Secondary Metabolites: Deterring Herbivores

Abstract

All plants produce and store secondary metabolites (SMs), which are not important for primary or energy metabolism of a plant. However, SMs are not waste products, but important for the ecological fitness and survival of the plants producing them. Apparently, plants have evolved the production and storage of SM as a means to defend themselves against herbivores, bacteria, fungi and viruses, as well as other competing plants. Most SMs can interfere with basic molecular targets of animals or microbes and thus provide plants with an adequate protection against a multitude of enemies. Plants usually produce complex mixtures of SMs, which can work in an additive or even synergistic way. Some defence chemicals address a single target, such as a neurotransmitter receptor or an ion channel; others have a broad‐activity spectrum and exhibit pleiotropic activities on several targets. SMs also serve as signal compounds attracting pollinating and fruit‐dispersing animals.

Key Concepts

  • Plants cannot run away when attacked by herbivores; they use defence chemicals to ward off enemies.
  • Plants do not have an elaborate immune system with specific antibodies to defend themselves against microbes, and instead use antimicrobial secondary metabolites (SMs) in their innate immune system.
  • Plants produce and store complex mixtures of SMs with additive or even synergistic activities.
  • SMs are important for chemical defence but are also used to attract pollinating and fruit‐dispersing animals.
  • The process of biosynthesis, transport and storage of SMs is energetically costly.
  • Some SMs specifically interact with a particular molecular target in herbivores or microbes, whereas other SMs are nonselective, thus being able to address a multitude of enemies.
  • Synthesis, transport and storage of SMs are optimised in space and time to fulfil the ecological functions.
  • Although some SMs are stored in a constitutive way, others are inducible and are only made in case of danger.
  • Jasmonic acid and salicylic acid are important signal molecules in the regulation of SM biosynthesis.
  • Herbivores have evolved effective biochemical adaptations towards the defence chemistry of plants, involving cytochrome p450 enzymes and ABC transporters.

Keywords: chemical defence; herbivores; microbes; allelochemicals; signal and defence compounds

Figure 1. Structures of representatives from classes of secondary metabolites (Table). (a) Amines: butylamine and , ‐dimethyltryptamine. Alkaloids: sparteine and nicotine. Nonprotein amino acids: canavanine. Cyanogenic glucosides: prunasin. Glucosinolates: glucobrassicin. Monoterpenes: thymol. Sesquiterpenes: helenalin. Diterpenes: ginkgolide B. Triterpenes: oleanolic acid. Steroids: diosgenin. (b) Tetraterpenes: β‐carotene. Polyketides: emodin. Polyenes: cicutoxin. Flavonoids: quercetin. Isoflavones: genistein. Anthocyanins: malvidin. Phenylpropanoids: rosmarinic acid.
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References

Aguiar R and Wink M (2005) Do naïve ruminants degrade alkaloids in the rumen? Journal of Chemical Ecology 31: 761–787.

Baldwin I (1994) Chemical changes rapidly induced by folivory. In: Bernays EA (ed) Insect–Plant Interactions, vol. 5, pp. 1–23. Boca Raton, FL: CRC Press.

Bekaert M, Edger PP, Hudson CM, Pres JC and Conant GC (2012) Metabolic and evolutionary costs of herbivory defense: systems biology of glucosinolate synthesis. New Phytologist 196: 596–605.

Bernays EA and Chapman RF (1994) Host–Plant Selection by Phytophagous Insects. New York: Chapman & Hall.

Cipollini ML and Levey DJ (1997) Secondary metabolites of fleshy vertebrate‐dispersed fruits: adaptive hypotheses and implications for seed dispersal. American Naturalist 150: 346–373.

Conn EE (1981) Secondary plant products. In: Stumpf PK and Conn EE (eds) The Biochemistry of Plants, vol. 7. New York: Academic Press.

Creelman RA and Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annual Review of Plant Physiology and Plant Molecular Biology 48: 355–381.

De Moraes CM, Lewis WJ, Paré PW, Alborn HT and Tumlinson JH (1998) Herbivore infested plants selectively attract parasitoids. Nature 393: 570–573.

Dean M, Hamon Y and Chimini G (2001) The human ATP‐binding cassette (ABC) transporter superfamily. Journal of Lipid Research 42: 1007–1017.

