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BIOENERGETICS AND PHOTOSYNTHESIS

Dual Role of the Plastid Terminal Oxidase in Tomato

Centre National de la Recherche Scientifique and Université Joseph Fourier, Laboratory Plastes et Différenciation Cellulaire, 38041 Grenoble, France (M.S., A.-M.L., M.K.); and Institut für Biologie I, Pflanzenphysiologie, Universität Leipzig, D–04103 Leipzig, Germany (M.G.)

The plastid terminal oxidase (PTOX) is a plastoquinol oxidase whose absence in tomato (Solanum lycopersicum) results in the ghost (gh) phenotype characterized by variegated leaves (with green and bleached sectors) and by carotenoid-deficient ripe fruit. We show that PTOX deficiency leads to photobleaching in cotyledons exposed to high light primarily as a consequence of reduced ability to synthesize carotenoids in the gh mutant, which is consistent with the known role of PTOX as a phytoene desaturase cofactor. In contrast, when entirely green adult leaves from gh were produced and submitted to photobleaching high light conditions, no evidence for a deficiency in carotenoid biosynthesis was obtained. Rather, consistent evidence indicates that the absence of PTOX renders the tomato leaf photosynthetic apparatus more sensitive to light via a disturbance of the plastoquinone redox status. Although gh fruit are normally bleached (most likely as a consequence of a deficiency in carotenoid biosynthesis at an early developmental stage), green adult fruit could be obtained and submitted to photobleaching high light conditions. Again, our data suggest a role of PTOX in the regulation of photosynthetic electron transport in adult green fruit, rather than a role principally devoted to carotenoid biosynthesis. In contrast, ripening fruit are primarily dependent on PTOX and on plastid integrity for carotenoid desaturation. In summary, our data show a dual role for PTOX. Its activity is necessary for efficient carotenoid desaturation in some organs at some developmental stages, but not all, suggesting the existence of a PTOX-independent pathway for plastoquinol reoxidation in association with phytoene desaturase. As a second role, PTOX is implicated in a chlororespiratory mechanism in green tissues.

www.plantphysiol.org/cgi/doi/10.1104/pp.107.106336

^* Corresponding author; e-mail marcel.kuntz{at}ujf-grenoble.fr.

Received July 26, 2007; accepted September 10, 2007; published September 14, 2007.

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