Funneliformis mosseae enhances drought tolerance in maize inbred lines through root transcriptomic reprogramming

Drought is a major constraint on maize productivity, and its increasing frequency due to climate change necessitates improved stress adaptation strategies. Arbuscular mycorrhizal fungi (AMF) can enhance plant drought tolerance; however, the integrated mechanisms linking root development, host transcriptional regulation, and microbiome activity remain poorly understood. Here, we investigated these interactions in maize using an integrated phenotyping-transcriptomic-metatranscriptomic approach under controlled greenhouse conditions. Two inbred lines with contrasting drought tolerance (K1, tolerant; K2, sensitive) and their hybrid (KH) were grown under well-watered (60% soil moisture) and drought (30%) conditions, with or without Funneliformis mosseae inoculation. Mycorrhizal colonization reached 51.3-62.5% under drought, confirming effective symbiosis. RNA-seq analysis (FDR ≤ 0.05, |log₂;FC| ≥ 1) revealed strong genotype-dependent transcriptional responses, with the drought-sensitive genotype showing the largest number of differentially expressed genes. Principal component analysis identified genotype as the primary driver of variation (PC1: 13%), followed by mycorrhizal status (PC2: 8%). AMF induced distinct, genotype-specific functional reprogramming. The drought-tolerant genotype showed moderated stress responses and maintained metabolic activity, whereas the drought-sensitive genotype exhibited sustained stress signaling and compensatory metabolic activation. The hybrid displayed a non-additive response associated with enhanced root remodeling and symbiosis-related functions. Metatranscriptomic analysis of the non-host root-associated transcript pool further revealed genotype-specific microbial functional activity patterns, ranging from activation to repression. These results demonstrate that AMF-mediated drought tolerance emerges from coordinated, genotype-dependent interactions among root development, host regulatory networks, and microbiome activity. This study provides a holobiont-level framework for understanding crop stress adaptation.