Plant Defences Against
Herbivore and Insect Attack
Christopher L Schardl, University of Kentucky, Lexington, Kentucky, USA
Secondary article
Article Contents
. Introduction
. Types of Herbivores and Interactions
. Types of Defences
Plants deploy a number of defences against herbivore and insect attack. A primary defence
is the production of toxins to poison the attackers. Other strategies include the
development of thorns and tough unpalatable tissue to deter herbivores, and the
recruitment of parasitoids and predators that attack herbivores.
. Coevolutionary Dynamics
. Plant Secondary Chemistry
. Interactions of Chemical Defences
. Temporal and Developmental Defences
. Biotechnology
Introduction
The story of Adam and Eve links eating a forbidden fruit
with death in the cycle of human existence (Genesis 3:1–
24). Indeed, to avoid poisoning, herbivores and omnivores
such as humans must be cautious in choosing which plants
and plant parts to eat. A prevailing hypothesis is that the
nearly ubiquitous antiherbivore metabolites in plants were
selected by coevolution with herbivores. Likewise, the
ability of a herbivore to detoxify or tolerate toxins of food
plants is essential for the herbivore’s survival. Plants may
largely escape herbivory if they are imbued with an
especially toxic cocktail, although the plants must also
have mechanisms for protection from their own toxins.
Other defences, such as thorns and tough or unpalatable
tissues, and recruitment of parasitoids and predators that
attack herbivores, all work in conjunction and synergy
with chemical defences. Plants survive only if they are able
at least partly to deter or avoid herbivory. Without
defences, plants would be driven to extinction, with the
consequent extinction of myriad herbivores, predators,
parasites and saprotrophs. Thus, the familiar species of our
biosphere and the fossil record of longstanding associations of plants with animals indicate a dynamic balance
struck between plants and those that eat them.
Types of Herbivores and Interactions
Any organism that consumes plant tissue is a herbivore.
The most intensely studied are vertebrates and insects, but
nematodes, molluscs, mites and parasitic microorganisms
are also important. These organisms can act together to
facilitate the consumption of a plant, or can act against one
another in surprising ways that help protect the plant from
devastation. Interesting examples of the latter phenomenon include plant mutualisms with ants and with endophytic
fungi. Stinging ants directly or indirectly (via aphids)
depend on plants for food and are fierce protectors of the
resource. Symbiotic microorganisms (endophytes) also
depend entirely on host plants for nutrition, but often
invest considerable resources in anti-insect and antiverte-
brate toxins that protect their host plants (Bush et al.,
1997). A counterexample is bark beetles and their fungal
symbionts, which act in concert to feed upon conifers.
Three-organism interactions such as highlighted in these
examples barely hint at the complexities underlying the
food webs for which plants are the base. Such complex
webs, which also include predators and parasites of the
herbivores, may be highly important for ecosystem
stability (Siemann, 1998).
Types of Defences
Chemical defences are ubiquitous and probably essential
for plant survival, but other defences are also important,
varied, and not always obvious. Plants accumulate tough
polymers such as cellulose, lignin, tannins and silicates,
which reduce palatability. Also, by minimizing the nutritive
value of their tissues plants may force a herbivore
(particularly an insect) to consume more. Though this
strategy may not seem advantageous, it actually forces the
herbivore to ingest larger amounts of plant toxins. Thorns,
barbs, stings and sticky resins exuded from resin ducts,
lactifers, or trichomes physically interfere with herbivory
and trap or kill herbivores. Lectins and proteinase inhibitors
produced in response to grazing interfere with digestion.
A significant protective strategy is to recruit as allies
parasitoids and predators that attack herbivores. This is
especially effective against insects. Plants under attack can
release a cocktail of volatile chemicals that act as cues for
these allies, which then attack, consume and reduce the
populations of herbivores (De Moraes et al., 1998). An
advantage to this strategy is that it may require relatively
little energy and nutrient resources to produce a highly
effective attractant.
Coevolutionary Dynamics
Herbivory often results in significant reduction in fitness of
a plant species, so plants come under strong selection to
ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net
1
Plant Defences Against Herbivore and Insect Attack
elaborate defences. Then, of course, the herbivores that
depend on plants must develop resistances and tolerances
to the defences. Thus emerges evolutionary dynamics that
take as many twists as there are potential strategies and
counterstrategies (Figure 1). As plants utilize combinations
of chemical, physical and developmental (phenological)
defences, and as they recruit allies, herbivores adapt to
greater or lesser degrees to all of these defences. Moreover,
adapted herbivores often benefit from the original plant
defences. Notably a herbivore that has adapted to a class of
plant toxins may utilize the same toxins against predators,
may appropriate the toxins as olfactory cues for its
preferred food plant (kairomones), or may even use them
as attractants for mates (pheromones). The coevolutionary
dynamics of plant defence and herbivore adaptations
necessitate the multifarious nature of plant defences, and
probably drive diversification of forms, species and
chemistries of plants.
