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PLANTS INTERACTING WITH OTHER ORGANISMS

Truffles Regulate Plant Root Morphogenesis via the Production of Auxin and Ethylene^{1,[C],[W],[OA]}

Department of Crop Sciences, Molecular Phytopathology and Mycotoxin Research (R.S., P.K.), Forest Botany and Tree Physiology, Buesgen-Institute (U.F.), and Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences (C.G., I.F.), Georg-August University, D–37077 Goettingen, Germany

Truffles are symbiotic fungi that form ectomycorrhizas with plant roots. Here we present evidence that at an early stage of the interaction, i.e. prior to physical contact, mycelia of the white truffle Tuber borchii and the black truffle Tuber melanopsorum induce alterations in root morphology of the host Cistus incanus and the nonhost Arabidopsis (Arabidopsis thaliana; i.e. primary root shortening, lateral root formation, root hair stimulation). This was most likely due to the production of indole-3-acetic acid (IAA) and ethylene by the mycelium. Application of a mixture of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid and IAA fully mimicked the root morphology induced by the mycelium for both host and nonhost plants. Application of the single hormones only partially mimicked it. Furthermore, primary root growth was not inhibited in the Arabidopsis auxin transport mutant aux1-7 by truffle metabolites while root branching was less effected in the ethylene-insensitive mutant ein2-LH. The double mutant aux1-7;ein2-LH displayed reduced sensitivity to fungus-induced primary root shortening and branching. In agreement with the signaling nature of truffle metabolites, increased expression of the auxin response reporter DR5::GFP in Arabidopsis root meristems subjected to the mycelium could be observed, confirming that truffles modify the endogenous hormonal balance of plants. Last, we demonstrate that truffles synthesize ethylene from L-methionine probably through the -keto--(methylthio)butyric acid pathway. Taken together, these results establish the central role of IAA and ethylene as signal molecules in truffle/plant interactions.

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 Splivallo (ricsi17{at}hotmail.com).

^[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.

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www.plantphysiol.org/cgi/doi/10.1104/pp.109.141325

^* Corresponding author; e-mail ricsi17{at}hotmail.com.

Received May 12, 2009; accepted June 12, 2009; published June 17, 2009.

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On the Inside

Peter V. Minorsky
Plant Physiol. 2009 150: 1762-1763. [Full Text]