Plant Defences against Herbivore Attack

Abstract

Different from animals, plants can usually not run away from their attackers, such as herbivores, and have thus evolved a diverse arsenal of defences. These defences can be constitutive or inducible, they can be directly affecting the attacker or be mediated by a third organism (indirect defence) and span from physical structures, such as thorns, and reinforced cell walls to chemical defences (plant secondary metabolites) with toxic, antidigestive and antinutritive mechanisms of action. Plant secondary metabolite production is characterised by a very high diversity within and between compound classes, high functional redundancy, and multifunctionality. Moreover, they do not only mediate direct defensive functions by poisoning their attackers, but are the language with which information is transferred between organisms and that meditates complex interactions within the plants' associated communities. Biotechnological, plant breeding and biological control approaches can use the power of natural plant defences to control pests in agriculture, sustainably.

Key Concepts

  • Plants employ various direct and indirect mechanisms to defend against herbivores.
  • Direct defences include chemical defences and physical defences.
  • Plant secondary metabolites can mediate direct defences but also function as a vehicle of information transfer between organisms and so mediate complex interactions within the plant‐associated communities.
  • Direct chemical defences can function as toxins, antidigestive or antinutrive agents and so reduce the nutritive value of the plant tissues for an attacking herbivore.
  • Some secondary metabolites and physical structures can facilitate the presence and prey‐search behaviour of natural enemies of herbivores and so mediate indirect resistance.
  • Plant defensive traits, in particular resistance‐mediating metabolites, tend to be functionally redundant, while individual compounds have multiple functions on different levels.
  • Chemical and physical traits can be combined or function synergistically to reduce herbivore pressure.
  • According to optimal defence theory, young tissues of high value to plant fitness tend to be chemically defended, whereas older tissues have relatively strong physical defences.
  • Chemical defences, especially induced chemical defences, are tightly regulated by a complex interaction between endogenous and external elicitors and a subsequent signalling pathway crosstalk.
  • Natural plant defences provide multiple sustainable options for pest control in agriculture.

Keywords: plant–herbivore interactions; plant secondary chemistry; chemical defences; co‐evolution; biotechnology; biological control; plant behaviour

Figure 1. Plant direct and indirect defences. (a) Physical direct defence; prickles on Solanum pyracanthum. (b) Urticating hairs of the stinging nettle (Urtica dioica) represent a combined direct physical and chemical defence because the sharp, pointed hairs break upon touch and inject a pain‐inducing mix of secondary metabolites into the attacker. (c) Gluey Latex oozing out of damaged tissue of the common milkweed (Asclepias syraica) directly and physically deters herbivores but also exposes the attacker to very toxic cardenolides. (d) Chemical information‐mediated indirect defence of the wild tobacco, Nicotiana attenuata. Herbivory induces volatile organic compound emissions that facilitate the prey search behaviour of predatory insects, such as Geocoris pallens, which is then killing the herbivore to the benefit of the signalling plant (Kessler and Baldwin, ). (e,f) The neotropical bull‐horn acacia, Vachelllia collinsii, produces protein‐rich food bodies at the tips of young leaflets (e) that provide the only food source for the brood of the obligate mutualist ant Pseudomyrmex spinicola. At the same time hollow thorns (f) provide a nesting place for the ants, and extrafloral nectaries provide sugary fuel for adult ants. The ants, in return, protect the tree from herbivores, pathogens and competing plants. The provision of food and shelter to facilitate the presence of a defending predator represents a resource‐mediated indirect defence mechanism. Photos (a), (d), (e), (f) taken by André Kessler, photo (b) taken by Danny Kessler, photo (c) taken by Ellen Woods.
Figure 2. Examples of herbivore resistance‐mediating secondary metabolites of plants. Shown are: ergovaline, and N‐formylloline, two alkaloids from the symbiotic fungi that enhance resistance of host plants to herbivores (Schardl et al., , ); gossypol, a sesquiterpene dimer from cotton; juvenile hormone III from sedge and juvocimene I from sweet basil, phytojuvenoids that interfere with insect development; labriformidin, a toxic cardenolide from milkweed; psoralen, a furanocoumarin from celery that damages DNA when exposed to ultraviolet light; caffeine, a well‐known plant alkaloid toxic to herbivores; myrcene, one of the monoterpene components of pine resin; E‐β‐caryophyllene, a sesquiterpene involved in indirect defence (Rasmann et al., ) and linalool, a monoterpene involved in both direct and indirect defences (Kessler and Baldwin, ). Lines indicate bonds that connect carbon atoms except where otherwise indicated, and hydrogen atoms are not generally shown.
Figure 3. The mustard oil bomb of Brassicaceae plants and its dismantling (counter defence) by insect herbivores. Upon Physical Tissue Damage (centre pathway, green background), vacuole‐stored, nontoxic glucosinolates (1) come into contact with the cytosolic enzyme myrosinase. Myrosinase catalyses the breakdown of glucosinolates into toxic hydrolysis products, isothicyanates (2), nitriles (3) and thiocyanates (4). Larvae of the Diamondback Moth (DBM, Plutella xylostella, pathway on the left) express glucosinolates sulfatase in their guts, which moves the chemical equilibrium away from the myrosinase‐catalysed breakdown of glucosinolates (1) and forms nontoxic desulfo‐glucosinolates (5). These sulfatases show activity on a wide variety of glucosinalates, which allows the caterpillars to feed on a diversity of Brassicaceae plants without experiencing the mustard oil bomb (Ratzka et al., ). Larvae of the Cabbage White Butterfly, Pieris rapae (pathway on the right), express nitrile specifiers proteins in their guts. These nitrile specifiers shift the plant myrosinase‐catalysed hydrolysis of glucosinolates (1) from the very toxic isothiocyanates (2) to the P. rapae caterpillars' less toxic nitriles (3). This controlled explosion of the mustard oil bomb is considered the key adaptation of P. rapae, allowing them to specialise on toxic Brassicace plants (Wittstock et al., ).
Figure 4. Herbivore counter‐defences. (a) Monarch butterflies, Danaus plexippus, (caterpillar shown), have evolved resistance to cardenolides, highly toxic secondary metabolites of their milkweed (Asclepias spp.) host plants. This resistance allows the herbivores to sequester these plant toxins in their body tissues and use them for their own defences against predators. The toxicity is advertised in the aposematic coloration of caterpillars and adults. (b) The coreid bug, Piezogaster regulus, is feeding on young leaves of the neotropical, obligate ant plant, Vachellia collinsii (bull‐horn acacia), without being attacked by the tree‐defending ants, P. spinicola. The bug overcomes the very potent resource‐mediated indirect defence of the ant plant by being chemically camouflaged. Ants do not identify the bug as ‘foreign’ because of cuticular compounds that mimic those of the ant hosts (Whitehead et al., ). Photo (a) taken by Ellen Woods, photo (b) taken by André Kessler.
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Walters D (2015) Physiological Responses of Plants to Attack. Chichester, UK: Wiley‐Blackwell. 248 pages. ISBN: 978‐1‐4443‐3329‐9.

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Kessler, André(Mar 2017) Plant Defences against Herbivore Attack. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001324.pub3]