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A Diffusible Signal from Arbuscular Mycorrhizal Fungi Elicits a Transient Cytosolic Calcium Elevation in Host Plant Cells^1,[W]

Dipartimento di Biologia, Università di Padova, 35131 Padova, Italy (L.N., R.M., B.B., P.M.); and Dipartimento di Biologia Vegetale, Università di Torino e Istituto per la Protezione delle Piante, Consiglio Nazionale delle Ricerche, 10125 Torino, Italy (A.G., M.N., P.B.)

The implication of calcium as intracellular messenger in the arbuscular mycorrhizal (AM) symbiosis has not yet been directly demonstrated, although often envisaged. We used soybean (Glycine max) cell cultures stably expressing the bioluminescent Ca²⁺ indicator aequorin to detect intracellular Ca²⁺ changes in response to the culture medium of spores of Gigaspora margarita germinating in the absence of the plant partner. Rapid and transient elevations in cytosolic free Ca²⁺ were recorded, indicating that diffusible molecules released by the mycorrhizal fungus are perceived by host plant cells through a Ca²⁺-mediated signaling. Similar responses were also triggered by two Glomus isolates. The fungal molecules active in generating the Ca²⁺ transient were constitutively released in the medium, and the induced Ca²⁺ signature was not modified by the coculture of germinating spores with plant cells. Even ungerminated spores were able to generate the signaling molecules, as proven when the germination was blocked by a low temperature. The fungal molecules were found to be stable to heat treatment, of small molecular mass (<3 kD), and, on the basis of extraction with an organic solvent, partially lipophilic. Evidence for the specificity of such an early fungal signal to the AM symbiosis is suggested by the lack of a Ca²⁺ response in cultured cells of the nonhost plant Arabidopsis (Arabidopsis thaliana) and by the up-regulation in soybean cells of genes related to Medicago truncatula DMI1, DMI2, and DMI3 and considered essential for the establishment of the AM symbiosis.

² These authors contributed equally to the paper.

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: Lorella Navazio (lorella.navazio{at}unipd.it).

^[W] The online version of this article contains Web-only data.

www.plantphysiol.org/cgi/doi/10.1104/pp.106.086959

^* Corresponding author; e-mail lorella.navazio{at}unipd.it; fax 39–049–8276295.

Received July 20, 2006; accepted November 21, 2006; published December 1, 2006.

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