Physiological and transcriptome analyses reveal that mid-fruit load improves the strength of source and sink in grapevine (Vitis Vinifera L.)

•In the present study, the assay for biochemical and molecular mechanism were used by 13C labeling, full-length RNA-seq and gene transformation.•We make a conclusion that 50%FL significantly improved the source and sink strength. As a prime candidate gene, overexpression of VvPUP1 in grape cells improved its sugar accumulation.•These results demonstrates that the optimal fruit load was about 50%. Appropriately adjusting fruit loads (FL) can promote plant productivity in the field. In the present study, physiological, transcriptomic, and gene function assays were conducted by 13C labeling, full-length RNA-seq, and gene transformation. A comparative analysis of three different FL treatments (25%FL, 50%FL, and 100% FL) was performed to identify the mechanism that response to different FL. The results showed that 50%FL significantly improved the source strength by enhancing photosynthesis. The sink strength of 50%FL also reached the maximum when considering soluble sugar, weight, 13C allocation, sugar metabolism-related enzyme activity, and composition in berries, and yield. In addition, full-length transcriptome profiling exploited 1,098 differently expressed genes (DEGs) in 25%FL and 100%FL, and 1,479 DEGs in 50%FL and 100%FL, respectively. Thirty-four genes, including PUP1 and FBA1, were identified in carbon transport and metabolism-related pathways. As a major candidate gene, VvPUP1 was found to enhance sugar accumulation when overexpressed in grape cells. The transgenic cells had high soluble sugar contents and sucrose synthase (SS), neutral invertase (NI), and sucrose phosphate synthase (SPS) activities. Overexpression of VvPUP1 in tomatoes increased fruit size and weight, soluble sugar concentration, and the expression levels of SlSUS1, SlSPS1, and SlBGLU13, suggesting that VvPUP1 can promote berry enlargement and sugar accumulation. These results provide novel insights into the response of grapevine to different FL, demonstrating the differences in the source (leaf) and sink (berry) strength among different FL grapes.