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Ann. Rev. Plant Physiol. 1977. 28:479-501
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SECONDARY COMPOUNDS

+7639

Annu. Rev. Plant. Physiol. 1977.28:479-501. Downloaded from www.annualreviews.org
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AS PROTECTIVE AGENTS
Tony Swain
Department of Biology, Boston University, Boston, Massachusetts 02215

CONTENTS
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Introduction ....................... ...... ....................................... ................ ......................

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Distribution of Secondary Compounds in Space and Time
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Function of Secondary Compounds . ..... .
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Secondary Compounds as Waste Products .... .........................................................
Secondary Compounds as Protective Agents .. .. . . .. . . .. . .... .. . . .. ...... . .... . .

479
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480
481
483
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484

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Introduction .. . . . . . . .. . .... . . . ...... ................... .......... ..... ......... ....................
Defenses on the Surface of Plants ............................................................................
Defensive Function of the Cell Wall . .. ..................................................................
Che"1ical Defenses within the Cell .... ...... ........................ ........ ................................
The Role of Tannins .......................................... ............. ........................... . . ... ..
The Role of Phytoalexins .. ........................................... .. . .. . . . . . . . . ... . ..

485
485
485
486
486
487

488

SECONDARY COMPOUNDS AND ALLELOPATHY
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489
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INTRODUCTION

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THE NATURE OF SECONDARY COMPOUNDS
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SECONDARY COMPOUNDS AND PLANT DISEASES
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The Complexity of Allelopathy
Allelopathic Activity of Secondary Compounds .. .. .. ....................................... .... .
Nonprotein Amino A cids and A llelopathy . .. . . . .. .. . .. . . ........................ ......
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SECONDARY COMPOUNDS AS INSECT DETERRENTS

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Introduction .................................................. ..... ............................ . . . . . . .
Insect Chemoreceptors ........................... . . . . . . . . . . . . . .. . . .. . .. .. .........
Insect-deterrent Properties of Secondary Compounds ... . .. .... .. ... .. .... .. ...........
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490
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492

SECONDARY COMPOUNDS AS PROTECTiVE AGENTS AGAINST OTHER
HERBIVORES

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Introduction ........................................... .. . .. . . .. .. . ... .. . .. ................. .... .. .
The Role of Cyanogenesis . .......................................... .......... ..................................
The Role of Alkaloids ............ . .... ..... .. .. .
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The Role of Tannins
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CONCLUSIONS

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493

493
494
494
495
495

INTRODUCTION

We live in a chemical world . . . a world dominated by color, by scent, and by taste
(67, 135). Many animal phyla have developed a discriminatory acuity in these latter
479


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480

SWAIN

two senses which rivals their sight (180, 181). Even ourselves, who possess the most
sophisticated means of aural and visual communication, depend on our olfactory
and gustatory senses in our overall perception of the living world. For the majority
of living organisms, however, chemical signals are the main means .of communica­
tion. Such signals have the virtue of persistance, of being unaffected by most spatial
barriers, and of denoting absolutely whether the organism from which they originate
is benign or hostile to the receiver (1S0).
The majority of chemical signals are complex. They contain mixtures of many
different compounds, the majority of which belong to the heterogeneous collection
of so-called "secondary products" (lOS). These compounds were so named because

they have no obvious metabolic function and their very diversity of structure and
distribution among living organisms has led to the idea that they are waste products
(117, lIS).
The majority of known secondary products are of plant origin (64, 7S), but many
are found in fungi, bacteria, or sessile marine animals (3S, 148, 169). A large number
are present in arthropods (46), but fewer are found in the chordates, whose diversity
mainly depends on variation in size, shape, and, above all, behavioral patterns (55,
l SI).
What is the value to the plant of the varied secondary products it contains? Are
they merely a result of the capricious whims of evolution, leading towards unneces­
sary diversity, or are they perhaps the counterpart of behavior in animals? It is the
purpose of this review to try to answer these questions-to show that all the varied
types of secondary products present in plants do have a most important function,
a function shaped by evolution (159-161). They are present to maintain the overall
integrity of the plant against competitors, predators, and pathogens. The enormous
variety of chemical structures found determines the infinite number of signals which
are required to maintain the complexity of the differing ecosystems found in nature
(27, 36, 5S-60, 65, 72, 79, 87, 131, 132, 154, 176).
To illustrate what I mean by ecological complexity, consider a temperate-zone
meadow in the height of summer. On average, each 100 square meters will contain
150,000 individual plants. Associated with these will be several hundred guilds of
herbivores and carnivores: diverse populations of insects, birds, and mammals total­
ing about 30,000. Above and below ground will exist 1,000 billion bacteria, fungi,
algae, and protozoa. The soil around the plants' roots will contain a billion nema­
todes, 5 million microarthropods, 2 million oligochaete worms, and 30,000 earth­
worms (132). A formidable array indeed! This is why one requires an enormous
diversity of chemical signals which attract or deter, nourish or kill.
THE NATURE OF SECONDARY COMPOUNDS

Introduction


There are over 10,000 known low-molecular weight secondary metabolites in higher
plants and fungi (19, 56, 64, 70, 73, 78, 81, 85, 125, 165). They are usually classed
according to their chemical structures as shown in Table I and Figure 1 (108). In
addition, there are an unknown number of proteins, polysaccharides, and other


SECONDARY COMPOUNDS AS PROTECTIVE AGENTS

48 1

Table 1 Secondary products as protective agents
No. o f

known

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Class

Example

structures

Afford protection
againsta

Ref.


