Lecture Secondary Compounds in Plants

Transcription

1 Ecology 1 Lecture Secondary Compounds in Plants Insects are currently the most diverse group of identified organisms on earth. Out of the approximately 1.5 million known species of living things on earth, there are currently 1.2 million + known insect species. (1/5 of the total number of all living species are beetles!) Approximately half of the insects (including nearly all of the moths and butterflies) feed on plants. Given that there are 300,000 + species of plants, herbivorous insects are much more diverse in life-styles than their nonphytophagous relatives. By feeding at the base of the food chain (primary producers), insects have access to an abundant supply of food. Approximately 10% of the annual plant production in natural systems is consumed by herbivores (Barbosa & Schultz 1987). (Values range from 2-3% for plants in desert ecosystems to as high as 60% for some African grasslands that are specifically managed for grazing. In North America and Europe, insects consume 5-15% of the leaf area in forests.) That 10% is more than the average biomass that plants allocate to reproductive structures. (Annual plants allocate 15-30% of their annual production to reproduction whereas herbaceous perennials allocate 1-15%). A reduction in fitness is the consequence of excessive herbivory. Natural selection has favored those plants with some sort of defense system. Physical defenses that readily come to mind include thorns, hairs, trichomes (some tipped with glands containing toxins) and toughness (i.e. being woody, or tough to chew). However, some plants produce chemicals that deter or poison the herbivores that feed on them. These secondary compounds are produced by plants and have been demonstrated to either reduce feeding, kill the herbivores or reduce their growth and/or fecundity. The primary importance of some of these compound to the plant itself were at first unknown, hence the terminology 'secondary compounds.' Upon further investigation it was found that many of these substances have no known metabolic function, nor do they appear to be by-products of other metabolic pathways. This has suggested a line of reasoning to some (Ehrlich and Raven 1964) that these compounds did indeed evolve in response to grazing pressure by herbivores. As a consequence of this new interpretation of their role, these secondary compounds are often called allelochemicals. Primary compounds, or metabolites, are those chemicals associated with the primary metabolism of the plant (anabolic and catabolic processes) and includes the functions of assimilation, transport, growth, and storage. Many phytophagous insects are highly host specific, and this host specificity has been driven in large part by the chemistry of the host plants on which they feed. In the escalating arms race between insects and plants, insects have developed behavioral and physiological countermeasures to the defenses of plants. However, no one species of insect can circumvent or cope with the vast array of defenses presented by the 300,000+ species of plants. In that regard, there are 2 broad types of strategies for dealing with the defense chemistry of plants. A phytophagous insect can be either a generalist or a specialist.

2 Ecology 2 The strategy adopted by an insect species determines, in part, the type of plant defenses it can cope with. This in turn determines the number of plant species that can be fed upon. A polyphagous species can feed upon many species of plants. (e.g. the gypsy moth (Lymantria dispar) can feed upon 360+ species of trees and shrubs in the U.S. alone). An oliphagous species feeds upon only a few different species of plants. Some species, like the eastern tent caterpillar (Malacosoma americana) are obligate feeders on members of the genus Prunus (mostly black, choke and pin cherry). Most species that are limited taxonomically can feed upon related species because the chemistry is similar, but they may concentrate the majority of their feeding on one species because it is the only one regionally available (e.g. Monarchs, Danaus plexippus, and common milkweed). We would call these species monophagous. Ecologists look for patterns in nature that can be predicted and so they look for ways to categorize the types and distributions of allelochemicals in plants. One such early attempt was the quantitative versus qualitative approach (Feeny, 1975; Rhoades and Cates 1976). A quantitative defense is one that: 1) Is (putatively) metabolically expensive for the plant to produce because it is made in large quantities (5-20% of dry weight for tannins). 2) Deters feeding or reduce the digestion efficiency of the herbivore. 3) Works in a dose-dependent manner. 4) Is generally a large molecules that has a generalized effect on the herbivore which is not easily circumvented. 5) Is produce by plants that are likely to be discovered by the herbivore (apparent plants). 6) These substances include tannins, lignin, resins, silica. A qualitative defense is one that: 1) Is metabolically inexpensive for the plant to produce because it is made in small quantities (< 2% dry weight). 2) Is toxic, thus killing the herbivore (and hence less is required - see #1) 3) Is a small molecule that may be metabolically circumvented by the herbivore. 4) Is produced by plants that are not likely to be discovered by the herbivore (unapparent or ephemeral plants). 5) These substances include alkaloids, glucosinolates (mustards), cardenolides, cyanogenic substances, proteinase inhibitors. It has been 25 years since the quantitative vs. qualitative theory has been put forth. In hindsight, I disagree with the notion that quantitative defenses are expensive. Although they are made in large quantities, the building blocks are relatively inexpensive carbon atoms, which are derived from photosynthesis. On the other hand, qualitative defenses rely upon nitrogen, the most limiting nutrient to plants (next to phosphorus). The use of nitrogen to make a defense compound in a nutrient limiting environment would be relatively expensive, since that nitrogen could also be used to make proteins for metabolic processes and growth. Plants in nutrient limiting environments could still photosynthesize and make carbohydrate, but they would not have to attach valuable nitrogen to the carbohydrate structure to make a quantitative defense.

