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CELL BIOLOGY AND SIGNAL TRANSDUCTION

Silencing of the Mitochondrial Ascorbate Synthesizing Enzyme L-Galactono-1,4-Lactone Dehydrogenase Affects Plant and Fruit Development in Tomato^1,[W],[OA]

Institut National de la Recherche Agronomique, Université Bordeaux 1, Université Victor Ségalen-Bordeaux 2, Institut Fédératif de Recherche 103, Unité Mixte de Recherche 619 sur la Biologie du Fruit, Centre de Recherche Institut National de la Recherche Agronomique de Bordeaux, BP 81, 33883 Villenave d'Ornon cedex, France (M.A., F.M., L.G., V.G., D.J., J.P., B.B., C.R., P.B.); and Max-Planck-Institut für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, 14467 Potsdam-Golm, Germany (A.N.-N., A.R.F.)

L-Galactono-1,4-lactone dehydrogenase (EC 1.3.2.3) catalyzes the last step in the main pathway of vitamin C (L-ascorbic acid) biosynthesis in higher plants. In this study, we first characterized the spatial and temporal expression of SlGalLDH in several organs of tomato (Solanum lycopersicum) plants in parallel with the ascorbate content. P_35S:Slgalldh^RNAi silenced transgenic tomato lines were then generated using an RNAi strategy to evaluate the effect of any resulting modification of the ascorbate pool on plant and fruit development. In all P_35S:Slgalldh^RNAi plants with reduced SlGalLDH transcript and activity, plant growth rate was decreased. Plants displaying the most severe effects (dwarf plants with no fruit) were excluded from further analysis. The most affected lines studied exhibited up to an 80% reduction in SlGalLDH activity and showed a strong reduction in leaf and fruit size, mainly as a consequence of reduced cell expansion. This was accompanied by significant changes in mitochondrial function and altered ascorbate redox state despite the fact that the total ascorbate content remained unchanged. By using a combination of transcriptomic and metabolomic approaches, we further demonstrated that several primary, like the tricarboxylic acid cycle, as well as secondary metabolic pathways related to stress response were modified in leaves and fruit of P_35S:Slgalldh^RNAi plants. When taken together, this work confirms the complexity of ascorbate regulation and its link with plant metabolism. Moreover, it strongly suggests that, in addition to ascorbate synthesis, GalLDH could play an important role in the regulation of cell growth-related processes in plants.

The author responsible for 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: Pierre Baldet (baldet{at}bordeaux.inra.fr).

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

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www.plantphysiol.org/cgi/doi/10.1104/pp.107.106500

^* Corresponding author; e-mail baldet{at}bordeaux.inra.fr.

Received July 31, 2007; accepted September 25, 2007; published October 5, 2007.