Plant defense against herbivory

    Plant defense against herbivory or host-plant resistance (HPR) includes a range of adaptations evolved by plants that improve their survival and reproduction by reducing the impact of herbivores.

There are four basic strategies plants use to reduce damage by herbivores. One strategy is to escape or avoid herbivores in time or in place, for example by growing in a location where plants are not easily found or accessed by herbivores or by repelling herbivores chemically (also termed non-preference or antixenosis). Another approach is the plant tolerates herbivores, by diverting the herbivore to eat non-essential parts of the plant, or developing an enhanced ability to recover from the damage caused by herbivory. Some plants encourage the presence of natural enemies of herbivores, which in turn protect the plant from herbivores. Finally, plants protect themselves by confrontation; the use of chemical or mechanical defenses, such as toxins that kill herbivores or reduce plant digestibility (also called antibiosis).^[1] These defenses can either be constitutive, always present in the plant, or induced, produced in reaction to damage or stress caused by herbivores.

Historically, insects have been the most significant herbivores, and the evolution of land plants is closely associated with the evolution of insects. While most plant defenses are directed against insects, others defenses have evolved that are aimed at vertebrate herbivores, such as birds and mammals. The study of plant defenses against herbivory is important, not only from an evolutionary view point, but also in the direct impact that these defenses have on agriculture, including human and livestock food sources, as well as the in the search for plants of medical importance.

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Evolution

  The earliest land plants evolved from aquatic plants around 440 mya in the Ordovician and Silurian periods. These early land plants were bryophytes that are related to mosses. They had no vascular system and required free water for their reproduction. Vascular plants appeared later and their diversification began in the Devonian era (about 400 mya). Their reduced dependence on water resulted from adaptations such as protective coatings to reduce evaporation from their tissues. Reproduction and dispersal of vascular plants in these dry conditions was achieved through the evolution of specialized seed structures. The diversification of flowering plants (angiosperms) during the Cretaceous period is associated with the sudden burst of speciation in insects.^[2] This diversification of insects represented a major selective force in plant evolution, and led to selection of plants that had defensive adaptations. Early insect herbivores were mandibulate and bit or chewed vegetation; but the evolution of vascular plants lead to the co-evolution of other forms of herbivory, such as sap-sucking, leaf mining, gall forming and nectar-feeding.^[3]

Co-evolution

  Herbivores depend on plants for food, and have evolved mechanisms to obtain this food despite the evolution of a diverse arsenal of plant defenses. Herbivore adaptations to plant defense have been likened to offensive traits and consist of adaptations that allow increased feeding and use of a host plant.^[4] Relationships between herbivores and their host plants often results in reciprocal evolutionary change, called co-evolution. When an herbivore eats a plant it selects for plants that can mount a defensive response. In cases where this relationship demonstrates specificity (the evolution of each trait is due to the other), and reciprocity (both traits must evolve), the species are thought to have co-evolved.^[5] The "escape and radiation" mechanism for co-evolution presents the idea that adaptations in herbivores and their host plants have been the driving force behind speciation,^[2][6] and have played a role in the radiation of insect species during the age of angiosperms.^[7] Some herbivores have evolved ways to hijack plant defenses to their own benefit, by sequestering these chemicals and using them to protect themselves from predators.^[2]

Types

Plant defenses can be classified generally as induced or constitutive. Constitutive defenses are always present in the plant species, while induced defenses are synthesized or mobilized to the site where a plant is injured. There are wide variations in the composition and concentration of constitutive defenses and these range from mechanical defenses to digestibility reducers and toxins. Most external mechanical defenses and large quantitative defenses are constitutive, as they require large amounts of resources to produce and difficult to mobilize.^[8]

Induced defenses include secondary metabolic products, as well as morphological and physiological changes.^[9] An advantage of inducible, rather than constitutive defenses, is that increased variability increases the effectiveness of the defenses.^[9] This advantage comes from the suggestion that if herbivores can choose among different plants and plant tissues, they may avoid eating plants that have both constitutive and induced defenses.^[4]

Chemical defenses

The evolution of chemical defenses in plants is linked to the emergence of chemical substances that are not involved in the essential photosynthetic and metabolic activities. These substances, secondary metabolites, are organic compounds that are not directly involved in the normal growth, development or reproduction of organisms,^[10] and often produced as by-products during the synthesis of primary metabolic products.^[11] These secondary metabolites play a major role in defenses against herbivores.^[12][10][2]

Secondary metabolites are often characterized as either qualitative or quantitative. Qualitative metabolites are defined as toxins that interfere with an herbivore’s metabolism, often by blocking specific biochemical reactions. Qualitative chemicals are present in plants in relatively low concentrations (often less than 2% dry weight), and are not dosage dependent. These defenses have morphological properties (i.e. water soluble, small molecules, and are energetically inexpensive) that facilitate rapid synthesis, transport, and storage. These chemicals are effective against non-adapted specialists and generalist herbivores.

