растителни токсини

1
Most recent investigations have focused on induced, rather
than constitutive, plant defenses. Yet significant research has
helped to illuminate some of the principal characteristics of
constitutive defenses, including mechanisms of action and
synergistic effects, as well as strategies used by herbivores
and pathogens to circumvent them.
Addresses
Max Planck Institute for Chemical Ecology, Department of
Biochemistry, Winzerlaer Strasse 10, Beutenberg Campus,
D-07745 Jena, Germany
*e-mail: wittstock@ice.mpg.de
†
e-mail: gershenzon@ice.mpg.de
Current Opinion in Plant Biology2002, 5:
1369-5266/02/$ — see front matter
© 2002 Elsevier Science Ltd. All rights reserved.
DOI 10.1016/
S1369-5266(02)00264-9
Abbreviations
cytochrome P450scytochrome-P450-dependent monooxygenases
DIBOA 2,4-dihydroxy-1,4-benzoxazin-3-one
DIMBOA 7-methoxy DIBOA
Introduction
Plants synthesize a broad range of secondary metabolites,
including alkaloids and terpenoids, that are toxic to herbi-
vores and pathogens, and so are believed to act as defense
compounds. Classical examples of plants that are poisonous
to humans, such as poison hemlock, foxglove, and aconite,
demonstrate how well natural products can defend plants,
at least against mammalian herbivores. Defensive chemicals
have long been thought to be costly for plants because of
the resources consumed in their biosynthesis, their toxicity
to the plant itself or the ecological consequences of their
accumulation [1,2] (see also Heil, this issue). One way for
a plant to reduce these costs is to synthesize defense
compounds only after initial damage by a herbivore or
pathogen. This strategy is obviously risky because the
initial attack may be too rapid or too severe for such
damage-induced defenses to be deployed effectively.
Consequently, plants that are likely to suffer frequent or
serious damage may be better off investing mainly in
constitutive defense, whereas plants that are attacked
rarely may rely predominantly on induced defenses [3].
When applied to individual plant organs or developmental
stages, the same considerations suggest that plant parts
that are of high fitness value or that are under a high risk
of attack may be best protected by constitutive defenses,
whereas others may be better defended by induced
responses. For example, a field survey has shown that
the reproductive organs of wild parsnip (Pastinaca sativa)
are attacked very frequently by herbivores. These
organs accumulate high constitutive levels of the toxic
furanocoumarin, xanthotoxin (Figure 1a), which are not
increased by artificial damage. In contrast, the roots of
wild parsnip are rarely attacked and have only low consti-
tutive levels of xanthotoxin, but these increase readily
upon wounding [4].
Thus, both constitutive and induced defenses may
contribute to the optimal protection of a plant against its
multitude of herbivorous and microbial enemies. Because
of the large variety of elicitors available for triggering the
accumulation of defense compounds and the development
of molecular tools for studying differential gene expression,
however, research in the past decade has largely focused on
induced defense [5,6,7
•
]. In contrast, studies on the roles
and mechanisms of constitutive chemical defense are rather
rare because of the difficulty of manipulating constitutive
compounds in experimental settings. This review discusses
recent progress in our understanding of some general prin-
ciples that underlie constitutive chemical defense, and
explores the use of molecular tools to study its role in plants.
Plant toxins act through various mechanisms
All plant compounds that have negative effects on the
growth, development or survival of another organism can
be regarded as toxins. The mechanisms of action of some
plant toxins are well known. For example, saponins
(Figure 1b) disrupt cellular membranes [8], hydrogen
cyanide released from cyanogenic glycosides (Figure 2)
inhibits cellular respiration [9], and cardenolides (Figure 1c)
are specific inhibitors of the Na
+/K
+-ATPase [10,11]. But the
modes of action of many other toxins still await discovery.
