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First published online April 10, 2009; 10.1104/pp.109.135566

Plant Physiology 150:670-683 (2009)
© 2009 American Society of Plant Biologists

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CELL BIOLOGY AND SIGNAL TRANSDUCTION

Arabidopsis Chloroplastic Glutathione Peroxidases Play a Role in Cross Talk between Photooxidative Stress and Immune Responses1,[W],[OA]

Christine C.C. Chang2,3, Ireneusz Slesak2, Lucía Jordá4, Alexey Sotnikov5, Michael Melzer, Zbigniew Miszalski, Philip M. Mullineaux, Jane E. Parker, Barbara Karpinska and Stanislaw Karpinski*

Department of Botany, Stockholm University, Frescati 10691 Stockholm, Sweden (C.C.C.C., A.S.); Institute of Plant Physiology, Polish Academy of Sciences, 30–239 Krakow, Poland (I.S., Z.M.); Department of Plant-Microbe Interactions, Max-Planck Institute for Plant Breeding Research, D–50829 Cologne, Germany (L.J., J.E.P.); Institute of Plant Genetics and Crop Plant Research, D–06466 Gatersleben, Germany (M.M.); Department of Biological Sciences, University of Essex, Colchester CO4 3SQ, United Kingdom (P.M.M.); and Department of Plants Genetics, Breeding, and Biotechnology, University of Life Sciences, 02–776 Warszawa, Poland (B.K., S.K.)

Glutathione peroxidases (GPXs; EC 1.11.1.9) are key enzymes of the antioxidant network in plants and animals. In order to investigate the role of antioxidant systems in plant chloroplasts, we generated Arabidopsis (Arabidopsis thaliana) transgenic lines that are depleted specifically in chloroplastic (cp) forms of GPX1 and GPX7. We show that reduced cpGPX expression, either in transgenic lines with lower total cpGPX expression (GPX1 and GPX7) or in a gpx7 insertion mutant, leads to compromised photooxidative stress tolerance but increased basal resistance to virulent bacteria. Depletion of both GPX1 and GPX7 expression also caused alterations in leaf cell and chloroplast morphology. Leaf tissues were characterized by shorter and more rounded palisade cells, irregular spongy mesophyll cells, and larger intercellular air spaces compared with the wild type. Chloroplasts had larger and more abundant starch grains than in wild-type and gpx7 mutant plants. Constitutively reduced cpGPX expression also led to higher foliar ascorbic acid, glutathione, and salicylic acid levels in plants exposed to higher light intensities. Our results suggest partially overlapping functions of GPX1 and GPX7. The data further point to specific changes in the chloroplast ascorbate-glutathione cycle due to reduced cpGPX expression, initiating reactive oxygen species and salicylic acid pathways that affect leaf development, light acclimation, basal defense, and cell death programs. Thus, cpGPXs regulate cellular photooxidative tolerance and immune responses.

1 This work was supported by the Polish Science Foundation strategic project Welcome 2008/1 and the Swedish Council for International Cooperation in Research and Higher Education (to S.K.), by a European Union Marie Curie fellowship (grant no. HPMF–CT–2001–01197 to L.J. and J.E.P.) and the Alexander von Humboldt Foundation, by the Institute of Plant Genetics and Crop Plant Research in Gatersleben, Germany (to M.M.), and by the Biotechnology and Biological Sciences Research Council (to P.M.M.).

2 These authors contributed equally to the article.

3 Present address: Carnegie Institution of Washington, 260 Panama Street, Stanford, CA 94305.

4 Present address: Departemento Biotecnología, Centro de Biotecnología y Genómica de Plantas, Campus Montegancedo Universidad Politécnica Madrid, Autopista M40, km38, 28223–Pozuelo de Alarcón, Spain.

5 Present address: Alexey Sotnikow Institute of Cytology RAS, 4 Tikhoretsky Avenue, 194064 St. Petersburg, Russia.

The author responsible for the distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Stanislaw Karpinski (stanislaw_karpinski{at}sggw.pl).

[W] The online version of this article contains Web-only data.

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www.plantphysiol.org/cgi/doi/10.1104/pp.109.135566

* Corresponding author; e-mail stanislaw_karpinski{at}sggw.pl.

Received January 13, 2009; accepted April 6, 2009; published April 10, 2009.

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