Background: Arbuscular mycorrhizal fungi (AMF) form a crucial symbiosis with most land plants, including maize (Zea mays L.), enhancing nutrient uptake in exchange for plant-derived carbon. The SWEET (Sugars Will Eventually be Exported Transporters) family of proteins are key mediators of sugar flux, but their specific roles in regulating carbon partitioning during maize-AMF symbiosis and the downstream effects on sugar accumulation in sink tissues are not well understood.

Methods: We conducted a greenhouse experiment to investigate the effects of inoculating maize with the AMF species Funneliformis mosseae. We compared inoculated (AM) and non-inoculated (NM) plants, measuring mycorrhizal colonization, plant growth parameters, photosynthetic efficiency, and soluble sugar (sucrose, glucose, fructose) concentrations in roots, leaves, and kernels. The expression levels of core ZmSWEET genes in root and leaf tissues were quantified using quantitative real-time PCR (qRT-PCR).

Results: AMF inoculation led to successful root colonization (~55%) and significantly increased plant biomass, and net photosynthetic rates compared to NM controls. Sugar concentrations were significantly elevated in the leaves and kernels of AM plants. In mycorrhizal roots, the expression of putative symbiosis-related genes ZmSWEET1b and ZmSWEET4c was upregulated by 4.2- and 3.5-fold, respectively. Critically, in the leaves of AM plants, the expression of key phloem-loading and sink-related genes, ZmSWEET11 and ZmSWEET13a, was also significantly enhanced by 2.8- and 3.1-fold, respectively.

Conclusion: Our findings demonstrate that AMF symbiosis orchestrates a sophisticated, dual regulation of the ZmSWEET gene family in maize. It localizes specific ZmSWEETs to the root-fungus interface to facilitate carbon delivery to the symbiont, while systemically upregulating different ZmSWEETs in source leaves. This systemic reprogramming enhances sugar transport efficiency throughout the plant, leading to increased sugar accumulation in kernels. This work elucidates a key molecular mechanism by which AMF can improve both the growth and nutritional quality of maize.