Dicke M, Sabelius MW, Takabayashi J, Bruin J and Posthumus MA (1990) Plant strategies of manipulating predator–prey interactions through allelochemicals: prospects for application in pest control. Journal of Chemical Ecology 16: 3091–3118.

Dictionary of Natural Products (1996) CD‐ROM. London: Chapman & Hall (version 5.1).

Facchini P (2001) Alkaloid biosynthesis in plants: biochemistry, cell biology, molecular regulation, and metabolic engineering applications. Annual Review of Plant Physiology and Plant Molecular Biology 52: 29–66.

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

Hartmann T and Witte L (1995) Chemistry, biology and chemoecology of the pyrrolizidine alkaloids. In: Pelletier SW (ed) Alkaloids: Chemical and Biological Perspectives, vol. 9, pp. 155–233. Oxford, UK: Pergamon Press.

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

Holzinger F and Wink M (1996) Mediation of cardiac glycoside insensitivity in the monarch butterfly (Danaus plexippus): role of an amino acid substitution in the ouabain binding site of Na+,K+‐ATPase. Journal of Chemical Ecology 22: 1921–1937.

Kissen R, Rossiter JT and Bones AM (2009) The ‘mustard oil bomb’: not so easy to assemble?! Localization, expression and distribution of the components of the myrosinase enzyme system. Phytochemical Reviews 8: 69–86.

Luckner M (1990) Secondary Metabolism in Microorganisms, Plants and Animals. Heidelberg, Germany: Springer.

Mann J (1992) Murder, Magic and Medicine. London: Oxford University Press.

Marasco EK and Schmidt‐Dannert C (2007) Biosynthesis of plant natural products and characterization of plant biosynthetic pathways in recombinant microorganisms. In: Verpoorte R, Alfermann AW and Johnson TS (eds) Applications of Plant Metabolic Engineering, pp. 1–43. Heidelberg: Springer.

Martinoia E, Klein M, Geisler M, et al. (2002) Multifunctionality of plant ABC transporters – more than just detoxifiers. Planta 214: 345–355.

Meinwald J (1990) Alkaloids and isoprenoids as defensive and signaling agents among insects. Pure and Applied Chemistry 62: 1325–1328.

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

Oksman‐Caldentey K‐M, Häkkinen ST and Rischer H (2007) Metabolic engineering of the alkaloid biosynthesis in plants: functional genomic approaches. In: Verpoorte R, Alfermann AW and Johnson TS (eds) Applications of Plant Metabolic Engineering, pp. 109–143. Heidelberg: Springer.

Petersen M (2007) Current status of metabolic phytochemistry. Phytochemistry 68: 2847–2860.

Putz A and Proksch P (2010) Chemical defence in marine ecosystems. In: Wink M (ed) Functions and Biotechnology of Plant Secondary Metabolites, 2nd edn, vol. 39, pp. 162–213. Annual Plant Reviews. Chichester, GB: Wiley‐Blackwell.

Rea PA (2007) Plant ATP‐binding cassette transporters. Annual Review of Plant Biology 58: 347–375.

Roberts MF and Wink M (1998) Alkaloids–Biochemistry, Ecology and Medicinal Applications. New York: Plenum Press.

Rosenthal GA (1982) Plant Nonprotein Amino Acids and Imino Acids. London: Academic Press.

Rosenthal GA and Janzen D (1991) Herbivores: their interactions with secondary plant metabolites. In: Rosenthal GA and Berenbaum MR (eds) The Chemical Participants, 2nd edn, vol. 1. San Diego, CA: Academic Press.

Rosenthal GA and Berenbaum MR (1992) Herbivores: their interactions with secondary plant metabolites. In: Rosenthal GA and Hanzen DH (eds) Ecological and Evolutionary Processes, 2nd edn, vol. 2. San Diego, CA: Academic Press.

Sakai K, Shitan N, Sato F, Ueda K and Yazaki K (2002) Characterization of berberine transport into Coptis japonica cells and the involvement of ABC protein. Journal of Experimental Botany 53: 1879–1886.

Schneider D (1992) 100 years of pheromone research. Naturwissenschaften 6: 241–250.

Stöckigt J, Panjikar S, Ruppert M, et al. (2007) The molecular architecture of the major enzymes from ajmaline biosynthetic pathway. Phytochemistry Reviews 6: 15–34.

