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Microbiology and Molecular Biology Reviews, September 1999, p. 708-724, Vol. 63, No. 3
Sainsbury Laboratory, John Innes Centre,
Norwich NR4 7UH, United Kingdom
1092-2172/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Fungal Resistance to Plant Antibiotics as a
Mechanism of Pathogenesis
SUMMARY
INTRODUCTION
PREFORMED ANTIFUNGAL COMPOUNDS
Saponins
Structure and biological activity.
Resistance of fungal pathogens.
(i) Degradation of oat saponins.
(ii) Degradation of steroidal glycoalkaloids of solanaceous
plants.
Cyanogenic Glycosides and Glucosinolates
Cyclic Hydroxamic Acids
Antifungal Compounds and Fruit Ripening
PHYTOALEXINS
Stilbenes
Potato Phytoalexins
Crucifer Phytoalexins
Legume Phytoalexins
Kievitone and phaseollidin.
Pisatin and maackiain.
CONCLUSIONS AND FUTURE DIRECTIONS
ACKNOWLEDGMENTS
REFERENCES
SUMMARY
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Many plants produce low-molecular-weight compounds which inhibit the growth of phytopathogenic fungi in vitro. These compounds may be preformed inhibitors that are present constitutively in healthy plants (also known as phytoanticipins), or they may be synthesized in response to pathogen attack (phytoalexins). Successful pathogens must be able to circumvent or overcome these antifungal defenses, and this review focuses on the significance of fungal resistance to plant antibiotics as a mechanism of pathogenesis. There is increasing evidence that resistance of fungal pathogens to plant antibiotics can be important for pathogenicity, at least for some fungus-plant interactions. This evidence has emerged largely from studies of fungal degradative enzymes and also from experiments in which plants with altered levels of antifungal secondary metabolites were generated. Whereas the emphasis to date has been on degradative mechanisms of resistance of phytopathogenic fungi to antifungal secondary metabolites, in the future we are likely to see a rapid expansion in our knowledge of alternative mechanisms of resistance. These may include membrane efflux systems of the kind associated with multidrug resistance and innate resistance due to insensitivity of the target site. The manipulation of plant biosynthetic pathways to give altered antibiotic profiles will also be valuable in telling us more about the significance of antifungal secondary metabolites for plant defense and clearly has great potential for enhancing disease resistance for commercial purposes.
INTRODUCTION
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Most plants produce antimicrobial secondary metabolites, either as part of their normal program of growth and development or in response to pathogen attack or stress. The possibility that these compounds may protect plants against disease has intrigued biologists since the early part of this century (111, 134). Preformed antifungal compounds that occur constitutively in healthy plants are likely to represent inbuilt chemical barriers to infection and may protect plants against attack by a wide range of potential pathogens (87, 120, 140, 186). In contrast, induced antifungal compounds (phytoalexins) are not present in healthy plants but are synthesized in response to pathogen attack or stress as part of the plant defense response and are restricted to the tissue colonized by the fungus and the cells surrounding the infection site (134, 147).
Clearly, if antimicrobial compounds are likely to influence the growth of fungal pathogens during plant infection, the pathogen must be exposed to effective concentrations of antifungal compounds at the time when fungal growth is arrested. Knowledge of the localization and concentration of these compounds within the plant tissue relative to the location of the invading pathogen is therefore valuable. The properties of some antifungal compounds have allowed them to be visualized (and sometimes quantified) in plants by noninvasive techniques. For example, the UV autofluorescence of the triterpenoid saponin avenacin A-1 has enabled this preformed compound to be localized to the epidermal cell layer of oat roots (Fig. 1A), consistent with a role in protecting the roots against invaders (144), and the pigmented 3-deoxyanthocyanidin flavonoid phytoalexins are synthesized in disease-resistant sorghum lines in response to fungal infection, first accumulating in the cell that is undergoing attack (196, 197) (Fig. 1B). Other antifungal compounds that are not readily detectable by simple microscopy have been visualized by a variety of techniques including histochemical procedures and immunolocalization (77, 93, 117). One of the most elegant examples of in situ localization of a phytoalexin involves analysis of the distribution of elemental sulfur (S8) in the vascular tissue of resistant cocoa (Theobroma cacao) genotypes in response to infection by the wilt fungus, Verticillium dahliae, by coupled scanning electron microscopy and energy-dispersive X-ray microanalysis (29) (Fig. 1C). Elemental sulfur is one of the oldest known fungicides (212). Recently it has also been shown to accumulate in tomato plants in response to challenge with V. dahliae and in tobacco leaves undergoing the hypersensitive response following inoculation with the bacterial pathogen Pseudomonas syringae pv. syringae, suggesting that elemental sulfur may have widespread significance as an antimicrobial phytoprotectant (30).
