Facultative symbiosis with a saprotrophic soil fungus promotes potassium uptake in American sweetgum trees.

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). The colonized root cortical cells were found to 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 was not altered by the symbiosis, but colonized roots contained the transcripts of three fungal genes with homology to K+ transporters (ACU and HAK) and channel (SKC). Heterologously expressed ChACU and ChSKC restored the growth of a yeast K+‐uptake‐defective mutant. Upregulation of ChACU transcript under low K+ conditions (0 and 0.05 mM K+) compared to control (5 mM K+) was demonstrated in planta and in vitro. Colonized plants displayed a larger accumulation of soluble sugars under 0.05 mM K+ than non‐colonized plants. The present study suggests reciprocal benefits of this novel tree‐fungus symbiosis under potassium limitation mainly through an exchange of additional carbon and potassium between both partners. The anatomic and nutritional aspects of the facultative biotrophic interaction between the Clitopilus hobsonii and American sweetgum tree are revealed. The mode of action of fungal contribution to plant K+ acquisition under the K+ limitation condition is proposed. This work represents a distinct mechanism underlying a novel root—fungal symbiosis. [ABSTRACT FROM AUTHOR]