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Epichloë festucae uses a siderophore‐mediated system to acquire iron, which is important to maintain endophyte–grass symbioses. Here we investigate the roles of the alternative iron acquisition system, reductive iron assimilation (RIA), via disruption of the fetC gene, which encodes a multicopper ferroxidase, either alone (i.e., ΔfetC) or in combination with disruption of the gene sidA, which encodes a siderophore biosynthesis enzyme (i.e., ΔfetC/ΔsidA). The phenotypic characteristics of these mutants were compared to ΔsidA and wild‐type (WT) strains during growth under axenic culture conditions (in culture) and in symbiosis with the host grass, perennial ryegrass (in planta). Under iron deficiency, the colony growth rate of ΔfetC was slightly slower than that of WT, while the growth of ΔsidA and ΔfetC/ΔsidA mutants was severely suppressed. Siderophore analyses indicated that ΔfetC mutants hyperaccumulate ferriepichloënin A (FEA) at low iron concentrations and ferricrocin and FEA at higher iron concentrations. When compared to WT, all mutant strains displayed hyperbranching hyphal structures and a reduced ratio of Epichloë DNA to total DNA in planta. Furthermore, host colonization and vertical transmission through infection of the host seed were significantly reduced in the ΔfetC/ΔsidA mutants, confirming that high‐affinity iron uptake is a critical process for Epichloë transmission. Thus, RIA and siderophore iron uptake are complementary systems required for the maintenance of iron metabolism, fungal growth, and symbiosis between E. festucae and perennial ryegrass. [ABSTRACT FROM AUTHOR]

Few studies have evaluated the effects of bacteria that form associations with fungi on plant-microbial symbioses. We investigated the effects of a novel symbiotic bacterium (E226) of Epichloë , a well-researched mutualistic fungal endophyte of grasses, on perennial ryegrass (Lolium perenne) also associated with Epichloë. We hypothesised that E226 would promote plant growth but would not interfere with the in-planta growth of Epichloë and its production of antiherbivore alkaloids. E226, identified as Micrococcus luteus, formed an ectosymbiotic relationship with Epichloë when cultured on artificial media (i.e., bacterial cells were located on the hyphal surface) and possessed plant-growth promoting traits identified through whole genome analysis. Seeds of L. perenne , already colonised by an Epichloë strain, were inoculated with E226. The bacterium established within the seedlings, and the abundance of M. luteus populations initially increased with plant age. In agreement with our hypotheses, plant inoculation with E226 enhanced the production of leaves and did not affect the growth of Epichloë or the concentration of Epichloë -derived alkaloids. The putative abilities of E226 to solubilise phosphate and produce vitamins and metabolic cofactors may explain the observed plant growth promotion. • Micrococcus luteus strain E226 was an ectosymbiont of Epichloë endophytes. • E226 promoted the growth of plants. • E226 did not compromise the Epichloë growth and alkaloid production. • E226 promoted the plant growth likely via enhancing the host nutrition. [ABSTRACT FROM AUTHOR]