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Published on October 23, 2009; 10.1104/pp.109.147231

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Received September 11, 2009
Accepted October 16, 2009

The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling

Judith Felten , Annegret Kohler , Emmanuelle Morin , Rishikesh P. Bhalerao , Klaus Palme , Francis Martin , Franck A. Ditengou , and Valerie Legue *

INRA and Nancy Universite, UMR INRA/Nancy Universite 1136 Interactions Arbres/Micro-organismes, IFR 110 "Genomique, Ecophysiologie et Ecologie Fonctionnelles", INRA Nancy, F-54280 Champenoux, France; Institutes of Biology II and Biology III, Faculty of Biology, Albert-Ludwigs-Universitat of Freiburg, Schanzlestrasse 1, D-79104 Freiburg, Germany; Umea Plant Science Center, Department of Plant Physiology, Umea University, SE-901 87 Umea, Sweden

* Corresponding author; email: Valerie.Legue{at}scbiol.uhp-nancy.fr.

The early phase of the interaction between tree roots and ectomycorrhizal (ECM) fungi, prior to symbiosis establishment, is accompanied by a stimulation of lateral root (LR) development. We aimed to identify gene networks that regulate LR development during the early signal exchanges between Populus tremula x Populus alba and the ECM fungus Laccaria bicolor with a focus on auxin transport and signaling pathways. Our data demonstrated that increased LR development in poplar and Arabidopsis thaliana interacting with L. bicolor is not dependent on the ability of the plant to form ectomycorrhizae. LR stimulation paralleled an increase in auxin accumulation at root apices. Blocking plant polar auxin transport with 1-naphthylphthalamic acid (NPA) inhibited LR development and auxin accumulation. An oligoarray-based transcript profile of poplar roots exposed to molecules released by L. bicolor revealed the differential expression of 2945 genes, including several components of polar auxin transport (PtaPIN and PtaAUX genes), auxin conjugation (PtaGH3) and auxin signaling (PtaIAA). Transcripts of PtaPIN9, the homolog of Arabidopsis AtPIN2, and several PtaIAAs accumulated specifically during the early interaction phase. Expression of these rapidly induced genes was repressed by NPA. Accordingly, LR stimulation upon contact with L. bicolor in Arabidopsis transgenic plants defective in homologs of these genes was decreased or absent. Furthermore, in Arabidopsis pin2 the root apical auxin increase during contact with the fungus was modified. We propose a model in which fungus-induced auxin accumulation at the root apex stimulates LR formation through a mechanism involving PtaPIN9-dependent auxin redistribution together with PtaIAA-based auxin-signaling.






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