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Internal fungal contamination in cereal grains may affect plant growth and result in health concerns for humans and animals. Fusarium verticillioides (F. verticillioides) is seed-borne fungus that can systemically infect maize. However, few efforts had been devoted to the genetic studies on maize resistance to seedborne F. verticillioides. In this study, we developed a disease evaluation method to identify the resistance to seedborne F. verticillioides in maize, by which a set of 121 diverse maize inbred lines were evaluated, and a 160 F10-generation recombinant inbred line (RIL) population derived from a cross of the resistant (BT-1) and susceptible (N6) inbred line was further used to identify major QTL for seedborne F. verticillioides resistance. Eighteen inbred lines with highly resistance to seedborne F. verticillioides were characterized and could be used as potential germplasm resources for genetic improvement of maize resistance. Six QTLs with highly heritability across multiple environments were detected on chromosomes 3, 4, 6, and 10, among which a major QTL, qISFR4-1, locating on chromosome 4 at the interval of 12922609-13418025 could explain 16.63% of the total phenotypic variance. Distinct expression profiles of eight candidate genes in qISFR4-1 between BT-1 and N6 inbred lines suggested their pivotal regulatory roles in seedborne F. verticillioides resistance. Taken together, these results will improve our understanding on the resistant mechanisms of seedborne F. verticillioides, and would provide valuable germplasm resources for disease resistance breeding in maize.

SummaryFusarium verticillioides (F. verticillioides) is a widely distributed phytopathogen that incites multiple destructive diseases in maize, posing a grave threat to corn yields and quality worldwide. However, there are few reports of resistance genes to F. verticillioides. Here, we reveal that a combination of two single nucleotide polymorphisms (SNPs) corresponding to ZmWAX2 gene associates with quantitative resistance variations to F. verticillioides in maize through a genome‐wide association study. A lack of ZmWAX2 compromises maize resistance to F. verticillioides‐caused seed rot, seedling blight and stalk rot by reducing cuticular wax deposition, while the transgenic plants overexpressing ZmWAX2 show significantly increased immunity to F. verticillioides. A natural occurrence of two 7‐bp deletions within the promoter increases ZmWAX2 transcription, thus enhancing maize resistance to F. verticillioides. Upon Fusarium stalk rot, ZmWAX2 greatly promotes the yield and grain quality of maize. Our studies demonstrate that ZmWAX2 confers multiple disease resistances caused by F. verticillioides and can serve as an important gene target for the development of F. verticillioides‐resistant maize varieties.

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