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J. Biol. Chem., Vol. 282, Issue 52, 37556-37566, December 28, 2007

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Light and Oxygen Are Not Required for Harpin-induced Cell Death^*

Marie Garmier¹, Pierrick Priault¹², Guillaume Vidal¹, Simon Driscoll^¶, Reda Djebbar^||, Martine Boccara^**, Chantal Mathieu, Christine H. Foyer^¶, and Rosine De Paepe³

From the Institut de Biotechnologie des Plantes, Université Paris-Sud 11, UMR-CNRS 8618, Bâtiment 630, 91405 Orsay cedex, France, Ecologie, Systématique et Evolution, Université Paris-Sud 11, UMR-CNRS 8079, Bâtiment 362, 91405 Orsay cedex, France, ^¶School of Agriculture, Food, and Rural Development, Agriculture Building, Newcastle University, Newcastle upon Tyne, NE1 7RU, United Kingdom, ^||Laboratoire de Physiologie Végétale, Faculté des Sciences Biologiques, Université des Sciences et de la Technologie Houari Boumedienne, BP 39, El Alia, Bab Ezzouar, 16111 Alger, Algeria, ^**Atelier de Bioinformatique, Université Pierre et Marie Curie Paris 6, 12 Rue Cuvier, Paris 75005, France

Nicotiana sylvestris leaves challenged by the bacterial elicitor harpin N_Ea were used as a model system in which to determine the respective roles of light, oxygen, photosynthesis, and respiration in the programmed cell death response in plants. The appearance of cell death markers, such as membrane damage, nuclear fragmentation, and induction of the stress-responsive element Tnt1, was observed in all conditions. However, the cell death process was delayed in the dark compared with the light, despite a similar accumulation of superoxide and hydrogen peroxide in the chloroplasts. In contrast, harpin-induced cell death was accelerated under very low oxygen (<0.1% O₂) compared with air. Oxygen deprivation impaired accumulation of chloroplastic reactive oxygen species (ROS) and the induction of cytosolic antioxidant genes in both the light and the dark. It also attenuates the collapse of photosynthetic capacity and the respiratory burst driven by mitochondrial alternative oxidase activity observed in air. Since alternative oxidase is known to limit overreduction of the respiratory chain, these results strongly suggest that mitochondrial ROS accumulate in leaves elicited under low oxygen. We conclude that the harpin-induced cell death does not require ROS accumulation in the apoplast or in the chloroplasts but that mitochondrial ROS could be important in the orchestration of the cell suicide program.

Received for publication, August 28, 2007 , and in revised form, October 19, 2007.

^* This work was supported by the Université Paris-Sud 11, the CNRS, Rothamsted Research (Crop Performance and Improvement Division), grants from the French Ministère de la Recherche et de la Technologie (to M. G., G. V., and P. P.), and joint project initiatives funded by the British Council, the UK Royal Society, and the French CNRS and Ministry of Research. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ These three authors contributed equally to this research.

² Present address: UMR UHP/INRA 1137 Ecologie et Ecophysiologie Forestières, Faculté des Sciences, Université Nancy I-BP 239, 54506 Vandoeuvre cedex, France.

³ To whom correspondence should be addressed. Tel.: 33-169153305; Fax: 33-169153423; E-mail: rosine.de-paepe{at}u-psud.fr.

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