8822), by the Finnish Centre of Excellence Program (2000-2005), by the European Union (grant no. FAIR-CT97-3493, TOMSTRESS), by Bayerisches Staatsministerium für Landesentwicklung und Umweltfragen, by Deutsche Forschungsgemeinschaft (grant no. SFB 607), and by the Biotechnology and Biological Sciences Research Council (grant no. 42/P09465).

2 Present address: Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, NY 14853.

3 Present address: MWG Biotech AG, Anzinger Str. 7, D-85560 Ebersberg, Germany.

4 Present address: North Savo Regional Environment Centre, POB 1049, FIN-70101 Kuopio, Finland.

5 Present address: Janssen-Cilag Oy, Metsänneidonkuja 8 FIN-02130 Espoo, Finland.

* Corresponding author; e-mail jaakko.kangasjarvi{at}utu.fi; fax 358-2-333-5549.

© 2002 American Society of Plant Biologists


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