The miR172y-AP2-1 module promotes sugarcane defoliation by regulating aerenchyma formation through ethylene and ROS signaling

Spontaneous defoliation at maturity constitutes a crucial agronomic trait for sugarcane harvesting, yet its underlying mechanisms remain elusive . Here, an integrated multi-omics and functional approach was employed to dissect this regulatory process. Phenotypic analysis revealed that sugarcane defoliation involved distinct morphological changes, including increased leaf angle and progressive sheath cracking, which were closely associated with enhanced aerenchyma development and H 2 O 2 accumulation during maturation. Transcriptomic and small RNA profiling demonstrated that leaf detachment was regulated by coordinated expression changes, with both differentially expressed genes and miRNAs showing significant enrichment in key biological processes such as cell wall reorganization and redox homeostasis. Integrated miRNA-mRNA network analysis identified AP2–1 and SPL12 as central hubs in the regulation of cell wall and cytoskeletal dynamics. Functional validation further defined the tissue-specific miR172y-AP2–1 module and confirmed that miR172y directly represses the nuclear-localized AP2–1. Overexpression of AP2–1 in transgenic rice enhanced aerenchyma formation and increased susceptibility to sheath detachment. These transgenic lines displayed elevated accumulation of 1-aminocyclopropane-1-carboxylic acid, cell wall components, and H₂O₂. AP2–1 overexpression resulted in coordinated alterations in ethylene biosynthesis (via ACO3/5 upregulation), ethylene signaling (via suppression of OsCTR2 and OsFbox072 ), and reactive oxygen species homeostasis (through catalase inhibition and RBOHF activation), collectively promoting aerenchyma development. These results provide a novel molecular framework underlying sugarcane defoliation, offering a new understanding of leaf detachment in perennial grasses as a process orchestrated by the miR172-AP2–1 module, and highlight actionable genetic targets for improving harvest efficiency in sugarcane. • A unique aerenchyma-mediated leaf shedding mechanism was revealed in sugarcane. • The miR172y-AP2–1 module was identified as central to defoliation regulation. • AP2–1 overexpression confers enhanced aerenchyma formation and sheath detachment. • AP2–1 coordinates ethylene, ROS and cell wall pathways to promote detachment.