Crossroads in the evolution of plant specialized metabolism

Abstract

The monophyletic group of embryophytes (land plants) stands out among photosynthetic eukaryotes: they are the sole constituents of the macroscopic flora on land. In their entirety, embryophytes account for the majority of the biomass on land and constitute an astounding biodiversity. What allowed for the massive radiation of this particular lineage? One of the defining features of all land plants is the production of an array of specialized metabolites. The compounds that the specialized metabolic pathways of embryophytes produce have diverse functions, ranging from superabundant structural polymers and compounds that ward off abiotic and biotic challenges, to signaling molecules whose abundance is measured at the nanomolar scale. These specialized metabolites govern the growth, development, and physiology of land plants-including their response to the environment. Hence, specialized metabolites define the biology of land plants as we know it. And they were likely a foundation for their success. It is thus intriguing to find that the closest algal relatives of land plants, freshwater organisms from the grade of streptophyte algae, possess homologs for key enzymes of specialized metabolic pathways known from land plants. Indeed, some studies suggest that signature metabolites emerging from these pathways can be found in streptophyte algae. Here we synthesize the current understanding of which routes of the specialized metabolism of embryophytes can be traced to a time before plants had conquered land.

Keywords: Apocarotenoids; Charophytes; Earliest land plants; Exaptation; Phenylpropanoids; Plant evolution; Plant terrestrialization; Specialized metabolism; Streptophyte algae; Stress physiology.