7 Chemotaxonomy Seen from a Phylogenetic Perspective and Evolution of Secondary Metabolism
Michael Wink
Institute of Pharmacy and Molecular Biotechnology, Heidelberg University, Heidelberg, Germany
Search for more papers by this authorFlavia Botschen
Institute of Pharmacy and Molecular Biotechnology, Heidelberg University, Heidelberg, Germany
Search for more papers by this authorChristina Gosmann
Institute of Pharmacy and Molecular Biotechnology, Heidelberg University, Heidelberg, Germany
Search for more papers by this authorHolger Schäfer
Institute of Pharmacy and Molecular Biotechnology, Heidelberg University, Heidelberg, Germany
Search for more papers by this authorPeter G. Waterman
Retired from Centre for Phytochemistry, Southern Cross University, NSW, Australia
Search for more papers by this authorMichael Wink
Institute of Pharmacy and Molecular Biotechnology, Heidelberg University, Heidelberg, Germany
Search for more papers by this authorFlavia Botschen
Institute of Pharmacy and Molecular Biotechnology, Heidelberg University, Heidelberg, Germany
Search for more papers by this authorChristina Gosmann
Institute of Pharmacy and Molecular Biotechnology, Heidelberg University, Heidelberg, Germany
Search for more papers by this authorHolger Schäfer
Institute of Pharmacy and Molecular Biotechnology, Heidelberg University, Heidelberg, Germany
Search for more papers by this authorPeter G. Waterman
Retired from Centre for Phytochemistry, Southern Cross University, NSW, Australia
Search for more papers by this authorAbstract
All plants produce secondary metabolites (SM); however, the structural types are often specific and restricted to taxonomically related plant groups. This observation was the base for the development of ‘chemotaxonomy’. A closer look indicates that a number of SM have a taxonomically restricted distribution. Very often, we also find the same SM in other plant groups which are not related in a phylogenetic context. Examples are given for several groups of alkaloids (including pyrrolizidine and quinolizidine alkaloids) and for cardiac glycosides. How to explain the patchy distribution? Theoretically, the occurrence of SM in unrelated taxa may be due to convergent evolution. Alternatively, the genes encoding the enzymes of secondary metabolism might be widely distributed in the plant kingdom, but switched on or off in a certain context. The analysis of nucleotide and amino acid sequences, which were generated in numerous genome projects during the past decades, provides evidence that most of the genes which encode key enzymes of SM formation have indeed a wide distribution in the plant kingdom. Examples discussed are tryptophan decarboxylase, tyrosine decarboxylase, phenylalanine ammonia-lyase, chalcone synthase, strictosidine synthase, berberine bridge enzyme and codeine reductase. It is speculated that these genes were introduced into the plant genome by horizontal gene transfer, i.e. via bacteria that developed into mitochondria and chloroplasts. Evidence is presented that a patchy distribution can also be due to the presence of endophytic fungi, which are able to produce SM (e.g. ergot alkaloids in Convolvulaceae). The evolution of plant secondary metabolism is a complex process that took place over the past 500 million years.
References
-
Abbott, H.C. de S.
(1886)
Certain chemical constituents of plants in relation to their morphology and evolution.
Bot. Gazz.,
11,
270–2.
10.1086/326016 Google Scholar
-
Adams, R.P.
(1972)
Chemosystematic and numerical studies of natural populations of Juniperus pinchoti Sudw.
Taxon,
21,
407–27.
10.2307/1219103 Google Scholar
- Adams, R.P. (1975) Gene flow versus selection pressure and ancestral differentiation in the composition of species: analysis of population variation in Juniperus ashei Buch. using terpenoid data. J. Mol. Evol., 5, 177–85.
- Adams, R.P. and Turner, B.L. (1970) Chemosystematic and numerical studies of natural populations of Juniperus ashei Buch. Taxon, 19, 728–51.
- Ahimsa-Müller, M.A., Markert, A., Hellwig, S., Knoop, V., Steiner, U., Drewke, C. and Leistner E. (2007) Clavicipitaceous fungi associated with ergoline alkaloid-containing Convolvulaceae. J. Nat. Prod., 70, 1955–60.