74

Wyerone

(I)
Lupanine (II)

Fungi
M amma ls

250
300

Canavanine (III)
(J-Carotene

Insects
Photoprotection

5
128
101

Coumarins
Cyanogenic

150

Scopoletin (IV)


Fungi

103

g lucosides
Flavon oids

50
1200

Linamarin (V)
Procyanidin
tannins (VI)
Sinigrin (VII)

Molluscs

94

Insects

50

Acetylenes
Alkalo id s
Amino adds
Carotenoids

G l u cosin ola tes
Lignans

Lipids

Phenolic acids

Polyketides
Quinones

Terpene sb
St eroid s

Miscellaneous
Proteins
Polysaccharides
Other polymers

750
4500

80
50
100
100
500
200
1100
600
500

?
?


Excelsin (VIII)
Waxes

Vanillic acid (IX)

Hircinol (X)
J uglone (Xl)
Glaucolide-A (XII)
Ecdysones
Tuliposide (XIII)
Lectins
Acylated
polysaccharides
Cutin

Insects

48

Insects
Fungi
Pla nt s
Fungi
P lan ts

Insects

141a
159

120
54
175
25

Insects
Fungi
Insect
Fungi

131
115
91
61

Fungi

III

a For other examples see text.
bExcluding carotenoids and steroids.

polymers which can be classed as secondary products insofar as they have no known
metabolic function in plants (21, III, 124, 142, 166).
The number of secondary metabolites presently known undoubtedly represents
the tip of the iceberg. In the majority of cases only the major components of a given
structural class have been examined from any one plant species. When a more
intensive search is carried out, the number of isolated secondary compounds usually
increases dramatically. For example, detailed investigation of Vinca rosea, a source
of antitumor indole alkaloids, showed the plant contains over 100 of these com­

pounds (149). Obviously it will also possess the expected complement of lipids,
phytosterols, carotenoids, phenolic acids, and flavonoids (78). It seems possible,
therefore, that the total number of all secondary products present in plants may well
equal the 400, 000 known species ( 126).
Distribution of Secondary Compounds in Space and Time

Secondary metabolites are not distributed evenly throughout the plant, either quan­
titatively or qualitatively, in space and time (72, 1I2, 1 13, 117, 176). Usually the


482

SWAIN

II

H�,

.
C-NH-O-(CHa)-CH-COOH
a

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H N�

I

N Ha,


CHP

-?'jr ° '?O

HO"�
IV

III

OH
OH

HO
HO

v

VI

NOS03

�
eH =CH_CH_e

.... s <4 1

VII

CHO

HO-

Q-

COOH

159

IX

HO

C

i:i',

r

;:,...

�I

HO

X

o

9i
XI


XII

XIII

Figure 1

Formulas of secondary products as protective agents.


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SECONDARY COMPOUNDS AS PROTECTIVE AGENTS

483

amounts are greatest in epidermal tissue, as might be expected if these compounds
function in defense (113). Nor are secondary products synthesized or accumulated
in any group of cells at all times during the life of the plant (112, 113, 149). For
example, seeds often contain high concentrations of such compounds which disap­
pear relatively quickly after germination and early seedling development (86). Again
this supports the view that they perform a protective function at the most vulnerable
period of growth.
The concentration of secondary compounds in many if not all plants also varies
diurnally, and in some cases gross changes have been shown to occur over periods
as short as an hour ( l SO). This suggests t�!it secondary metabolites are turned over
and their accumulation is under genetic control.
Finally, the concentration of these metabolites may be altered by climatic and
edaphic factors, by exposure to microorganisms, to grazing herbivores, or even to

air-borne pollutants (112, 113). Reports of their presence or absence in a given plant
should not, therefore, be taken as evidence that they do or do not play a specific
role-unless data are available to enable one to determine the location, the amount,
and the variation with time of the secondary metabolite concerned.
Function 0/ Secondary Compounds

As I pointed out earlier, none of the secondary metabolites is universally essential
in cellular biochemical processes. However, some have been shown to have an
overall function in the whole organism (112, 150). Thus carotenoids are important
in protecting cells or organelles against photodestruction (101), while the major
carotenoid in the brown algae, fucoxanthin, is a light receptor in photosynthesis
(67). Plant steroids, like their animal counterparts, undoubtedly play an important
part in membrane structures (70). Flavonoids, besides their importance as insect
guides in flower pollination (20), may regulate plant growth through their mediation
of IAA metabolism or of phosphorylation (99, 112). Alkaloids, some of which are
known to intercalate with DNA, might affect the regulation of protein synthesis
(134).
Secondary Compounds as Waste Products

Overall, the functions ascribed to secondary metabolites seem minor in relation to
their rich diversity of structure. This has led many investigators to suggest that
secondary compounds are either waste products of metabolism or, at best, inert
storage materials which are called into play at times of emergency (108, 117, 118).
Others assert that they enable organisms to keep open primary pathways under
conditions in which cell growth is unfavorable (169). I believe that neither of these
postulates stands up to the facts (161).
First, let us consider the nature of organic wastes. In animals, they are products
resulting either from the breakdown of existing molecules or from detoxification of
both the latter substances and ingested foreign compounds (26, 179). No cases are
known where waste products are structurally much more complex than the starting

materials. One would expect the same to be true for all organisms; otherwise the


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484

SWAIN

metabolic costs of excretion in solid form would be prohibitive. In other words,
plants would be expected to excrete nitrogen in some simple conjugated form, not
as strychnine.
Second, take storage products. To be effective, without straining the energy
budget, these need to be readily synthesized and the reserves easily recoverable to
primary metabolism in a directly usable form. Since plants utilize starch (and other
homopolymers) and proteins in this way, there again seems no need for them to
synthesize complex galactomannans or hard-to-degrade alkaloids for this purpose.
The most telling arguments against the "waste products" lobby are, however, the
facts that: (0) secondary metabolites are in a state of dynamic flux within the cell
(112, 150); and (b) these compounds have changed in structural complexity and
variety during the course of evolution (159, 160). As mentioned earlier, the first fact
indicates genetic control of their synthesis, degradation, and accumulation in one
cell and not another. The second fact, together with other data, shows that second­
ary metabolites have been under strong selective pressure through the coevolution
of animals, pathogens, and other plants. One could not imagine that the evolution­
ary changes which have taken place could have been dictated by new fashions in
excretion, in storage compounds, or in ways to allow primary metabolism to tick
over!
Secondary Compounds as Protective Agents