Quantitative chemicals are those that are present in high concentration in plants (5 – 40% dry weight) and are equally effective against all specialists and generalist herbivores. Most quantitative metabolites are digestibility reducers that make plant cell walls indigestible to animals. The effects of quantitative metabolites are dosage dependent and the higher these chemicals’ proportion in the herbivore’s diet, the less nutrition the herbivore can gain from ingesting plant tissues. Because they are typically large molecules, these defenses are energetically expensive to produce and maintain, and often take longer than smaller, qualitative chemicals to synthesize and transport, therefore these chemicals are expected to serve an important purpose within the plant.^[13]

Types of chemical defenses

Plants have developed many secondary metabolites involved in plant defense, which are collectively known as antiherbivory compounds and can be classified into three sub-groups: nitrogen compounds (including alkaloids, cyanogenic glycosides and glucosinolates), terpenoids, and phenolics.^[14]

Alkaloids are derived from various amino acids. Over 3000 known alkaloids exist, examples include nicotine, caffeine, morphine, colchicine, ergolines, strychnine, and quinine.^[15] Alkaloids have pharmacological effects on humans and other animals. Some alkaloids can inhibit or activate enzymes, or alter carbohydrate and fat storage by inhibiting the formation phosphodiester bonds involved in their breakdown.^[16] Certain alkaloids bind to nucleic acids and can inhibit synthesis of proteins and affect DNA repair mechanisms. Alkaloids can also affect cell membrane and cytoskeletal structure causing the cells to weaken, collapse, or leak, and can affect nerve transmission.^[17] Cyanogenic glycosides become toxic when they are broken down by enzymes in the herbivore's digestive tract and release hydrogen cyanide or prussic acid, which blocks cellular respiration. Glucosinolates can cause gastroenteritis, salivation, diarrhea, and irritation of the mouth.^[18]

The terpenoids, sometimes referred to as isoprenoids, are organic chemicals similar to terpenes, derived from five-carbon isoprene units. There are over 10,000 known types of terpenoids.^[19] Most are multicyclic structures which differ from one another in both functional groups, and in basic carbon skeletons.^[20] Monoterpenoids, continuing 2 isoprene units, are volatile essential oils such as citronella, limonene, menthol, camphor, and pinene. Diterpenoids, 4 isoprene units, are widely distributed in latex and resins, and can be quite toxic. Diterpenes are responsible for making Rhododendron leaves poisonous. Plant steroids and sterols are also produced from terpenoid precursors, including vitamin D, glycosides (such as digitalis) and saponins (which lyse red blood cells of herbivores).^[21]

Phenolics, sometimes called phenols, consist of an aromatic 6-carbon ring bonded to a hydroxy group. Some phenols have antiseptic properties, while others disrupt endocrine activity. Phenolics range from simple tannins to the more complex flavonoids that give plants much of their red, blue, yellow, and white pigments. Complex phenolics called polyphenols are capable of producing many different types of effects on humans, including antioxidant properties. Some examples of phenolics used for defense in plants are: lignin, silymarin and cannabinoids.^[22] Condensed tannins, polymers composed of 2 to 50 (or more) flavonoid molecules, inhibit herbivore digestion by binding to consumed plant proteins and making them more difficult for animals to digest, and by interfering with protein absorption and digestive enzymes.^[23] Silica and lignins, which are completely indigestible to animals, grind down insect mandibles (appendages necessary for feeding).

In addition to the three larger groups of substances mentioned above, fatty acid derivates, amino acids and even peptides^[24] are used as defence. The cholinergic toxine, cicutoxin of water hemlock, is an polyyne derived from the fatty acid metabolism.^[25] β-N-Oxalyl-L-α,β-diaminopropionic acid as simple amino acid is used by the sweet pea which leads also to intoxication in humans.^[26] The synthesis of fluoroacetate in several plants is an example for the use of small molecules to disturb the metabolism of the herbivore, in this case the citric acid cycle.^[27]

Mechanical defenses

  Plants have many external structural defenses that discourage herbivory. Depending on the herbivore’s physical characteristics (i.e. size and defensive armor), plant structural defenses on stems and leaves can deter, injure, or kill the grazer. Some defensive compounds are produced internally but are released onto the plant’s surface; for example, resins, lignins, silica, and wax cover the epidermis of terrestrial plants and alter the texture of the plant tissue. The leaves of holly plants, for instance, are very smooth and slippery making feeding difficult. Some plants produce gummosis or sap that traps insects.

