The transcriptional landscape and dynamics regulating organ differentiation and dormancy in <i>Curcuma alismatifolia</i>

The emergence of specialized organs represents key evolutionary innovations that enable plants to thrive in diverse environments. However, the developmental mechanisms underlying these traits, particularly those of underground storage organs like rhizomes, remain poorly understood. Siam tulip (Curcuma alismatifolia Gagnep.), with its unique suite of modified organs (such as bracts, rhizomes, and tuberous roots) and dual reproductive strategies through seeds and rhizomes, serves as an ideal model for exploring organ differentiation and dormancy regulation. Through a comprehensive organ-wide transcriptomic analysis, we revealed functional differentiation and conservation across C. alismatifolia organs. For example, the outer bracts retain photosynthetic capacity similar to leaves, while the inner bracts have lost this function. The rhizome, a critical reproductive organ, acts as both a nutrient reservoir and a dormancy-driven survival mechanism in adverse conditions. Using Weighted Gene Co-expression Network Analysis, we identified transcription factors (TFs) associated with ABRE cis-acting elements as key regulators of rhizome development. By integrating transcriptomic data with high-temperature and phytohormone treatments, heterologous expression, dual-luciferase reporter assays and yeast 1-hybrid assays, we demonstrated the central role of cytochrome P450 (P450) genes, particularly ABA 8'-hydroxylase 1 (CYP707A1), in regulating rhizome dormancy release and high-temperature responses. Moreover, we showed that CYP707A1 is regulated by the MYB TF 96 (MYB96), WRKY TF 35 (WRKY35), AP2/ERF and B3 domain-containing TF RAV1 (RAV1), and Two-component response regulator ARR18 (ARR18) TFs, offering potential strategies for year-round production. This study establishes C. alismatifolia as a powerful model for investigating the formation and specialization of evolutionary innovations like rhizomes and bracts, highlighting their adaptive mechanisms and resilience to environmental challenges in Zingiberaceae.