As I stated earlier, based on numerous cited examples, the function of secondary
plant metabolites is as chemical signals in the ecosystem. This alone can account
for their structural diversity, their evolutionary selection, their specific location in
the plant in space and time, and the rapidity of their turnover and translocation.
This does not mean that every secondary compound found in plants will have a
readily recognizable or even discernable role. In some cases they may be evolution­
ary relicts; in other cases they may be called into play only under special circum­
stances. Often the effects of secondary products in any situation will be found to be
marginal. They may only enhance the survival value of the plant by a few percent,
changes which are easily overlooked by chemical ecologists seeking an all-or-noth­
ing effect. But in the finely tuned ecological situations we find in nature, such small
changes could lead to survival or extinction.
Almost all the classes of compounds which we will consider (Table I, Figure I)
have more than one defensive function. This is not surprising since many of them
(nonprotein amino acids, alkaloids, terpenoid lactones, polyketides) exert their
physiological activity at the cellular level. Such compounds are thus equally likely
to affect fungi, plants, insects, and mammals depending on varying rates of translo­
cation and detoxification. But, as I have stressed, nothing is simple in nature.
Compounds which are toxic to one species may well be inert against a close relative.
The effects we observe are usually due to a mUltiplicity of causes and of compounds.
So instead of dealing in turn with each class of compound outlined in Table 1, I shall
pinpoint some examples of the defensive actions of plant secondary compounds in
disease, allelopathy, and insect and higher animal predation. This should serve to
illustrate the rich diversity of protective strategies which the possession of secondary
metabolites confers on plants.


SECONDARY COMPOUNDS AS PROTECTIVE AGENTS


485

SECONDARY COMPOUNDS AND PLANT DISEASES

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Introduction

Plants are at all times exposed to an enormous number of various guilds of fungi,
bacteria, and viruses that change in composition throughout the year (87). Such
exposure generally has no apparent effect on the healthy plant. Indeed, the numbers
of species of potential disease-causing organisms for any given plant is very small
indeed (174, 182). Why is this so? It appears that very few microorganisms which
alight on a plant mUltiply in sufficient numbers and then penetrate into the underly­
ing epidermal cells. This is probably due, at :east in part, to the presence of fungi­
static and bacteriostatic compounds on the surface of the plant and the inability of
the microorganism to penetrate the cutin or suberin layer (174, 182). Even where
invasion takes place, it may be quickly halted in the cells of the epidermis by toxic
compounds either already present or synthesized de novo. However, all this is
supposition, since we know little about the chemical responses of plants challenged
by nonpathogens. Most of the work has been done with necrotrophic parasites (107)
which are responsible for the obvious diseases of cultivated plants. Pathogens, as
well as mutualistic biotrophs (107) like nitrogen-fixing bacteria, which readily in­
vade plants, elicit a highly specific reaction within the host which overcomes the
latter's general defense mechanisms. The recent suggestion that the specificity of the
interaction and the switching on of defense mechanisms may be mediated by special
antigen-like glycoproteins on the surface of the microorganism, which interact with
resistance gene-controlled proteins in the host, is of great interest (2). While this
could explain the specificity of the reaction, it cannot be the whole story since the

chemical defenses of all plants so far studied can be activated in a variety of other
ways; for example, by asceptic wounding, by the application of solutions of a number
of discrete chemical compounds, including several simple metal salts, and by antibi­
otics (44, 103). It appears likely that the key event in the mobilization of plant
defenses is the molecular change which follows partial necrosis of the first cells to
be invaded (7, 103).
Defenses on the Surface of Plants

As mentioned above, it appears highly likely that the surface of the plants plays an
important role in defense against nonpathogens. In many cases the surfaces are
covered by trichomes of various types which may act as a physical barrier or be a
potent source of defensive compounds (106). Even without such structures, the
surfaces of leaves and stems still possess an important barrier to pathogens: that is
their coating with a mixture of waxes, alkanes, and other lipids. These undoubtedly
confer a great additional advantage to the plant by reducing water loss. Equally
important, however, is the molecular orientation of the mixture of compounds on
the surface. Scanning electron microscopy shows that the layer presents a tortur­
ously rough but regular appearance with many ridges and spikes (159). These can
keep fungal and bacterial cells sufficiently far from the wall of the epidermis to
prevent their direct ingress. The lipid layer on the surface coat of higher plants is
also very resistant to microbial degradation, and this property again limits potential
pathogens in their attack (81).


