Phloem sieve elements (PSE), the primary conduits collaborating with neighboring phloem pole pericycle cells to facilitate unloading in Arabidopsis roots, undergo a series of developmental stages before achieving maturation and functionality. However, the mechanism that maintains the proper progression of these differentiation stages remains largely unknown. Here we identified a gain-of-function mutant altered phloem pole pericycle 1 Dominant (app1D), producing a truncated, nuclear-localized active form of NAC with Transmembrane Motif 1-like (NTL9). This mutation leads to ectopic expression of its downstream target CALLOSE SYNTHASE 8 (CalS8), thereby inducing callose accumulation, impeding SE differentiation, impairing phloem transport, and inhibiting root growth. The app1D phenotype could be reproduced by blocking the symplastic channels of cells within APP1 expression domain in wild-type roots. The wild-type APP1 is primarily membrane-tethered and dormant in the root meristem cells but entries into the nucleus in several cells in phloem pole pericycle near the unloading region, and this import is inhibited by blocking the symplastic intercellular transport in differentiating SE. Our results suggest a potential maintenance mechanism involving an APP1-CalS8 module, which induces CalS8 expression and modulates symplastic communication, and the proper activation of this module is crucial for the successful differentiation of SE in the Arabidopsis root.