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Since the growth of a successful pathogen is not arrested by antifungal compounds during infection of its host plant, pathogens must have strategies for circumventing or countering the effects of these compounds. Preformed antifungal compounds are commonly sequestered in vacuoles or organelles of healthy plants, and so necrotrophic pathogens may be expected to encounter fungitoxic levels of these compounds because they cause extensive tissue damage. However, there is also some evidence that preformed antifungal compounds may also affect the growth of biotrophic pathogens during infection of plants (126). Phytoalexin induction may be avoided or delayed by evading recognition by the surveillance system of the host plant. There is also evidence that fungi may produce molecules that suppress plant defense responses including phytoalexin biosynthesis (94, 191, 237). Inevitably, some fungal pathogens will be exposed directly to antifungal compounds during infection of plants and so must be able to tolerate or combat the toxic effects of these compounds. Strategies may include the production of degradative enzymes, innate resistance of the target site, or efflux mechanisms that prevent intracellular antifungal compounds from building up to toxic levels (141, 220). There have been a number of comprehensive reviews on antifungal compounds in plants (11, 17, 73, 87, 101, 102, 120, 139, 140, 186, 192). This review focuses on recent developments in our knowledge of mechanisms of resistance to antimicrobial compounds in phytopathogenic fungi and on the evidence for and against a role for antifungal compounds in plant defense.
PREFORMED ANTIFUNGAL COMPOUNDS
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The term "phytoanticipin" has been proposed to distinguish preformed antimicrobial compounds from phytoalexins (216). Some secondary metabolites, such as cyanogenic glycosides, glucosinolates, and some saponins, are stored in plant cells as inactive precursors but are readily converted into biologically active antibiotics by plant enzymes in response to pathogen attack. These compounds can also be regarded essentially as "preformed," since the plant enzymes that activate them are already present in healthy plant tissue but are separated from their substrates by compartmentalization, enabling rapid activation without a requirement for the transcription of new gene products (216). Although preformed inhibitors are, by definition, present in healthy plants at levels that are anticipated to be antimicrobial, their levels may increase further in response to challenge by pathogens (22, 165). Some antifungal compounds may be present constitutively in one part of a plant but induced as phytoalexins in other organs (24, 82, 216). Numerous constitutive plant compounds have been reported to have antifungal activity in vitro and so have been implicated as antimicrobial phytoprotectants (73, 87, 120, 139, 140, 186, 220). For some of these compounds, their significance in determining the outcome of encounters between potential fungal pathogens and plants has been investigated in detail and is considered below.
Saponins
Structure and biological activity.
Saponins are
glycosylated triterpenoid, steroid, or steroidal alkaloid molecules
which occur constitutively in a great many plant species and which
often have antifungal activity (85, 139, 161). These
molecules have an oligosaccharide chain, attached at the C-3 position,
which may consist of up to five sugar molecules, usually glucose,
arabinose, glucuronic acid, xylose, or rhamnose (85). Some
saponins also have an additional sugar moiety (normally one glucose) at
C-26 or C-28. Examples of saponins that have been studied in relation
to their potential role in plant defense against attack by
phytopathogenic fungi are shown in Fig.
2. Avenacin A-1 from oat roots (a
triterpenoid) and the steroidal glycoalkaloids 
-tomatine and
-chaconine (from tomato and potato, respectively) all have a single
sugar chain attached to C-3. The steroidal oat leaf saponins
avenacosides A and B both have two sugar chains, one at C-3 and one at
C-26 (206, 207). Avenacosides A and B are biologically
inactive but are converted into antifungal 26-desglucoavenacosides in
response to tissue damage or pathogen attack by a plant glucosyl hydrolase that is specific for the C-26 glucose molecule (75, 76).
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Resistance of fungal pathogens.
Fungi that infect
saponin-containing plants are often more tolerant of host plant
saponins in vitro than are nonpathogens of these plants, suggesting
that saponin resistance is a prerequisite for infection (9, 23,
34, 116, 143, 182, 199, 200, 211). Mechanisms of saponin
resistance may vary. The resistance of Oomycete pathogens such as
Pythium and Phytophthora to saponins has been
associated with the lack of membrane sterols in these fungi
(9). The importance of membrane composition is further emphasized by the isolation of sterol-deficient mutants of
Neurospora crassa and Fusarium solani with
increased resistance to the steroidal glycoalkaloid -tomatine
(36, 190). Sterol-deficient F. solani mutants are
able to infect the -tomatine-rich green fruits of tomato, while the
wild type is pathogenic only to the ripe fruits (which contain low
levels of the saponin), indicating that resistance to -tomatine may
be important for pathogens of tomato (36, 37). Whereas
saponin resistance can be conferred by nondegradative mechanisms, a
number of phytopathogenic fungi degrade the saponins of their
respective host plants, usually by hydrolysis of sugar molecules from
the sugar chain attached to C-3 of the saponin backbone (139,
220). Research on enzymatic degradation of saponins by fungi has
focused on pathogens of oat and of solanaceous plants and is considered
in greater depth below.
(i) Degradation of oat saponins.
The importance of
saponin detoxification has been demonstrated for the oat root-infecting
pathogen Gaeumannomyces graminis var. avenae,
which encounters the triterpenoid avenacin saponins. This fungus
produces the extracellular enzyme avenacinase, which detoxifies
avenacins by removal of the terminal D-glucose molecules from the sugar chains (34, 143, 211). Avenacinase is a
-glucosyl hydrolase and is related to fungal cellobiose-degrading
enzymes and xylosyl hydrolases (18, 123, 142, 155). Fungal
mutants that are specifically defective in the ability to produce
avenacinase have been generated by targeted gene disruption and shown
to be unable to infect oats, indicating that avenacinase is an
essential determinant of host range for G. graminis var.
avenae (18). Avenacin detoxification is not
unique to G. graminis var. avenae and has been
described for another oat pathogen, Fusarium avenaceum (34). A survey of a collection of fungi isolated from the
roots of field-grown oat plants has indicated that the ability to
hydrolyze sugars from avenacins is widespread among a variety of fungi
belonging to different taxonomic groups (23) and may
represent a common resistance mechanism for fungi that inhabit oat roots.
