This study investigates the molecular mechanisms underlying fruit cracking in Akebia trifoliata, a phenomenon that significantly impacts fruit quality and marketability. Through comprehensive physiological, biochemical, and transcriptomic analyses, we identified key changes in cell wall components and enzymatic activities during fruit ripening. Our results revealed that ventral suture tissues exhibit significantly elevated activities of polygalacturonase (PG) and β-galactosidase compared to dorsoventral line tissues, indicating their crucial roles in cell wall degradation and structural weakening. The cellulose content in VS tissues peaked early and declined during ripening, while DL tissues maintained relatively stable cellulose levels, highlighting the importance of cellulose dynamics in fruit cracking susceptibility. Transcriptomic analysis revealed differentially expressed genes (DEGs) associated with pectin biosynthesis and catabolism, cell wall organization, and oxidoreductase activities, indicating significant transcriptional regulation. Key genes like AKT032945 (pectinesterase) and AKT045678 (polygalacturonase) were identified as crucial for cell wall loosening and pericarp dehiscence. Additionally, expansin-related genes AKT017642, AKT017643, and AKT021517 were expressed during critical stages, promoting cell wall loosening. Genes involved in auxin-activated signaling and oxidoreductase activities, such as AKT022903 (auxin response factor) and AKT054321 (peroxidase), were also differentially expressed, suggesting roles in regulating cell wall rigidity. Moreover, weighted gene co-expression network analysis (WGCNA) identified key gene modules correlated with traits like pectin lyase activity and soluble pectin content, pinpointing potential targets for genetic manipulation. Our findings offer valuable insights into the molecular basis of fruit cracking in A. trifoliata, laying a foundation for breeding programs aimed at developing crack-resistant varieties to enhance fruit quality and commercial viability.
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