Genome-wide analysis of the AP2 transcription factor family in cultivated sugarcane reveals ShAP2-1 as an enhancer of drought tolerance

Sugarcane (Saccharum spp. hybrid) is a primary global source of sugar and a vital feedstock for bioethanol, yet its productivity is severely limited by abiotic stresses, particularly drought. The AP2 family, belong to the APETALA2/ ethylene-responsive factor (AP2/ERF) superfamily, plays crucial roles in plant development and stress adaptation. However, a comprehensive analysis of the AP2 family in the complex polyploid genome of cultivated sugarcane remains lacking, limiting its potential for genetic improvement. A genome-wide survey of the AP2 family in the sugarcane cultivar XTT22 identified 211 members, representing a significant expansion compared to wild relatives. Phylogenetic analysis classified them into euAP2, euANT, and basalANT clades, with a notable dominance of the euANT subfamily. Their expansion was primarily driven by whole-genome/segmental duplication, with only 4.59% of duplicated pairs under positive selection. Promoter analysis revealed a predominance of hormone- and stress-responsive cis-elements. Expression profiling demonstrated distinct tissue-specific patterns (e.g., leaf-preferential ShAP2-1 and stem-specific ShAP2-56) and rapid, transient induction by abscisic acid, with stronger responses in young leaves. Functional validation showed that ShAP2-1 overexpression enhanced drought tolerance in transgenic rice by both markedly promoting primary root growth (2.4-fold) to improve water uptake, and mitigating oxidative stress by elevating superoxide dismutase activity while reducing malondialdehyde accumulation. This study provides the first comprehensive characterization of the AP2 transcription factor family in cultivated sugarcane, elucidating its expansion history, structural diversity, and spatiotemporal regulation. ShAP2-1 enhanced drought tolerance by promoting root growth for water acquisition and activating antioxidant defenses for cellular protection.