(ii) Degradation of steroidal glycoalkaloids of solanaceous
plants.
Steroidal glycoalkaloids are found primarily in members of
the family Solanaceae, which include the major crops tomato
and potato. Tomato plants contain -tomatine, which has a
tetrasaccharide group consisting of two molecules of
D-glucose and one each of D-galactose and
D-xylose (-lycotetraose) attached to C-3 (Fig. 2).
Assuming a uniform distribution, the concentration of -tomatine in
tomato leaves is estimated to be around 1 mM (8), which is
adequate to inhibit the growth of nonpathogens of tomato in vitro
(8, 182). Thus, this saponin may be expected to contribute to the protection of tomato leaves against attack by
-tomatine-sensitive fungi. A number of pathogens of tomato produce
enzymes that detoxify -tomatine, generally by the removal of sugars
from the C-3 sugar chain. These include Septoria
lycopersici, Botrytis cinerea, Fusarium oxysporum f. sp. lycopersici, Verticillium
albo-atrum, and Alternaria solani (reviewed in
reference 139). More recently, an extensive survey
of a wider collection of fungi has indicated that the ability to
hydrolyze sugars from -tomatine is common among tomato pathogens (182). The degradation of -tomatine by S. lycopersici, B. cinerea, and F. oxysporum f.
sp. lycopersici (Fig. 4) has
been investigated in detail, although the significance of this process
for pathogenicity of these different fungi to tomato has not yet been
established.
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-1,2-linked D-glucose molecule from the tetrasaccharide
moiety of the saponin to give 2-tomatine (7, 53,
142, 181). Although G. graminis var. avenae
avenacinase and S. lycopersici tomatinase enzymes are
specific for their respective host saponins, both enzymes hydrolyze the
terminal -1,2-linked D-glucose molecule from their substrates and so have similar mechanisms of action (142)
(Fig. 4). Comparison of the properties of the two enzymes and the
isolation of the DNA encoding tomatinase has established that
tomatinase also belongs to the same family of -glucosyl hydrolases
as the G. graminis avenacinase enzyme (142).
The broad-host-range necrotroph B. cinerea also infects
tomato leaves, causing grey mold disease. There are various reports describing different mechanisms of degradation of -tomatine by different B. cinerea isolates, including the removal of the
intact -lycotetraose group (221) and conversion of
-tomatine to an unidentified, less polar compound which still
contains the -lycotetraose group (214). Quidde et al.
(173), however, found that B. cinerea isolates
from a number of different plants degraded -tomatine by removal of
the terminal D-xylose molecule to give
1-tomatine (Fig. 4). A B. cinerea xylosyl
hydrolase that degrades -tomatine has been purified
(173), but its relationship to other fungal glycosyl
hydrolases is unclear because the gene encoding the enzyme has not yet
been cloned.
In contrast to S. lycopersici and B. cinerea, the
vascular wilt fungus F. oxysporum f. sp.
lycopersici grows mainly in the roots and stems of tomato
plants and is likely to encounter lower levels of -tomatine than
those experienced by necrotrophic foliar pathogens of tomato
(176). Nevertheless, a comparison of the resistance of
F. oxysporum isolates has indicated that nonpathogens of
tomato are generally sensitive to -tomatine while highly pathogenic F. oxysporum f. sp. lycopersici isolates show
relatively high tolerance, leading to the suggestion that a threshold
level of -tomatine tolerance is required for pathogenicity to tomato
(200). F. oxysporum f. sp. lycopersici
produces an inducible extracellular tomatinase activity which
detoxifies -tomatine by cleaving the glycoalkaloid into the
tetrasaccharide lycotetraose and the aglycone tomatidine (58,
103) (Fig. 4). The cDNA encoding F. oxysporum f. sp.
lycopersici tomatinase has now been obtained by screening a
cDNA expression library with anti-tomatinase antisera, and its identity
has been confirmed by expression in Escherichia coli (180). The cloned DNA does not have homology to the family
of saponin glucosyl hydrolases which contains G. graminis
var. avenae avenacinase and S. lycopersici
tomatinase, but it does show relatedness to xylanases. Some isolates of
F. solani also hydrolyze -tomatine to give the aglycone
and -lycotetraose, but this tomatinase activity differs from the
F. oxysporum f. sp. lycopersici enzyme in
molecular mass and immunological properties (104).
Pathogens of potato are also likely to encounter a variety of
antifungal compounds, including the steroidal glycoalkaloids -chaconine (Fig. 2) and -solanine. Gibberella
pulicaris, which causes storage rot of potato tubers, can
metabolize both of these steroidal glycoalkaloids (227), and
an enzyme capable of degrading -chaconine to
2-chaconine by removing the terminal -1,2-linked L-rhamnose molecule has been purified from this fungus
(16). Removal of either of the rhamnose molecules from
-chaconine destroys the ability of -chaconine to disrupt
membranes and so is likely to represent a detoxification event
(96, 177), although the importance of -chaconine
degradation for pathogenicity of G. pulicaris to potato has
not yet been assessed by the generation of chaconinase-minus mutants.
