Translational profiling uncovers a tonoplast sugar transporter essential for vascular system development and cell wall composition

ABSTRACT The inflorescence stem of Arabidopsis thaliana is a powerful model to study vascular development and carbon allocation, yet the translational landscape underlying xylem differentiation remains poorly defined. Here, we address this gap using tissue-specific Translating Ribosome Affinity Purification sequencing (TRAP-seq) to resolve the translatomes of xylem vessels, xylem parenchyma, and interfascicular fibers. We show that the very early stage of metaxylem differentiation involves coordinated activation of primary metabolism, plastid functions, and cell wall biosynthesis, supporting the metabolic demands of secondary wall formation. Xylem parenchyma displays enrichment in hormone signaling, stress, and immune pathways, consistent with a role in integrating environmental and metabolic cues. Interfascicular fibers exhibit increased translation of ribosomal proteins and spliceosome components, pointing to high translational activity and a role for alternative splicing during late development and programmed cell death. We further identify the tonoplast sugar transporter SUGAR WILL EVENTUALLY BE EXPORTED TRANSPORTER 2 (SWEET2) as a key regulator of stem radial growth. Preferentially translated in early stage of metaxylem differentiation, SWEET2 acts as a rate-limiting component of vacuolar sugar exchange, controlling cytosolic hexose availability for secondary wall biosynthesis. By contrast, SWEET16 and SWEET17 exert more specialized, tissue-specific functions. Together, our findings establish subcellular sugar partitioning as a central determinant of vascular development and highlight the power of translatome profiling.