Metabolome adjustments in ectomycorrhizal Populus × canescens associated with strong promotion of plant growth by Paxillus involutus despite a very low root colonization rate.

It is believed that resource exchange, which is responsible for intensified growth of ectomycorrhizal plants, occurs in the fungus-plant interface. However, increasing evidence indicates that such intensified plant growth, especially root growth promotion, may be independent of root colonization. Nevertheless, the molecular adjustments in low-colonized plants remain poorly understood. Here, we analysed the metabolome of Populus × canescens microcuttings characterized by significantly increased growth triggered by inoculation with Paxillus involutus, which successfully colonized only 2.1 ± 0.3% of root tips. High-throughput metabolomic analyses of leaves, stems and roots of Populus × canescens microcuttings supplemented with leaf proteome data were performed to determine ectomycorrhiza-triggered changes in N-, P- and C-compounds. The molecular adjustments were relatively low in low-colonized (M) plants. Nevertheless, the levels of foliar phenolic compounds were significantly increased in M plants. Increases of total soluble carbohydrates, starch as well as P concentrations were also observed in M leaves along with the increased abundance of the majority of glycerophosphocholines detected in M roots. However, compared with the leaves of the non-inoculated controls, M leaves presented lower concentrations of both N and most photosynthesis-related proteins and all individual mono- and disaccharides. In M stems, only a few compounds with different abundances were detected, including a decrease in carbohydrates, which was also detected in M roots. Thus, these results suggest that the growth improvement of low-colonized poplar trees is independent of an increased photosynthesis rate, massively increased resource (C:N) exchange and delivery of most nutrients to leaves. The mechanism responsible for poplar growth promotion remains unknown but may be related to increased P uptake, subtle leaf pigment changes, the abundance of certain photosynthetic proteins, slight increases in stem and root amino acid levels and the increase in flavonoids (increasing the antioxidant capacity in poplar), all of which improve the fitness of low-colonized poplars.