- Alston, R.E. and Turner, B.L. (1959) Applications of paper chromatography to systematics: recombination of parental biochemical components in a Baptisia hybrid population. Nature, 184, 285–6.
- Alston, R.E. and Turner, B.L. (1963) Biochemical Systematics. Prentice-Hall, New Jersey.
- APG-II; Angiosperm Phylogeny Group (2003) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot. J. Linn. Soc., 141, 399–436.
- Angiosperm Phylogeny Group (2009). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc., 161, 105–21.
- Bate-Smith, E.C. (1948) Paper chromatography of anthocyanins and related substances in petal extracts. Nature, 161, 835–8.
-
Bate-Smith, E.C.
(1958)
Plant phenolics as taxonomic guides.
Proc. Linn. Soc.,
169,
198–211.
10.1111/j.1095-8312.1958.tb01474.x Google Scholar
- Bate-Smith, E.C. (1962) The phenolic constituents of plants and their taxonomic significance. Bot. J. Linn. Soc., 58, 95–173.
- Bate-Smith, E.C. (1973) Chemotaxonomy of Geranium. Bot. J. Linn. Soc., 67, 347–59.
- Bell, E.A., Lackey, J.A. and Polhill, R.M. (1978) Systematic significance of canavanine in the Papilionoideae. Biochem. Syst. Ecol., 6, 201–12.
- Bemays, E., Edgar, J.A. and Rothschild, M. (1977) Pyrrolizidine alkaloids sequestered and stored by the aposematic grasshopper, Zonocerus variegatus . J. Zool., 182, 85–7.
- Bohlmann, F., Burkhardt, T. and Zdero, C. (1973) Naturally Occurring Polyacetylenes. Academic Press, London.
- Brower, L.P., Edmunds, M. and Moffitt, C.M. (1975) Cardenolide content and palatability of a population of Danaus chrysippus butterflies from West Africa. J. Entomol., 49, 183–96.
- Brown, K.S. and Trigo, J.R. (1995) The ecological activity of alkaloids, in The Alkaloids (ed. G.A. Cordell). Academic Press, New York, pp. 227–54.
- Candolle, A.P. de (1804) Essai sur les propriétés medicales des Plantes, comparées avec leur formes extéieures et leur classification naturelle, 1st edn. Méquignon, Paris.
- Cassady, J.M., Chan, K.K., Floss, H. and Leistner, E. (2004) Recent developments in the maytansinoid antitumor agents. Chem. Pharm. Bull., 52, 1–26.
- Dahlgren, R.M.T. (1980) A revised system of classification of the angiosperms. Bot. J. Linn. Soc., 80, 91–124.
- Donnelly, D.M.X. (1985) Neoflavonoids, in The Biochemistry of Plant Phenolics (eds C.F. Sumere and P.J. Lea). Clarendon, Oxford, pp. 199–220.
- Doyle, J. (1992) Gene trees and species trees: molecular systematics as one-character taxonomy. Syst. Bot., 17, 144–63.
- Doyle, J.J. (1993) DNA, phylogeny and the flowering of plant systematics. Bio. Sci., 43, 380–9.
- Doyle, J.J. (1994) Phylogeny of the Legume family: an approach to understanding the origins of nodulation. Anna. Rev. Ecol. Syst., 25, 325–49.
- Eyberger, A.L., Dondapati, R. and Porter, J.R.J. (2006) Endophyte fungal isolates from Podophyllum peltatum produce podophyllotoxin. J. Nat. Prod., 69, 1121–4.
- Geissmann, T.A. and Crout, D.H.G. (1969) Organic Chemistry of Secondary Plant Metabolism. Freeman Cooper, San Francisco.
- Gemeinholzer, B. and Wink, M. (2001) Solanaceae: occurrence of secondary compounds versus molecular phylogeny, in Solanaceae V: Advances in Taxonomy and Utilization (eds R.G. Berg, G.W.M. Barendse, G.M. Weerden and C. Mariani). Nijmegen University Press, Nijmegen, the Netherlands, pp. 165–78.
-
Gottlieb, O.R.
(1982)
Micromolecular Evolution, Systematics and Ecology.
Springer Verlag,
Berlin.
10.1007/978-3-642-68641-2 Google Scholar
- Gray, A.I. and Waterman, P.G. (1978) Coumarins in the Rutaceae. Phytochemistry, 17, 845–64.
