Potassium limitation promotes the Sweetgum-Clitopilus symbiosis

Several species of soil free-living saprotrophs can sometimes establish biotrophic symbiosis with plants, but the basic biology of this association remains largely unknown. Here, we investigate the symbiotic interaction between a common soil saprotroph, Clitopilus hobsonii (Agaricomycetes), and the American sweetgum (Liquidambar styraciflua). Notably, the colonized root cortical cells contain numerous microsclerotia-like structures. Fungal colonization led to increased plant growth and facilitated potassium uptake, particularly under potassium limitation (0.05 mM K+). The expression of plant genes related to potassium uptake is not altered during symbiosis, whereas the transcripts of three fungal genes encoding ACU, HAK, and SKC involved in K+ nutrition is found in colonized roots. We confirmed the K+ influx activities by expressing the ChACU and ChSKC genes into a yeast K+-uptake-defective mutant. Upregulation of the ChACU under 0.05 mM K+ and no K+ conditions was demonstrated in planta and in vitro compared to normal condition (5 mM K+). In addition, colonized plants displayed a larger accumulation of soluble sugars under 0.05 mM K+. The present study highlights that potassium limitation promotes this novel tree-fungus symbiosis mainly through a reciprocal transfer of additional carbon and potassium to both partners, and the role of dual soil saprotroph/symbiotroph in tree nutrition.