In recent studies, the active principle of water hemlock
(Cicuta virosa), the polyacetylene cicutoxin (Figure 1f), was
shown to act by prolonging the repolarization phase of
neuronal action potentials, presumably by blocking
voltage-dependent potassium channels [12]. Thanks to this
mechanism, water hemlock is one of the most poisonous
plants of the Northern Hemisphere. The analgesic morphine
from opium poppy (Papaver somniferum) has pronounced
effects on the central nervous system owing to its binding
to opiate receptors. A possible additional mode of action of
morphine in defense against pathogens was recently
described [13]. Upon mechanical damage, constitutive mor-
phine is quickly metabolized to bismorphine (Figure 1d),
which accumulates in the cell wall and becomes cross-
linked to pectins, making them resistant to hydrolysis by
pectinases. Bismorphine formation requires a pre-existing
peroxidase and H
2O
2that may arise from the oxidative
burst triggered upon pathogen attack.
Constitutive plant toxins and their role in defense against
herbivores and pathogens
Ute Wittstock*and Jonathan Gershenzon
†

Recently, some compounds that are well known for their
other functions in primary or secondary metabolism have
also been found to be involved in plant defense [14,15].
For example, phytic acid, a strong cation chelator, whose
salts serve as the major storage form of phosphorus in the
seeds and fruits of many plants, has been suggested to
function in antiherbivore defense on the basis of its
ability to bind essential dietary nutrients. Larvae of the
two lepidopterans, Depressaria pastinacella(which feeds on
immature reproductive structures) and Trichoplusia ni
(which feeds on foliage) all died when fed an artificial diet
supplemented with 1% phytic acid. However, the
seed-feeding Heliothis virescenswere not killed by the
same diet [15].
The ways in which plant toxins are stored are often crucial
for their effectiveness. Certain plant species accumulate
toxins in resin ducts, laticifers (Figure 3) [16
•
] or glandular
trichomes (Figure 4) [17,18]. The toxins are released in
large amounts as soon as these structures are ruptured by
herbivore feeding, movement on the plant surface or the
growth of pathogens.
2Biotic interactions
Figure 1
β-D-glu(1→3) β- D-glu(1→2)
β-
D-glu(1→)
3
26
(b) Avenacoside B
O O O
OH
(a) Xanthotoxin
OH
HO-CH
2
(f) Cicutoxin
(d) Bismorphine
α-L-rha(1→4)
O
O
O
O
OH
OH
OH
O
CH
O
(c) Calotropin
O
O
O
CH
2
O
N
O O
O
OH
CH
3
O
(g) DIMBOA-glucoside
O
O
OH
OH
N
OH
OH
N
CH
3
CH
3
(←1)β-D-glu
(←1)β-D-glu
O
O
N
O
O
OH
O
(e) Senecionine N-oxide
Current Opinion in Plant Biology
Examples of constitutive plant toxins. (a)A furanocoumarin from
Pastinaca sativa, (b)a saponin from Avena sativa, (c)a
cardenolide from Asclepias currassavica, (d)the product of
wound-induced dimerization of the preformed alkaloid morphine
from Papaver somniferum(morphine monomers shown in orange
and blue), (e)a pyrrolizidine alkaloid from Senecio jacobaea,
(f)a polyacetylene from Cicuta virosa, (g)a benzoxazinone
glucoside from Zea mays. Sugar residues highlighted in red are
released by endogenous plant enzymes upon tissue damage leading
to the activation of the toxins. Sugar residues highlighted in green
are released by glycosidases of pathogens that are able to
overcome the plant toxins.

The power of synergism: one plus one equals
more than two
Plants are not only able to synthesize individual defense
metabolites with diverse chemical structures but also
produce complex mixtures of defense compounds, such
as the terpenes of essential oils. Many of the individual
constituents of essential oils are acutely toxic to insects
[19] and pathogens [20]. However, the toxicity of these
compounds can be potentiated in mixtures, so that the
activity of the mixture is higher than would be expected by
adding up the activities of its individual constituents. This
phenomenon, known as synergism, has recently been
demonstrated for mixtures that each contained two essential-
oil constituents, which were fed to larvae of the generalist
lepidopteran Spodoptera litura[21]. These mixtures were
up to nine times more toxic than would have been expected
from the simple additive effects of the constituents.