- J.B. Harborne (ed.) (1964) Biochemistry of Phenolic Compounds. Academic Press, London.
- Harborne, J.B. (1966) The evolution of flavonoid pigments in plants, in Comparative Phytochemistry (ed. T. Swain). Academic Press, London, pp. 271–95.
- J.B. Harborne (ed.) (1967) Comparative Biochemistry of the Flavonoids. Academic Press, London.
- Harborne, J.B. and Turner, B.L. (1984) Plant Chemosystematics. Academic Press, London.
- Harborne, J.B. (1993) Introduction to Ecological Biochemistry, 4th edn. Academic Press, London.
- J.B. Harborne, D. Boulter and B.L. Turner (eds) (1971) Chemotaxonomy of the Leguminosae. Academic Press, London.
-
Hartmann, T. and
Witte, L.
(1995)
Chemistry, biology and chemoecology of the pyrrolizidine alkaloids, in
Alkaloids: Chemical and Biological Perspectives (ed.
S.W. Pelletier).
Pergamon,
Oxford, pp.
155–233.
10.1016/B978-0-08-042089-9.50011-5 Google Scholar
- Hegnauer, R. (1961) Die Gliederung der Rhoedales sensu Wettstein im Licht der Inhaltstoffe. Planta Med., 9, 37–46.
-
Hegnauer, R.
(1963)
The taxonomic significance of alkaloids, in
Chemical Plant Taxonomy (ed.
T. Swain).
Academic Press,
London, pp.
389–427.
10.1016/B978-0-12-395540-1.50018-X Google Scholar
-
Hegnauer, R.
(1962–1990)
Chemotaxonomie der Pflanzen, Vols
1–9.
Birkhäuser,
Basle.
10.1007/978-3-0348-9389-3 Google Scholar
-
Hegnauer, R. and
Hegnauer, M.
(1992–2001)
Chemotaxonomie der Pflanzen, Vols 10, 11a and 11b.
Birkhäuser,
Basle.
10.1007/978-3-0348-8649-9 Google Scholar
-
Hegnauer, R. and
Hegnauer, M.
(1994)
Chemotaxonomie der Pflanzen, Vol. XIa.
Leguminosae, Birkhäuser Verlag,
Basle.
10.1007/978-3-0348-8494-5 Google Scholar
- Herendeen, P.S. and Dilcher, D.L. (1992) Advances in Legume Systematics, Part 4, The Fossil Record. The Royal Botanical Gardens, Kew.
- Herout, V. and Sorm, F. (1969) Chemotaxonomy of the sesquiterpenes of the Compositae, in Perspectives in Phytochemistry (eds J.B. Harborne and T. Swain). Academic Press, London, pp. 139–65.
- Hillis, D.M., Moritz, C. and Mable, B.K. (1996) Molecular Systematics. Sinauer Associates, Sunderland, MA.
- Ingham, J.L. (1983) Naturally occurring isoflavonoids. Fortschr. Chem. Org. Naturst., 43, 1–266.
- Jensen, S.R., Nielsen, B. and Dahlgren, R. (1975) Iridoid compounds, their occurrence and systematic importance on the angiosperms. Bot. Notiser., 128, 148–80.
- Jensen, U. (1968) Serologische beiträge zur systematik der ranunculaceae. Bot. Jahrb., 88, 204–68.
- Käss, E. and Wink, M. (1995) Molecular phylogeny of the Papilionoideae (family Leguminosae): rbcL gene sequences versus chemical taxonomy. Bot. Acta, 108, 149–62.
- Käss, E. and Wink, M. (1996) Molecular evolution of the Leguminosae: phylogeny of the three subfamilies based on rbcL-sequences. Biochem. Syst. Ecol., 24, 365–78.
- Käss, E. and Wink, M. (1997a) Phylogenetic relationships in the papilionoideae (family Leguminosae) based on nucleotide sequences of cpDNA (rbcL) and ncDNA (ITS1 and 2). Mol. Phylogenet Evol, 8, 65–88.
- Käss, E. and Wink, M. (1997b) Molecular phylogeny and phylogeography of the genus Lupinus (family Leguminosae) inferred from nucleotide sequences of the rbcL gene and ITS 1+2 sequences of rDNA. Plant Syst. Evol., 208, 139–67.