Terasaka K, Shitan N, Sato F, et al. (2003) Application of vanadate‐induced nucleotide trapping to plant cells for detection of ABC proteins. Plant Cell Physiology 44: 198–200.

Teuscher E and Lindequist U (1994) Biogene Gifte. Stuttgart: Gustav Fischer.

Van Wyk BE and Wink M (2004) Medicinal Plants of the World. Pretoria, South Africa: Briza.

Van Wyk BE and Wink M (2015) Phytomedicines, Herbal drugs and Poisons. Cambridge, USA: Cambridge University Press.

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. 4, pp. 131–166. Boca Raton, FL: CRC Press.

Wink M (1993) Allelochemical properties or the raison d'être of alkaloids. In: Cordell GA (ed) The Alkaloids, vol. 43, pp. 1–118. San Diego, CA: Academic Press.

Wink M, Hofer A, Bilfinger M, et al. (1993) Geese and plant dietary allelochemicals – food palatability and geophagy. Chemoecology 4: 93–107.

Wink M (1997) Compartmentation of secondary metabolites and xenobiotics in plant vacuoles. Advances in Botanical Research 25: 141–169.

Wink M (2000) Interference of alkaloids with neuroreceptors and ion channels In: Atta‐Ur‐Rahman (ed). In: Bioactive Natural Products, pp. 1–127. Amsterdam: Elsevier.

Wink M and Theile V (2002) Alkaloid tolerance in Manduca sexta and phylogenetically related sphingids (Lepidoptera: Sphingidae). Chemoecology 12: 29–46.

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: Cordell G (ed) The Alkaloids, vol. 64, pp. 1–48. San Diego, CA: Academic press.

Wink M (2008a) Evolutionary advantage and molecular modes of action of multi‐component mixtures used in phytomedicine. Current Drug Metabolism 9: 996–1009.

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

Wink M and Van Wyk BE (2008) Mind‐Altering and Poisonous Plants of the World. Pretoria, South Africa: Briza.

Wink M (2010a) Function and biotechnology of plant secondary metabolites. In: Annual Plant Reviews, 2nd edn, vol. 39. Chichester: Wiley‐Blackwell.

Wink M (2010b) Biochemistry of plant secondary metabolism. In: Annual Plant Reviews, 2nd edn, vol. 40. Chichester: Wiley‐Blackwell.

Wink M and Schimmer O (2010) Molecular modes of action of defensive secondary metabolites. In: Wink M (ed) Functions and Biotechnology of Plant Secondary Metabolites, 2nd edn, vol. 39, pp. 21–161, Annual Plant Reviews. Chichester: Wiley‐Blackwell.

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.

Yazaki K (2005) Transporters of secondary metabolites. Current Opinion in Plant Biology 8: 301–307.

Yazaki K (2006) ABC transporters involved in the transport of plant secondary metabolites. FEBS Letters 580: 1183–1191.

Zenk MH and Juenger M (2007) Evolution and current status of the phytochemistry of nitrogenous compounds. Phytochemistry 68: 2757–2772.

Ziegler J and Facchini PJ (2008) Alkaloid biosynthesis: metabolism and trafficking. Annual Review of Plant Biology 59: 735–769.

Further Reading

Dewick PM (2002) Medicinal Natural Products. A Biosynthetic Approach, 2nd edn. New York: Wiley.

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.

Marston A (2007) Role of advances in chromatographic techniques in phytochemistry. Phytochemistry 68: 2786–2798.

Mol J, Grotewold E and Koes R (1998) How genes paint flowers and seeds. Trends in Plant Science 3: 212–217.

Murata J, Roepke J, Gordon H and De Luca V (2008) The leaf epidermone of Catharanthus roseus reveals its biochemical specialization. Plant Cell 20: 524–542.

Uefuji H, Tatsumi Y, Morimoto M, et al. (2005) Caffeine production in tobacco plants by simultaneous expression of three coffee N‐methyltransferases and its potential as a pest repellant. Plant Molecular Biology 59: 221–227.

Verpoorte R, Alfermann AW and Johnson TS (2007) Applications of Plant Metabolic Engineering. Heidelberg: Springer.

Wu S and Chappell J (2008) Metabolic engineering of natural products in plants; tools of the trade and challenges for the future. Current Opinion in Biotechnology 19: 145–152.

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Wink, Michael(Jan 2016) Secondary Metabolites: Deterring Herbivores. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000918.pub3]