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ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

Phosphate (Pi) Starvation Effect on the Cytosolic Pi Concentration and Pi Exchanges across the Tonoplast in Plant Cells: An in Vivo ³¹P-Nuclear Magnetic Resonance Study Using Methylphosphonate as a Pi Analog^1,[W],[OA]

Laboratoire de Physiologie Cellulaire Végétale, Unité Mixte de Recherche 5168, Institut de Recherche en Technologies et Sciences pour le Vivant, Commissariat à l'Energie Atomique, 38054 Grenoble cedex 9, France (J.P., A.-M.B., E.G., R.B., R.D.); and Station Alpine Joseph Fourier, Unité Mixte de Service 2925, Université Joseph Fourier, 38041 Grenoble cedex 9, France (S.A.)

In vivo ³¹P-NMR analyses showed that the phosphate (Pi) concentration in the cytosol of sycamore (Acer pseudoplatanus) and Arabidopsis (Arabidopsis thaliana) cells was much lower than the cytoplasmic Pi concentrations usually considered (60–80 µM instead of >1 mM) and that it dropped very rapidly following the onset of Pi starvation. The Pi efflux from the vacuole was insufficient to compensate for the absence of external Pi supply, suggesting that the drop of cytosolic Pi might be the first endogenous signal triggering the Pi starvation rescue metabolism. Successive short sequences of Pi supply and deprivation showed that added Pi transiently accumulated in the cytosol, then in the stroma and matrix of organelles bounded by two membranes (plastids and mitochondria, respectively), and subsequently in the vacuole. The Pi analog methylphosphonate (MeP) was used to analyze Pi exchanges across the tonoplast. MeP incorporated into cells via the Pi carrier of the plasma membrane; it accumulated massively in the cytosol and prevented Pi efflux from the vacuole. This blocking of vacuolar Pi efflux was confirmed by in vitro assays with purified vacuoles. Subsequent incorporation of Pi into the cells triggered a massive transfer of MeP from the cytosol to the vacuole. Mechanisms for Pi exchanges across the tonoplast are discussed in the light of the low cytosolic Pi level, the cell response to Pi starvation, and the Pi/MeP interactive effects.

² Present address: Internationella Engelska, Gymnasiet Södermalm Allahelgonagatan 4, 118 58 Stockholm, Sweden.

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: Richard Bligny (rbligny{at}cea.fr).

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

^[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.109.144626

^* Corresponding author; e-mail rbligny{at}cea.fr.

Received July 10, 2009; accepted September 4, 2009; published September 15, 2009.