Research on the morphogenesis of Notopterygium incisum rhizomes and its mechanism: multiomics integration analysis reveals the formation mechanism of silkworm-like rings

Notopterygium incisum (Umbelliferae) is a rare medicinal plant. Its rhizome product ‘Can Qiang’ is valued for its silkworm-like ring patterns. However, no studies have reported how these rings form. This study aimed to elucidate the structural basis, key developmental stages, and molecular regulatory mechanisms underlying the formation of these characteristic rings. Our anatomical analysis reveals that the ring pattern results from uneven secondary growth, driven by localized cork cambium activity and programmed cortical cell death during a critical differentiation period from 126 to 139 days post-germination (early autumn). Mechanical pressure from the expanding secondary xylem compresses the cortex, leading to cavity formation. Integrated multi-omics analyses uncovered a systemic metabolic and transcriptional reprogramming underlying this morphology. Metabolomic profiling showed a pronounced shift in carbon allocation toward the phenylpropanoid pathway, marked by substantial accumulation of lignin precursors (e.g., coniferyl alcohol, coniferin), which serve as substrates for secondary wall deposition and ring lignification. Concurrently, a decrease in core energy metabolites such as succinate suggests a metabolic trade-off. Transcriptomic analysis identified a root-specific NAC-ERF-bHLH transcriptional hub that orchestrates this process by activating genes involved in phenylpropanoid/flavonoid biosynthesis and starch metabolism, thereby directing carbon flux toward structural reinforcement. Key genes encoding phenylpropanoid enzymes (e.g., PAL, C4H) and ABC transporters were strongly correlated with the observed anatomical and metabolic changes. The silkworm-like ring likely results from a carbon flow allocation strategy triggered by early autumn environmental signals. These signals activate the phospholipid system and transcriptional network, redirecting phenylpropane pathway carbon flux. Lignin precursors accumulate, regulating cork cambium activation and secondary xylem proliferation. This forms multilayered rings and cortical cavities. Lignified rings improve mechanical strength; a hollow cortex buffers heat stress. Together, they maintain organ stability and allow the compartmentalized storage of medicinal components. This study provides a theoretical basis for the cultivation, breeding, and harvesting of N. incisum .