Fusarium ear rot (FER) caused by Fusarium verticillioides is one of the most common diseases affecting maize production worldwide. FER results in severe yield losses and grain contamination with health-threatening mycotoxins. Although most studies to date have focused on comprehensive analysis of gene regulation in maize during defense responses against F. verticillioides infection, less is known about the role of microRNAs (miRNAs) in this process. We used deep sequencing to compare small RNA libraries from the maize kernels of susceptible (N6) or resistant (BT-1) inbred lines from uninfected plants and upon F. verticillioides infection. We found that pathogen exposure was accompanied by dynamic alterations in expression levels of multiple miRNAs, including new members of previously annotated miRNA families. A combination of transcriptomic, degradomic, and bioinformatics analyses revealed that F. verticillioides-responsive miRNAs and their potential target genes displayed opposite expression patterns in the susceptible and resistant genotypes. Functional category analysis uncovered preferential enrichment of the pathogen-responsive miRNAs and their targets in the phenylpropanoid metabolic processes, plant–pathogen interactions, and plant phytohormone signal transduction pathways. Furthermore, transgenic maize plants overexpressing miR408b exhibited reduced resistance to F. verticillioides infection in a susceptible maize line. These findings provide new insights into the regulatory roles of miRNAs in maize immunity against FER and new resources for breeding disease resistance into maize.

枯萎镰刀菌引起的镰刀菌腐烂是影响全球玉米生产的最常见疾病之一。FER导致严重的产量损失，并威胁健康的霉菌毒素污染谷物。尽管迄今为止，大多数研究都集中在对玉米对细小镰刀菌感染的防御反应过程中玉米基因调控的综合分析上，但对微RNA（miRNA）在此过程中的作用了解甚少。我们使用深度测序比较了来自未感染植物和拟南芥的玉米（N6）或抗性（BT-1）自交系玉米粒的小RNA文库感染。我们发现病原体暴露伴随着多个miRNA表达水平的动态变化，包括先前注释的miRNA家族的新成员。转录，degradomic和生物信息学分析的组合表明，F.轮枝响应性miRNA和它们的潜在靶基因显示在敏感和抗性基因型相反的表达模式。功能类别分析揭示了病原体响应性miRNA及其靶标在苯丙烷代谢过程，植物与病原体的相互作用以及植物激素信号转导途径中的优先富集。此外，转基因玉米植物过量表达miR408b出降低的耐F.轮枝在易感玉米系中感染。这些发现为miRNA在玉米对FER的免疫中的调控作用提供了新的见识，并为将抗病性培育到玉米中提供了新资源。