In plant cells, carbohydrates serve multiple essential roles, including central metabolism, storage as soluble or insoluble sugars, and polysaccharide synthesis. They also act as signaling molecules and protective agents during abiotic stress responses. Effective intercellular and intracellular sugar transport is essential for regulating sugar partitioning at the subcellular level and for enabling cell-to-cell and long-distance translocation, both of which contribute to overall carbon allocation at the tissue and plant levels. The vascular system comprising of phloem, (pro)cambium, and xylem, is crucial for sugar transport. At the cellular level, cytosolic sugar availability is regulated through sugar exchanges at the plasma membrane and tonoplast, driven by active and passive sugar transporters. This sophisticated regulation indicates a finely tuned balance of sugar transport and homeostasis within the vascular tissues. However, the role in vascular tissue development of sugar availability in vascular cells remains incompletely understood. To identify novel molecular players linking sugar transport and xylem development, we conducted TRAP-seq analysis in Arabidopsis thaliana stem using cell type-specific promoters (pVND7, pVND6, pLAC17, pNST1, and pSWEET17) to profile the translatome in interfascicular fibers and xylem cell types. We also developed an R Shiny app, Arabidopsis Gene Network Explorer (ARAGNE), which enables user-friendly gene functional analysis (GO and KEGG) and network generation and visualization in Cytoscape. This approach revealed new gene networks associated with different cell types, including several genes coding for sugar transporters differentially expressed between interfascicular fibers and xylem cell types, notably members of the tonoplastic ESL and SWEET transporter families. An in-depth functional characterization of tonoplastic SWEET transporters expressed in these tissues allowed us to demonstrate their critical role in vascular system development. Our findings highlight the importance of precisely regulating intracellular sugar transport to ensure proper plant growth and vascular tissue differentiation.