Although G. pulicaris is rarely isolated from tomato plants,
it is also able to hydrolyze -lycotetraose from -tomatine to give
tomatidine, in the same way as F. oxysporum f. sp.
lycopersici (228). The G. pulicaris
tomatinase gene has been isolated by transforming a cosmid library of
G. pulicaris DNA into Aspergillus nidulans and
screening for the ability to metabolize -tomatine. DNA sequence
analysis indicates that the predicted gene product, like F. oxysporum f. sp. lycopersici tomatinase, is closely
related to xylanases (225).
Cyanogenic Glycosides and Glucosinolates
Cyanogenic glycosides are found in over 200 plant species including gymnosperms, ferns, monocots, and dicots (35). They are synthesized by the conversion of amino acid precursors to oximes, which are then glycosylated (86). In healthy plants, cyanogenic glycosides are separated by compartmentalization from enzymes that catalyze their degradation. In response to tissue damage, these glycosides are broken down to release hydrogen cyanide and an aldehyde or ketone (35, 159) (Fig. 5A). The generation of hydrogen cyanide, a potent respiratory poison, may represent a defense mechanism that protects cyanogenic plants against pathogens and herbivores (62, 86). Fungi that infect these plants are generally able to tolerate hydrogen cyanide, and tolerance mechanisms may include cyanide-resistant respiration (110, 156) or enzymatic detoxification (63). The association between the ability to produce the cyanide-detoxifying enzyme cyanide hydratase and the ability to infect cyanogenic plants has been tested for the fungus Gloeosporioides sorghi, which is a pathogen of the cyanogenic plant sorghum (220, 223). Cyanide hydratase-deficient mutants of G. sorghi generated by targeted gene disruption were more sensitive than wild-type fungi to hydrogen cyanide in vitro, confirming that the enzyme could confer resistance to hydrogen cyanide. Pathogenicity to sorghum, however, was unaffected, indicating either that the ability to tolerate hydrogen cyanide is not required for infection of sorghum by G. sorghi or that the fungus has some alternative means of cyanide tolerance which protects it during growth in sorghum tissue.
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Glucosinolates are sulfur-containing glucosides that are found in
dicots, including members of the Brassica genus and the cruciferous weed Arabidopsis thaliana (25, 52,
56). These compounds can be subdivided into three major classes
determined by the nature of their side chains, which may be derived
from aliphatic, indolyl, or aralkyl -amino acids (Fig. 5B). There are a number of similarities between cyanogenic glycosides and glucosinolates. Both classes of compound are synthesized from amino
acids via oxime intermediates, and it has been suggested that some of
the biosynthetic steps may be carried out by homologous enzymes
(12, 79, 160). Glucosinolates, like cyanogenic glycosides, are activated by plant enzymes in response to tissue damage or pathogen
attack (56) and have been implicated in defense against pests and pathogens (25, 66, 132). Activation involves the plant thioglucosidase myrosinase, and degradation gives rise to a
variety of products including isothiocyanates, nitriles, and thiocyanates (Fig. 5B). Interestingly, myrosinase belongs to the same
family of glucosyl hydrolases as linamarinase, which activates cyanogenic glycosides. This family also includes enzymes that activate
saponins with two sugar chains, such as the oat avenacoside saponins
(75, 76, 88, 108, 145). Glucosinolates are likely to be
localized in the vacuole, while myrosinase is believed to be
sequestered in specialized "myrosin" cells, although recent experiments involving the immunological localization of the
glucosinolate sinigrin and myrosinase in Brassica juncea
indicate that myrosinase not only is present in myrosin granules but
also may be colocalised with its substrate in protein bodies
(93).
The toxicity of isothiocyanates (the major glucosinolate breakdown products generated in Brassica), and of other products of glucosinolate hydrolysis to a range of fungi (including some Brassica pathogens) has been demonstrated, but the mechanism of toxicity is not known (25, 27, 74, 97, 124, 131, 133, 195). The development of a series of Brassica napus lines with contrasting glucosinolate profiles and variable total glucosinolate content has allowed the contribution of glucosinolates to protection against pests and fungal pathogens to be assessed (66, 67). These differences in glucosinolate content had significant effects on Brassica-herbivore interactions: increases in the levels of specific glucosinolates increased damage caused by specialist pests and reduced the extent of grazing by generalists (66). However, enhanced levels of glucosinolates were not associated with correspondingly high levels of resistance to Brassica pathogens and may even have led to increased susceptibility (67). This is perhaps not surprising, since these pathogens are likely to have become adapted to tolerate glucosinolate breakdown products. Whether the ability of fungal pathogens of Brassica to tolerate or detoxify the products of glucosinolate hydrolysis is important for pathogenicity is an area that does not appear to have been investigated in detail.
