Wang, S.; Ma, J.; Wang, Q.; Guan, Y.; Hu, X.; Sun, H.; Huang, J.

Major physiological and developmental innovations, such as stress tolerance and three-dimensional growth, are key to land plant adaptation and evolution, but their genetic basis remains to be fully understood. Although lipocalins are known for their role to optimize adaptation and development in animals, they are heavily understudied in plants. Here we show that lipocalins in the moss Physcomitrium patens are versatile regulators for some key physiological and developmental processes. Phylogenetics analyses revealed three major groups of plant lipocalins, including a newly identified group that is restricted seedless plants. The temperature-induced lipocalin gene in P. patens (PpTIL) is functionally conserved with flowering plants in response to various abiotic stresses (e.g., heat, cold, salt, and dehydration). We demonstrate that PpTIL not only regulates protonemal development and the transition from two-dimensional to three-dimensional growth, but also affects many other processes such as lipid transport and metabolism, auxin transport and biosynthesis, and chlorophyll catabolism. These findings provide major insights into the important role of lipocalins in land plant evolution.