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

Abstract

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 analyzed 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 ECM-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.

Pb Stress and Ectomycorrhizas: Strong Protective Proteomic Responses in Poplar Roots Inoculated with Paxillus involutus Isolate and Characterized by Low Root Colonization Intensity

“…In roots inoculated with P. involutus characterized by a very low colonization ratio, most of the root surface was not covered with fungal hyphae and thus was deprived of fungal biofilters influencing the plant cell response to heavy metal stress [ 8 , 14 , 24 , 25 , 26 , 27 , 28 , 29 ]. For this reason, when the differences between the control and Pb-exposed poplar roots were analyzed, the molecular adjustments were, in many aspects, very similar in the noninoculated and inoculated plants (for the plant molecular adjustments caused by the analyzed P. involutus strain under control conditions see [ 40 ]).…”

“…The proteome study was supplemented with metabolomic analysis to detect the final level of the compounds of interest. For molecular adjustments between NM-Control and M-control, see Szuba et al [ 40 ].…”

Common and lifestyle‐specific traits of mycorrhizal root metabolome reflect ecological strategies of plant–mycorrhizal interactions

“…The colonization of PITA roots by Sl was also low (~6%) but included for chemical analysis, as this low colonization resulted in an improved growth (Table 1). Low EM colonization (~2%) was also shown in a prior study to promote plant growth and modify plant metabolites (Szuba et al, 2020). We note that the chemical alterations observed in PITA×Sl should be interpreted with caution due to the small sample size and low colonization.…”

Ectomycorrhizal symbiosis prepares its host locally and systemically for abiotic cue signaling

“…Modulation of the leaf metabolome by mycorrhizas has been reported in poplar (Luo et al, 2011;Pfabel et al, 2012;Kaling et al, 2018;Szuba et al, 2020;see Dreischhoff et al, 2020 for a review). It involves terpenes and nitrogenous, sulfurous, and phenolic compounds.…”