Metabolomic compounds identified in Piriformospora indica-colonized Chinese cabbage roots delineate symbiotic functions of the interaction

Mo Da-Sang Hua,Rajendran Senthil Kumar,Yuan-Bin Cheng,Zhihong Tian,Kai-Wun Yeh,Ralf Oelmüller,Lie-Fen Shyur

doi:10.1038/s41598-017-08715-2

Abstract

Root colonization by endophytic fungus Piriformospora indica facilitating growth/development and stress tolerance has been demonstrated in various host plants. However, global metabolomic studies are rare. By using high-throughput gas-chromatography-based mass spectrometry, 549 metabolites of 1,126 total compounds observed were identified in colonized and uncolonized Chinese cabbage roots, and hyphae of P. indica. The analyses demonstrate that the host metabolomic compounds and metabolite pathways are globally reprogrammed after symbiosis with P. indica. Especially, γ-amino butyrate (GABA), oxylipin-family compounds, poly-saturated fatty acids, and auxin and its intermediates were highly induced and de novo synthesized in colonized roots. Conversely, nicotinic acid (niacin) and dimethylallylpyrophosphate were strongly decreased. In vivo assays with exogenously applied compounds confirmed that GABA primes plant immunity toward pathogen attack and enhances high salinity and temperature tolerance. Moreover, generation of reactive oxygen/nitrogen species stimulated by nicotinic acid is repressed by P. indica, and causes the feasibility of symbiotic interaction. This global metabolomic analysis and the identification of symbiosis-specific metabolites may help to understand how P. indica confers benefits to the host plant.

Highlights

Piriformospora indica of the Sebacinales, Basidiomycota, can colonize a broad spectrum of plants[1]
We have demonstrated that the observed phenotype is associated with a strong, transient increase of the auxin level in the roots, which results in upregulation of Chinese cabbage genes correlated with growth- and auxin signaling-related functions, such as genes for P-type/V-type H+-ATPases and nutrient/ion transporters, root hair-forming phosphoinositide phosphatase 4 (RHD4), cell wall loosening/synthesizing proteins involved in cell wall growth, and auxin transportation/responses[2]
The compounds which were identified in the P. indica-colonized, but not in uncolonized roots should be induced in the symbiotic interaction, and can be of plant or fungal origin

Summary

Introduction

Piriformospora indica of the Sebacinales, Basidiomycota, can colonize a broad spectrum of plants[1]. Besides an overall stimulation of root and shoot growth by the endophyte, the substantial increment of lateral root development results in a bushy root phenotype Such a strong stimulation of lateral root development has not yet been described for another plant species colonized by P. indica. This has prompted us to investigate the symbiotic interaction of P. indica with Chinese cabbage roots in more details, since the strong effect of the fungus on root growth and proliferation might be important for agricultural applications. The increased concentrations were found in organic acids, carbohydrate, ascorbate, glucosinates and hydroxycinnamic acids, and a decreased concentration found in nitrogen-rich amino acids This important finding has contributed to validate the symbiotic mechanism between plant host and P. indica

Methods

Results

Conclusion