Cyclic Hydroxamic Acids
1,4-Benzoxazinones are cyclic hydroxamic acids that occur constitutively as glucosides in a number of members of the Gramineae (reviewed in reference 135). They are found in all plant parts but occur at higher levels in the vascular bundles (4, 5). In rye the main hydroxamic acid is a glucoside of DIBOA (2,4-dihydroxy-1,4-benzoxazin-3-one), whereas in maize and wheat it is the glucoside of the methoxylated form, DIMBOA (2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one) (Fig. 6A). These compounds are not found in rice, barley, or oats (135). The glucosides are hydrolyzed in response to infection or physical damage to produce the aglycones DIBOA and DIMBOA, which in turn decompose rapidly to the benzoxazolinones, 2-benzoxazolinone (BOA) and 6-methoxy-2-benzoxazolinone (MBOA), respectively, with liberation of formic acid (84, 230) (Fig. 6). The benzoxazinone aglycones and their degradation products exhibit fungistatic and bacteriostatic activity, as well as antifeeding activity against insects, whereas the parent glucosides are essentially inactive (135). The concentrations of DIMBOA and DIBOA glucosides are highest in young seedlings a few days after germination and then decrease, suggesting that the benzoxazinones act as preformed defense compounds in the juvenile stages of growth (4, 89). They may also act as phytoalexins in certain interactions (22).
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Benzoxazinones and benzoxazolinones are inhibitory to a number of fungal pathogens of plants, including Helminthosporium turcicum (31), Stagonospora nodorum (13), Microdochium nivale (222), Fusarium moniliforme (175, 229), Fusarium culmorum (61), and Gaeumannomyces graminis (61). Some isolates of G. graminis, F. culmorum, F. moniliforme, F. subglutinans, and of a number of other Fusarium species are able to degrade benzoxazolinone compounds to products which are less inhibitory to fungal growth (60, 61, 175, 233). The primary degradation products are N-(2-hydroxyphenyl)malonamic acid and N-(2-hydroxy-4-methoxyphenyl)malonamic acid, derived from BOA and MBOA, respectively, although 2-amino-3H-phenoxazin-3-one has been identified as an additional BOA degradation product generated by G. graminis (60, 61, 233) (Fig. 6B). Thus, it appears that a variety of grass pathogens may use common mechanisms for detoxification of benzoxazolinones (60, 61). A detailed investigation of the mechanism of degradation of benzoxazolinones by an F. subglutinans isolate has indicated that the first metabolization step of both MBOA and BOA involves the cleavage of the NH---C==O bond, leading to the formation of an o-aminophenol intermediate. The aminophenol is then converted to the corresponding malonamic acid by an N-malonyltransferase (60) (Fig. 6B).
It is not yet known whether these fungal degradative enzymes are
important for infection of plants that produce benzoxazinones. However,
benzoxazineless (bx1) maize mutants that are
unable to synthesize DIMBOA are more susceptible to insect and pathogen attack (81), indicating that these antimicrobial compounds
do play a protective role. The BX1 gene has been cloned from
maize by using the Mutator transposon-tagging system and
found to encode a tryptophan synthase homologue which is not
required for normal growth of maize (59). This enzyme
catalyzes the conversion of indole-3-glycerol phosphate to indole and
represents the first committed step toward DIBOA and DIMBOA
biosynthesis. Four maize cytochrome P-450-dependent monooxygenase genes
BX2, BX3, BX4, and BX5,
belonging to the CYP71C subfamily, have also been isolated, and their products have been shown to catalyze the sequential conversion of indole-3-phosphate to DIBOA (59). Remarkably, BX1 to BX5 are all clustered on the same arm of
one maize chromosome, representing the first example of clustered genes
for secondary metabolism in plants. The transferral of this relatively
short pathway into other plants offers exciting challenges for
metabolic engineering for improved disease resistance.
Antifungal Compounds and Fruit Ripening
The resistance of unripe fruits to fungal decay has been associated with the presence of preformed antifungal compounds in the peel (164, 165, 201). Pathogens often infect unripe fruits but then remain quiescent, with the onset of decay coinciding with decreases in the concentrations of antifungal compounds to subtoxic levels as the fruit ripens. Thus, quiescence may represent a mechanism for avoiding toxic levels of antifungal plant compounds. This area has been studied in particular detail for interactions involving Colletotrichum gloeosporioides and the subtropical fruits mango and avocado. The peel of unripe mango fruit contains a mixture of the antifungal 5-alkylated resorcinols 5-12-cis-heptadecenyl resorcinol and 5-pentadecyl resorcinol (51), while avocado peel contains antifungal monoenes and dienes (1-acetoxy-2,4-dihydroxy-n-heptadeca-16-ene and 1-acetoxy-2-hydroxy-4-oxo-heneicosa-12,15-diene) (167, 168) (Fig. 7). The levels of these compounds decrease during fruit ripening, and this decrease occurs more rapidly in disease-susceptible cultivars, suggesting that the presence of inhibitory levels of these antifungal substances in the peel of unripe fruit may arrest fungal growth and cause latency (51, 168, 170).