A plant's leaves and stem may be covered with sharp spines or trichomes- hairs on the leaf often with barbs, sometimes containing irritants or poisons. Plant structural features like spines and thorns reduce feeding by large ungulate herbivores (e.g. kudu, impala, and goats) by restricting the herbivores' feeding rate, or by wearing down the molars as in pears.^[28] The structure of a plant, its branching and leaf arrangement may also be evolved to reduce herbivore impact. The shrubs of New Zealand have evolved special wide branching adaptations believed to be a response to browsing birds such as the moas.^[29] Similarly, Acacias have dense thorns on the outside, but none in the middle of the crown, which is safe from herbivores such as giraffes.^[30]

Mimicry and camouflage

Some plants mimic the presence of insect eggs on their leaves, dissuading insect species from laying their eggs there. Because female butterflies are less likely to lay their eggs on plants that already have butterfly eggs, some species of neotropical vines of the genus Passiflora (Passion flowers) contain physical structures resembling the yellow eggs of Heliconius butterflies on their leaves, which discourage oviposition by butterflies.^[31]

Indirect defenses

  Another category of plant defenses are those features that indirectly protect the plant by enhancing the probability of attracting the natural enemies of herbivores. One such feature are semiochemicals, given off by plants. Semiochemicals are a group of volatile organic compounds involved in interactions between organisms. One group of semiochemicals are allelochemics; consisting of allomones, which play a defensive role in interspecies communication, and kairomones, which are used by members of higher trophic levels to locate food sources. When a plant is attacked it releases allelochemics containing an abnormal ratio of volatiles.^[32] Predators sense these volatiles as food cues, attracting them to the damaged plant, and to feeding herbivores. The subsequent reduction in the number of herbivores confers a fitness benefit to the plant and demonstrates the indirect defensive capabilities of semiochemicals. Induced volatiles also have drawbacks, however; some studies have supported the idea that these volatiles also attract herbivores.^[32]

Plants also provide housing and food items for natural enemies of herbivores, known as “biotic” defense mechanisms, as a means to maintain their presence. For example, trees from the genus Macaranga have adapted their thin stem walls to create ideal housing for an ant species (genus Crematogaster), which, in turn, protects the plant from herbivores.^[33] In addition to providing housing, the plant also provides the ant with its exclusive food source; from the food bodies produced by the plant. Similarly, some Acacia tree species have developed thorns that are swollen at the base, forming a hollowing structure that acts as housing. Theses Acacia trees also produce nectar in extrafloral nectaries on their leaves as food for the ants.^[34]

There have been suggestions that leaf shedding may be a response that provides protection against diseases and certain kinds of pests such as leaf miners and gall forming insects.^[35] Other responses such as the change of leaf colours prior to fall have also been suggested as adaptations that may help undermine the camouflage of herbivores.^[36] Autumn leaf color has also been suggested to act as an honest warning signal of defensive commitment towards insect pests that migrate to the trees in autumn.^[37][38]

Costs and benefits

Defensive structures and chemicals are costly as they require resources that could otherwise be used by plants to maximize growth and reproduction. Many models have been proposed to explore how and why some plants make this investment in defenses against herbivores.

Optimal defense hypothesis

The optimal defense hypothesis attempts to explain how the kinds of defenses a particular plant might use reflect the threats each individual plant faces.^[39] This model considers three main factors, namely: risk of attack, value of the plant part, and the cost of defense.^[40][41]

The first factor determining optimal defense is risk: how likely is it that a plant or certain plant parts will be attacked? This is also related to the plant apparency hypothesis, which states that a plant will invest heavily in broadly effective defenses when the plant is easily found by herbivores.^[42] Examples of apparent plants that produce generalized protections include long-living trees, shrubs, and perennial grasses.^[42] Unapparent plants, such as short-lived plants of early successional stages, on the other hand, preferentially invest in small amounts of qualitative toxins that are effective against all but the most specialized herbivores.^[42]

The second factor is the value of protection: would the plant be less able to survive and reproduce after removal of part of its structure by a herbivore? Not all plant parts are of equal evolutionary value, thus valuable parts contain more defenses. A plant’s stage of development at the time of feeding also affects the resulting change in fitness. Experimentally, the fitness value a plant structure is determined by removing that part of the plant and observing the effect.^[43] In general, reproductive parts are not as easily replaced as vegetative parts, terminal leaves have greater value than basal leaves, and the loss of plant parts mid-season has a greater negative effect on fitness than removal at the beginning or end of the season.^[44][45] Seeds in particular tend to be very well protected. For example, the seeds of many edible fruits and nuts contain cyanogenic glycosides such as amygdalin. This results from the need to balance the effort needed to make the fruit attractive to animal dispersers while ensuring that the seeds are not destroyed by the animal.^[46][47]

