Plant potassium nutrition in ectomycorrhizal symbiosis: TOK potassium channels

What is it about?

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.

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Why is it important?

Nutrient transfer in ectomycorrhizal symbiosis requires specialized and bidirectional transport, ensuring uptake of mineral nutrients from the soil by fungal hyphae and secretion towards the plant root. Potassium nutrition has been shown to be improved in ectomycorrhizal plants but the molecular players involved are not yet completely uncovered. Tandem-pore outward-rectifying potassium (TOK) channels that are described in yeast to mediate K+ efflux have been found specifically in fungi. Here, TOK channels are reported for the first time in an ectomycorrhizal fungus, and represent good candidates to be involved in symbiotic potassium transfer. Hebeloma cylindrosporum harbors three TOK channels belonging to two subfamilies with distinct properties and roles.