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J. Biol. Chem., Vol. 282, Issue 36, 26057-26066, September 7, 2007

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Molecular and Functional Characterization of a Na⁺-K⁺ Transporter from the Trk Family in the Ectomycorrhizal Fungus Hebeloma cylindrosporum^*

Claire Corratgé¹, Sabine Zimmermann, Raphaël Lambilliotte¹, Claude Plassard, Roland Marmeisse^¶, Jean-Baptiste Thibaud, Benoît Lacombe, and Hervé Sentenac^¶2

From the Biochimie et Physiologie Moléculaire des Plantes, UMR5004, CNRS/INRA/SupAgro/UM2 and Rhizosphère and Symbiose, UMR1222 INRA/SupAgro, Place Viala, F-34060 Montpellier, France and ^¶Ecologie Microbienne, UMR 5557 CNRS/UCBL1, 43 bd du 11 Novembre 1918, F-69622 Villeurbanne, France

Ectomycorrhizal symbiosis between fungi and woody plants strongly improves plant mineral nutrition and constitutes a major biological process in natural ecosystems. Molecular identification and functional characterization of fungal transport systems involved in nutrient uptake are crucial steps toward understanding the improvement of plant nutrition and the symbiotic relationship itself. In the present report a transporter belonging to the Trk family is identified in the model ectomycorrhizal fungus Hebeloma cylindrosporum and named HcTrk1. The Trk family is still poorly characterized, although it plays crucial roles in K⁺ transport in yeasts and filamentous fungi. In Saccharomyces cerevisiae K⁺ uptake is mainly dependent on the activity of Trk transporters thought to mediate H⁺:K⁺ symport. The ectomycorrhizal HcTrk1 transporter was functional when expressed in Xenopus oocytes, enabling the first electrophysiological characterization of a transporter from the Trk family. HcTrk1 mediates instantaneously activating inwardly rectifying currents, is permeable to both K⁺ and Na⁺, and displays channel-like functional properties. The whole set of data and particularly a phenomenon reminiscent of the anomalous mole fraction effect suggest that the transport does not occur according to the classical alternating access model. Permeation appears to occur through a single-file pore, where interactions between Na⁺ and K⁺ might result in Na⁺:K⁺ co-transport activity. HcTrk1 is expressed in external hyphae that explore the soil when the fungus grows in symbiotic condition. Thus, it could play a major role in both the K⁺ and Na⁺ nutrition of the fungus (and of the plant) in nutrient-poor soils.

Received for publication, December 19, 2006 , and in revised form, July 5, 2007.

^* This work was supported in part by the program Toxicologie Nucléaire Environnementale Transporters. 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 nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AM396516 [GenBank] and AM396517 [GenBank] .

¹ Supported by a Ministère de l'Education Nationale, de la Recherche et de la Technologie doctoral fellowship.

² To whom correspondence should be addressed: Biochimie et Physiologie Moléculaire des Plantes, UMR5004 CNRS/INRA/SupAgro/UMII, place Viala, F-34060 Montpellier cedex, France. Tel.: 33-499-612-605; Fax: 33-467-525-737; E-mail: sentenac{at}supagro.inra.fr.

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