Transcriptomic and primary metabolic profiles reveal the mechanism of development and maturation of fuji apple grafted onto different dwarfed intermediate rootstocks

• Using different rootstocks significantly affects the levels of soluble sugars, starch and maturity in fruits. Compared M26 rootstock, SXND6 fruit matured earlier, potentially due to faster starch degradation and higher accumulation of soluble solids. • Through comprehensive transcriptome and metabolome analyses, we identified key pathways and DEGs involved in starch and sucrose metabolism, as well as plant hormone signaling pathways (especially abscisic acid and ethylene signaling). These pathways play crucial roles in regulating fruit early ripening and quality improvement. • The WGCNA results showed that genes in the MEturquoise module, which positively regulated sugar metabolism and fruit ripening, were upregulated in SXND6 at 135 DAFB. Conversely, genes in MEbrown module, which were negatively correlated with sugar and fruit maturity, were downregulated in SXND6 compared to M26. • Specifically, we identified positively regulating genes such as AGL9, bZIP6 , and ERF5 , as well as negatively associated genes like WRKY17 and NAC18 , that facilitate fruit maturation and sugar metabolism. Fruit development and ripening are complex processes involving various physiological and biochemical changes. Apple rootstocks significantly regulate fruit ripening, quality, and nutrient accumulation. To study the impact of SXND6 and M26 rootstocks on fruit development and maturation, we investigated fruit traits including single fruit weight, shape index, firmness, soluble solids content, titratable acidity, starch content, index of absorbance difference (IAD), endogenous hormone levels, as well as the transcriptome and metabolic profiles. At the transcript level, 9219 differentially expressed genes (DEGs) were identified in apple fruits grafted on SXND6 and M26 rootstocks at 135, 150, and 165 DAFB. Additionally, 116 differentially expressed primary metabolites were identified between the two rootstocks at 165 DAFB. An integrative analysis of the transcriptome and primary metabolic expression patterns revealed some key pathways and DEGs involved in early maturity and better quality mediated by various dwarf intermediate rootstocks. This primarily included starch and sucrose metabolism ( SS, AMY, BAM, SORD, PFK, SPS , and SUS ) and plant hormone signal transduction pathways, especially abscisic acid ( NACED, PP2C, SnRK , and ABF ) and ethylene ( ACS, ACO, ETR , and ERF ). Moreover, we employed weighted gene co-expression network analysis (WGCNA) to investigate the co-expression patterns of genes encoding transcription factors linked with sugar, organic acid, starch, and IAD. AGL9, bZIP6 , and ERF5 were identified as key hub genes within the MEturquoise module, as well as NAC, MADS, MYB , and C2C2 genes, which positively regulated sugars metabolism and fruit ripening. In contrast, WRKY17 and NAC18 were found in MEbrown module, as well as MYB related genes and MADS family genes, which were negatively correlated with sugar and fruit maturity. These findings provide new insights into the regulatory mechanisms by which rootstocks enhance fruit quality and promote fruit ripening. This knowledge contributes to improved rootstock selection for apple cultivation and management, while also facilitating the development of early-ripening apple varieties with high economic value in the future.