Evolution of Secondary Plant Metabolism


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.


Ahimsa‐Müller MA, Markert A, Hellwig S, et al. (2007) Clavicipitaceous fungi associated with ergoline alkaloid‐containing Convolvulaceae. Journal of Natural Products 70: 1955–1960.

APG II (2003) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Botanical Journal of the Linnean Society 141: 399–436.

Cassady JM, Chan KK, Floss H and Leistner E (2004) Recent developments in the maytansinoid antitumor agents. Chemical & Pharmaceutical Bulletin 52: 1–26.

Dahlgren RMT (1980) A revised system of classification of the Angiospermae. Botanical Journal of the Linnean Society 90: 91–124.

Dewick PM (2002) Medicinal Natural Products. A Biosynthetic Approach. New York: John Wiley & Sons, Inc. 507pp.

Eyberger AL, Dondapati R and Porter JRJ (2006) Endophyte fungal isolates from Podophyllum peltatum produce podophyllotoxin. Journal of Natural Product 69: 1121–1124.

Harborne JB and Turner BL (1984) Plant Chemosystematics. London: Academic Press.

Harborne JB (1993) Introduction to Ecological Biochemistry, 4th edn. London: Academic Press.

Kusari S, Lamshöft M, Zühlke S and Spiteller M (2008) An endophytic fungus from Hypericum perforatum that produces hypericin. Journal of Natural Product 71: 159–162.

Lehtonen P, Helander M, Wink M, Sporer F and Saikkonen K (2005) Transfer of endophyte origin defensive alkaloids from a grass to hemiparasitic plant. Ecology Letters 8: 1256–1263.

Mabry TG, Neuman P and Philipson WR (1978) Hectorella, a member of the betalain sub‐order Chenopodiineae of the order Centrospermae. Plant Systematics and Evolution 130: 163–165.

Mothes K, Schütte HR and Luckner M (1985) Biochemistry of Alkaloids. Verlag Chemie: Weinheim.

Puri SC, Verma V, Amna T, Qazi GN and Spiteller M (2005) An endophytic fungus from Nothapodytes foetida that produces camptothecin. Journal of Natural Product 68: 1717–1719.

Ralphs MH, Creamer R and Baucom D (2008) Relationship between the endophyte Embellisia spp. and the toxic alkaloid swainsonine in major locoweed species (Astragalus and Oxytropis). Journal of Chemical Ecology 34: 32–38.

Remy W, Taylor TN, Hass H and Kerp H (1994) Four hundred‐million‐year‐old vesicular arbuscular mycorrhizae. Proceedings of the National Academy of Sciences of the USA 91: 11841–11843.

Roberts MF and Wink M (1998) Alkaloids‐Biochemistry, Ecological Functions and Medical Applications. New York: Plenum.

Rosenthal GA and Berenbaum MR (1991) Herbivores: Their Interactions with Secondary Plant Metabolites, vol. 1. The Chemical Participants. San Diego: Academic Press.

Rosenthal GA and Berenbaum MR (1992) Herbivores: Their Interactions with Secondary Plant Metabolites, vol. 2. Ecological and Evolutionary Processes. San Diego: Academic Press.

Seigler DS (1998) Plant Secondary Metabolism. Dordrecht, London, Boston: Kluwer Academic Publishers.

Shitan N and Yazaki K (2007) Accumulation and membrane transport of plant alkaloids. Current Pharmaceutical Biotechnology 8: 244–252.

Simon L, Bousquet J, Levesque C and Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 263: 67–69.

Stierle A, Strobel G and Stierle D (1993) Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Science 260: 214–216.

Waterman PG and Gray AI (1988) Chemical systematics. Natural Products Reports 4: 175–203.

Wink M and Witte L (1983) Evidence for a wide spread occurrence of the genes of quinolizidine alkaloid biosynthesis. Induction of alkaloid accumulation in cell suspension cultures of alkaloid – “free” species. FEBS Letters 159: 196–200.

Wink M (1988) Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theoretical and Applied Genetics 75: 225–233.

Wink M (1992) The Role of quinolizidine alkaloids in plant insect interactions. In: Bernays EA (ed) Insect – Plant Interactions, vol. IV, pp. 133–169. Boca Raton: CRC Press.

Wink M and Waterman P (1999) Chemotaxonomy in relation to molecular phylogeny of plants. In: Wink M (ed) Biochemistry of Plant Secondary Metabolism. Annual Plant Reviews, vol. 2, pp. 300–341. Sheffield: Sheffield Academic Press.

Wink M (2003) Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64: 3–19.

Wink M and Mohamed GIA (2003) Evolution of chemical defence traits in the Leguminosae: mapping of distribution patterns of secondary metabolites on a molecular phylogeny inferred from nucleotide sequences of the rbcL gene. Biochemical Systematics and Ecology 31: 897–917.

Wink M (2008) Plant secondary metabolism: Diversity, function and its evolution. Natural Products Communications 3: 1205–1216.

Wink M (2010a) Biochemistry of Plant Secondary Metabolism. Annual Plant Reviews, vol. 40. Chichester: Wiley‐Blackwell.

Wink M (2010b) Function of Plant Secondary Metabolites and Their Exploitation in Biotechnology. Annual Plant Reviews, vol. 39. Chichester: Wiley‐Blackwell.

Wink M, Botschen F, Gosmann C, Schäfer H and Peter G (2010) Waterman evolution and origin of plant secondary metabolism – implications for chemotaxonomy. In: Wink M (ed) Biochemistry of Plant Secondary Metabolism. Annual Plant Reviews, vol. 40. Chichester: Blackwell‐Wiley.

Wink M (2013) Evolution of secondary metabolites in legumes (Fabaceae). South African Journal of Botany 89: 164–175.

Wink M (2015a) Modes of action of herbal medicines and plant secondary metabolites. Medicines 2: 251–286.

Wink M (2015b) Vom Pfeilgift bis zum Rauschmittel: Sekundärstoffe‐die Geheimwaffen der Pflanzen. BIUZ 45: 225–235.

Further Reading

Beckers GJM and Spoel SH (2005) Fine‐tuning plant defense signaling: salicylate versus jasmonate. Plant Biology 8: 1–10.

Davies KM and Schwinn KE (2003) Transcriptional regulation of secondary metabolism. Functional Plant Biology 30: 913–925.

Facchini PJ, Bird DA and St. Pierre B (2004) Can Arabidopsis make complex alkaloids? Trends in Plant Science 9: 116–122.

Hartmann T (2007) From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochemistry 68: 2831–2846.

Kadereit JW, Körner C, Kost B and Sonnewald U (2014) Strasburger ‐ Lehrbuch der Pflanzenwissenschaften, 37th edn. Heidelberg: Springer‐Spektrum.

Krauss GJ and Nies DH (2014) Ecological Biochemistry. Environmental and Interspecific Interactions. Weinheim: Wiley‐VCH.

Larsson S (2007) The “new” chemosystematics: phylogeny and phytochemistry. Phytochemistry 68: 2904–2908.

Memelink J (2005) The use of genetics to dissect plant secondary pathways. Current Opinion in Plant Biology 8: 230–235.

Ober D (2005) Seeing double: gene duplication and diversification in plant secondary metabolism. Trends in Plant Science 10: 444–449.

Reynolds T (2007) The evolution of chemosystematics. Phytochemistry 68: 2887–2895.

Waterman PG (2007) The current status of chemical systematics. Phytochemistry 68: 2896–2903.

Zenk MH and Juenger M (2007) Evolution and current status of the phytochemistry of nitrogenous compounds. Phytochemistry 65: 2757–2772.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
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]