The Root-Colonizing Endophyte Piriformospora indica Supports Nitrogen-Starved Arabidopsis thaliana Seedlings with Nitrogen Metabolites

The root-colonizing endophytic fungus Piriformospora indica promotes root and shoot growth of its host plants. We show that growth promotion of Arabidopsis leaves is abolished when the seedlings are grown on media with nitrogen (N) limitation. The fungus neither stimulated the total N content nor did it promote 15NO3- uptake from agar plates to the leaves of the host under N-sufficient or N-limiting conditions. However, when the roots were co-cultivated with 15N-labelled P. indica, more label can be detected in the leaves of N-starved host plants, but not of plants supplied with sufficient N. Amino acid and primary metabolite profiles, as well as expression analyses of N metabolite transporter genes suggest that the fungus alleviates the adaptation of its host to the N limitation condition. P. indica alters the expression of transporter genes which participate in relocation of NO3-, NH4+ and N metabolites from the roots to the leaves under N limitation. We propose that P. indica participates in the plant´s metabolomic adaptation to N limitation by delivering reduced N metabolites to the host, alleviating metabolic N starvation responses, and reprogramming the expression of N-metabolism related genes.