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(Homo)glutathione Depletion Modulates Host Gene Expression during the Symbiotic Interaction between Medicago truncatula and Sinorhizobium meliloti^[C],[W]

Interactions Biotiques et Santé Végétale, Unité Mixte de Recherche, Institut National de la Recherche Agronomique 1301, Centre National de la Recherche Scientifique 6243, Université de Nice-Sophia Antipolis, 06903 Sophia Antipolis cedex, France (C.P., G.I., A.L., J.H., M.C., M.P., N.P., A.P., P.F.); and Department of Plant Systems Biology, Flanders Institute for Biotechnology, and Department of Plant Biotechnology and Genetics, Ghent University, 9052 Ghent, Belgium (W.V.d.V., S.G., M.H.)

Under nitrogen-limiting conditions, legumes interact with symbiotic rhizobia to produce nitrogen-fixing root nodules. We have previously shown that glutathione and homoglutathione [(h)GSH] deficiencies impaired Medicago truncatula symbiosis efficiency, showing the importance of the low M_r thiols during the nodulation process in the model legume M. truncatula. In this study, the plant transcriptomic response to Sinorhizobium meliloti infection under (h)GSH depletion was investigated using cDNA-amplified fragment length polymorphism analysis. Among 6,149 expression tags monitored, 181 genes displayed significant differential expression between inoculated control and inoculated (h)GSH depleted roots. Quantitative reverse transcription polymerase chain reaction analysis confirmed the changes in mRNA levels. This transcriptomic analysis shows a down-regulation of genes involved in meristem formation and a modulation of the expression of stress-related genes in (h)GSH-depleted plants. Promoter-β-glucuronidase histochemical analysis showed that the putative MtPIP2 aquaporin might be up-regulated during nodule meristem formation and that this up-regulation is inhibited under (h)GSH depletion. (h)GSH depletion enhances the expression of salicylic acid (SA)-regulated genes after S. meliloti infection and the expression of SA-regulated genes after exogenous SA treatment. Modification of water transport and SA signaling pathway observed under (h)GSH deficiency contribute to explain how (h)GSH depletion alters the proper development of the symbiotic interaction.

² Present address: Plant and Crop Physiology Laboratory, Scuola Superiore Santa Anna, Via Mariscoglio 34, 56124 Pisa, Italy.

³ Present address: Institut des Sciences du Végétal, Centre National de la Recherche Scientifique, bat 23, avenue de la Terrasse, 91198 Gif-sur-Yvette cedex, France.

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: Alain Puppo (puppo{at}unice.fr).

^[C] Some figures in this article are displayed in color online but in black and white in the print edition.

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

www.plantphysiol.org/cgi/doi/10.1104/pp.109.142034

^* Corresponding author; e-mail puppo{at}unice.fr.

Received May 25, 2009; accepted July 1, 2009; published July 8, 2009.