Summary: Salvia miltiorrhiza Bunge, a renowned medicinal herb in traditional Chinese medicine, displays distinctive root texture and high phenolic acid content, traits influenced by genetic and environmental factors. However, the underlying regulatory networks remain unclear. Here, we performed multi‐omics analyses on ecotypes from four major Chinese regions, focusing on environmental impacts on root structure, phenolic acid accumulation and lignin composition. Lower temperatures and increased UV‐B radiation were associated with elevated rosmarinic acid (RA) and salvianolic acid B (SAB) levels, particularly in the Sichuan ecotype. Structural models indicated that the radial arrangement of xylem conduits contributes to greater root hardness. Genomic assembly and comparative analysis of the Sichuan ecotype revealed a unique phenolic acid metabolism gene cluster, including SmWRKY40, a WRKY transcription factor essential for RA and SAB biosynthesis. Overexpression of SmWRKY40 enhanced phenolic acid levels and lignin content, whereas its knockout reduced root hardness. Integrating high‐throughput (DNA affinity purification sequencing) and point‐to‐point (Yeast One‐Hybrid, Dual‐Luciferase and Electrophoretic Mobility Shift Assay) protein‐DNA interaction detection platform further identified SmWRKY40 binding sites across ecotypes, revealing specific regulatory networks. Our findings provide insights into the molecular basis of root texture and bioactive compound accumulation, advancing breeding strategies for quality improvement in S. miltiorrhiza.

The maintenance of adaptability to the exposure to agroecological extreme environments is generally a feature after the long-term domestication of crops. Auxin influences plant growth in all environments. At present, the research on the auxin response factors (ARFs) has been very in-depth. However, there is still a large gap in the research on the origin, evolution, and regulatory networks of the Auxin-responsive protein (AUX/IAA) family. Here, we identified 495 AUX/IAAs from 19 representative species covering aquatic algae to angiosperms and found that they originated from early bryophytes and mainly expanded by polyploidy in angiosperms. In the domesticated crop quinoa, the evolutionary model of the IAA family is relatively independent and forms a robust regulatory network with auxin signals and energy metabolism pathways. In the nitrogen-deficient environment, CqIAAs (Chenopodium quinoa AUX/IAAs), auxin signals, and TCA pathway genes induced expression in young roots to promote root elongation and could regulate the balance of carbon and nitrogen metabolism to maintain the adaptation of early seedlings in poor environments. Furthermore, a rapidly evolving CqIAA (AUR62011942) not only has different expression levels in two quinoa seeds but also has a significant stress response when seedlings face nitrogen deficiency stress, which may be a key factor in the adaptive regulation of the barren environment. Our research provides valuable clues for understanding the origin, evolution, and functional innovation of auxin signaling and also provides a reference for future agricultural breeding in the context of global environmental changes.