Integrated physiological, hormonal, and transcriptomic analyses reveal pistil responses to pollen sources of varying compatibility in ‘Fengtang’ plum (Prunus salicina)

Cross-pollination is crucial for commercial plum production, as pollen sources influence pollen tube growth and fruit set. However, the precise mechanisms underlying pollen-pistil interactions remain poorly understood. This study aimed to systematically investigate the dynamic physiological, hormonal, and transcriptomic responses of ‘Fengtang’ plum pistils following pollination with five distinct pollen sources. Five pollination combinations, including high-compatibility pollens (‘Fenghuang’, ‘Siyue’, and mixed pollen) and low-compatibility pollens (‘Yinhong’ and self-pollen), were established. ‘Fengtang’ pistils exhibited distinct temporal and multi-level responses dependent on pollen source. Physiological analyses revealed that highly compatible pollen induced rapid metabolic mobilization and a robust activation of antioxidant enzymes during the early stages of pollen tube elongation (24–48 h after pollination). Conversely, low-compatibility and self-pollinated pistils exhibited prolonged oxidative stress, characterized by delayed antioxidant responses and higher malondialdehyde accumulation. Hormonal profiling demonstrated the involvement of auxins, cytokinins, abscisic acid, ethylene, salicylic acid, and jasmonic acid in modulating pistil responses. Higher compatibility correlated with improved hormonal balance. Comparative transcriptomic analysis revealed significant transcriptional reprogramming orchestrating these divergent responses. Differentially expressed genes (DEGs) were significantly enriched in plant hormone signal transduction, MAPK signaling, starch and sucrose metabolism, amino acid biosynthesis, and flavonoid biosynthesis pathways. Furthermore, weighted gene co-expression network analysis identified hub transcription factors (e.g., ORR21 , C3H27 , ERF34 ) as potential regulators mediating these post-pollination pistil responses. Our integrated analysis indicates that pistils can differentially respond to pollen sources through coordinated changes in ROS homeostasis, metabolic status, and hormonal signaling, and provides a candidate framework for understanding compatibility-related responses in fruit tree reproduction.