The final consideration is cost: how much will a particular defensive strategy cost a plant in energy and materials? This is particularly important, as energy spent on defense cannot be used for other functions, such as reproduction and growth. The optimal defense hypothesis predicts that plants will allocate more energy towards defense when the benefits of protection outweigh the costs, specifically in situations where there is high herbivore pressure.^[48]

Carbon:nutrient balance hypothesis

The carbon:nutrient balance hypothesis, also known as the environmental constraint hypothesis, states that the various types of plant defenses are responses to variations in the levels of nutrients in the environment.^[49][50] This hypothesis predicts that plants will use defensive compounds constructed from the most abundant nutrient available. For example, plants growing in nitrogen-poor soils will use carbon-based defenses (mostly digestibility reducers), while those growing in low-carbon environments (such as shady conditions) are more likely to produce nitrogen-based toxins. The hypothesis further predicts that plants can change their defences in response to changes in nutrients. For example, if plants are grown in low-nitrogen conditions, then these plants will implement a defensive strategy composed of constitutive carbon-based defenses. If nutrient levels subsequently increase, by for example the addition of fertilizers, these carbon-based defenses will decrease.

Growth rate hypothesis

The growth rate hypothesis, also known as the resource availability hypothesis, states that defense strategies are determined by the inherent growth rate of the plant, which is in turn determined by the resources available to the plant. A major assumption is that available resources are the limiting factor in determining the maximum growth rate of a plant species. This model predicts that the level of defense investment will increase as the potential of growth decreases.^[51] Additionally, plants in resource-poor areas, with inherently slow-growth rates, tend to have long-lived leaves and twigs, and the loss of plant appendages may result in a loss of scarce and valuable nutrients.^[52]

A recent test of this model involved a reciprocal transplants of seedlings of 20 species of trees between clay soils (nutrient rich) and white sand (nutrient poor) to determine whether trade-offs between growth rate and defenses restrict species to one habitat. Seedlings originating from the nutrient-poor sand had higher levels of constitutive carbon-based defenses, but when they were transplanted into nutrient-rich clay soils, they experienced higher mortality from herbivory. These finding suggest that defensive strategies limit the habitats of some plants.^[53]

Growth-differentiation balance hypothesis

The growth-differentiation balance hypothesis states that plant defenses are a result of the energy being divided between “growth-related processes” and “differentiation-related processes” in different environments.^[54] Differentiation-related processes are defined as “processes that enhance the structure or function of existing cells (i.e. maturation and specialization).”^[39] A plant will produce chemical defenses only when energy is available from photosynthesis and plants with the highest concentrations of secondary metabolites are the ones with an intermediate level of available resources.^[54] Support for this hypothesis came from studies of the phenolic content in tomatoes when grown at four different nitrate levels. The highest concentration of phenolics were measured when the tomatoes were grown at an intermediate nitrate level.^[55]

Importance to humans

Agriculture

The variation of plant susceptibility to pests was probably known even in the early stages of agriculture in humans. In historic times, the observation of such variations in susceptibility have provided solutions for major socio-economic problems. The grape phylloxera was introduced from North America to France in 1860 and in 25 years it destroyed nearly a third (100,000 km²) of the French grape yards. Charles Valentine Riley noted that the American species Vitis labrusca was resistant to Phylloxera. Riley, with J. E. Planchon, helped save the French wine industry by suggesting the grafting of the susceptible but high quality grapes onto Vitis labrusca root stocks.^[56] The formal study of plant resistance to herbivory was first covered extensively in 1951 by Reginald (R.H.) Painter, who is widely regarded as the founder of this area of research, in his book Plant Resistance to Insects.^[1] While this work pioneered further research in the US, the work of Chesnokov was the basis of further research in the USSR.^[57]

Fresh growth of grass is sometimes high in prussic acid content and can cause poisoning of grazing livestock. The production of cyanogenic chemicals in grasses is primarily a defense against herbivores.^[58][59]

The human innovation of cooking may have been particularly helpful in overcoming many of the defensive chemicals of plants. Many enzyme inhibitors in cereal grains and pulses, such as trypsin inhibitors prevalent in pulse crops, are denatured by cooking, making them digestible.^[60][61]

