Transcriptome analysis reveals ZmERF055 contributes to waterlogging tolerance in sweetcorn

Waterlogging is a major disaster damaging crop production. However, most sweetcorn cultivars are not tolerant to waterlogging, which severely threatens their production. In order to understand the genetic mechanisms underlying waterlogging tolerance in sweetcorn, this study conducted a comprehensive investigation of sweetcorn waterlogging tolerance at the levels of physiology, biochemistry, and transcriptome in two sweetcorn CSSLs (chromosome segment substitution lines), D120 and D81. We found that D120 showed increased plant height, root length, root area, adventitious root numbers, antioxidant enzyme activities, and aerenchyma area ratio compared to D81. The transcriptome results showed that 2492 and 2351 differentially expressed genes (DEGs) were obtained at 4 h and 8 h of waterlogging treatment, respectively. Genes involved in reactive oxygen species (ROS) homeostasis, photosynthesis, and alcohol fermentation are sensitive in the waterlogging tolerant genotype D120, resulting in enhanced ROS scavenging ability, adventitious roots, and aerenchyma formation. Additionally, ethylene-, auxin-, and ABA-related genes exhibited different responses to waterlogging stress in sweetcorn. We integrated transcriptome and differential chromosomal fragments data and identified that ZmERF055 on chromosome 9 was directly involved in waterlogging stress. ZmERF055-overexpressing plants consistently exhibited significantly increased waterlogging tolerance and ROS homeostasis in Arabidopsis. These results offer a network of plant hormone signaling, ROS homeostasis, and energy metabolism co-modulating waterlogging tolerance in sweetcorn. Additionally, the findings support ZmERF055 as a potential ideal target gene in crop breeding to improve plant waterlogging tolerance. [Display omitted] •Aerenchyma formation vary in waterlogging tolerant and sensitive sweetcorn genotypes.•Enhanced ROS homeostasis contributes to the waterlogging tolerance.•Energy metabolism is important for sweet corn growth and survival under waterlogging.•ZmERF055 contributes to waterlogging tolerance.