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.

Divergent responses in desiccation experiments in two ecophysiologically different Zygnematophyceae

“…Concomitantly, cysteine breakdown is upregulated, likely leading to more sulphur accumulation ( cf . Romero et al 2014); this aligns with the increased transcriptional responses related to mitochondrial biology (Figure 3‐5) where cysteine catabolism is occurring and the idea that stress‐related metabolism can be best conceptualized in networks (see discussions in Dadras et al, 2023b). The involvement of sulfur metabolism in response to drought stress has been studied extensively in land plants (Mannan et al 2022; Malcheska et al 2017; Hanson et al 1994).…”

“…It was interesting to find that Zygnema showed little enrichment among its differential gene expression patterns that pointed to genes for signaling components. cysteine catabolism is occurring and the idea that stress-related metabolism can be best conceptualized in networks (see discussions in Dadras et al, 2023b). The involvement of sulfur metabolism in response to drought stress has been studied extensively in land plants (Mannan et al 2022;Malcheska et al 2017;Hanson et al 1994).…”

A multidisciplinary view on plant terrestrialization and the evolution of land plants

“…Text next to lineages or last common ancestor (LCA) nodes give a brief account on the findings of the studies highlighted in this editorial. Figure modified from Dadras et al (2023b) with permission.…”

An ancient route towards salicylic acid and its implications for the perpetual Trichormus–Azolla symbiosis

“…The PAL-dependent pathway is less-explored as a source for SA in land plants compared to ICS-dependent synthesis of SA. The PALdependent pathway, despite being highly radiated, has homologs for all enzymes being present at least in the last common ancestor of all streptophytes-going hand in hand with the idea that parts of this pathway were part of the genetic building blocks that allowed for the radiation of specialized metabolism in land plants (Dadras et al, 2023;Fürst-Jansen et al, 2020). This is most likely explained by the fact that this pathway is not a highly specialized pathway for SA biosynthesis, but instead recruits steps from other pathways, such as the phenylpropanoid pathway.…”