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The levels of antifungal diene in peel of unripe avocados are subject to complex regulation and may be modulated by lipoxygenase, for which the diene is a substrate (166), and also by the flavan-3-ol epicatechin, an inhibitor of lipoxygenase (3, 169). Lipoxygenase activity increases during fruit ripening, while epicatechin levels decline, suggesting that these events are linked to the decrease in diene concentrations. In freshly harvested unripe avocado fruits, diene concentrations can be further enhanced by a variety of biotic and abiotic treatments including challenge with C. gloeosporioides, wounding, irradiation, exposure to ethylene (at levels that do not induce ripening) or carbon dioxide, and treatment with lipoxygenase inhibitors (163, 165, 169, 171, 172). Treatment with either carbon dioxide or lipoxygenase inhibitors results in increased disease resistance (169, 171), offering potential strategies for the manipulation of fruit physiology for control of postharvest diseases. Interestingly, inoculation of freshly harvested avocado fruit with a nonpathogenic mutant strain of Colletotrichum magna also confers protection against C. gloeosporioides, possibly by the induction of epicatechin and modulation of the level of the antifungal diene (162). Taken together, this evidence suggests that at least for the avocado-C. gloeosporioides interaction, preformed antifungal compounds may contribute to the resistance of unripe fruits to decay.
PHYTOALEXINS
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Phytoalexins are a group of structurally diverse molecules that are generally lipophilic, nonspecific in their antifungal activity, and not particularly potent (73, 192). The mechanisms of antimicrobial action of phytoalexins are not well understood. The basis of their toxicity is likely to involve disruption of membranes, although a variety of physiological and biochemical processes other than changes in membrane permeability may also be affected (179, 192). In contrast to preformed antifungal compounds, phytoalexins are not present in healthy plant tissue and are synthesized from remote precursors in response to pathogen attack or stress, probably as a result of de novo synthesis of enzymes. The accumulation of phytoalexins represents one of an array of induced defense responses associated with plant disease resistance (49, 105). Although both disease-resistant and -susceptible plants may respond to pathogen attack by producing phytoalexins, these compounds generally accumulate more rapidly and to higher levels in resistant plants. Clear correlations between tolerance of host plant phytoalexins in vitro and pathogenicity have been demonstrated for a number of phytopathogenic fungi, and the discovery that many of these fungi are able to metabolize phytoalexins has focused attention on the importance of phytoalexins in restricting the growth of potential pathogens (217, 218). Considerable progress has been made in elucidating the contribution of phytoalexin degradation to fungal pathogenesis, and this part of the review concentrates on plant-pathogen interactions that have been investigated in the most detail in this respect.
Stilbenes
The leaves and fruits of grapevines synthesize a group of related phenolics in response to fungal infection and abiotic treatment. These molecules belong to a group of stilbenes that also occur constitutively in a number of herbaceous and woody plants and which have been postulated to play a role in disease resistance (82, 83). Fungal challenge of vine leaves and berries results in the production of resveratrol (trans-3,5,4'-trihydroxystilbene) and related compounds which have antifungal activity toward a number of fungal pathogens, including Rhizopus stolonifer, Plasmopara viticola, and B. cinerea (Fig. 8) (1, 90, 106, 183).
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There are a number of indications that stilbenes may contribute to disease resistance in grapevine. There are positive correlations between stilbene production and resistance of vine varieties to fungal attack (42, 106, 183). Furthermore, the ability of B. cinerea to infect grapevine has been associated with its capacity to degrade stilbene phytoalexins (184) and laccase-mediated oxidation of resveratrol by a number of enzymes has been described (2, 19, 121, 122, 157, 158). Laccases are polyphenol oxidases that act on a variety of polyphenol substrates and that have been implicated in a wide range of biological processes (205). The contribution of the B. cinerea laccases to stilbene detoxification and to pathogenicity remains to be determined. However, evidence that stilbenes do protect plants against attack by fungal pathogens comes from experiments in which expression of resveratrol synthase from grapevine in a number of other plant species increased disease resistance (78, 107, 198, 204).
Potato Phytoalexins
During infection of potato tubers, the dry rot fungus G. pulicaris is likely to encounter not only the preformed steroidal glycoalkaloids but also phenolics such as chlorogenic acid, caffeic acid, and scopoletin, as well as a number of sesquiterpenes. The levels of many of these compounds increase in response to infection with G. pulicaris (47, 100, 174). The sesquiterpenes rishitin, lubimin, and solavetivone are the major phytoalexins that accumulate in potato tubers in response to fungal infection (47, 100). The relationship between resistance to rishitin and lubimin (Fig. 9) and pathogenicity of G. pulicaris to potato has been investigated in detail and has provided good evidence to indicate that high levels of pathogenicity are associated with tolerance to both lubimin and rishitin (43, 45, 46, 226) and that degradative mechanisms may be the basis of tolerance (43-46). The ability to tolerate and metabolize rishitin is associated with two independent loci (RIM1 and RIM2), only one of which (RIM1) is linked to pathogenicity (44). Genetic analysis of the association between lubimin resistance and pathogenicity has not been carried out because of the lack of fertile lubimin-sensitive isolates.