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486

SWAIN


Associated with the lipid layer are a wide variety of other compounds, usually
in small amounts (174, 182). As might be expected from studies on aJlelopathy (133,
167) (see below), almost all the classes of compounds shown in Table I have been
found, although simple phenolic acids which are potent antibiotics seem to be the
most common. Unfortunately, we know little about the quantitative or qualitative
variations in these surface substances from organ to organ or with time. Nor do we
know much about the method by which they are exuded onto the surface (141) or
whether mechanisms exist to increase secretion when the plant is under attack by
phytopathogens. The greater incidence of plant infection after a prolonged rainy
speJl may be partly due to the removal of these surface antibiotics, and the triggering
of fungal germination under such circumstances may be important to their survival.
It is no good emerging into a hail of chemical bullets!
The outer surface of the epidermis of plants is covered with the complex lipid
polymers, cutin or suberin 011). It is known that chemical changes take place in
cutin when pathogens invade epidermal cells (182), but detailed studies on the
importance of such changes do not appear to have been carried out. The initial
attack by the pathogen may be via the plasmodesmata, which presumably are the
sites of excretion of the surface defensive substances.
Defensive Function of the Cell Wall

The plant cell wall is undoubtedly a most important line of defense against invasive
parasites (1, 124). Until recently it was believed that variation in the polysaccharide
composition of the cell wall might determine the specificity of the host-parasite
reaction (1). However, this suggestion has now been discounted on the grounds that
the overall combination of different polysaccharides in the cell walls of the major
subclasses of plants is virtually the same (2). While this may be true, the intricate
mixture of differently branched hemicelluloses (124) which must require a combina­
tion of hydrolases for degradation might act as a moat around the perimeter of the
cell which holds up the pathogen for a sufficient length of time to allow the plant

to mobilize more effective defenses.
Recently it has been shown that the polysaccharides of most cell walls are acy­
lated with hydroxy aromatic acids, especially ferulic acid (75, 92, 159). The degree
of acylation is not large but increases as the plant ages or is infected (61, 75, 77).
Examination of cell wall fragments, isolated in neutral medium, suggests that the
acylation is mainly on the cellulose fibrils and that the greater the degree of esterifi­
cation the less the wall fraction is degradable by cellulase and other carbohydrases.
It seems likely, therefore, that it represents a primitive defense mechanism against
pathogens and perhaps certain herbivores. It should be noted that recently diferulic
acid has been isolated from the plant cell wall and adds support to an earlier
suggestion that this phenomenon of acylation was also a forerunner of lignification
(76, 159).
Chemical Defenses Within the Cell

When plants are invaded by a pathogen several often quite rapid changes take place
. in the primary metabolism of the affected cells. Respiration may rise twofold, and


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SECONDARY COMPOUNDS AS PROTECTIVE AGENTS

487

there are equally large variations in the rates of metabolism of nucleic acids, pro­
teins, and carbohydrates (103, 182). None of these changes seem to be effective
defenses in the short term, although reduction in basic nutrients might affect the
subsequent rate of growth of the pathogen (182). However, it is possible that certain
variations in the primary metabolic pathways may constitute a triggering mecha­

nism which sets off the increased synthesis of the more effective secondary defensive
products.
Almost all secondary products which have been tested show some antibiotic
activity (115). but it is difficult to determine the overall effect of the usual mixture
of compounds existing in the cell. For example, pathogens become more benign in
the presence of high concentrations of sugars (107), and this affects the antibiotic
potential of other compounds. Much more needs to be known also about possible
synergistic or antagonistic effects at different relative concentrations of two or more
potential antibiotics. All that seems to be true is that many of the secondary
compounds present in the cell increase enormously in concentration on infection,
even where their antibiotic activity against the invading pathogen is low (103). It
seems possible, however, that such compounds play a role in general antisepsis,
preventing other, usually noninvasive, organisms from obtaining a foothold.
The Role of Tannins

A most important group of defensive secondary metabolites is the tannins (11, 12,
23, 136, 158, 164). They are divided into two types, hydrolysable and condensed.
The former consist of a sugar core, usually glucose, the hydroxyl groups of which
are acylated by gallic acid or its congeners (11), while the latter are polymerized C-C
linked polyhydroxyftavans (12, 158). In both cases, the MW of the average tannin
is 1200-1500 daltons, although condensed tannins can be considerably larger. These
compounds are important because of their ability to precipitate all proteins by the
formation of multiple hydrogen bonds between the phenolic hydroxyl groups of the
tannin and the various nitrogen containing groups of the protein. They thus inhibit
most enzymes and render protein present in a food nutritionally unavailable since
tanned protein cannot be hydrolyzed by proteases (49).
The condensed tannins, usually now referred to as proanthocyanins, are found in
all classes of plants from Equisetum upwards, apparently evolving as plants devel­
oped more extensive vascularization. In angiosperms they are mainly confined to
woody species, but are found in grasses and other herbs. The hydrolyzable tannins,

on the other hand, occur only in dicotyledons. They have the advantage that they
are two to five times more effective as protein precipitants on a weight basis than
the proanthocyanins, and, of course, they are biodegradable (159, 162).
Tannins are quite potent antibiotics. Where they occur in large quantities they
can change a whole environment. For example, the observed low productivity and
paucity of animal life in certain tropical nutrient-poor white sand areas is ascribed
to the high concentration of tannins in the plants, which leads to an almost negligible
rate of decay of the leaf litter and pollution of the rivers by tannins washed out of
the leaves (88). In temperate trees, tannins and related phenolic compounds preserve
heartwood from fungal decay and inhibit extracellular hydrolases from invading
pathogens, thus preventing their rapid development in the plant (105, 152).