- Kinghorn, A.D. and Balandrin, M.F. (1984) Quinolizidine alkaloids of the Leguminosae: structural types, analysis, chemotaxonomy and biological activities, in Alkaloids: Chemical and Biological Perspectives (ed. W.S. Pelletier). Wiley, New York, pp. 105–48.
- Kubitzki, K., Mesquita, A.A.L. and Gottlieb, O.R. (1978) Chemosystematic implications of xanthones in Bonnetia and Archyteae . Biochem. Syst. Ecol., 6, 185–7.
- Kusari, S., Lamshöft, M., Zühlke, S. and Spiteller, M. (2008) An endophytic fungus from Hypericum perforatum that produces hypericin. J. Nat. Prod., 71, 159–62.
- Lehtonen, P., Helander, M., Wink, M., Sporer, F. and Saikkonen, K. (2005) Transfer of endophyte origin defensive alkaloids from a grass to hemiparasitic plant. Ecol. Lett. 8, 1256–63.
- Mabry, T.J. (1966) The betacyanins and betaxanthins, in Comparative Phytochemistry (ed. T. Swain). Academic Press, London, pp. 231–44.
-
Mabry, T.J.,
Markham, K.R. and
Thomas, M.B.
(1970)
The Systematic Identification of Flavonoids.
Springer Verlag,
Berlin.
10.1007/978-3-642-88458-0 Google Scholar
- Malcolm, S.B. (1990) Chemical defence in chewing and sucking insect herbivores: plant-derived cardenolids in the Monarch butterfly and oleander aphid. Chemoecology, 1, 12–21.
-
Marasco, E.K. and
Schmidt-Dannert, C.
(2007)
Biosynthesis of plant natural products and characterization of plant biosynthetic pathways in recombinant microorganisms, in
Applications of Plant Metabolic Engineering (eds
R. Verpoorte,
A.W. Alfermann and
T.S. Johnson).
Springer,
Heidelberg, pp.
1–43.
10.1007/978-1-4020-6031-1_1 Google Scholar
- Markert, A., Steffan, N., Ploss, K., Hellwig, S., Steiner, U. Drewke, C., Li, S.-M-., Boland, W. and Leistner, E. (2008) Biosynthesis and accumulation of ergoline alkaloids in a mutualistic association between Ipomoea asarifolia (Convolvulaceae) and a Clavicipitalean fungus. Plant Physiol., 147, 296–305.
- Mattocks, A.R. (1972) Acute hepatotoxicity and pyrrolic metabolites in rats dosed with pyrrolizidine alkaloids. Chem. Biol. Interact., 5, 227–42.
- McLean, E. (1970) The toxic actions of pyrrolizidine (Senecio) alkaloids. Pharmacol. Rev., 22, 430–83.
-
McNair, J.B.
(1935)
Angiosperm phylogeny on a chemical basis.
Bull. Torrey Bot. Club,
62,
515–32.
10.2307/2481192 Google Scholar
- Minami, H., Kim, J.-S., Ikezawa, N., Takemura, T., Katayama, T., Kumagai, H. and Sato, F. (2008) Microbial production of plant benzoquinoline alkaloids. Proc. Natl. Acad. Sci. USA, 105, 7393–8.
- Mothes, K., Schütte, H.R. and Luckner, M. (1985) Biochemistry of Alkaloids. Verlag Chemie, Weinheim.
- Murray, M.J. (1960) The genetic basis for the conversion of menthone to menthol in Japanese mint. Genetics, 45, 925–9.
- Murray, R.D.H., Mendez, J. and Brown, S.A. (1982) The Natural Coumarins. Wiley Interscience, New York.
- Nickisch-Rosenegk von, E., Detzel, A., Wink, M. and Schneider, D. (1990) Carrier-mediated uptake of digoxin by larvae of the cardenolide sequestering moth. Syntomeida epilais. Naturwissenschaften, 77, 336–8.
-
Oksman-Caldentey, K.-M.,
Häkkinen, S.T. and
Rischer, H.
(2007)
Metabolic engineering of the alkaloid biosynthesis in plants: functional genomic approaches, in
Applications of Plant Metabolic Engineering (eds
R. Verpoorte,
A.W. Alfermann and
T.S. Johnson).
