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

Abstract

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.

Specific Plant Mycorrhizal Responses Are Linked to Mycorrhizal Fungal Species Interactions

“…Thus, the plant-AMF interactions are always not positive, but range from positive to neutral and even negative (Pankova et al, 2018;Neuenkamp et al, 2019). For example, Kaur et al (2022) inoculated two sorghum accessions with two AMF species (Rhizophagus irregularis and Gigaspora gigantea) and observed both positive and negative effects. He then found that the positive outcome of R. irregularis was associated with a faciliatory root metabolome, while the higher relative abundance of sugars in the G. gigantea treatment may indicate a potential carbon drain and lead to negative effects.…”

Positive feedback between peanut and arbuscular mycorrhizal fungi with the application of hairy vetch in Ultisol

“…Soil AMFs are beneficial for the absorption of soil nutrients ( de Gruyter et al, 2022 ). The Glomeraceae showed the highest P uptake efficiency and antagonistic activities against plant pathogens ( Kaur et al, 2022 ). However, Gigasporaceae showed a negative impact on the plant growth potential ( Li et al, 2008 ).…”

“…and antagonistic activities against plant pathogens (Kaur et al, 2022). However, Gigasporaceae showed a negative impact on the plant growth potential (Li et al, 2008).…”

Root and Rhizosphere Processes under Drought: Digging Deeper to Enhance Ecosystem Resilience

“…Since ellagitannins have antimicrobial properties, their lower content indicates an adaptive response of fine roots to promote the ectomycorrhizal association. The chemical construct of fine roots can thus vary with the type and extent of mycorrhizal association (Xia et al 2021, Kaur et al 2022. Drought did not alter the content and composition of lignin while they varied across root orders.…”