A model for the adaptation of Euryale ferox leaves to aquatic environments through EfCGT1-controlled flavonoid C-glycoside-specific accumulation in epidermis cells.

With changes in complex environments, plants, especially their leaves, are constantly adapting. Aquatic plants face more diverse and harsh survival situations. However, their adaptive mechanisms are largely unknown. Euryale ferox is a floating leaf aquatic plant characterized by large and rapidly expanding leaves that serve as a model for studying the environmental adaptability of aquatic plants. Single-cell transcriptional maps of key developmental nodes in E. ferox leaves were constructed using single-cell technology. The environmental adaptation strategies of E. ferox leaves exhibited significant differences when transitioning from submergence to emergence from water. Epidermis cells (ECs) preferentially differentiated during the submerged stage, involving the expression of numerous ribosomal proteins and plant immunity genes. During the floating stage, a significant number of mesophyll cells and hydathode cells undergo differentiation, with energy metabolism genes exhibiting high activity. Furthermore, the specific accumulation of flavonoid C-glycosides (FCGs) in ECs was another adaptation exhibited by E. ferox leaves. The genes involved in FCG biosynthesis demonstrated EC-specific expression, and a crucial C-glycosyltransferase gene, EfCGT1, was characterized. A transcriptional regulatory network was constructed in which the EfZHD17-EfZHD19 module regulated EfCGT1 activity. To our knowledge, this work is the first to elucidate the molecular mechanisms by which E. ferox adapts to aquatic ecology at a single-cell resolution, offering a model for aquatic plants.