Springer,
Heidelberg, pp.
109–43.
10.1007/978-1-4020-6031-1_4 Google Scholar
- Ottaggio, L., Bestoso, F., Amirotti, A., Balbi, A., Damonte, G., Mazzei, M., Sancandi, M. and Miele, M. (2008) Taxanes from shells and leaves of Corylus avellana . J. Nat. Prod., 71, 58–60.
- Penfold, A.R. and Morrison, F.R. (1927) The occurrence of a number of varieties of Eucalyptus dives as determined by chemical analysis of the essential oils. J. Proc. Roy. Soc. N.S.W., 61, 54–67.
- Polhill, R.M. (1994) Classification of the Leguminosae, in Phytochemical Dictionary of the Leguminosae (ed. I.W. Southon). Chapman & Hall, London, pp. 35–57.
- Polhill, R.M., Raven, P.H., Crisp, M.D. and Doyle, J.J. (1981b) Advances in Legume Systematics, Part 2. The Royal Botanical Gardens, Kew.
- Polhill, R.M., Raven, P.H. and Stirton, C.H. (1981a) Evolution and systematics of the Leguminosae, in Advances in Legume Systematics, Part 1. Royal Botanical Gardens, Kew, pp. 1–26.
- Puri, S.C., Verma, V., Amna, T., Qazi, G.N. and Spiteller, M. (2005) An endophytic fungus from Nothapodytes foetida that produces camptothecin. J. Nat. Prod., 68, 1717–9.
- Ralphs, M.H., Creamer, R., Baucom, D., Gardner, D.R., Welsh, S.L., Graham, J.D., Hart, C., Cook, D. and Stegelmeier, B.L. (2008) Relationship between the endophyte Embellisia spp. and the toxic alkalod swainsonine in major locoweed species (Astragalus and Oxytropis). J. Chem. Ecol., 34, 32–8.
- Remy, W., Taylor, T.N., Hass, H. and Kerp, H. (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Natl. Acad. Sci., USA, 91, 11841–3.
- Roberts, M.F. and Wink, M. (1998) Alkaloids: Biochemistry, Ecological Functions and Medical Applications. Plenum, New York.
- Roeder, E. (1995) Medicinal plants in Europe containing pyrrolizidine alkaloids. Pharmazie, 50, 83–98.
- Rosenthal, G.A. (1982) Plant Nonprotein Amino and Imino Acids. Academic Press, New York, 1982.
- Rothschild, M. (1966) Experiments with captive predators and the poisonous grasshopper, Poekilocerus bufonius . Proc. R. Entomol. Soc. Lond., 31, 32–3.
- Rothschild, M. (1972) Secondary plant substances and warning coloration in insects, in Insect/Plant Relationships (ed. H.E. Emden). Blackwell, Oxford, pp. 59–83.
- Rothschild, M., Aplin, R.T., Cockrum, P.A., Edgar, J.A., Fairweather, P. and Lees, R. (1979) Pyrrolizidine alkaloids in arctiid moths. Biol. J. Linn. Soc., 12, 305–26.
- Rothschild, M., Reichstein, T., Euw, J. and Alpin, R. (1970a) Toxic Lepidoptera. Toxicon, 8, 293–9.
- Rothschild, M., Von Euw, J. and Reichstein, T. (1970b) Cardiac glycosides in the oleander aphid, Aphis nerii . Insect Physiol., 16, 1141–5.
- Rothschild, M., Von Euw, J. and Reichstein, T. (1971) Heart poisons (cardiac glycosides) in the lygaeid bugs, Caenocoris nerii and Spilostethus pandorus . Insect Biochem., 1, 373–84.
- Rothschild, M., Von Euw, J. and Reichstein, T. (1973) Cardiac glycosides, heart poisons in the Polka-Dot moth, Syntomeida epilais (Ctenuchidae Lepidoptera). Proc. R. Soc. Lond. B, 183, 227–47.
- Rowell-Rahier, M., Witte, L., Ehmke, A. and Hartmann, T. (1991) Sesquestration of plant pyrrolizidine alkaloids by chrysomelid beetles and selective transfer into the defensive secretions. Chemoecology, 2, 41–8.
