Accessible versatility underpins the deep evolution of plant specialized metabolism

Abstract

The evolution of several hallmark traits of land plants is underpinned by phytochemical innovations. The specialized metabolism of plants can appear like a teeming chaos that has yielded an ungraspable array of chemodiversity. Yet, this diversity is the result of evolutionary processes including neutral evolution, drift, and selection that have shaped the metabolomic networks. Deciphering the evolutionary history of the specialized metabolome in the context of plant terrestrialization has only just begun. Studies on phytochemistry of model organisms and crop plants enabled the sketch of a blueprint for the biochemical landscape of land plants and a good idea on the diversity that can be explored. Evolutionary metabolomics has in the past been successfully used to identify traits that were critical for domestication of angiosperms or to unravel key innovations in land plants. Owing to recent advances in the study of non-model land plants and their close streptophyte algal relatives we can now begin to appreciate the variation of metabolic networks across the green lineage—and understand convergent solutions to similar environmental challenges and effects that plant terrestrialization had on these networks. Here, we highlight the significant progress made with regard to identifying metabolomic diversity by adding non-model organisms to the equation. We discuss the role of neutral evolution in the context of metabolomic diversity and the effects that environmental challenges had on the lineage-specific specialized metabolism from an evolutionary point of view.