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Analysis of the mechanisms of phytoalexin metabolism by G. pulicaris has involved only a few isolates. A rishitin-tolerant isolate degraded rishitin to 11,12-epoxyrishitin (Fig. 9), which was then rapidly broken down to uncharacterized products (64), while a rishitin-sensitive isolate was unable to metabolize rishitin but was tolerant of and could degrade 11,12-epoxyrishitin. Thus, it is not clear whether the initial conversion of rishitin to 11,12-epoxyrishitin represents a detoxification step or whether detoxification occurs as a consequence of the breakdown of 11,12-epoxyrishitin to other products. A lubimin-metabolizing isolate converted lubimin to isolubimin via intermediates (45) (Fig. 9). Isolubimin, however, is still toxic to G. pulicaris and was further metabolized to a nontoxic tricyclic compound, cyclodehydroisolubimin. This was subsequently processed to other nontoxic metabolites including 11,12-epoxides (45, 46). It appears that epoxidization, which may be crucial for rishitin detoxification, is of only minor significance for lubimin detoxification. A lubimin-sensitive isolate could also convert lubimin to isolubimin but was unable to process this toxic metabolite further. Since these studies have involved only a very limited number of isolates, it is possible that other pathogenic strains of G. pulicaris degrade rishitin and lubimin in different ways. The cloning and subsequent mutation of genes such as RIM1, which presumably encode phytoalexin-detoxifying enzymes, will allow the importance of these degradative processes for pathogenicity to be assessed.
Crucifer Phytoalexins
The resistance of the wild crucifers Camelina sativa (false flax) and Capsella bursa-pastoris (shepherds purse) to different Brassica pathogens including Alternaria brassicae has been associated with the production of phytoalexins (27, 28, 91, 92). Purification and structure elucidation of phytoalexins following challenge with fungal pathogens revealed that both of these plants produce the thiazoyl-substituted indole camalexin (Fig. 10A) as the major antifungal compound, as well as smaller quantities of a related compound, 6-methoxycamalexin (21, 27, 92). C. bursa-pastoris also produces the minor metabolite N-methylcamalexin (92). Toxicity tests with Cladosporium sp. indicate that camalexin is more toxic to this fungus than is 6-methoxycamalexin (10). Camalexin and related compounds are structurally similar to the synthetic systemic fungicide thiabendazole, which is used extensively for control of plant diseases (21). While camalexin and 6-methoxycamalexin are not present in healthy leaves of C. sativa, they do occur in uninoculated roots, and their levels increase in response to inoculation with the root rot fungus Rhizoctonia solani (27). Leptosphaeria maculans (anamorph Phoma lingam) and A. brassicae are apparently unable to metabolize camalexin in vitro, but R. solani converts this phytoalexin to the less toxic 5-hydroxycamalexin (Fig. 10A) (150-152). Although camalexin detoxification may contribute to the pathogenicity of R. solani to C. sativa, correlations between detoxification and pathogenicity have not yet been established.
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Arabidopsis thaliana also synthesises camalexin on challenge with bacterial and fungal pathogens, and this appears to be the only phytoalexin produced by this plant (208). The amenability of A. thaliana to phytopathological studies and to molecular genetics has established it as a model host for the dissection of plant defense mechanisms. A number of mutants of A. thaliana that are defective in camalexin biosynthesis have been isolated (69-71). These mutants are known as pad (for "phytoalexin-deficient") mutants, and they define five complementation groups representing the genes PAD1 to PAD5. PAD1, PAD2, PAD3, and PAD4 are all required for full resistance to avirulent isolates of the downy mildew fungus Peronospora parasitica, with some combinations of double mutants showing additive effects on susceptibility (71). The pad3 mutant is more susceptible to another fungal pathogen, Alternaria brassicicola (203), but not to Botrytis cinerea (20). This mutant is highly likely to be defective in the production of a camalexin biosynthesis enzyme. The PAD3 gene has recently been cloned and is predicted to encode a cytochrome P-450-dependent monooxygenase belonging to the same family as the maize enzymes involved in the synthesis of DIBOA, another secondary metabolite derived from indole (235). Some of the other pad mutants may have pleiotropic defects in defense responses in addition to phytoalexin deficiency. This is certainly the case for PAD4, which plays a central role in defense-related signal transduction (70, 236). Nevertheless, the increased susceptibility of pad3 to P. parasitica and A. brassicicola indicates that camalexin probably does contribute to the resistance of A. thaliana to at least some pathogens.
Cultivated Brassica species such as Brassica rapa and Brassica napus produce a different group of sulfur-containing phytoalexins belonging to the brassinin family following challenge with pathogens (reviewed in reference 151). Brassinin consists of an indole ring linked to a dithiocarbamate moiety (Fig. 10B). A number of reports describe the metabolism of brassinin and related phytoalexins by L. maculans, although the significance of these chemical conversions for pathogenicity has not been established. L. maculans can metabolize brassinin (148, 154), brassicanal A (149), brassilexin (151), and cyclobrassinin (153). With the exception of brassinin, however, the rates of metabolism are low, making it unlikely that degradation of these other phytoalexins constitutes a major detoxification mechanism. Brassinin is detoxified in vitro by oxidation of the thiocarbamate group to produce brassinin-S-oxide, which is considerably less toxic to L. maculans than is brassinin (Fig. 10B) (148). Brassinin-S-oxide is subsequently processed to other molecules including indole-3-carboxaldehyde and indole-3-carboxylic acid (148). The rapid conversion of brassinin to less toxic molecules suggests that this detoxification may have relevance for fungal pathogenicity, although further biochemical and genetic evidence is required before any definitive conclusions can be made.