-
Sato, F.,
Inai, K. and
Hashimoto, T.
(2007)
Metabolic engineering in alkaloid biosynthesis: case studies in tyrosine and putrescine derived alkaloids, in
Applications of Plant Metabolic Engineering (eds
R. Verpoorte,
A.W. Alfermann and
T.S. Johnson).
Springer,
Heidelberg, pp.
145–73.
10.1007/978-1-4020-6031-1_6 Google Scholar
- Schmeller, T., EI-Shazly, A. and Wink, M. (1997) Allelochemical activities of pyrrolizidine alkaloids: interactions with neuroreceptors and acetylcholine-related enzymes. J. Chem. Ecol., 23, 399–416.
- Schmeller, T., Sauerwein, M., Sporer, F., Mdller, W.E. and Wink, M. (1994) Binding of quinolizidine alkaloids to nicotinic and muscarinic receptors. J. Nat. Prod., 57, 1316–9.
- Simon, L., Bousquet, J., Levesque, C. and Lalonde, M. (1993) Origin and diversification of endomycorrhizal fungi and coinidence with vascular land plants. Nature, 263, 67–9.
- Smith, P.M. (1976) The Chemotaxonomy of Plants. Edward Arnold, London.
-
Soltis, P.,
Soltis, D.E. and
Doyle, J.J.
(1992)
Molecular Systematics of Plants.
Chapman & Hall,
London.
10.1007/978-1-4615-3276-7 Google Scholar
- Soltis, P., Soltis, D.E. and Doyle, J.J. (1998) Molecular Systematics of Plants II. DNA Sequencing. Kluwer, Boston.
-
Southon, I.W.
(1994)
Phytochemical Dictionary of the Leguminosae.
Chapman & Hall,
London.
10.1007/978-1-4899-3047-7 Google Scholar
- Sprent, J.I. and McKey, D. (1994) Advances in Legume Systematics, Part 5, The Nitrogen Factor. The Royal Botanical Gardens, Kew.
-
Stermitz, F.
(1998)
Plant parasites, in
Alkaloids: Biochemistry, Ecological Functions and Medical Applications (eds
M.F. Roberts and
M. Wink).
Plenum,
New York, pp.
327–36.
10.1007/978-1-4757-2905-4_13 Google Scholar
- Stierle, A., Strobel, G. and Stierle, D. (1993) Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Science, 260, 214–6.
- Stirton, C.H. (1987) Advances in Legume Systematics, Part 3. The Royal Botanical Gardens, Kew.
- Sutherland, M.D. and Park, R.J. (1967) Sesquiterpenes and their biogenesis in Myoporum desertii A. Cunn, in Terpenoids in Plants (ed. J. Pridham). Academic Press, London, pp. 147–57.
- T. Swain (ed.) (1963) Chemical Plant Taxonomy. Academic Press, London.
- T. Swain (ed.) (1966) Comparative Phytochemistry. Academic Press, London.
- Teuscher, E. and Lindequist, U. (1994) Biogene Gifte. Biologie, Chemie, Pharmakologie. G. Fischer, Stuttgart.
-
Thorne, R.F.
(1968)
Synopsis of a putative phylogenetic classification of the flowering plants.
Aliso,
6,
57–66.
10.5642/aliso.19680604.06 Google Scholar
-
Thorne, R.F.
(1976)
A phylogenetic classification of the Angiospermae.
Evol. Biol.,
9,
35–106.
10.1007/978-1-4615-6950-3_2 Google Scholar
-
Verpoorte, R.,
Alfermann, A.W. and
Johnson, T.S.
(2007)
Applications of Plant Metabolic Engineering.
Springer,
Heidelberg.
10.1007/978-1-4020-6031-1 Google Scholar
- Waterman, P.G. (1975) Alkaloids of the Rutaceae: their distribution and systematic significance. Biochem. Syst. Ecol., 3, 149–80.
- Waterman, P.G. (1997) Chemical taxonomy, in The Alkaloids (ed. G.A. Cordell), vol. 50. Academic Press, New York, pp. 537–65.
- Waterman, P. (2007) The current status of chemical systematics. Phytochemistry, 68, 2896–903.
