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Metabolome analysis of Arabidopsis thaliana roots identifies a key metabolic pathway for iron acquisition.

ABSTRACT: Fe deficiency compromises both human health and plant productivity. Thus, it is important to understand plant Fe acquisition strategies for the development of crop plants which are more Fe-efficient under Fe-limited conditions, such as alkaline soils, and have higher Fe density in their edible tissues. Root secretion of phenolic compounds has long been hypothesized to be a component of the reduction strategy of Fe acquisition in non-graminaceous plants. We therefore subjected roots of Arabidopsis thaliana plants grown under Fe-replete and Fe-deplete conditions to comprehensive metabolome analysis by gas chromatography-mass spectrometry and ultra-pressure liquid chromatography electrospray ionization quadrupole time-of-flight mass spectrometry. Scopoletin and other coumarins were found among the metabolites showing the strongest response to two different Fe-limited conditions, the cultivation in Fe-free medium and in medium with an alkaline pH. A coumarin biosynthesis mutant defective in ortho-hydroxylation of cinnamic acids was unable to grow on alkaline soil in the absence of Fe fertilization. Co-cultivation with wild-type plants partially rescued the Fe deficiency phenotype indicating a contribution of extracellular coumarins to Fe solubilization. Indeed, coumarins were detected in root exudates of wild-type plants. Direct infusion mass spectrometry as well as UV/vis spectroscopy indicated that coumarins are acting both as reductants of Fe(III) and as ligands of Fe(II).

SUBMITTER: Schmidt H

PROVIDER: S-EPMC4109925 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Metabolome analysis of Arabidopsis thaliana roots identifies a key metabolic pathway for iron acquisition.

Schmidt Holger H Günther Carmen C Weber Michael M Spörlein Cornelia C Loscher Sebastian S Böttcher Christoph C Schobert Rainer R Clemens Stephan S

PloS one 20140724 7

Fe deficiency compromises both human health and plant productivity. Thus, it is important to understand plant Fe acquisition strategies for the development of crop plants which are more Fe-efficient under Fe-limited conditions, such as alkaline soils, and have higher Fe density in their edible tissues. Root secretion of phenolic compounds has long been hypothesized to be a component of the reduction strategy of Fe acquisition in non-graminaceous plants. We therefore subjected roots of Arabidopsi ...[more]

PMID: 25058345

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Project description:While the plant host metabolome drives distinct enrichment of detrimental and beneficial members of the microbiome, the mechanistic interomics relationships remain poorly understood. Here, we studied microbiome and metabolome profiles of two Arabidopsis thaliana accessions after Fusarium oxysporum f.sp. mathioli (FOM) inoculation, Landsberg erecta (Ler-0) being susceptible and Col-0 being resistant against FOM. By using bacterial and fungal amplicon sequencing and targeted metabolite analysis, we observed highly dynamic microbiome and metabolome profiles across FOM host progression, while being markedly different between FOM-inoculated and noninoculated Col-0 and Ler-0. Co-occurrence network analysis revealed more robust microbial networks in the resistant Col-0 compared to Ler-0 during FOM infection. Correlation analysis revealed distinct metabolite-OTU correlations in Ler-0 compared with Col-0 which could possibly be explained by missense variants of the Rfo3 and Rlp2 genes in Ler-0. Remarkably, we observed positive correlations in Ler-0 between most of the analyzed metabolites and the bacterial phyla Proteobacteria, Bacteroidetes, Planctomycetes, Acidobacteria, and Verrucomicrobia, and negative correlations with Actinobacteria, Firmicutes, and Chloroflexi. The glucosinolates 4-methyoxyglucobrassicin, glucoerucin and indole-3 carbinol, but also phenolic compounds were strongly correlating with the relative abundances of indicator and hub OTUs and thus could be active in structuring the A. thaliana root-associated microbiome. Our results highlight interactive effects of host plant defense and root-associated microbiota on Fusarium infection and progression. Our findings provide significant insights into plant interomic dynamics during pathogen invasion and could possibly facilitate future exploitation of microbiomes for plant disease control. IMPORTANCE Plant health and fitness are determined by plant-microbe interactions which are guided by host-synthesized metabolites. To understand the orchestration of this interaction, we analyzed the distinct interomic dynamics in resistant and susceptible Arabidopsis ecotypes across different time points after infection with Fusarium oxysporum (FOM). Our results revealed distinct microbial profiles and network resilience during FOM infection in the resistant Col-0 compared with the susceptible Ler-0 and further pinpointed specific microbe-metabolite associations in the Arabidopsis microbiome. These findings provide significant insights into plant interomics dynamics that are likely affecting fungal pathogen invasion and could possibly facilitate future exploitation of microbiomes for plant disease control.

Dataset Information

Metabolome analysis of Arabidopsis thaliana roots identifies a key metabolic pathway for iron acquisition.

Publications

Metabolome analysis of Arabidopsis thaliana roots identifies a key metabolic pathway for iron acquisition.

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