Mycorrhizal Regulation of Core ZmSWEET Genes Governs Sugar Accumulation in Maize

Mycorrhizal symbiosis relies on the host’s supply of carbohydrates, while sugar transport within plants is governed by the SWEET sugar transporter family. Although the symbiotic association between arbuscular mycorrhizal fungi (AMF) and maize is critical for its growth and sugar regulation, different AMF species have varying impacts on the host. The aim of this study was to analyze the effects of inoculating six different AMF species [Diversispora epigaea (De), Rhizophagus intraradices (Ri), Paraglomus occultum (Po), Entrophospora etunicata (Ee), Glomus heterosporum (Gh), and Funneliformis mosseae (Fm)] on plant growth, leaf photosynthetic capacity, glomalin-related soil protein content, leaf sugar content, and SWEET gene expression of maize under potted conditions for two months. AMF species colonize maize roots and showed significant species-specific variation, where Ri and Fm colonized treatment had the greatest rates (66~68%). All six fungi significantly increased biomass and stem diameter, with Ee treatment yielding the thickest stems, and enhanced leaf photosynthetic performance and glomalin-related soil protein fractions to some extent, with species-specific enhancements. All AMF species in particular significantly increased leaf sucrose; all except Ri treatment significantly increased fructose; while only Po and Fm treatments significantly increased glucose. AMF inoculations consistently upregulated the expression of ZmSWEET1b/3a/3b/4a/4b/14a and 16 genes, consistently downregulated the expression of ZmSWEET6b/11b/12a/13a/13b/13c and 17b genes, and induced treatment-specific regulation in the other gene expression. Root AMF colonization clustered with sugars and specific ZmSWEETs, with ZmSWEET4a/15b and 14b central to sucrose/glucose based on principal component analysis, indicating that these genes have specific regulatory effects in response to AMF treatments. In short, AMF inoculation reprogrammed ZmSWEET expression in a species-specific manner, with core ZmSWEET genes mediating sugar accumulation to support symbiosis.