Plant potassium nutrition in ectomycorrhizal symbiosis: properties and roles of the three fungal TOK potassium channels in Hebeloma cylindrosporum

Maria del Carmen Guerrero (1) , Amandine Delteil (2) , Kevin Garcia (1, 3, 4) , Gabriella Houdinet (1) , Geneviève Conejero (1, 5, 6, 7) , Isabelle Gaillard (1) , Herve Sentenac (1) , Sabine Zimmermann (1)

1 BPMP - Biochimie et Physiologie Moléculaire des Plantes
2 Laboratoire de biochimie et physiologie des plantes
3 Biology and Microbiology Department
4 SDSTATE - South Dakota State University
5 Plateforme Histocytologie et Imagerie Cellulaire Végétale
6 INRA - Institut National de la Recherche Agronomique
7 Cirad - Centre de Coopération Internationale en Recherche Agronomique pour le Développement

Ectomycorrhizal fungi play an essential role in the ecology of boreal and temperate forests through the improvement of tree mineral nutrition. Potassium (K+) is an essential nutrient for plants and is needed in high amounts. We recently demonstrated that the ectomycorrhizal fungus Hebeloma cylindrosporum improves the K+ nutrition of Pinus pinaster under shortage conditions. Part of the transport systems involved in K+ uptake by the fungus has been deciphered, while the molecular players responsible for the transfer of this cation towards the plant remain totally unknown. Analysis of the genome of H. cylindrosporum revealed the presence of three putative tandem-pore outward-rectifying K+ (TOK) channels that could contribute to this transfer. Here we report the functional characterization of these three channels through two-electrode voltage-clamp experiments in oocytes and yeast complementation assays. The expression pattern and physiological role of these channels were analyzed in symbiotic interaction with P. pinaster. Pine seedlings colonized by fungal transformants overexpressing two of them displayed a larger accumulation of K+ in shoots. This study revealed that TOK channels have distinctive properties and functions in axenic and symbiotic conditions, and suggested that HcTOK2.2 is implicated in the symbiotic transfer of K+ from the fungus towards the plant.

Mots clés: maritime pine; shaker potassium channel

Mots clés: absorption du potassium; ion potassium; nutrition minérale; champignon mycorhizien; pinus pinaster; hebeloma cylindrosporum; canaux potassiques shaker

Domaines: Biologie végétale

Maria del Carmen Guerrero, Amandine Delteil, Kevin Garcia, Gabriella Houdinet, Geneviève Conejero, et al.. Plant potassium nutrition in ectomycorrhizal symbiosis: properties and roles of the three fungal TOK potassium channels in Hebeloma cylindrosporum. Environmental Microbiology, 2018, 20 (5), pp.1873-1887. ⟨10.1111/1462-2920.14122⟩. ⟨hal-01764383⟩