Elsevier

Phytochemistry

Volume 64, Issue 1, September 2003, Pages 3-19
Phytochemistry

Review
Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective

https://doi.org/10.1016/S0031-9422(03)00300-5Get rights and content

Abstract

Secondary metabolites, at least the major ones present in a plant, apparently function as defence (against herbivores, microbes, viruses or competing plants) and signal compounds (to attract pollinating or seed dispersing animals). They are thus important for the plant's survival and reproductive fitness. Secondary metabolites therefore represent adaptive characters that have been subjected to natural selection during evolution. Molecular phylogenies of the Fabaceae, Solanaceae and Lamiaceae were reconstructed and employed as a framework to map and to interpret the distribution of some major defence compounds that are typical for the respective plant families; quinolizidine alkaloids and non-protein amino acids for legumes; tropane and steroidal alkaloids for Solanaceae, and iridoids and essential oils for labiates. The distribution of the respective compounds appears to be almost mutually exclusive in the families studied, implying a strong phylogenetic and ecological component. However, on a closer look, remarkable exceptions can be observed, in that certain metabolites are absent (or present) in a given taxon, although all the neighbouring and ancestral taxa express (or do not express, respectively) the particular trait. It is argued that these patterns might reflect differential expression of the corresponding genes that have evolved earlier in plant evolution. The inconsistent secondary metabolite profiles mean that the systematic value of chemical characters becomes a matter of interpretation in the same way as traditional morphological markers. Thus, the distribution of secondary metabolites has some value for taxonomy but their occurrence apparently reflects adaptations and particular life strategies embedded in a given phylogenetic framework.

Molecular phylogenies of the families Fabaceae, Solanaceae and Lamiaceae were reconstructed and employed as a framework to map and to interpret the distribution of some major defence compounds that are typical for the respective plant families. Profiles of adaptive secondary metabolites are often inconsistent which apparently reflect particular life strategies embedded in a given phylogenetic framework

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Section snippets

Defence and signal molecules

Secondary metabolites (SM) are present in all higher plants, usually in a high structural diversity (Table 1). As a rule, a single group of SM dominates within a given taxon. A few major compounds are often accompanied by several derivatives and minor components. Altogether, the pattern of SM in a given plant is complex; it changes in a tissue- and organ specific way; regularly, differences can be seen between different developmental stages (e.g., organs important for survival and reproduction

Distribution patterns of secondary metabolites and chemotaxonomy

The systematic and phylogenetic analysis of plants was traditionally based on macroscopic and microscopic morphological characters. Since secondary metabolites are often similar within members of a clade, their occurrence or absence might be taken as an indication of common descent and thus relatedness. While the potential value of plant secondary metabolites to taxonomy has been recognised for nearly 200 years (Candolle, 1804, Abbott, 1896) their practical application has been restricted to

Conclusions

When analysing the profiles of typical secondary metabolites in Fabaceae, Solanaceae, Lamiaceae and other plant families we observe in some instances that almost all members of a monophyletic clade share a chemical characteristic; this would favour its use as a taxonomic marker. In other instances a particular SM may occur in several unrelated clades and/or plant families (Wink and Waterman, 1999, Gemeinholzer and Wink, 2001, Wink and Mohamed, 2003). The erratic SM distribution can be due to

Acknowledgements

The work reviewed in this contribution was supported by grants of the Deutsche Forschungsgemeinschaft (DFG). I would like to thank my former co-workers E. Kaess, I. Kaufmann, B. Gemeinholzer and G. Mohamed for their contributions to molecular systematics of Fabaceae, Lamiaceae and Solanaceae.

Michael Wink is the Director of the Institute of Pharmacy and Molecular Biotechnology and professor of Pharmaceutical Biology of Heidelberg University (Germany). He was trained in biology and chemistry (Diploma 1977, University of Bonn) before obtaining a Dr. rer. nat. (1980) in Pharmaceutical biology (alkaloid biochemistry and physiology) at the Technical University of Braunschweig. 1984/85 he obtained his habilitation at Braunschweig and a Heisenberg fellowship of the German Science

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    Michael Wink is the Director of the Institute of Pharmacy and Molecular Biotechnology and professor of Pharmaceutical Biology of Heidelberg University (Germany). He was trained in biology and chemistry (Diploma 1977, University of Bonn) before obtaining a Dr. rer. nat. (1980) in Pharmaceutical biology (alkaloid biochemistry and physiology) at the Technical University of Braunschweig. 1984/85 he obtained his habilitation at Braunschweig and a Heisenberg fellowship of the German Science Foundation. Afters stays at the Max-Planck-Institute for Plant Breeding Research (Cologne) and the Gencentre of Munich University (1986-1988) he accepted a professorship in Pharmaceutical Biology at the University of Mainz (1988-1989). M. Wink became a professor of Pharmaceutical biology of Heidelberg University in the Faculty of Pharmacy in 1989. He also served as dean or vice dean for more than 9 years. His research program ranges from phytochemistry, pharmacology, chemical ecology, and molecular biotechnology to molecular evolution.

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