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488

SWAIN

The concentration and range of molecular weights of tannins usually both in­
crease in the leaves of woody plants during the growing season (41,50,157). This
accounts for the fact that older leaves are less susceptible to disease and less attrac­
tive to phytophagous insects and other herbivores. It also leads to the greater
sequestration of protein in the leaf which accounts for the slow release of nitrogen
into the soil from the leaf litter of tanniniferous species, a factor which can have
enormous consequences in the ecosystem (23, 164).
Many simple low molecular weight phenolic compounds present in plants may
be readily polymerized by oxidation to yield brown tannin-like substances contain­
ing quinonoid groups. These can also precipitate protein and cross-link to other

polymers. They are often formed in necrotic cells after invasion by a pathogen, as
shown by the browning which takes place in and around the area. The importance
of enzyme-catalyzed browning reactions in plant defense has long been suggested
but there is little hard evidence of their value (6, 103, 136).
The Role of Phytoalexins

The other important group of secondary metabolites which play a defensive role
against pathogens are the phytoalexins (44, 103). These are compounds which can
inhibit the development of the pathogen but are only formed or activated when the
latter comes into contact with the host cells. Phytoalexins are nonspecific toxins, and
the difference between resistant and susceptible hosts lies in the speed of formation
of the antibiotics (33). Their synthesis can be induced by a variety of pathogens and
nonpathogens including viruses, by several different types of chemical' compounds,
and by mechanical or radiation damage (103). It has recently been shown that
certain peptide and glycoprotein fractions from the pathogens stimulate phytoalexin
formation, but it is not clear what the mechanism is (2, 103). Usually the amounts
of each compound synthesized are different depending on the plant cultivated and
race of pathogens used. Phytoalexin formation has also been shown to be increased
by higher temperatures and longer days but is independent of light intensity (35).
Early experiments indicated that each plant produced one specific phytoalexin
(33). It is now known that usually two or more closely related compounds are
formed with differing antibiotic activities and at different speeds (6). It has also been
shown that the same or different phytoalexins can be evoked by a single fungus in
several closely related species, the distribution of the compounds being of taxonomic
significance (84).
The overall activity of phytoalexins depends not only on their speed of synthesis
but also their rate of turnover. Degradation within the plant has not been examined,
but several pathogens have been shown to detoxify various phytoalexins (34, 74).
So far only a few classes of compound have been identified as phytoalexins. The
vast majority are pterocarpans and isoflavans (171), but this may only be because

most of the experiments have been carried out with legumes. Other classes of
compounds are sesquiterpenes, especially from the Solanaceae (156), acetylenes
(74), and the phenanthrenes from orchids (54). It is to be expected that many other
substances will be found when a wider search is instituted, especially in families
which are known to accumulate several different classes of compounds other than
those outlined above.


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SECONDARY COMPOUNDS AND ALLELOPATHY

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Introduction

The term allelopathy was introduced by Molisch (116) 40 years ago to cover
biochemical interactions, both beneficial and harmful, between plant species includ­
ing fungi and bacteria. Now the term is usually limited to the detrimental effects
that one species of higher plant, the donor, has on another, the recipient, especially
those involving gross reduction in the germination efficiency, growth, and develop­
ment of the latter (119, 120, 133, 141, 167, 175). Allelopathic interactions are only
one aspect of competition between plants and the struggle for light (or shade),
moisture or inorganic and organic nutrients are of equal importance (120).
In all cases studied, allelopathic effects have been shown to be due to the release
from the donor of phytotoxic secondary metabolites (133, 167). These may be
released by volatilization, washing of the surface by rain or fog drip, or by exudation

from the living plant (141), or leached from its litter, including dropped fruit and
seeds, into the soil around the recipient. Naturally the phytotoxins have to accumu­
late in enough quantity and have sufficient chemical stability to persist for a long
enough time to exert their action. This is why allelopathic phenomena are particu­
larly difficult to study. An examination of the washings from fresh plant leaves may
reveal several potent phytotoxins, but each may be readily broken down in the soil
or be released from the plant in an erratic manner and thus never pose a threat to
other plants. Others may have no effect when tested but are modified after release
to yield a powerful allelopathic agent. Perhaps the best known example of the latter
type is the nontoxic 4-{3 -glucoside of hydrojuglone which occurs in the leaves and
fruit of the walnut Juglans regia ( 165); when washed into the soil by rain, this
compound is hydrolyzed and oxidized to the naphthoquinone juglone, which
severely inhibits the germination and development of many but not all undergrowth
species (133).
The Complexity of Allelopathy

Allelopathy obviously is a much more complex phenomenon than any of the others
dealt with in this review, for in the other cases the interaction between the plant and
its attacker is a direct one and is not bedeviled by the possible activity of other
organisms or dependent on the direct intervention of climatic and edaphic factors.
We know little about the processes of volatilization, washing, leaching, or even
exudation and even less about the chemical and biochemical degradative reactions
in the soil, all of which make interpretation of the results extremely difficult. For
example, p-hydroxybenzoic and vanillic acids and the related cinnamic acids have
been shown to be present in the rain washings from the leaves of several plants which
show allelopathic effects and to inhibit the germination of a wide spectrum of
angiosperm seeds (120, 133, 175). However, these same compounds are widely
present in soils, presumably arising either from the breakdown of lignin or by release
from insoluble forms in the leaf litter. Obviously it must be the local concentration
of such compounds which is important, and there is precious little information

about such matters.


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Allelopathic Activity of Secondary Compounds

It is not surprising from what was outlined in the previous section that our knowl­
edge of allelopathy is very incomplete. Most of the reported work has been carried
out by ecologists seeking to explain phenomena such as succession in regenerating
subhumid deciduous forests or after fire cycles in the soft Californian chapparal,
zonation of vegetation around stands of certain shrubs or trees, and the replant
problems ofa number of commercial fruit trees such as peach, apple, and citrus (120,
133, 175). As Muller & Chou have pointed out (120), the establishment of an
allelopathic interaction in these situations is usually a sufficient goal for the majority
of investigators who lack the expertise to investigate the complexities of the underly­
ing chemistry and biochemistry. So we find in the literature many reports of the
allelopathic effects of the addition to soil of ground-up leaf litter, of extracts from
whole plants, or washings from leaf surfaces (15, 40, 133, 168). But there are few
examples of the quantitative effects of individual phytotoxins or of the identification
of more than a handful ofallelopathic agents from a given ecological situation (133).
Of course, there is plenty of evidence regarding the deleterious effects of secondary
metabolites on germination (173), including autoxins present in many seed coats,
but the overall picture has been grossly neglected. As might be expected, almost all
classes of secondary metabolites have been shown to be potentially effective al­

lelopathic agents when tested in the laboratory (69, 133). The very diversity of these
substances and our lack of knowledge of any synergistic effects add to the problems.
Compounds obtained from soils are mainly stable substances such as the phenolic
acids mentioned earlier, but coumarins, flavonoids, terpenoids, alkaloids, cyano­
genic glycosides, and glucosinolates have all been implicated (133).
Nonprotein Amino Acids and Allelopathy