- Waterman, P.G. and Gray, A.I. (1988) Chemical systematics. Nat. Prod. Rep., 4, 175–203.
- Waterman, P.G. and Mole, S. (1989) Extrinsic factors influencing production of secondary metabolites in plants, in Insect–Plant Interactions (ed. E.A. Bernays). CRC Press, Boca Raton, pp. 107–34.
- Wink, M. (1988) Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theoret. Appl. Genet., 75, 225–33.
- Wink, M. (1992) The role of quinolizidine alkaloids in plant–insect interactions, in Insect–Plant Interactions (ed. E.A. Bernays). CRC Press, Boca Raton, pp. 131–66.
- Wink, M. (1993a) Quinolizidine alkaloids, in Methods in Plant Biochemistry (ed. P.G. Waterman). Academic Press, London, pp. 197–239.
- Wink, M. (1993c) Allelochemical properties and the raison d'être of alkaloids, in The Alkaloids (ed. G.A. Cordell). Academic Press, New York, pp. 1–118.
- Wink, M. (2000) Interference of alkaloids with neuroreceptors and ion channels, in Bioactive Natural Products (ed. Atta-Ur-Rahman), Vol 11. Elsevier, Amsterdam, pp. 3–129.
- Wink, M. (2003) Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry, 64, 3–19.
- Wink, M. (2007) Molecular modes of action of cytotoxic alkaloids – from DNA intercalation, spindle poisoning, topoisomerase inhibition to apoptosis and multiple drug resistance, in The Alkaloids (ed. G. Cordell), vol. 64. Academic Press, San Diego, pp. 1–48.
- Wink, M. (2008) Plant secondary metabolism: diversity, function and its evolution. Nat. Prod. Commun., 3, 1205–16.
- Wink, M. and Kaufmann, M. (1996) Phylogenetic relationships between some members of the subfamily Lamioideae (family Labiatae) inferred from nucleotide sequences of the rbcL-gene. Botanica Acta, 109, 139–48.
-
Wink, M.,
Kaufmann, M. and
Kaess, E.
(1993)
Molecular versus chemical taxonomy.
Planta Med.,
59(Suppl. 7),
A594–5.
10.1055/s-2006-959803 Google Scholar
- Wink, M., Meiβner, C. and Witte, L. (1995) Patterns of quinolizidine alkaloids in 56 species of the genus Lupinus . Phytochemistry, 38, 139–53.
- Wink, M. and Mohamed, G.I.A. (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. Biochem. Syst. Ecol., 31, 897–917.
- Wink, M., Schmeller, T. and Latz-Brüning, B. (1998) Modes of action of allelochemical alkaloids: interaction with neuroreceptors, DNA and other molecular targets. J. Chem. Ecol., 24, 1881–937.
- Wink, M. and Van Wyk, B.E. (2008) Mind-Altering and Poisonous Plants of the World. BRIZA, Pretoria.
- Wink, M. and von Nickisch-Rosenegk, E. (1997) Sequence data of mitochondrial 16S rDNA of Arctiidae and Nymphalidae (Lepidoptera): evidence for a convergent evolution of pyrrolizidine alkaloid and cardiac glycoside sequestration. J. Chem. Ecol., 23, 1549–68.
- Wink, M. and Waterman, P. (1999) Chemotaxonomy in relation to molecular phylogeny of plants, in Annual Plant Reviews, Vol. 2: Biochemistry of Plant Secondary Metabolism (ed. M. Wink). Sheffield Academic Press, Sheffield, pp. 300–41.
- Wink, M. and Witte, L. (1983) Evidence for a widespread occurrence of the genes of quinolizidine alkaloid biosynthesis. FEBS Lett., 159, 196–200.
- Woolley, J.G. (1993) Tropane alkaloids, in Methods in Plant Biochemistry (ed. P.G. Waterman), vol. 8. Academic Press, London, pp. 133–73.
- Wu, S. and Chappell, J. (2008) Metabolic engineering of natural products in plants; tools of the trade and challenges for the future. Curr. Opin. Biotechnol., 19, 145–52.
- Zavarin, E., Cobb, F.W., Bergot, J. and Bawber, H.W. (1971) Variation of the Pinus ponderosa needle oil with season and age. Phytochemistry, 10, 3107–14.
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