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

Int J Mol Sci. 2023 Oct 19;24(20):15372. doi: 10.3390/ijms242015372.


The root-colonizing endophytic fungus Piriformospora indica promotes the root and shoot growth of its host plants. We show that the growth promotion of Arabidopsis thaliana 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 labels were detected in the leaves of N-starved host plants but not in plants supplied with sufficient N. Amino acid and primary metabolite profiles, as well as the expression analyses of N metabolite transporter genes suggest that the fungus alleviates the adaptation of its host from the N limitation condition. P. indica alters the expression of transporter genes, which participate in the 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 against N limitation by delivering reduced N metabolites to the host, thus alleviating metabolic N starvation responses and reprogramming the expression of N metabolism-related genes.

Keywords: Piriformospora indica; amino acid transporter; ammonium transporter; endophyte; nitrate transporter; nitrogen metabolism; nitrogen starvation.

MeSH terms

  • Arabidopsis* / metabolism
  • Basidiomycota* / physiology
  • Endophytes / metabolism
  • Gene Expression Regulation, Plant
  • Nitrogen / metabolism
  • Plant Roots / metabolism
  • Seedlings / metabolism


  • Nitrogen

Supplementary concepts

  • Serendipita indica

Grants and funding

This project was financially supported by the collaborative ICPS research project executed in the framework of the EIG CONCERT-Japan joint call on Food Crops and Biomass Production Technologies and the related national funding agencies: grants 01DR17007A and 01DR17007B from the Federal Ministry of Education and Research (BMBF), Germany, to R.O.; grant EIG_JC1JAPAN-045 from the Centre National de la Recherche Scientifique (CNRS), France, to A.K.; grant PCIN-2016–037 from the Ministry of Economy and Competitiveness (MINECO), Spain, to J.V.-C. and S.P.; and grant JPMJSC16C3 from the Japan Science and Technology Agency (JST) to H.S. This work was further supported by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) CRC1127 ChemBioSys (project ID: 239748522) for R.O. This work benefited from the support of IJPB’s Plant Observatory technological platforms. The IJPB benefits from additional support of Saclay Plant Sciences-SPS (ANR-17-EUR-0007).