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J. Biol. Chem., Vol. 283, Issue 45, 31218-31226, November 7, 2008

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Flavonoids Redirect PIN-mediated Polar Auxin Fluxes during Root Gravitropic Responses^*

Diana Santelia¹, Sina Henrichs, Vincent Vincenzetti, Michael Sauer, Laurent Bigler^¶, Markus Klein, Aurélien Bailly, Youngsook Lee^||, Jií Friml², Markus Geisler³, and Enrico Martinoia^||4

From the Laboratory of Molecular Plant Physiology, Institute of Plant Biology, University of Zürich, Zollikerstrasse 107, 8008 Zürich, Switzerland, the Department of Plant Cell Biology, University of Göttingen, Untere Karspüle 2, 30073 Göttingen, Germany, the ^¶Institute of Organic Chemistry, University of Zürich, Winterthurerstrasse 190, 8057 Zürich, Switzerland, and the ^||Postech-UZH Global Research Laboratory, Pohang University of Science and Technology, Pohang 790-784, Korea

The rate, polarity, and symmetry of the flow of the plant hormone auxin are determined by the polar cellular localization of PIN-FORMED (PIN) auxin efflux carriers. Flavonoids, a class of secondary plant metabolites, have been suspected to modulate auxin transport and tropic responses. Nevertheless, the identity of specific flavonoid compounds involved and their molecular function and targets in vivo are essentially unknown. Here we show that the root elongation zone of agravitropic pin2/eir1/wav6/agr1 has an altered pattern and amount of flavonol glycosides. Application of nanomolar concentrations of flavonols to pin2 roots is sufficient to partially restore root gravitropism. By employing a quantitative cell biological approach, we demonstrate that flavonoids partially restore the formation of lateral auxin gradients in the absence of PIN2. Chemical complementation by flavonoids correlates with an asymmetric distribution of the PIN1 protein. pin2 complementation probably does not result from inhibition of auxin efflux, as supply of the auxin transport inhibitor N-1-naphthylphthalamic acid failed to restore pin2 gravitropism. We propose that flavonoids promote asymmetric PIN shifts during gravity stimulation, thus redirecting basipetal auxin streams necessary for root bending.

Received for publication, December 12, 2007 , and in revised form, August 21, 2008.

^* This work was supported by the Swiss National Foundation Grant 3100AO-111912 (to M. G.) and a grant to E. M. (within the NCCR Plant Survival), a grant from the Novartis foundation (to M. G.) and by a grant from the Ministry of Science and Technology of South Korea (to Y. L. and E. M.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. S1-S3 and Tables S1 and S2.

¹ Present address: Institute of Plant Science, ETH Zürich, Universitätstrasse 2, 8092 Zürich, Switzerland.

² Present address: Dept. of Plant Systems Biology, VIB, and Dept. of Molecular Genetics, Ghent University, 9052 Gent, Belgium.

³ To whom correspondence may be addressed. Tel.: 41-44-634-8277; Fax: 41-44-634-8204; E-mail: markus.geisler{at}botinst.uzh.ch.

⁴ To whom correspondence may be addressed. Tel.: 41-44-634-8222; Fax: 41-44-634-8204; E-mail: enrico.martinoia{at}botinst.uzh.ch.

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