Crops can be adversely affected by a variety of biotic and abiotic factors. Waterlogging stress has become increasingly severe in frequency and severity (Bailey-Serres et al., 2012a; Hirabayashi et al., 2013). Most crops are highly susceptible to waterlogging, leading to an average yield reduction of 20%. Approximately 12% of cropping areas experience waterlogging stress annually, which is on the rise (Bailey-Serres et al., 2012). Excess water results in a significant reduction in available oxygen in the soil (Gibbs and Greenway, 2003), which quickly depleted by plant roots and soil microorganisms and leads to severe hypoxic or even anoxic conditions in waterlogged soils, impeding root growth and function and triggering the formation of reactive oxygen species (ROS) (Santosa et al., 2007; Najeeb et al., 2015). Prolonged root hypoxia affects shoot growth, decreasing the photosynthetic rate and leaf growth, causing aboveground organs to wither, and altering plant–water relationships (Zheng et al., 2009; Xuewen et al., 2014; Zhou et al., 2020a). Plants have evolved specific physiological and morphological adaptations that counteract or tolerate the adverse effects of waterlogging stress. These include the formation and development of aerenchyma tissues and adventitious roots (ARs), as well as other physiological adjustments, such as the activation of antioxidant machinery that scavenges the excessive ROS produced during stress (Campbell et al., 2015; Voesenek and Bailey-Serres, 2015; Wang et al., 2020; Mano and Nakazono, 2021).

Transcription factors (TFs), integral components of signaling networks, play crucial roles in stress responses (Xiong et al., 2002; Yamaguchi-Shinozaki and Shinozaki, 2006). These proteins regulate the expression levels of downstream genes, leading to morphological and physiological changes that enable plants to adapt to environmental variations (Song et al., 2016; Samad et al., 2017). Various TFs from different families are responsible for the abiotic-stress responses, including the AP2/ethylene response factor (ERF), WRKY, bZIP, and NAC TF families (Chen et al., 2012; Cao et al., 2021; Xiang et al., 2021b). AP2/ERF TFs, with their conserved AP2/ERF domain, constitute one of the most prominent TF families in plants and play critical roles in growth, development, and environmental adaptation (Mizoi et al., 2012; Licausi et al., 2013; Xie et al., 2019). AP2/ERF TFs can activate or inhibit the expression of target genes by binding to specific regulatory elements in their promoters, such as GCC-box motifs (Nakano et al., 2006; Sharma et al., 2010). Within this family, the group VII ERFs (ERFVIIs) have been identified in multiple species and are essential for regulating hypoxic responses (Bui et al., 2015; Gibbs et al., 2015). In Arabidopsis thaliana, the ERFVII group comprises five members: AtHRE1, AtHRE2, AtRAP2.12, AtRAP2.2, and AtRAP2.3. These TFs modulate the expression of genes responsive to low-oxygen levels, thereby improving survival under hypoxic conditions (Bui et al., 2015). The OsSUB1A, OsSK1, and OsSK2 ERFVII genes in rice (Oryza sativa) confer submergence tolerance (Xu et al., 2006; Hattori et al., 2009), while in wheat (Triticum aestivum), the constitutive stable expression of TaERFVII.1 has been shown to enhance tolerance to waterlogging stress (Wei et al., 2019). Additionally, the overexpression of CmRAP2.3 in Chrysanthemum (Chrysanthemum morifolium) has been found to strengthen waterlogging tolerance by decreasing ROS levels (Li et al., 2023). Other ERF subgroups are also involved in the response to waterlogging stress; for example, AtRAP2.6L overexpression reduces water loss and membrane damage under waterlogging stress in Arabidopsis (Liu et al., 2012). Moreover, when MaRAP2-4, encoding an ERF TF from wild mint (Mentha arvensis), is transgenically expressed in Arabidopsis, it regulates the bidirectional sugar transporter AtSWEET10, thereby modulating the waterlogging stress response (Phukan et al., 2018).

Maize (Zea mays) is a globally important crop that is highly sensitive to waterlogging stress (Liang et al., 2020), which poses a significant threat to its production (Hu et al., 2022). Although several genetic loci associated with waterlogging tolerance have been identified in the maize genome (Liang et al., 2020), the specific genes involved in this response remain poorly understood, and only a limited number have been cloned and characterized. A total of 19 ERFVIIs were identified in maize, most of which are induced by waterlogging (Yu et al., 2019; Yu et al., 2020). A cluster consisting of ZmEREB179, ZmEREB180, ZmEREB181, and ZmEREB182 was discovered on chromosome 1 of the maize genome, with ZmEREB179 and ZmEREB180 observed to be induced by waterlogging (Yu et al., 2019). Additionally, through candidate gene association studies and transgenic evidence, ZmEREB180 was shown to function as a positive regulator of waterlogging tolerance in maize seedlings (Yu et al., 2019). Different variants of ZmEREB179 were also found to have significantly different effects on the waterlogging survival rate (SR) (Yu et al., 2019); however, the specific function of ZmEREB179 under waterlogging remains unclear.

In this study, we focused on characterizing ZmEREB179 using transgenic lines and molecular strategies. We found that ZmEREB179 was highly expressed under waterlogging conditions and that the protein was localized to the nucleus. By examining ZmEREB179-overexpressing and -knockout mutant lines in maize, this ERFVII was observed to play a negative role in regulating waterlogging tolerance during the seedling stage. ZmEREB179 was found to regulate the expression of various stress-related genes and directly bind to the promoter region of ZmEREB180, decreasing its expression. Through association analyses using 220 randomly selected maize inbred lines, we identified nine variations in the ZmEREB179 promoter region that significantly correlated with maize waterlogging tolerance. The variations were grouped into two haplotypes, one associated with significantly greater waterlogging tolerance in the inbred collection and was further verified in two F2 populations. These findings provide valuable insights into the function of ERFVIIs in regulating the waterlogging response in maize.