The most interesting group of allelopathic compounds, from the viewpoint of their
mode of action, are the nonprotein amino acids (16, 17, 56, 57, 104). Many of these
compounds are homologs of normal protein amino acids, yet they are not incorpo­
rated into proteins in the plants in which they accumulate. For example, azetidine-2carboxylic acid, the four-membered ring lower homolog of proline, is present in up
to 3% concentration in shoots of Convallaria majalis without dire effects. However,
when this compound is supplied to Phaseo/us aureus, replacement of proline occurs
in the protein of the bean (17). This difference has been shown to be because the
prolyl-tRNA synthetase of Convallaria, unlike that of Phaseo/us, is able to discrimi­
nate between the two metabolites. Since many seeds contain extremely high concen­
trations of nonprotein amino acids, (e.g. 14% of the weight of Griffonia simp/icifolia
seed is 5-hydroxytryptophan) it seems likely that they will exert allelopathic effects
on their competitors in the near environment (17).
SECONDARY COMPOUNDS AS INSECT DETERRENTS

Introduction

Our knowledge about the defensive role of secondary metabolites in plants has been
greatly aided by studies on insect plant relationships (14, 43, 45, 51, 58, 65, 71, 89,
145, 170). Most of the information on this subject has been obtained by entomolo-


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SECONDARY COMPOUNDS AS PROTECTIVE AGENTS

491

gists anxious to solve the question as to how insects select plants for both food and
as sites for ovipositing. Early in this century, VerschaffeIt (172) showed that several
classes of natural products were important in attracting or deterring insects to
various species of plants. However, due to the paucity of information about the
nature and distribution of plant secondary metabolites, his pioneering efforts were
not properly followed up until the 1940s (42). In the last quarter of a century,
enough evidence has accrued to show that secondary products are indeed the main
determinants in plant selection by insects. It now seems highly likely, as Feeny has
pointed out (51), that without such compounds the majority of species of higher
plants could not long withstand the voracious and destructive appetites of the
various guilds of herbivorous insect pests.
Insect Chemoreceptors

Insects possess a range of chemoreceptors, mainly on their antennae and mouth
parts, which enable them to discriminate a wide variety of chemical compounds at
often unbelievably low concentrations (180, 181). For example, male moths can
detect their female partners' sex pheromone with their antennae when it is present
in concentrations as low as one molecule/IO cmm (ca 10-16 g/liter) (180). The
sensitivity of antennae to other volatiles is much lower (ca 10-9 g/liter) (153), while
for nonvolatiles which are mainly sensed by the insects' mouth parts the limit of
detection is above the mg/liter range (113) or even higher in some cases (29, 96,
144). Even so, these quantities are by and large well below the amounts which may
have deleterious effects on the animals and the quantities found in many plant cells.
This means that if an insect alights on a plant which contains toxic chemicals, the
red light blinks almost before touchdown and he can escape without harm.

The number of chemoreceptors and their discriminatory power differs from one
insect species to another. For example, the receptors in the mouth parts of larval
lepidoptera (caterpillars) number 20 or so, while grasshoppers possess over 2000
(29). This difference is somewhat expected, since for most larval forms the host plant
is selected by the ovipositing habits of their parents (109), while flying insects have
a high chance of landing on an unpalatable plant species (28, 144).
What constitutes an unpalatable plant? Leaving aside nutritional factors, unpala­
tability is largely determined by the presence of secondary metabolites in sufficient
concentration to exert an undesirable physiological effect (147). In most cases, this
concentration will be much higher than that for an injected dose, since insects
possess a variety of sophisticated detoxification mechanisms (100), and some can
sequester extremely large quantities of toxic compounds in their hemolymph with­
out adverse effects (4, 22, 140, 183).
Insects which are mono- or oligophagous undoubtedly have evolved both the
ability to deal with the potentially harmful metabolites of their specific hosts and
the behavioral cues to ensure that only plants which contain such classes of metabo­
lites are selected as food (52, 144). Polyphagous insects, on the other hand, have a
greater detoxification capacity, which enables them to sample a wider range of
plants without harm (51, 100). However, a balance has to be struck between the
choice of eating all and every plant and the metabolic cost of more generalized
detoxification.


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Insect-deterrent Properties of Secondary Compounds

