Jasmonate signaling restricts root soluble sugar accumulation and drives root-fungus symbiosis loss at flowering by antagonizing gibberellin biosynthesis

Jasmonate restricts accumulation of constitutive and fungus-induced root soluble sugars at flowering stage, and thus reduces root beneficial fungal colonization, but little is known about how these are achieved. To determine whether jasmonate-mediated depletion of soluble sugars is the result of direct phytohormonal cross-talk or indirect induced defensive secondary metabolism, we first profiled soluble sugar and tryptophan (Trp)-derived defensive secondary metabolites in the roots of wild-type and jasmonate signaling-impaired Arabidopsis thaliana at flowering upon a beneficial fungus Phomopsis liquidambaris inoculation. Next, jasmonate and gibberellin signaling were manipulated to determine the relationship between jasmonate and gibberellin, and to quantify the effects of these phytohormones on fungal colonization degree, soluble sugar accumulation, Trp-derived secondary metabolites production, and sugar source-sink transport and metabolism. Gibberellin complementation increased Ph. liquidambaris colonization and rescued jasmonate-dependent root soluble sugar depletion and phloem sugar transport and root invertase activity without influencing jasmonate-induced Trp-derived secondary metabolites production at flowering. Furthermore, jasmonate signaling antagonized gibberellin biosynthesis in Ph. liquidambaris-inoculated roots. Our results suggest a phytohormonal antagonism model that jasmonate signaling restricts root soluble sugar accumulation through antagonizing gibberellin biosynthesis rather than through promoting Trp-derived secondary metabolites production and thus drives beneficial fungal colonization decline at flowering.