Root metabolome of plant–arbuscular mycorrhizal symbiosis mirrors the mutualistic or parasitic mycorrhizal phenotype

• Published in: The New phytologist Vol. 234; no. 2; pp. 672 - 687
• Main Authors: Kaur, Sukhmanpreet, Campbell, Barbara J., Suseela, Vidya
• Format: Journal Article
• Language: English
• Published: England Wiley Subscription Services, Inc 01.04.2022
• Subjects: Abundance; arbuscular mycorrhizal fungi; Arbuscular mycorrhizas; Fungi; Fungicides; Genotype & phenotype; Genotypes; Gigaspora; Growth rate; Host plants; Inoculation; Metabolic response; Metabolism; Metabolites; Metabolome; metabolomics; Mixtures; Mutualism; Mycorrhizae - physiology; Organic acids; Parasitism; Phenotype; Phenotypes; Phosphorus; Plant growth; Plant Roots - physiology; Rhizophagus; Rhizophagus irregularis; Sorghum; Sorghum bicolor; specialized metabolites; Species; Symbionts; Symbiosis; Uptake; Gigaspora; Sorghum bicolor; arbuscular mycorrhizal fungi; Rhizophagus; metabolomics; symbiosis; parasitism; specialized metabolites
• ISSN: 0028-646X; 1469-8137
• DOI: 10.1111/nph.17994

Summary The symbiosis of arbuscular mycorrhizal fungi (AMF) with plants, the most ancient and widespread association, exhibits phenotypes that range from mutualism to parasitism. However, we still lack an understanding of the cellular‐level mechanisms that differentiate and regulate these phenotypes. We assessed the modulation in growth parameters and root metabolome of two sorghum accessions inoculated with two AMF species (Rhizophagus irregularis, Gigaspora gigantea), alone and in a mixture under phosphorus (P) limiting conditions. Rhizophagus irregularis exhibited a mutualistic phenotype with increased P uptake and plant growth. This positive outcome was associated with a facilitatory metabolic response including higher abundance of organic acids and specialized metabolites critical to maintaining a functional symbiosis. However, G. gigantea exhibited a parasitic phenotype that led to plant growth depression and resulted in inhibitory plant metabolic responses including the higher abundance of p‐hydroxyphenylacetaldoxime with antifungal properties. These findings suggest that the differential outcome of plant–AMF symbiosis could be regulated by or reflected in changes in the root metabolome that arises from the interaction of the plant species with the specific AMF species. A mutualistic symbiotic association prevailed when the host plants were exposed to a mixture of AMF. Our results provide a metabolome‐level landscape of plant–AMF symbiosis and highlight the importance of the identity of both AMF and crop genotypes in facilitating a mutualistic AMF symbiosis.