The range of secondary metabolites which deter insects is enormously wide and, as
in the other phenomena described above, covers almost all the classes of compound
shown in Table I (28, 145). The tannins are again of great importance because of
their ability to inhibit proteases and other digestive enzymes in the insects' gut and
to reduce protein availability from their food (31, 49, 50). There are numerous
reports about the effect of other phenolic compounds and related quinones (95, 121),
alkaloids (98, 129), terpenoids (24, 25, 47, 90), glucosinolates (48), and cyanogenic
glycosides (31, 129). Four classes of secondary metabolites are of special interest:
nonprotein amino acids, ecdysones, protease inhibitors, and lectins.
The deterrent effects of nonprotein amino acids against insects have been studied
widely, especially in relation to predation of tropical legume seeds by bruchids (18,
37, 86, 128). In many cases the concentration of the deterrent is over 5% of the dry
weight of the seed (17, 128), and yet as little as 0.25% of these compounds added
to a control diet can increase mortality two- to threefold (37, 128, 130). As men­
tioned in the section on allelopathy, the toxicity of the nonprotein amino acids is
due to their being incorporated into proteins instead of the normal homolog. This
conclusion is borne out by a recent report on a canavanine-resistant bruchid that
can subsist on the seeds of Dioclea megacarpa which contains up to 8% of the toxin.
It was shown that the arginyl-tRNA synthetase of the bruchid larva discriminates
between L-arginine and L-canavanine and so the latter is not incorporated into
protein (137)-an interesting case of coevolution.
The insect moulting hormones (127, 177), the ecdysones, occur in relatively high
concentrations in a number of plants, especially ferns and gymnosperms (163, 178,
184). They have profound effects when ingested by insects, inducing extra moults
and deformed adults, even when as little as .0.2 /-tg/g body weight is given (109a,
151, 178). The presence of ecdysones in the ferns indicates an earlier phase of
insect-plant coevolution (82). It is of interest that they are less widespread in the
more ancient evolutionary orders which also lack the range of secondary metabolites

found in higher taxa (163).
Protease inhibitors are widespread in higher plants (68, 142, 143) and may consti­
tute as much as 10% of the soluble protein in certain tissues. it has been shown that
they increase in concentration in the' plant cells after wounding, including insect
damage (143). This increase is not localized, due to the production of an inducing
factor which is translocated to other parts of the plant. Protease inhibitors have been
shown to affect the enzymes in the insect gut, but their overall effect on insect feeding
remains to be tested ( 143). For example, the bruchids lack proteases and are not
affected by soybean trypsin inhibitor at the I % level in the diet (91).
The lectins (phytohemagglutinins) are widespread in legume seeds where they
occur in relatively high concentration, 0.5-2.0 percent (1 66). They are glycoproteins
of 50,000-100, 000 mol wt which agglutinate erythrocytes at high dilution, and many
show mitogenic properties (166). They are toxic to many mammals and birds when
ingested (39). Recently it has been shown that this applies also to insects. Feeding
experiments with a bruchid which' normally lives on lectin-free seeds has shown that
addition of I % of the lectin from black beans to its diet kills 90% of the larvae (91).


SECONDARY COMPOUNDS AS PROTECTIVE AGENTS

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The interaction between plants and insects, as can be seen, is extremely complex.
Compounds which deter one insect species are the bread and butter of another.
Many phytophagous insect species, if not all, rely entirely on plants for the starting
products for the synthesis of pheromones (80, 83), for coloring matters (53, 139),
and for toxins against predators (3, 140). It is to be hoped that future investigations

will concentrate on the underlying biochemical diversity of these observations.
SECONDARY COMPOUNDS AS PROTECTIVE AGENTS
AGAINST OTHER HERBIVORES

Introduction

In spite of our overwhelming interest in our own well-being and that of our domestic
animals, we really know very little about the role that secondary metabolites play
in our choice of foods (5, 8, 60, 97). This is mainly because we have consciously
selected and bred those crops that are largely free from metabolites which are
deleterious to our health. Yet we are as sophisticated as other animals in our
chemosensory responses and go to great lengths to enhance the flavors of our food
and drink by adding herbs and spices containing desirable secondary compounds
(135). Even though we may have replaced our sex pheromones (114) by Chanel and
Brut, we can still tell the difference!
As far as we know all higher animals have the same type of chemoreceptors, but
discrimination and sensitivity vary widely. Here I am going to concentrate on
gustatory responses, since these seem to be highly important in the selection of food
by herbivores. It has been shown that if herbivorous animals encounter a food which
some time after ingestion causes a temporary malaise due to the presence of physio­
logically active chemical or other factors, then it is the taste (including texture),
rather than appearance and odor, which causes subsequent aversion to it (63, 138).
Gustatory responses are thought to be quite simple. We usually follow the ancient
Greeks in assuming there are only four discriminatory types of chemoreceptor for
taste (sweet, sour, salt, and bitter), ascribing other differences in oilr perception to
olfactory responses. This simplification is, in my opinion, unjustified. We respond
orally to astringency, sulfurous compounds, meatiness, and many more, but in the
examples given below, I am going to concentrate ori astringency (8), which is elicited
by the tannins, and bitterness which is given by a wide variety of different classes
of secondary metabolites including alkaloids, terpenoid lactones, and cyanogenic

glycosides (62, 102).
The evolutionary development of taste responses to bitter and astringent com­
pounds has had important consequences to the survival of various classes of verte­
brate herbivores (60, 62, 162). The majority of the compounds which impart these
tastes are highly toxic, especially to young animals. This does not mean that all
plants containing such compounds are always avoided, since many higher animals,
such as insects, have effective detoxification or excretory mechanisms which enable
them to avert any undesirable effects (60). By and large, however, toxic plants are
not eaten by all herbivores except in times of stress, when they may be sampled in
small amounts (60).


