Evolution of Secondary Plant Metabolism

Abstract

The biosynthesis of secondary metabolites (SMs), which are important for the fitness of the plants as defence against herbivores and microbes and also as signal compounds to attract pollinators and fruit dispersers, occurs universally in higher plants and shows very high structural diversity. The evolution of SMs in higher plants rests on variation in the enzymatic manipulation of a relatively small number of primary precursors. Evidence is presented that at least some of the genes encoding key enzymes of biosynthesis probably have reached plants by ancient horizontal gene transfer (HGT), for example, from protobacteria or cyanobacteria which later became mitochondria and plastids. Another source of SMs can be ectomycorrhizal and endophytic fungi; they can directly provide plants with defence compounds or might have transferred their pathway genes into the genome of their host plants times ago.

Key Concepts

  • Plants have evolved secondary metabolites as bioactive substances as a measure to protect themselves against herbivores.
  • Secondary metabolites are part of the innate immune system of plants, used to defend themselves against bacteria, fungi and viruses.
  • Secondary metabolism is dynamic and can react in case of a herbivoral or microbial attack by activating prodrugs, by either increasing the concentration of existing SM or by inducing the synthesis of new SMs (phytoalexins).
  • Secondary metabolites occur in a broad diversity and functionality.
  • Secondary metabolites derive from primary metabolites using a limited number of key pathways. Functional diversity is gained by adding diverse combinations of reactive functional groups.
  • Terpenoids and phenolics are present in almost all plants, whereas alkaloids and other nitrogenā€containing SMs are more common in angiosperms.
  • Some groups of SMs occur in a few restricted plant genera only, which are often not related.
  • The patchy distribution can be due to convergent evolution of the corresponding pathways.
  • Alternatively, the genes for SM biosynthesis have been introduced into the plant genome by horizontal gene transfer from protobacteria (which became mitochondria) and cyanobacteria (which became chloroplast).
  • Some SMs are produced by endophytic fungi, which infect a limited number of often unrelated species. As a consequence, this can also lead to a patchy distribution of SMs.

Keywords: secondary metabolites; distribution; defence and signal compounds; innate immune system; evolutionary changes; horizontal gene transfer

Figure 1. The evolution of five different classes of alkaloids from a common amino acid precursor, tyrosine. A given symbol always indicates the same carbon throughout the reaction scheme.
Figure 2. Distribution of 1‐btiq alkaloids in angiosperms mapped on a phylogenetic framework (APG II). Branches in which 1‐btiq are produced are printed in black and bold.
Figure 3. Distribution of quinolizidine alkaloid (QA) and pyrrolizidine alkaloids (PAs) in angiosperms mapped on a phylogenetic framework (APG II). Branches in which QA are produced are printed in blue, those with /PA in red.
Figure 4. Molecular phylogeny of (a) PAL and (b) CHS inferred from derived amino acid sequences of the corresponding genes. Adapted with permission from Wink et al. (2010) © Wiley‐Blackwell.
Figure 5. Phylogeny of (a) strictosidine synthase (STS) and (b) berberine bridge enzyme (BBE) inferred from derived amino acid sequences. Taxa, which produce respective alkaloids, are marked by an arrow and printed in bold. Adapted with permission from Wink et al. (2010) © Wiley‐Blackwell.
Figure 6. Hypothetical scheme for the evolution of secondary metabolism in plants.
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Wink, Michael(Feb 2016) Evolution of Secondary Plant Metabolism. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001922.pub3]