Soil waterlogging is a major abiotic stress that severely impairs maize growth and development by inducing hypoxic conditions that disrupt essential physiological processes. Transcription factors (TFs) play crucial roles in modulating plant responses to waterlogging stress by regulating the expression of stress-related genes that enhance or diminish stress tolerance. In this study, we conducted an association analysis to identify 11 TFs closely associated with waterlogging stress in maize. Notably, the PLATZ family emerged as a novel and significant contributor to waterlogging stress. Overexpression of ZmPLATZ15 resulted in increased sensitivity to waterlogging at maize seedlings. Conversely, ZmEREB200, a member of the maize Group VII ERF (ZmERFVII) family, was significantly downregulated in the ZmPLATZ15 overexpression lines under waterlogging stress. Promoter analysis revealed that ZmPLATZ15 regulates ZmEREB200 by binding to the A/T-rich motifs in the ZmEREB200 promoter. Interestingly, overexpression of ZmEREB200 was found to enhance waterlogging tolerance at maize seedlings. To further elucidate their roles, we analyzed the transcriptomic profiles of ZmPLATZ15 and ZmEREB200 overexpression lines under waterlogging stress. The overlapping differentially expressed genes in both ZmPLATZ15 and ZmEREB200 overexpression lines were significantly enriched in pathways associated with redox balance and salicylic acid metabolism, both of which are crucial for modulating waterlogging tolerance at maize seedlings. Metabolomic analysis revealed that antioxidant enzyme activity, salicylic acid, and glutathione levels were decreased in OE-ZmPLATZ15, while these metabolites were significantly increased in OEZmEREB200. These contrasting metabolic responses in overexpression lines may underlie their different tolerances to waterlogging stress. Our findings provide valuable insights into the regulatory mechanisms underlying maize's response to waterlogging stress and highlight the potential of TFs as tools for developing maize varieties with enhanced waterlogging tolerance.
