Molecular Basis of Phenotypic Plasticity: Understory-Induced DNA Methylation and Phytohormone Shifts Optimize Atractylodes lancea (Thunb.) DC Quality.

Atractylodes lancea (Thunb.) DC. (A. lancea) is a crop with medicinal and food properties. Currently, the majority of A. lancea available on the market is cultivated in extensive agricultural fields. This led to phenotypic variation in the plant and a reduction in the content of active ingredients. However, the cultivation of the understory can facilitate the phenotype of A. lancea. This, in turn, aligns with the characteristics of "excellent shape" and "high quality." Nonetheless, there is a paucity of research focusing on the phenotypic changes and molecular mechanisms underlying quality formation in understory-cultivated A. lancea. In this study, a comprehensive analysis of DNA methylation, phytohormone network regulation, and changes in energy metabolism in A. lancea across different habitats was performed through the integration of transcriptomic and proteomic data, representative phytohormone assays, and methylation-sensitive amplified polymorphism analysis. The results of the study revealed that the cultivation of A. lancea in the understory was predominantly characterized by a demethylation pattern, with its total methylation rate closely approximating that of the wild type. Understory-cultivated A. lancea maintains resource allocation equilibrium between growth and defense by upregulating genes (e.g., Lipoxygenase) and proteins associated with the jasmonic acid synthesis and signaling pathway, while downregulating genes (e.g., indole-3-pyruvate monooxygenase) and proteins linked to the auxin synthesis and signaling pathway. This cultivation method optimizes primary and secondary metabolism, thereby enhancing the bioactive components of A. lancea. The findings of this study provide a molecular-level theoretical framework for further advancement and implementation of the forest-medicine composite planting model.