Plant Defense Against Herbivory

Plant defense against herbivory or host-plant resistance (HPR) describes a range of adaptations evolved by plants which improve their survival and reproduction by reducing the impact of herbivores. Plants can sense being touched, and they can use several strategies to defend against damage caused by herbivores. Many plants produce secondary metabolites, known as allelochemicals, that influence the behavior, growth, or survival of herbivores. These chemical defenses can act as repellents or toxins to herbivores or reduce plant digestibility. Another defensive strategy of plants is changing their attractiveness. To prevent overconsumption by large herbivores, plants alter their appearance by changing their size or quality, overall decreasing their consumption rate.

Other defensive strategies used by plants include escaping or avoiding herbivores at any time and/or in any place, for example, by growing in a location where plants are not easily found or accessed by herbivores or by changing seasonal growth patterns. Another approach diverts herbivores toward eating non-essential parts or enhances the ability of a plant to recover from the damage caused by herbivory. Some plants encourage the presence of natural enemies of herbivores, which in turn protect the plant. Each type of defense can be either ''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, other 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 viewpoint, but also for the direct impact that these defenses have on agriculture, including human and livestock food sources; as beneficial 'biological control agents' in biological pest control programs; and in the search for plants of medical importance.

Evolution of defensive traits

The earliest land plants evolved from aquatic plants around (Ma) in the Ordovician period. Many plants have adapted to an iodine-deficient terrestrial environment by removing iodine from their metabolism; in fact, iodine is essential only for animal cells. An important antiparasitic action is caused by the blockage in the transport of iodide of animal cells, inhibiting sodium-iodide symporter (NIS). Many plant pesticides are glycosides (such as cardiac digitoxin) and cyanogenic glycosides that liberate cyanide, which, by blocking cytochrome c oxidase and NIS, is poisonous only for a large part of parasites and herbivores and not for the plant cells, in which it seems useful in the seed dormancy phase. Iodide is not a pesticide but is oxidized, by vegetable peroxidase to iodine, which is a strong oxidant able to kill bacteria, fungi, and protozoa.

The Cretaceous period saw the appearance of more plant defense mechanisms. The diversification of flowering plants (angiosperms) at that time is associated with the sudden burst of speciation in insects. This diversification of insects represented a major selective force in plant evolution and led to the 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.

The relative abundance of different species of plants in ecological communities including forests and grasslands may be determined in part by the level of defensive compounds in the different species. Since the cost of replacing damaged leaves is higher in conditions where resources are scarce, it may also be that plants growing in areas where water and nutrients are scarce may invest more resources into anti-herbivore defenses, resulting in slower plant growth.

Records of herbivores

Our understanding of herbivory in geological time comes from three sources: fossilized plants, which may preserve evidence of defense (such as spines) or herbivory-related damage; the observation of plant debris in fossilised animal feces; and the construction of herbivore mouthparts.

Long thought to be a Mesozoic phenomenon, evidence for herbivory is found almost as soon as fossils can show it. As previously discussed, the first land plants emerged around 450 million years ago; however, herbivory, and therefore the need for plant defenses, has undoubtedly been around for longer. Herbivory first evolved due to marine organisms within ancient lakes and oceans. Within under 20 million years of the first fossils of sporangia and stems towards the close of the Silurian, around , there is evidence that they were being consumed. Animals fed on the spores of early Devonian plants, and the Rhynie chert also provides evidence that organisms fed on plants using a "pierce and suck" technique. Many plants of this time are preserved with spine-like enations, which may have performed a defensive role before being co-opted to develop into leaves.

During the ensuing 75 million years, plants evolved a range of more complex organs – from roots to seeds. There was a gap of 50 to 100 million years between each organ's evolution and it being fed upon. Hole feeding and skeletonization are recorded in the early Permian, with surface fluid feeding evolving by the end of that period.

Co-evolution

Herbivores are dependent 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. Relationships between herbivores and their host plants often result 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.

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 and have played a role in the radiation of insect species during the age of angiosperms. 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. Plant defenses against herbivores are generally not complete, so plants also tend to evolve some tolerance to herbivory.

Types

Plant defenses can be classified generally as constitutive or induced. Constitutive defenses are always present in the plant, while induced defenses are produced or mobilized to the site where a plant is injured. There is wide variation in the composition and concentration of constitutive defenses and these range from mechanical defenses to digestibility reducers and toxins. Many external mechanical defenses and large quantitative defenses are constitutive, as they require large amounts of resources to produce and are difficult to mobilize. A variety of molecular and biochemical approaches are used to determine the mechanism of constitutive and induced plant defenses responses against herbivory.

Induced defenses include secondary metabolites, as well as morphological and physiological changes. An advantage of inducible, as opposed to constitutive defenses, is that they are only produced when needed, and are therefore potentially less costly, especially when herbivory is variable. Modes of induced defence include systemic acquired resistance and plant-induced systemic resistance.

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, and often produced as by-products during the synthesis of primary metabolic products. Some of which include Phenolics, Flavonoids, and Tannins. Although these secondary metabolites have been thought to play a major role in defenses against herbivores, a meta-analysis of recent relevant studies has suggested that they have either a more minimal (when compared to other non-secondary metabolites, such as primary chemistry and physiology) or more complex involvement in defense. Furthermore, plants can release volatile organic compounds (VOCs) to warn other plants in the area of stressful conditions. These toxic compounds can be used to deter the herbivore or even attract the herbivore's predator. Finally, some plants can also produce plant defensive proteins, which upon ingestion, end up poisoning the herbivore.

