Gene Coexpression Network Reveals Insights into the Origin and Evolution of a Theanine-Associated Regulatory Module in Non-Camellia and Camellia Species

Theanine (thea) is one of the most important plant-derived characteristic secondary metabolites and a major healthcare product because of its beneficial biological activities, such as being an antianxiety agent, promoting memory, and lowering blood pressure. Thea mostly accumulates in Camellia plants and is especially rich in Camellia sinensis (tea plant). Although some functional genes (e.g., TS, GOGAT, and GS) attributed to thea accumulation have been separately well explored in tea plants, the evolution of a regulatory module (highly interacting gene group) related to thea metabolism remains to be elaborated. Herein, a thea-associated regulatory module (TARM) was mined by using a comprehensive analysis of a weighted gene coexpression network in Camellia and non-Camellia species. Comparative genomic analysis of 84 green plant species revealed that TARM originated from the ancestor of green plants (algae) and that TARM genes were recruited from different evolutionary nodes with the most gene duplication events at the early stage. Among the TARM genes, two core transcription factors of NAC080 and LBD38 were deduced, which may play a crucial role in regulating the biosynthesis of thea. Our findings provide the first insights into the origin and evolution of TARM and indicate a promising paradigm for identifying vital regulatory genes involved in thea metabolism.