Towards a functional understanding of the plant metabolome

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Plants are true organic chemists—the chemical diversity of plant metabolomes goes hand in hand with functional diversity. New, often unexpected roles are being reported for both evolutionarily conserved and well-characterised central metabolites such as amino acids, nucleotides, and sugars, and for specialized/secondary metabolites such as carotenoids, glucosinolates, and terpenoids. Our review aims to highlight recent studies reporting novel roles of metabolites and to emphasize the importance of cell-wide identification of metabolite–protein complexes for the comprehensive, functional understanding of the plant metabolome.

Introduction

Plants are amazing organic chemists, with the plant metabolome ranging from tens to hundreds of thousands of small molecules. Novel chemistry is being uncovered even in extensively studied plant species such as Arabidopsis thaliana. A great and recent example is the discovery of more than 50 previously unknown triterpene compounds produced by Arabidopsis roots and employed to assemble and modulate root microbiota [1]. At present, we fail to grasp the full complexity of plant metabolomes and the mode of action for many of the known metabolites. At the same time, new functionalities are being assigned to previously characterised compounds. For example, a recent study demonstrated the role of the amino acid glutamate in the activation of a long-distance, calcium-based plant defence signalling [2,3]. Our review aims to highlight recent studies (focusing on the last five years) that demonstrate the multiple and often unexpected roles of plant metabolites beyond the canonical division of primary and specialized metabolism. To exemplify, we will focus on nucleotides, a group of evolutionarily conserved primary compounds characterised by well-known and emerging functionalities. We will also briefly discuss recent examples of specialized metabolites that defy the simple notion of defence compounds. Finally, we will discuss how emerging biochemical approaches for cell-wide identification of small-molecule-protein complexes, such as small-molecule limited-proteolysis (Lip-SMap) [4••], could be exploited to provide a comprehensive understanding of the plant metabolome.

Section snippets

Nucleotides, from building blocks to signals

Nucleotides are the building blocks of DNA and RNA, although they have many other essential roles in both metabolism and signal transduction. With typically low-to-mid (mM) intracellular concentrations, adenosine triphosphate (ATP) is among the most abundant compounds measured in living cells [5]. ATP is best known for being the energy store used to fuel energy-dependent biochemical reactions, such as metabolic conversions, transport, and cytoskeletal rearrangements. ATP is also a critical

More than defence compounds: regulatory roles of specialized metabolites

Historically, plant secondary (specialized) metabolites were discussed as either attractants or defence compounds enabling plants to tolerate both biotic (e.g., herbivory and pathogen attack) and abiotic (e.g., light and temperature fluctuations) stress conditions. Nowadays, it is clear that specialized metabolites can have other equally essential functionalities.

Carotenoid-derived small molecules (apocarotenoids) are possibly the best example of specialized metabolites and comprise abscisic

From interaction to function

Biological entities, including proteins, nucleic acids, and small molecules, rarely act alone but rather as part of a complex. Along similar lines, metabolites exert most of their function via interaction with a macromolecular partner, most commonly a protein. Therefore, cell-wide identification of metabolite-protein complexes is considered an effective way to learn about metabolite function as attested by the ATP example above [4••,6]. Knowledge of the protein partners is also central for the

Conclusions

There are plenty of small-molecules that remain to be identified and many of the known ones to be functionally characterised. Small molecule identification and characterisation is an exciting research frontier with significant potential for discovery. There are clearly several experimental strategies that could be exploited. Cell-wide identification of protein–metabolite complexes is a promising approach, which nevertheless needs to be complemented with a careful biological validation.

Declaration of interest

None.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

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