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First published online February 22, 2005; 10.1104/pp.104.055681

Plant Physiology 137:1092-1104 (2005)
© 2005 American Society of Plant Biologists

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Right arrow Reactive Oxygen Species
ENVIRONMENTAL STRESS AND ADAPTATION

Ozone-Induced Programmed Cell Death in the Arabidopsis radical-induced cell death1 Mutant1

Kirk Overmyer2, Mikael Brosché, Riikka Pellinen3, Tero Kuittinen, Hannele Tuominen4, Reetta Ahlfors, Markku Keinänen5, Mart Saarma, Dierk Scheel and Jaakko Kangasjärvi*

Department of Biological and Environmental Sciences (K.O., M.B., R.P., H.T., R.A., M.K., J.K.) and Institute of Biotechnology (K.O., R.P., T.K., H.T., M.K., M.S., J.K.), University of Helsinki, FIN–00014 Helsinki, Finland; and Department of Stress and Developmental Biology, Leibniz Institute of Plant Biochemistry, D–06120 Halle/Saale, Germany (D.S.)

Short, high-concentration peaks of the atmospheric pollutant ozone (O3) cause the formation of cell death lesions on the leaves of sensitive plants. Numerous similarities between the plant responses to O3 and pathogens suggest that O3 triggers hypersensitive response-like programmed cell death (PCD). We examined O3 and superoxide-induced cell death in the O3-sensitive radical-induced cell death1 (rcd1) mutant. Dying cells in O3-exposed rcd1 exhibited several of the typical morphological characteristics of the hypersensitive response and PCD. Double-mutant analyses indicated a requirement for salicylic acid and the function of the cyclic nucleotide-gated ion channel AtCNGC2 in cell death. Furthermore, a requirement for ATPases, kinases, transcription, Ca2+ flux, caspase-like proteolytic activity, and also one or more phenylmethylsulfonyl fluoride-sensitive protease activities was shown for the development of cell death lesions in rcd1. Furthermore, mitogen-activated protein kinases showed differential activation patterns in rcd1 and Columbia. Taken together, these results directly demonstrate the induction of PCD by O3.

1 This work was supported by the Academy of Finland (grant nos. 43671 and 37995), by the Finnish Centre of Excellence Programme (2000–2005), and by an Academy of Finland/German Academic Exchange Service grant (SA10256/313–SF–PPP–pz). R.P. was supported by the Finnish Graduate program in Environmental Physiology, Molecular Biology, and Ecotechnology, the University of Kuopio, and The Finnish Graduate School in Environmental Science and Technology, Åbo Akademi.

2 Present address: Biology Department, CB No. 3280, University of North Carolina, Chapel Hill, NC 27599–3280.

3 Present address: A.I. Virtanen Institute, University of Kuopio, FIN–70211 Kuopio, Finland.

4 Present address: Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, SE–90187 Umeå, Sweden.

5 Present address: Department of Biology, University of Joensuu, PO Box 111, FIN–80101 Joensuu, Finland.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.055681.

* Corresponding author; e-mail jaakko.kangasjarvi{at}helsinki.fi; fax 358–9–191–59552.

Received October 27, 2004; returned for revision December 20, 2004; accepted December 27, 2004.




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