An integrated functional approach to dissect systemic responses in maize to arbuscular mycorrhizal symbiosis

Most terrestrial plants benefit from the symbiosis with arbuscular mycorrhizal fungi (AMF) mainly under nutrient-limited conditions. Here the crop plant Zea mays was grown with and without AMF in a bi-compartmented system separating plant and phosphate (Pi) source by a hyphae-permeable membrane. Thus, Pi was preferentially taken up via the mycorrhizal Pi uptake pathway while other nutrients were ubiquitously available. To study systemic effects of mycorrhizal Pi uptake on leaf status, leaves of these plants that display an increased biomass in the presence of AMF were subjected to simultaneous ionomic, transcriptomic and metabolomic analyses. We observed robust changes of the leaf elemental composition, that is, increase of P, S and Zn and decrease of Mn, Co and Li concentration in mycorrhizal plants. Although changes in anthocyanin and lipid metabolism point to an improved P status, a global increase in C versus N metabolism highlights the redistribution of metabolic pools including carbohydrates and amino acids. Strikingly, an induction of systemic defence gene expression and concomitant accumulation of secondary metabolites such as the terpenoids alpha- and beta-amyrin suggest priming of mycorrhizal maize leaves as a mycorrhiza-specific response. This work emphasizes the importance of AM symbiosis for the physiological status of plant leaves and could lead to strategies for optimized breeding of crop species with high growth potential.