Zhenban Rootstock Optimizes Shatian Pomelo Fruit Quality by Coordinating Primary and Secondary Metabolism.

BACKGROUND/OBJECTIVES: Rootstock application is a critical strategy for improving citrus fruit quality, yet conventional combinations frequently suffer from an inherent sugar and acid imbalance. This study aimed to comprehensively evaluate the physiological and molecular impacts of three diverse rootstocks, including Trifoliate orange (Pt), Sour pomelo (Cg), and Zhenban pomelo (Zb), on Shatian pomelo to identify optimal grafting combinations and elucidate the underlying mechanisms governing superior fruit quality. METHODS: Shatian pomelo scions were grafted onto three distinct rootstocks (Pt, Cg, and Zb) and compared against self-rooted Shatian pomelo plants (CK) under identical field conditions. We conducted a comparative physiological evaluation of specific fruit traits, explicitly examining single fruit weight, total soluble solids, dry matter content, as well as the dynamic accumulation of individual sugars, citric acid, and ascorbic acid. To uncover the underlying molecular regulatory networks, we integrated comprehensive transcriptomic and metabolomic analyses of the developing fruits, mapping the precise gene expression profiles and metabolite fluxes across the different treatments. RESULTS: While the Pt and Cg rootstocks induced nonspecific metabolic fluctuations, the Zb rootstock uniquely optimized internal fruit quality without compromising fundamental fruit morphology. Zb grafted fruits exhibited superior sweetness, significantly reduced citric acid, and massively elevated ascorbic acid content. Integrative multiomics data revealed that Zb orchestrates a highly precise resource reallocation strategy. By transcriptionally suppressing energy-consuming pathways, specifically glycolysis and broad flavonoid biosynthesis, the Zb rootstock efficiently conserved vital structural carbon skeletons. This redirected carbon flux was seamlessly coordinated with the robust upregulation of SWEET sugar transporters and key enzymes in the L galactose pathway, thereby maximizing carbohydrate sink strength and vitamin C production. Concurrently, the downregulation of specific degradation enzymes ensured the stability of these targeted nutritional pools. CONCLUSIONS: The targeted carbon reallocation driven by the Zb rootstock effectively overcomes the traditional flavor bottlenecks in pomelo cultivation. These mechanistic insights not only highlight a highly efficient agricultural strategy for citrus improvement but also advance our fundamental understanding of metabolic regulation in grafted plants.