Synergistic effects are also known for antimicrobial peptides.
In vitroassays have demonstrated that snakin-1, a constitutive
peptide from potato that is mainly expressed in tubers and
reproductive organs, acts synergistically against Clavibacter
michiganensissubsp. sepedonicuswith the potato defensin
PTH1, which has a similar expression pattern [22]. The
growth inhibition caused by the combination of these two
peptides exceeded their calculated additive effect by
100%. The mechanisms behind such synergisms are
unknown, but may involve the ability of one component of
a mixture to inhibit the detoxification of others or to
enhance the absorption of others from the gut [23].
Plants must live with their own toxins
Many defense compounds are toxic to the plant itself, and
so plants that rely on constitutive chemical defense must
be able to synthesize and store these substances without
poisoning themselves. One strategy is to store toxins as
inactive precursors, for example as glycosides [24], separate
from activating enzymes. For example, it has long been
known that the glucosinolates found in plants of the order
Constitutive plant toxins and their role in defenseWittstock and Gershenzon 3
Figure 2
COOH
NH
2
OH
OH
N
OH
OH
OH
CN
OH
CN
O
Glu
OH
N
SH
OH
OH
N
S
O
Glu
SO
3
HCN
CYP79A1
CYP71E1
sbHMNGT β-Glucosidase
OH
CHO
Tyrosine
Dhurrin
p-Hydroxybenzylglucosinolate
Current Opinion in Plant Biology
Metabolic engineering of the biosynthetic pathway of the cyanogenic
glucoside dhurrin into Arabidopsis thaliana[57
··
]. Upon the
introduction of the three enzymes (shown in blue) catalyzing dhurrin
biosynthesis in Sorghum bicolorinto A. thaliana, A. thaliana
accumulated the glycoside dhurrin (glucose residue highlighted in
blue). The engineered plants were toxic to Phyllotreta nemorum, a
specialized herbivore of crucifers, as hydrolysis of the glucoside upon
tissue damage leads to the release of the metabolic poison hydrogen
cyanide (shown in red). If just CYP79A1 is transferred to A. thaliana,
endogenous A. thalianaenzymes (green arrows) convert the aldoxime
intermediate into the respective glucosinolate, and the plants are
readily consumed by P. nemorum[58].

Capparales (Figure 5) [25–27] are compartmentalized
separately from their activating enzyme, the thioglucosidase
myrosinase. Glucosinolates are found in many plant
tissues, whereas myrosinase is localized in scattered
‘myrosin’ cells that seem to be glucosinolate-free. In
Arabidopsis thaliana, recent studies suggest that sulfur-rich
cells (S-cells) that are situated between the phloem and the
endodermis of the flower stalk contain high concentrations
of glucosinolates [28], whereas myrosinase is localized in
adjacent phloem parenchyma cells (Figure 5) [29]. Upon
tissue damage, the glucosinolates contact myrosinase and
are hydrolyzed irreversibly into an unstable aglycone. The
aglycone rearranges into a variety of biologically active
compounds, typically isothiocyanates and nitriles (Figure 4).
The defensive function of the isothiocyanates released
upon glucosinolate hydrolysis (‘the mustard oil bomb’)
became apparent in a recent study in which larvae of the
generalist lepidopteran T. n iavoided A. thalianaecotypes
that produced predominantly isothiocyanates upon
4Biotic interactions
Figure 3
Larvae of some lepidopterans avoid
intoxication by severing (i.e. ‘trenching’) the
laticifers upstream of their intended feeding
site; however, during trenching they may
encounter potent doses of latex toxins.
(a)Larva of Erinnyis alopestarting to feed
after severing a Carica papayaleaf.
(b)Larva of Trichoplusia nihangi