The plant-beneficial fungus Gongronella butleri w5 reallocates plant-derived sucrose to enrich IAA-producing bacteria to promote plant root development in phosphorus-rich soil

Mucoromycotina fungi are known to enhance plant performance under nutrient-deficient conditions by restructuring rhizosphere microbial communities and mobilizing soil nutrients. However, their functional roles in nutrient-rich soils remain poorly understood. Here, we investigated whether the plant-beneficial fungus Gongronella butleri w5 (w5) can promote the growth of Solanum lycopersicum under phosphorus-rich conditions and explored the underlying tripartite interactions among plants, fungi, and bacteria. Greenhouse experiments, soil microcosm analyses, high-throughput sequencing, functional assays, and host-induced gene silencing revealed that w5 significantly enhanced plant biomass, root development, and photosynthetic efficiency despite not altering soil nutrient availability. w5 inoculation reshaped the rhizosphere microbiome, enriching indole-3-acetic acid (IAA)-producing bacterial taxa. Bacillus megaterium and Bacillus zanthoxyli , identified as key IAA producers, were isolated from the w5 hyphosphere. Tripartite interaction assays showed that w5 imports plant-derived sucrose through the transporter GspSUT1, hydrolyzes it into glucose and fructose, and releases these hexoses into the rhizosphere, thereby facilitating bacterial colonization and enhancing IAA biosynthesis. Silencing GspSUT1 significantly impaired hexose secretion and subsequent bacterial IAA production, thereby disrupting the synergistic plant growth promotion effect. Our findings reveal a carbon-driven mechanism by which Mucoromycotina fungi establish a metabolic niche to drive synergistic plant development in nutrient-rich soils. By acting as an ecological “invertase” to reallocate plant sucrose into hexoses, w5 enriches IAA-producing bacteria. This carbon-hormone coupling synergistically improves root architecture, photosynthetic capacity, and nutrient uptake. These insights highlight the functional plasticity of Mucoromycotina fungi in shaping rhizosphere microbiomes and their potential as sustainable biological inputs. Video Abstract