Comprehensive transcriptome and proteome analyses reveal genotype-specific regulatory networks under drought stress in Maize

Abstract

Maize is a major crop for global food security, yet its productivity is increasingly threatened by drought stress, especially in arid and semi-arid regions. Understanding the molecular mechanisms underlying drought tolerance is essential for improving yield stability. In this study, drought-tolerant (PHBA6) and drought-sensitive (J63) maize inbred lines were compared at the flowering stage under identical drought-stress conditions using integrated transcriptomic and proteomic approaches to elucidate the genotype- and tissue-specific molecular differences that distinguish their contrasting drought tolerance. A total of 9,595 differentially expressed genes (DEGs) and 3,140 differentially expressed proteins (DEPs; fold change ≥ 1.2 or ≤ 0.83, p  ≤ 0.05) were identified from genotype- and tissue-based comparisons under drought stress, revealing distinct genotype-specific regulatory patterns. DEGs involved in regulating antioxidant metabolism and scavenging reactive oxygen species (ZmPOD), sucrose synthesis and osmotic adjustment (ZmSPS), and trehalose biosynthesis (ZmTPP) were successfully identified. In the drought-tolerant genotype, ZmHSP70 and ZmGST were more abundant than in the drought-sensitive genotype, highlighting their potential roles in antioxidant defense, protein stability, and detoxification. Conversely, the drought-sensitive genotype showed reduced abundance of ZmRBCS and ZmPR1, along with other stress-related DEPs such as ZmPsbP and ZmMDAR. Additionally, weighted gene coexpression network analysis (WGCNA) identified key modules associated with genotype- and trait-related differences under drought stress, which were significantly enriched in ion transport, hydrolase activity, oxidative phosphorylation, and carbon fixation. Integrated transcriptomic, proteomic, and coexpression network analyses revealed that the molecular differences between the drought-tolerant and drought-sensitive genotypes under drought stress involve coordinated regulation of ROS detoxification, photosynthetic maintenance, energy metabolism, and stress signaling pathways. Enhanced antioxidant capacity, sustained photosynthetic performance, and efficient energy utilization collectively distinguish the tolerant genotype from the sensitive one under drought, providing candidate genes and molecular targets for improving drought resilience in maize.