Plant Secondary Chemistry
Plants generally produce chemicals with toxicity to a wide
variety of potential herbivores, or which deter herbivores
from feeding. These chemicals are almost certainly of
major importance for defence against generalist herbivores, and even for restricting the degree of damage caused
by specialist herbivores exhibiting some resistance to the
chemical defences. Different plant groups (e.g. families)
tend to have different chemical characteristics. Thus,
alteration in chemical profiles appears to be a slow
evolutionary process. Likewise, when herbivores shift
diets to new food plants, such shifts are most likely to be
Plants
Herbivores
New phenotype
Generalist feeding
Protection from
generalist feeders
(feeding deterrents,
attractants for predators, etc.)
New resistance, tolerance
or avoidance mechanisms
Adaptive radiation
Elaboration of defences:
Additional new defences
Adaptive variance of expression
and timing of defences
Adaptive radiation
Kairomones
Antipredator defences
Further adaptations
Figure 1 A simplified scheme for coevolution between plants and their
herbivores.
2
between plant species with similar secondary chemistries
(Becerra, 1997).
It is difficult to demonstrate that the functions of
chemicals produced by plants are to reduce or prevent
herbivory. This is because herbivores must have adapted to
the defences of at least some plants to at least some degree
or they would have become extinct long ago. Nevertheless,
the observation that so many plant secondary metabolites
are active against so many animals and pathogenic
microorganisms strongly suggests a defensive role. Information about some of the more common classes of
antiherbivore chemicals in vascular plants is given below.
Alkaloids
Alkaloids include any of a wide variety of chemicals that
incorporate amines. Since many neurotransmitters are
biogenic amines, many alkaloids have neurotropic effects
ranging from extreme bitterness to causing stupor or death.
Activities on multiple neuroreceptors are common. An
example is the ergot alkaloid class (Figure 2) characteristic
of the plant family Convolvulaceae and protective
symbionts (endophytes) in grasses. They affect the
mammalian central nervous system and interfere with
appetite, water homeostasis, temperature regulation, and
even fertility. The same alkaloids acting on the peripheral
nervous system cause miscarriages and, by reducing blood
flow, anoxia and gangrene of the limbs (Bush et al., 1997).
Other alkaloids, such as pyrrolizidines and steroidal
glycoalkaloids, are directly toxic to cells. These are
normally confined to the vacuole of the plant cell to
prevent autotoxicity. Herbivores break open the vacuoles
during feeding, releasing the toxins that then damage both
herbivore and plant tissues. Plants are far more capable
than animals of recovering from these insults, so the
animals generally lose this chemical battle.
Terpenoids, steroids and other prenyl
derivatives
Metabolites derived from five-carbon units called isoprenes are extremely varied in their properties and
biological activities. Steroid and terpenoid hormones are
critical in animal development and signalling, making the
receptors for these compounds obvious targets for antiherbivore chemicals. Particularly interesting examples are
the phytojuvenoids (Figure 2). These plant compounds
mimic juvenile hormones and can thereby stop or cause
inappropriate development of herbivorous insects. However, like the alkaloids, some isoprene-derived defences are
toxic directly to cells. These include saponins, which are
sugar-linked terpenoids, steroids or sterol alkaloids with
broad toxicity to animals and microbes. Some plant
pathogenic fungi have saponin-detoxifying enzymes that
ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net
Plant Defences Against Herbivore and Insect Attack
OH
O
N
O
N
N
H
N
O
O
Ergovaline
N
H
O
CH 3
O
O
OH
H
O
Juvocimene I
O
H
H
H
CH 3
O
HO
O
O
O
OH
Juvenile hormone III
O
CH 3
Myrcene
O
Labriformidin
O
HO
O
O
OH HO
OH
OH
HO
Gossypol
Psoralen
O
O
O
Figure 2 Examples of chemical defences of plants against herbivores. Shown are: ergovaline, an alkaloid from the fungal endophyte Epichloe festucae that
enhances host resistance to herbivores (Bush et al., 1997); juvenile hormone III from sedge and juvocimene I from sweet basil, phytojuvenoids that interfere
with insect development; labriformidin, a toxic cardenolide from milkweed; myrcene, one of the monoterpene components of pine resin; gossypol, a
sesquiterpene dimer from cotton; and psoralen, a furanocoumarin from celery that damages DNA when exposed to ultraviolet light. Branches connect
carbon atoms except where otherwise indicated, hydrogen atoms are not shown except where needed to indicate stereochemistry, and hexagons with
circles indicate aromatic six-carbon rings.
are essential for survival on host plants that produce those
saponins (Bowyer et al., 1995).