Plants can also communicate through the air. Pheromone release and other scents can be detected by leaves and regulate plant immune response. In other words, plants produce volatile organic compounds (VOC) to warn other plants of danger and change their behavioral state to better respond to threats and survival. These warning signals produced by infected neighboring trees allow the undamaged trees to provocatively activate the necessary defense mechanisms. Within the plant itself, it transmits warning, nonvolatile signals as well as airborne signals to surrounding undamaged trees to strengthen their defense/immune system. For instance, poplar and sugar maple trees demonstrated that they received tannins from nearby damaged trees. In sagebrush, damaged plants send out airborne compounds, such as methyl jasmonate, to undamaged plants to increase proteinase inhibitor production and resistance to herbivory. Further observations illustrated that damaged plants release various VOCs and hormones to receiver plants as a form of communication for defense and regulating their immune system.

The release of unique VOCs and extrafloral nectar (EFN) allow plants to protect themselves against herbivores by attracting animals from the third trophic level. For example, caterpillar-damaged plants guide a parasitic wasp to prey on its victims through the release of chemical signals.The sources of these compounds are most likely from glands in the leaves which are ruptured upon the chewing of an herbivore. The injury by herbivores induces the release of linolenic acid and other enzymatic reactions in an octadecanoid cascade, leading to the synthesis of jasmonic acid, a hormone which plays a central role in regulating immune responses. Jasmonic acid induces the release of VOCs and EFN which attract parasitic wasps and predatory mites to detect and feed on herbivores. These volatile organic compounds can also be released to other nearby plants to be prepared for the potential threats. Studies have shown that the volatile compounds emitted by plants are easy to be detected by third trophic level organisms as these signals are unique to herbivore damage. An experiment conducted to measure the VOCs from growing plants shows that signals are released instantaneously upon the herbivory damage and slowly dropped after the damage stopped. It was also observed that plants release the strongest signals during the time of day which animals tend to forage.

Since trees are sessile, they've established unique internal defense systems. For instance, when some trees experience herbivory, they release compounds that make their vegetation less palatable. The herbivores saliva left on the leaves of the tree sends a chemical signal to the tree's cells. The tree cells respond by increasing the concentration of salicylic acid (hormone) production. Salicylic acid is a phytohormone that is one of the essential hormones for regulating plants' immune systems. This hormone then signals to increase the production of tree chemicals called tannins within its leaves. Tannins affect palatability and digestibility of vegetation while also increasing the concentration of growth hormones, encouraging new leaf growth. The increased production of tannins makes it difficult for deers to digest, which makes the leaves less appealing to eat. The research experiment done by Bettina Ohse, et al. found that a group of field-grown Saplings of European beach and Sycamore Maple trees could sense whether it was specifically a deer eating at its leaves. The Scientists realized saliva caused an increase in tannin concentration, due to their experiment of having broken leaves that contain saliva and ones that don't. The leaves that contained the deer saliva showed an increase in tannin and experienced an increase in the growth of the leaves of the tree, but the leaves without the deer saliva did not experience these changes. The increase in tannin concentration is one internal mechanism that trees use to combat mobile predators, like deer. This tannin increase is done by the trees immune system and is a key defense strategy used by plants of all kinds.

Qualitative and quantitative metabolites

Secondary metabolites are often characterized as either '' qualitative'' or ''quantitative''. Qualitative metabolites are defined as toxins that interfere with a 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. They are usually small, water-soluble molecules, and therefore can be rapidly synthesized, transported and stored with relatively little energy cost to the plant. Qualitative allelochemicals are usually effective against non-adapted 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 to synthesize and transport.

The geranium, for example, produces the amino acid, quisqualic acid in its petals to defend itself from Japanese beetles. Within 30 minutes of ingestion the chemical paralyzes the herbivore. While the chemical usually wears off within a few hours, during this time the beetle is often consumed by its own predators.

Antiherbivory compounds

Plants have evolved 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'', ''glucosinolates'' and ''benzoxazinoids''), terpenoids, and phenolics.

Alkaloids are derived from various amino acids. Over 3000 known alkaloids exist, examples include nicotine, caffeine, morphine, cocaine, colchicine, ergolines, strychnine, and quinine. 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. 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. Although alkaloids act on a diversity of metabolic systems in humans and other animals, they almost uniformly invoke an aversively bitter taste.

Cyanogenic glycosides are stored in inactive forms in plant vacuoles. They become toxic when herbivores eat the plant and break cell membranes allowing the glycosides to come into contact with enzymes in the cytoplasm releasing hydrogen cyanide which blocks cellular respiration. Glucosinolates are activated in much the same way as cyanogenic glucosides, and the products can cause gastroenteritis, salivation, diarrhea, and irritation of the mouth. Benzoxazinoids, such as DIMBOA, are secondary defence metabolites characteristic of certain grasses (Poaceae). Like cyanogenic glycosides, they are stored as inactive glucosides in the plant vacuole. Upon tissue disruption they get into contact with β-glucosidases from the chloroplasts, which enzymatically release the toxic aglucones. Whereas some benzoxazinoids are constitutively present, others are only synthesised following herbivore infestation, and thus, considered inducible plant defenses against herbivory.

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. Most are multicyclic structures which differ from one another in both functional groups, and in basic carbon skeletons. 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).

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. 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.

In addition, some plants use fatty acid derivatives, amino acids and even peptides as defenses. The cholinergic toxin, cicutoxin of water hemlock, is a polyyne derived from the fatty acid metabolism. Oxalyldiaminopropionic acid is a neurotoxic amino acid produced as a defensive metabolite in the grass pea (''Lathyrus sativus''). The synthesis of fluoroacetate