Unravelling tissue-specific transcriptional response for waterlogging tolerance in maize (Zea mays L.)

• This comprehensive transcriptome study reveals that root-specific transcriptional reprogramming drives waterlogging tolerance in tolerant maize. • The tolerant genotype demonstrated enhanced glycolysis, which improves anaerobic energy metabolism. • The upregulation of cell wall remodelling genes facilitated improved structural adaptation to waterlogging. • Maintenance of photosynthetic activity and elevated aquaporin expression ensured effective water homeostasis. • Stress resilience was further enhanced by strong activation of ROS-scavenging and osmotic adjustment pathways. Waterlogging poses a major constraint to maize productivity by inducing hypoxia and perturbing metabolic homeostasis. To elucidate the molecular basis of tolerance, we performed comparative RNA-seq profiling of leaf and root tissues from a waterlogging-tolerant (IML 7-308) and a susceptible (IML 7-312) genotype. Furthermore, qRT-PCR was used to validate the expression of key genes. Waterlogging triggered pronounced tissue- and genotype-dependent transcriptional reprogramming, with tolerant roots exhibiting the largest DEG set, underscoring their central role in stress adaptation. Furthermore, GO and KEGG enrichment revealed that glycolysis/fermentation, starch and sucrose metabolism, plant hormone signalling cascades, and secondary metabolite biosynthesis pathways are key components of the adaptive response. Tolerant plants showed marked upregulation of cell wall remodelling genes ( XTH ; xyloglucan endotransglucosylase), aquaporins ( PI2PA ), and ion transporters, supporting enhanced aerenchyma and adventitious root formation, hydraulic conductance, and ion homeostasis under waterlogging conditions. Network analysis (WGCNA) identified PIP2A, ACCO20, PIN3, IAA2, XTH, and ALDH2 as key hub genes orchestrating stress-responsive modules in the tolerant genotype. Together, these findings resolve the transcriptional architecture underpinning waterlogging tolerance in maize and offer molecular targets for engineering stress-resilient cultivars.