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The Role of Cyanogenesis

Perhaps the earliest attempt to examine the role of plant secondary products as
defensive compounds were the experiments carried out with snails by Stahl nearly
90 years ago (155). His work on these animals was not followed up until the 1960s
when Jones began his investigation on the relationship between cyanogenesis in
Lotus corniculatus and browsing by slugs and snails (94). As in many, if not all,
plant species which produce HCN on crushing, the condition in L. corniculatus is
genetically polymorphic (93). There are cyanogenic forms which contain the cyano­
genic glucoside and the corresponding fi-glucosidase and acyanogenic forms which
may be one of three types; two lack either the substrate or the enzyme, and the third

lacks both. It was found that the molluscs preferred acyanogenic forms of either
type, but the problem of polymorphism remains an intriguing one (3). In European
populations of Trifolium repens, acyanogenic forms predominate at higher altitudes
and in those areas where the mean temperature in January is below 2°C (94). This
may be because frost damage might cause release of sufficient HCN in cyanogenic
forms to kill the plant. Equally, it might be argued that predator pressure is reduced
by low temperature and cyanogenesis, which incurs some metabolic cost, is selected
against, or the plant uses other deterrents such as tannins (10).
The deterrent effect of cyanogenesis on higher animals is well documented, but
the effects are tempered by the fact that many mammals possess the liver enzyme
rhodanese which detoxifies HCN by transforming it into thiocyanate (94). Providing
animals graze continuously, they can tolerate a daily intake of the poison 10-20
times higher than the minimum lethal dose. Nevertheless, selective feeding of
acyanogenic forms of bracken by deer and sheep has been demonstrated recently
(32). It was also shown that locusts greatly preferred acyanogenic forms of the .fern
even when these contained the cyanogenic glucoside, in this case prunasin, but not
the hydrolase. This demonstrates that it is the production of HCN which is impor­
tant rather than the content of the secondary metabolite (32). However, it seems
possible that the taste cues which enable animals to avoid cyanogenic plants might
be related to the aldehydes and ketones (or cyanhydrins) formed during hydrolysis,
since many of these elicit a bitter response.
The Role of Alkaloids

Many other bitter-tasting substances have been shown to be important in deterring
mammalian herbivores. While sesqui- and diterpenoid lactones (24, 102) are obvi­
ously important, the major group of compounds in this class are the alkaloids (5,
8, 62, 113). By and large these compounds are absent from nonflowering plants, and
it seems likely that their structural diversity in the angiosperms is a result of
coevolution with mammals (159, 162). This suggestion is reinforced by the finding
that reptiles are 30 times less sensitive to alkaloids than mammals, and it has been

postulated that this might have had important consequences in the demise of the
dinosaurs (162). Alkaloids certainly deter sheep (5), and analyses of the feeding
preferences of the mountain gorilla (8) and Colobus monkeys (122) indicated that
they too avoided alkaloidal and other bitter-tasting plants. Similarly, the opossum


SECONDARY COMPOUNDS AS PROTECTIVE AGENTS

495

has been shown to be deterred from eating willows and poplars containing suffi­
ciently high concentrations of the bitter compound salicin ( 1 1 0). As Bate-Smith (8)
concluded, bitterness is a universally repellent character in foodstuffs.

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The Role of Tannins

Let us now turn to astringency. We are all aware of the unacceptable taste of unripe
fruits especially bananas, persimmons, and most pomaceous species (66). Although
higher acidity plays a part, the main deterrents are the tannins. As fruits ripen these
compounds apparently polymerize further and perhaps become bound to the cell
wall so the "taste" they evoke is no longer experienced (66). Obviously this is of
great advantage to the plant, which could not satisfactorily reproduce if its seed­
bearing organs were eaten before maturity. It is of interest, however, that many seed
coats contain tannins, often in large amounts, even in species where these polymers
are absent from other organs of the plant ( 1 3).
As mentioned earlier, the astringency, and hence the degree of defense they afford
against herbivores and pathogens, is dependent on structure and size. This means

that if tannin concentrations are determined by colorimetric measurements, they
give completely false ideas about the relationships being investigated (9, 10). For
example, the dimeric proanthocyanadins A and B, which differ only in that A has
an extra link between the two monomeric nuclei, show a three- to fourfold difference
in color yield on heating in alcoholic mineral acid but have almost equal astringen­
cies as measured by hemanalysis (12). Coupled with variations in extractability and
stability, it appears that a reappraisal is required of our analytical approach to
tannin determination in ecological situations.
Leaving aside the analytical problems, there is sufficient evidence to show that the
presence of tannins in sufficient concentration deters animal herbivores. Surveys of
the concentration of tanning in the food and nonfood plants of Aldabra tortoises
(30) and Colobus monkeys (122) showed that in both cases animals preferred plants
with little or no tannin. For the giant tortoises, it was interesting that the upper
concentration of tannin tolerated was more or less equivalent to the experimentally
determined limit of rejection when tannin was added to the food of the Mediter­
ranean tortoise (162). Obviously we need further surveys of this type if we are going
to understand the overall role of tannins as deterrents to herbivores.
CONCLUSIONS

The study of the importance of plant secondary compounds as protective agents
against predators and pathogens is only in its infancy. There are, as I have shown,
much data to show the qualitative importance of some hundred or so compounds
from all structural classes. But we have little quantitative data on the variation in
their concentrations in plants in both space and time, nor on their short- or long­
term effects at different dose levels on any of the major pests (for example, might
there be a mutation or selection if bruchids were kept for several generations on
sublethal doses of dopa?). Furthermore, most workers are still examining the effects
of a single compound out of the 40 or so which may accumulate in each plant in



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sufficient amounts to ensure some protection, even if only marginal. We need to
know more about the synergistic and antagonistic effects of different compounds and
whether the diurnal or hourly changes in the concentration of several secondary
products are perhaps important in imparting cryptic signals to pests. We must
obtain information about detoxification and other counter defenses and, if possible,
the biochemical basis for the many mutualistic associations which exist between
plants and other organisms. Finally, we need a broader look at the whole ecosystem,
the dependence and interdependence of organisms which determine habitat com­
plexity (3).
One hopes that the number of practitioners in the field will continue to expand,
and by the time the next review on this subject appears we will have a more rounded
picture of the role of secondary products as protective agents.
ACKNOWLEDGMENTS

I should like to thank Professors J. B. Harborne, D. M. Janzen, and L. Schoonhoven
for discussions and encouragement by example. I am grateful to Mrs. A. McNamara
for her careful preparation of the manuscript.
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