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

Abstract

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.

Keywords: RNA-seq; endophytes; mycorrhizal fungi; root-fungus symbiosis; soil saprotrophs; soluble sugars.