Towards a systemic metabolic signature of the arbuscular mycorrhizal interaction

Abstract

Our experiments addressed systemic metabolic effects in above-ground plant tissue as part of the plant's response to the arbuscular mycorrhizal (AM) interaction. Due to the physiology of this interaction, we expected effects in the areas of plant mineral nutrition, carbon allocation and stress-related metabolism, but also a notable dependence of respective metabolic changes on environmental conditions and on plant developmental programs. To assess these issues, we analyzed metabolite profiles from mycorrhizal and non-mycorrhizal Lotus japonicus grown under greenhouse conditions at three different time points in the growing season in three different above-ground organs (flowers, sink leaves and source leaves). Statistical analysis of our data revealed a number of significant changes in individual experiments with little overlap between these experiments, indicating the expected impact of external conditions on the plant's response to AM colonization. Partial least square-discriminant analysis (PLS-DA) nevertheless revealed considerable similarities between the datasets, and loading analysis of the component separating mycorrhizal and non-mycorrhizal plants allowed the defining of a core set of metabolites responsible for this separation. This core set was observed in experiments with and without mycorrhiza-induced growth effects. It corroborated trends already indicated by the significant changes from individual experiments and suggested a negative systemic impact of AM colonization on central catabolic metabolism as well as on amino acid metabolism. In addition, metabolic signals for an increase in stress experienced by plant tissue were recorded in flowers and source leaves.

Metabolomics Suggests That Soil Inoculation with Arbuscular Mycorrhizal Fungi Decreased Free Amino Acid Content in Roots of Durum Wheat Grown under N-Limited, P-Rich Field Conditions

“…Means across standardised data of identified compounds suggested that soil inoculation with AMF alone decreased concentrations of low molecular weight compounds in roots, particularly AA and saturated FA&E. Similar results were found by [49] for Lotus japonicus grown with or without AM fungi under different conditions. Information about the effects of AMF on the root metabolome is scarce.…”

High specificity in plant leaf metabolic responses to arbuscular mycorrhiza

“…Volcano plots 48 including all metabolic features of a given plant species with fold changes (mean intensity in mycorrhizal plants divided by mean intensity in control plants, presented on a log 2 scale for symmetry) were plotted in MATLAB (7.10.0.499; The MathWorks, Natick, MA, USA). To take into account that multiple testing may influence the results, all metabolic features had to pass two thresholds, namely unadjusted P valueso0.05 (Mann-Whitney U-tests) as well as a fold change o0.67 (corresponding too À 0.58 on a log 2 scale) for a decrease in metabolite pool size or 41.5 (40.58 on a log 2 scale) for an increase in metabolite pool size to be considered as modulated by AM, according to Fester et al 6 These thresholds were set with unadjusted P values, since adjustments (which are also given) are highly conservative due to the large numbers of metabolic features (see above). For each species, a w 2 -test was performed to test whether the number of decreased and increased features differed from a uniform distribution.…”

“…However, most knowledge on modulation considering a substantial set of metabolites relies on studies of few model plant species (for example, Arabidopsis thaliana 5 , Lotus spec. 6,7 , Medicago truncatula 8 , Plantago spec. 4,9,10 ) and the transferability of findings from these models to other plant systems is debatable.…”

“…Third, arbuscular mycorrhizas are of considerable agricultural importance, as AMF enhance nutritional values and yields of crops, modulate plant pest and stress resistance, and influence global C and P cycling, ecosystem services, and primary productivity [15][16][17] . In contrast to the roots, whose metabolism under AM symbiosis is well characterized 8 , systemic effects of AMF, whose morphological structures are restricted to the roots, on shoot metabolic phenotypes are sparse and were mainly studied for certain targets or metabolomes of single species yet 6,[18][19][20][21][22][23] .…”

Medicago truncatula Mtha1-2 mutants loose metabolic responses to mycorrhizal colonization

“…3 The most prominent changes are visible in the catabolic and amino acid metabolism, probably due to the improved carbon sink strength and an improved P-and N-level. 4 However, not only P and N, but also S provided by the symbiotic uptake pathway leads to changes in the metabolic response. 5 The recent identification of M. truncatula mutants defective in the symbiotic transfer of nutrients across the periarbuscular space allows us now to study the impact of fungal colonization independent of the improved nutrition of the plant.…”