Some of the best known interactions of plants and
herbivores involve steroid toxins such as the cardenolides
(Figure 2). Because of their pharmacological properties at
low doses, sugar-linked cardenolides such as digitalis
(actually a cardenolide mixture) are called cardiac glycosides. Cardenolide activity and toxicity is due to their
effects on ion transport across cell membranes. In the
milkweeds (Calotropis and Asclepias species of the
Asclepiadaceae) the cardenolides are dissolved in the
sticky terpenoid latex stored in specialized cells called
lactifers. Some insects have intricate feeding habits that
minimize exposure to this toxic latex. Furthermore, insects
that feed on cardenolide-laden plants often secrete or
sequester these toxins as potent deterrents to predators.
This appropriation of a plant defence is exemplified by the
monarch butterfly (Danaus plexippus) whose larvae feed on
milkweeds, accumulate cardenolides, and display bright
colours that warn away potential predators.
Terpenoids and related compounds comprise a huge
group of chemicals with numerous biological activities.
One of the most apparent classes is the resin-producing
terpenoids of pines and other conifers (Figure 2). These
resins directly interfere with feeding or even trap herbivores. Also included in this class are important toxins such
ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net
3
Plant Defences Against Herbivore and Insect Attack
as gossypol (Figure 2) in cotton and the iridoids common
among angiosperms.
Cyanide and glucosinolates
Cyanogens are known from all major plant groups. The
cyanogenic glycosides, if unaltered, are relatively nontoxic.
However, removal of a sugar moiety by action of a
glycosidase enzyme leaves unstable intermediates whose
subsequent spontaneous breakdown results in cyanide
release. The cyanide poisons respiration and can thereby
cause death.
Glucosinolates, like cyanogens, are nontoxic forms
compartmentalized away from the myrosinase enzymes
that cause release of their toxic components. When plant
tissue is damaged and vacuoles are ruptured, glucosinolates come in contact with the cytosolic myrosinases that
then catalyse their cleavage into a sugar moiety (usually
glucose) and an unstable intermediate. The intermediate
rapidly breaks down to form sulfate and mustard oils of the
form R-SCN (where R represents any of various linked
chemical groups), R-CN 1 S, or related structures. Considerable evidence indicates that glucosinolates are toxic
to a broad range of mammalian and insect herbivores
as well as plant-pathogenic fungi and water moulds
(Oomycetes).
Coumarins
Coumarins are derivatives of phenylalanine. As such they
are related to the major components of lignin and suberin,
and branch early from the pathway to flavonoids and
tannins. Furanocoumarins such as psoralen (Figure 2) are
common in the plant family Apiaceae. Furanocoumarins
are phototoxic, forming toxic intermediates in the presence
of light. Ultraviolet light in particular causes furanocoumarins to become highly reactive and crosslink DNA.
Thus, these compounds tend to have very broad toxicity to
animals and microorganisms.
Interactions of Chemical Defences
The advantage of a defence would appear to be obvious:
energy and photosynthetic assimilates of the plant remain a
resource for survival and reproduction of the plant rather
than of the secondary consumers. However, the defence
itself requires expenditures of these resources. Thus, if a
plant suffers relatively little herbivory the cost of the
defence may not be recovered in increased fitness.
Furthermore, if one of several potential herbivores is
undeterred by the plant’s defences, the advantage of the
defence might not be realized. Thus, several strategies must
be employed that are more sophisticated than simple
assault with toxic chemicals.
4
Production of more than one toxin, particularly if they
are not chemically related, can be an effective counterstrategy to a herbivore’s resistance against any single toxin.
Different chemical classes often act in synergy against
herbivores. Also, developmental changes in chemical
profiles can reduce herbivory by restricting the time period
that herbivores adapted to the first defence can continue to
feed on the plant. Changes in profiles over the age of the
plant are frequently observed. Also, herbivory may change
the expression of biochemical pathways so that those that
are initially prevalent are turned off and those that are
quiescent at first are turned on. Thus, a herbivore may
begin to feed on a plant with chemical profiles to which it is
resistant; the chemical profile may then change to one less
favourable for the herbivore.
Temporal and Developmental Defences
Growing plant tissues have high nutritive value and tend to
be heavily grazed by herbivores, so they must be well
protected. Typically, young tissues have higher concentrations of chemical toxins whereas older tissues are tougher
and less palatable. Polymers such as tannins and lignin,
terpenoid resins, and silicate deposits contribute to
toughness. Also, in some plants the chemical toxins change
with development so that herbivores that begin feeding on
younger tissues may be unable to cope with the older
tissues.