3 Ecology 3 The type of herbivore that one might expect to find feeding on plants with quantitative versus qualitative defenses will also differ. Plants with quantitative defenses that reduce growth and feeding are apparent. That is, they do not hide from herbivores in space or time. Virtually all plants possess some quantitative defenses; hence these defenses are widely encountered and are fed upon by generalist insects. Plants that are unapparent generally possess a qualitative defense that is unique to a taxonomic group of plants (many members of the Umbelliferae family possess coumarins and furanocoumarins; milkweeds possess cardiac glycosides). Unapparent plants are small, ephemeral and may not grow in large populations, hence they may escape herbivores in space or time. Generalists that do encounter them cannot feed upon them because special adaptations are required detoxify the qualitative defenses. Such a group of plants (1 species or a group of related species) represents an unexploited niche. Insects that can circumvent these defenses will have little or no competition, thereby making the investment in counter-defense measures worthwhile. Insects that possess this strategy are called specialists. Some examples of plant secondary compounds and their effects Compound Class Approximate # Plant Immediate Effect Examples of structures Distribution Alkaloids 5,500 Angiosperms Bitter, toxic Nicotine, caffeine Cyanogenic glycosides 30 Widespread, Rosaceae, Poisonus as HCN Amygdalin in almond seeds Nonprotein amino acids Legumes 400 Seeds of Legumes Many toxic;incorrectly assimilated into protiens Acrid and Bitter L-canavanine substitutes for Arginine Glucosinolates 75 All Cruciferae + 10 other familes Isothiocyanates, an irritant Monoterpenes 1,000 Wide, essential Pleasant smelling Pine resins oils Cucurbitacins 50 Cucumbers Toxic and bitter Cardenolides 150 Apocynaceae, Bitter-tasting and Heart poison Asclepiadacaea, toxic from Digitalis Scrophularaceae Simple phenols 200 Universal Bitter, antimicrobrial Flavonoids 4,000 Universal Reduced digestion Caffeic acid in thyme and tarragon Tannins, catechin in green tea Secondary compounds can also be classified as constitutive or inducible. Constitutive defenses, or their immediate precursors, are maintained in plants at biologically active levels (i.e. at levels that are effective against herbivores or pathogens). Constitutive defenses therefore provide

4 Ecology 4 'round-the-clock' protection to a plant. Digestibility reducers such as tannins and lignins, as well as toxins such as glucosinolates and cyanogenic glycosides are examples of defenses that are primarily constitutive. Inducible defense differ in that they are normally present at very low levels, but can be synthesized relatively rapidly (within hours or days) following plant stress or wounding. Proteinase inhibitors and a number of oxidative enzymes that reduce the nutritive value of plant tissue are examples of induced defenses. Many constitutive defenses are present in low concentrations, but can be induced to higher concentrations by herbivory. The benefits of induced defenses are two-fold. 1) Because defenses of any kind are metabolically expensive, induced defenses are theoretically less expensive since they are only manufactured in response to real damage. 2) Consistency is the key to natural selection. A defense that is constantly expressed may be evaded through natural selection. Induced defenses introduce variability, making the evolution of counter-measures less likely. Evolutionarily, it is unclear which benefit was selected for. Literature Cited Barbosa, P. and Schultz, J.C. (1987) Insect outbreaks. Academic Press, San Diego, CA. in Shoonhoven, L.M., Jermy, T. and van Loon, J. J. A. (1998) Insect-Plant Biology. Chapman & Hall, London. Bell, R. A., and F. G. Joachim Techniques for rearing laboratory colonies of tobacco hornworm and pink bollworm. Annals of the Entomological Society of America. 69: Bloem, K.A., K.C. Kelley, and S.S. Duffey Differential effects of tomatine and its alleviations by cholesterol on larval growth and efficiency of food utilization in Heliothis zea and Spodoptera exigua. Journal of Chemical Ecology. Doares, S.H., T. Syrovets, E.W. Weiler and C.A. Ryan Oligogalacturonides and chitosan activate plant defensive genes through the octadeconaoid pathway. Proc. Natl. Acad. Sci. 92: *Edwards, P.J., S. D. Wratten and H. Cox Wound-induced changes in the acceptability of tomato to larvae Spodoptera littoralis: a laboratory bioassay. Ecological Entomology 10: Eherlich, P.R. and P.H. Raven Butterflies and plants: A study in coevolution. Evolution 18: Farmer, E.E. and C.A. Ryan Interplant communication: Airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc. Natl. Acad. Sci. 87:

5 Ecology 5 Feeny, P. P. (1975). Biochemical coevolution between plants and their insect herbivores. In, Coevolution of Animals and Plants (L.E. Gilbert and P.H. Raven, eds.), pp Univ. of Texas Press, Austin. Isman, M.B. and S.S. Duffey Toxicity of tomato phenolic compounds to the fruitworm, Heliothis zea. Entomolo. Exp. Appl. 31: Lindau, Anna & Rodrigo Trigosso-Venario. Does herbivory affect reproductive effort in herbaceous plants? NnlsJJtsC: vory&hl=en&ie=utf-8 Rhoades, D.F. and R.G. Cates Toward a general theory of plant antiherbivore chemistry. Recent Advances in Phytochemistry. 10: Stamp, N.E., and Y. Yang Response of insect herbivores to multiple allelochemicals under different thermal regimes. Ecology. 77: *Stout, M.J., J. Workman and S. Duffey Differerential induction of tomato foliar proteins by arthropod herbivores. Journal of Chemical Ecology. 20: Thaler, J.S. Jasmonic Acid Mediated Interactions between plants, herbivores, parasitoids, and pathogens: A review of field experiments in tomato. Pp in, A.A. Agrawal, S. Tuzun, and E. Bent (eds) Inducible plant defenses against pathogens and herbivores: Biochemistry, ecology, and agriculture. American Phytopathalogical Society. Traugott, M.S. and N.E. Stamp Effects of chlorgenic acid and tomatine fed caterpillars on performance of an insect predator. Oecologia 109: