Establishment of the grass lignin metabolic network during monocot evolution

Abstract

Plants produce a vast diversity of chemical compounds, yet the evolutionary history of the underlying complex metabolic networks remains poorly understood. Grasses (Poaceae family) possess a unique lignin metabolic network that can utilize both phenylalanine and tyrosine as precursors to synthesize canonical lignin as well as non-canonical acylated and tricin-conjugated lignin subunits. This study traces the evolutionary remodeling and establishment of the grass lignin metabolic network by combining phylogenomics with biochemical and chemical analyses across Poaceae, Poales, and other monocot species. These multidisciplinary comparative analyses reveal that the acylated lignin evolved in commelinids, followed by tyrosine-derived lignin biosynthesis in non-grass graminids through fine-tuning of pathway enzymes and transcriptional factors. Later, biosynthesis and incorporation of the flavonoid tricin into the cell wall took place within the core grasses via the evolution of chrysoeriol 5'-hydroxylase (C5'H) activity within the CYP75B enzyme family. These findings illustrate the emergence of different network modules at distinct times during monocot evolution that became integrated into the complex yet coherent metabolic network underlying the unique lignin chemical diversity of grasses.