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ENVIRONMENTAL STRESS AND ADAPTATION

A Role for Auxin Redistribution in the Responses of the Root System Architecture to Phosphate Starvation in Arabidopsis¹

Laboratoire de Biochimie and Physiologie Moléculaire des Plantes, Unité Mixte de Recherche 5004, Institut National de la Recherche Agronomique/Centre National de la Recherche Scientifique/Ecole Nationale Supérieure Agronomique de Montpellier/Université Montpellier 2, F–34060 Montpellier cedex 1, France (P.N., G.C., M.R., P.D.); Laboratoire d'Ecophysiologie des Plantes sous Stress Environnementaux, Unité Mixte de Recherche 759, Institut National de la Recherche Agronomique/Ecole Nationale Supérieure Agronomique de Montpellier, F–34060 Montpellier cedex 1, France (B.M.); and Laboratory of Plant Physiology and Biochemistry, University of Antwerp, Campus Drie Eiken, B-2610 Wilrijk, Belgium (A.A., H.V.O.)

The changes in root system architecture (RSA) triggered by phosphate (P) deprivation were studied in Arabidopsis (Arabidopsis thaliana) plants grown for 14 d on 1 mM or 3 µM P. Two different temporal phases were observed in the response of RSA to low P. First, lateral root (LR) development was promoted between days 7 and 11 after germination, but, after day 11, all root growth parameters were negatively affected, leading to a general reduction of primary root (PR) and LR lengths and of LR density. Low P availability had contrasting effects on various stages of LR development, with a marked inhibition of primordia initiation but a strong stimulation of activation of the initiated primordia. The involvement of auxin signaling in these morphological changes was investigated in wild-type plants treated with indole-3-acetic acid or 2,3,5-triiodobenzoic acid and in axr4-1, aux1-7, and eir1-1 mutants. Most effects of low P on RSA were dramatically modified in the mutants or hormone-treated wild-type plants. This shows that auxin plays a major role in the P starvation-induced changes of root development. From these data, we hypothesize that several aspects of the RSA response to low P are triggered by local modifications of auxin concentration. A model is proposed that postulates that P starvation results in (1) an overaccumulation of auxin in the apex of the PR and in young LRs, (2) an overaccumulation of auxin or a change in sensitivity to auxin in the lateral primordia, and (3) a decrease in auxin concentration in the lateral primordia initiation zone of the PR and in old laterals. Measurements of local changes in auxin concentrations induced by low P, either by direct quantification or by biosensor expression pattern (DR5::-glucuronidase reporter gene), are in line with these hypotheses. Furthermore, the observation that low P availability mimicked the action of auxin in promoting LR development in the alf3 mutant confirmed that P starvation stimulates primordia emergence through increased accumulation of auxin or change in sensitivity to auxin in the primordia. Both the strong effect of 2,3,5-triiodobenzoic acid and the phenotype of the auxin-transport mutants (aux1, eir1) suggest that low P availability modifies local auxin concentrations within the root system through changes in auxin transport rather than auxin synthesis.

² Present address: Laboratoire de Protéomique, UR 1199 Institut National de la Recherche Agronomique, 2 place Viala, F–34060 Montpellier cedex 1 France.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.060061.

^* Corresponding author; e-mail nacry{at}ensam.inra.fr; fax 33–4–67–52–57–37.

Received January 24, 2005; returned for revision April 13, 2005; accepted May 10, 2005.

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