Coordinated and rapid flushes of new growth may
outpace herbivores. Similarly, mast fruiting can outpace
seedeaters. Bamboos are famous for worldwide coordination of their flowering and seed production. This is thought
to be a trait selected because bamboo seeds are highly
nutritious and are not well protected by chemical defences.
The sudden abundance of bamboo seeds in mast fruiting
would outpace the herbivores and allow a large number to
establish a new generation of plants (Janzen, 1976).
Biotechnology
A major objective of biotechnology is to modify crops and
horticultural plants for enhanced resistance to herbivores
and pathogens, preferably with the benefit to the environment that chemical sprays will be reduced. To introduce
new antiherbivore activities it will be necessary to identify
all genes required for their production. Therefore, the first
such introductions have been of genes for single antiherbivore proteins. Various subspecies of the bacterium
Bacillus thuringiensis produce a variety of d-endotoxins (Bt
toxins) with broad or narrow activities against insects
(Hofte and Whiteley, 1989). The first report of Bt toxin in
transgenic plants was in 1987 (Vaeck et al., 1987). Now
significant acreage of soya beans, cotton and corn are
ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net
Plant Defences Against Herbivore and Insect Attack
projected to be composed of such transgenic plants. An
important concern is that overuse of particular Bt toxins in
transgenics, or excessive reliance on Bt toxins in general,
will select resistant insects (Tabashnik et al., 1998). The
concerns point to a well-founded but sometimes ignored
principle: reliance on individual defences against potentially devastating herbivores is dangerous, so multiple and
varied defences should be sought and employed.
Reliance on single proteins like Bt toxins is very limiting.
Secondary metabolites will continue to be important where
they occur naturally and potentially where they can be
introduced by plant transformation. However, it is a
daunting prospect to identify and move multiple genes for
defensive chemicals from one plant or endophyte into a
distantly related plant. Nevertheless, the observation that
coevolutionary relationships between plants and herbivores tend to track chemical relationships (Becerra, 1997)
suggests that expression of new chemical classes in
transgenic crops would be highly effective against their
specialized herbivores.
Though transformation of plants with new defensive
genes is potentially powerful, it is unwise to opt routinely
for this approach. Furthermore, an abundance of other
possibilities are available or yet to be discovered. Deployment of parasites, pathogens or endophytes against
herbivores, and identifying novel pest resistance genes in
wild or regional germplasms, are two approaches with
considerable promise. Keeping in mind the value of
multiple strategies, a thorough understanding of the
multifarious defences naturally employed by plants is
crucial when devising such defences for agricultural and
horticultural plants. After all, in nature many remarkable
and often subtle defence mechanisms underlie the survival
of diverse plants and the organisms that depend on them.
References
Becerra JX (1997) Insects on plants: macroevolutionary chemical trends
in host use. Science 276: 253–256.
Bowyer P, Clarke BR, Lunness P, Daniels MJ and Osbourn AE (1995)
Host range of a plant pathogenic fungus determined by a saponin
detoxifying enzyme. Science 267: 371–374.
Bush LP, Wilkinson HH and Schardl CL (1997) Bioprotective alkaloids
of grass–fungal endophyte symbioses. Plant Physiology 114: 1–7.
De Moraes CM, Lewis WJ, Par PW, Alborn HT and Tumlinson JH
(1998) Herbivore-infested plants selectively attract parasitoids. Nature
393: 570–573.
Hofte H and Whiteley HR (1989) Insecticidal crystal proteins of Bacillus
thuringiensis. Microbiological Reviews 53: 242–255.
Janzen DH (1976) Why bamboos wait so long to flower. Annual Review
of Ecology and Systematics 7: 347–391.
Siemann E (1998) Experimental tests of effects of plant productivity and
diversity on grassland arthropod diversity. Ecology 79: 2057–2070.
Tabashnik BE, Liu YB, Malvar T et al. (1998) Insect resistance to
Bacillus thuringiensis: uniform or diverse? Philosophical Transactions
of the Royal Society of London B: Biological Sciences 353: 1751–1756.
Vaeck M, Reynaerts A, Höfte H et al. (1987) Transgenic plants protected
from insect attack. Nature 328: 33–37.
Further Reading
Coley PD and Barone JA (1996) Herbivory and plant defenses in tropical
forests. Annual Review of Ecology and Systematics 27: 305–335.
Rosenthal GA and Berenbaum MR (eds) (1992) Herbivores: Their
Interactions with Secondary Plant Metabolites, vols I–II. San Diego,
CA and London: Academic Press.
ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net
5