It has been known since the late 17th century that plants contain noxious chemicals which are avoided by insects. These chemicals have been used by man as early insecticides; in 1690 nicotine was extracted from tobacco and used as a contact insecticide. In 1773, insect infested plants were treated with nicotine fumigation by heating tobacco and blowing the smoke over the plants.^[62] The flowers of Chrysanthemum species contain pyrethrin which is a potent insecticide. In later years, the applications of plant resistance became an important area of research in agriculture and plant breeding, particularly because they can serve as a safe and low-cost alternative to the use of pesticides.^[63] The important role of secondary plant substances in plant defense was described in the late 1950s by Vincent Dethier and G.S. Fraenkel.^[64][10] The use of botanical pesticides is widespread and notable examples include Azadirachtin from the neem (Azadirachta indica), d-Limonene from Citrus species, Rotenone from Derris, Capsaicin from Chili Pepper and Pyrethrum.^[65]

The selective breeding of crop plants often involves selection against the plant's intrinsic resistance strategies. This makes crop plant varieties particularly susceptible to pests unlike their wild relatives. In breeding for host-plant resistance, it is often the wild relatives that provide the source of resistance genes. These genes are incorporated using conventional approaches to plant breeding, but have also been augmented by recombinant techniques, which allow introduction of genes from completely unrelated organisms. The most famous transgenic approach is the introduction of genes from the bacterial species, Bacillus thuringiensis, into plants. The bacterium produces proteins that, when ingested, kill lepidopteran caterpillars. The gene encoding for these highly toxic proteins, when introduced into the host plant genome, confers resistance against caterpillars, when the same toxic proteins are produced within the plant. This approach is controversial, however, due to the possibility of ecological and toxicological side effects.^[66]

Pharmaceutical

Many currently available pharmaceuticals are derived from the secondary metabolites plants use to protect themselves from herbivores, including opium, aspirin, cocaine, and atropine.^[67] These chemicals have evolved to affect the biochemistry of insects in very specific ways. However, many of these biochemical pathways are conserved in vertebrates, including humans, and the chemicals act on human biochemistry in ways similar to that of insects. It has therefore been suggested that the study of plant-insect interactions may help in bioprospecting.^[68]

There is evidence that humans began using plant alkaloids in medical preparations as early as 3000 B.C.^[16] Although the active components of most medicinal plants have been isolated only recently (beginning in the early 19th century) these substances have been used as drugs throughout the human history in potions, medicines, teas and as poisons. For example, to combat herbivory by the larvae of some Lepidoptera species, Cinchona trees produce a variety of alkaloids, the most familiar of which is quinine. Quinine is extremely bitter, making the bark of the tree quite unpalatable, it is also an anti-fever agent, known as Jesuit's bark, and is especially useful in treating malaria.^[69]

Throughout history mandrakes (Mandragora officinarum) have been highly sought after for their reputed aphrodisiac properties. However, the roots of the mandrake plant also contain large quantities of the alkaloid scopolamine, which, at high doses, acts as a central nervous system depressant, and makes the plant highly toxic to herbivores. Scopolamine was later found to be medicinal use in pain management before and during labor; in smaller doses it is used to prevent motion sickness.^[70] One of the most well-known medicinally valuable terpenes is an anticancer drug, taxol, isolated from the bark of the Pacific yew, Taxus brevifolia, in the early 1960s.^[71]

See also

• Chemical ecology
• Canavanine
• Endophyte
• Frugivore
• Laticifer
• Lectin
• Raphides
• Pollination
• Phytoalexin
• Rapid plant movement
• Seed predation
• Thigmonasty

References

Further reading

Titles with links are available in the form of a Google Books "limited preview".

• Robert S. Fritz and Ellen L. Simms (editors) (1992). Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. Chicago: University of Chicago Press. ISBN 0-226-26553-6. 
• Howe, H. F., and L. C. Westley. 1988. Ecological relationships of plants and animals. Oxford University Press, Oxford, UK.
• Pierre Jolivet,. Interrelationship Between Insects and Plants. Boca Raton: CRC. ISBN 1-57444-052-7. 
• Richard Karban and Ian T. Baldwin (1997). Induced responses to herbivory. Chicago: University of Chicago Press. ISBN 0-226-42495-2. 
• Martin R. Speight, Mark D. Hunter, Allan D. Watt (1999). Ecology of insects: concepts and applications. Oxford: Blackwell Science. ISBN 0-86542-745-3. 
• John N. Thompson (1994). The coevolutionary process. Chicago: University of Chicago Press. ISBN 0-226-79759-7.