Legume Phytoalexins
Kievitone and phaseollidin. Kievitone and phaseollidin are isoflavonoid phytoalexins that are produced by the legume Phaseolus vulgaris (French bean) and can, along with other bean phytoalexins, be detoxified by the pathogen Fusarium solani f. sp. phaseoli (193, 234). The detoxification of both of these phytoalexins involves hydration of a double bond of the allyl group linked to the isoflavonoid moiety (Fig. 11A). Whereas some isolates of Fusarium that are not pathogenic to bean have kievitone hydratase activity, all isolates that are highly pathogenic to bean have this enzyme activity, suggesting a link between kievitone degradation and ability to infect this host (194). The association between phaseollidin degradation and pathogenicity to bean is less clear. Although a single pathogenic isolate of F. solani has both kievitone and phaseollidin hydratase activities, it is not known whether this is true of all isolates that are pathogenic to bean. The phaseollidin hydratase enzyme has been purified, but the gene encoding the enzyme has not yet been cloned (209, 210). The kievitone hydratase gene has been isolated from F. solani (109), and its identity has been confirmed by heterologous expression in Neurospora crassa and Aspergillus nidulans. It should now be possible to directly test the importance of kievitone detoxification in pathogenicity.
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Pisatin and maackiain. Isolates of Nectria haematococca mating-population VI (MPVI) (anamorph Fusarium solani) infect a number of different plants including pea (Pisum sativum) and chickpea (Cicer arietinum) (215). Although some isolates are pathogenic to both pea and chickpea, the ability to cause disease on these two hosts is not necessarily correlated (215). Both of these plants produce isoflavonoid phytoalexins; pea produces pisatin, while chickpea produces maackiain and medicarpin. Extensive characterization of field isolates of N. haematococca MPVI from diverse sources has revealed strong correlations between pathogenicity and the ability to detoxify legume phytoalexins, implying that phytoalexin detoxification contributes to pathogenicity (114, 217, 219).
Isolates of N. haematococca MPVI that are pathogenic to pea can detoxify pisatin by cytochrome P-450-mediated demethylation to 6(a)-hydroxymaackiain (125) (Fig. 11B). Natural isolates can be divided into three groups on the basis of pisatin-demethylating ability. Some isolates are unable to detoxify pisatin (Pda
), some produce low levels of pisatin demethylase
activity after prolonged exposure to pisatin (PdaL), and
others are capable of rapid pisatin-induced production of moderate to
high levels of pisatin demethylase activity (PdaH)
(118, 224). A total of six pisatin demethylase
(PDA) genes have been identified by genetic analysis. These
include three PDAL genes and three
PDAH genes (217, 224). The products
of all these genes have similar biochemical properties, and the major
difference between the two classes seems to be in their expression
patterns (65). High levels of pathogenicity to pea are
associated with the PdaH phenotype, suggesting that
effective detoxification of pisatin contributes to the ability to cause
disease on this plant (217). Further evidence to support
this has come from the demonstration that the introduction of a cloned
PDAH gene into Pda isolates of
N. haematococca MPVI or into other fungal pathogens can
enhance the ability to cause lesions on pea (15, 26, 185). Despite this, recent experiments indicate that pisatin detoxification makes only a relatively minor contribution to pathogenicity. Mutants of
highly pathogenic isolates that have undergone targeted disruption of
the PDA1 gene (a PDAH-type gene) have
an increased level of sensitivity to pisatin that is comparable to that
of a naturally occurring Pda isolate of N. haematococca MPVI. However, these mutants show only a moderate
reduction in pathogenicity and are still considerably more pathogenic
than naturally occurring Pda isolates (224).
PDA1 is located on a conditionally dispensable 1.6-Mb
chromosome (128). In contrast to mutants that are
specifically defective in Pda1, transformants that have lost the entire
1.6-Mb dispensable chromosome harboring the PDA1 gene or
that have undergone deletion of a 100-kb chromosomal fragment flanking
this gene have clearly reduced pathogenicity. This reduced level of
pathogenicity is comparable to that of Pda isolates,
indicating that other genes on the 1.6-Mb chromosome in addition to the
PDA1 gene are required for full pathogenicity to pea
(98, 224). These genes do not appear to be required for
resistance to pisatin in vitro, and their function is as yet unknown
(224).
Very similar experiments have been performed to determine the
importance of phytoalexin detoxification for pathogenicity of the same
fungus to chickpea. Maackiain and medicarpin are believed to be
detoxified by the same enzymes, but only maackian detoxification has
been examined in detail (33, 114, 130). Four genes for maackiain detoxification have been identified in N. haematococca MPVI (MAK1 to MAK4) (33,
129, 130). Mak1 and Mak2 convert maackiain to
1(a)-hydroxymaackiain (Fig. 11C), Mak3 converts this phytoalexin to
6(a)-hydroxymaackiain, and the products of degradation by Mak4 are
unknown. 1(a)-hydroxymaackiain and 6(a)-hydroxymaackiain are both less
toxic to fungal growth than is maackiain (40). The
MAK1 and MAK2 genes are associated with high
pathogenicity to chickpea (130). MAK1 has been
cloned and encodes a predicted flavin adenine dinucleotide-binding
monoxygenase (33). This gene, like the PDA1
genes, is located on a conditionally dispensable chromosome (32,
33, 130). Targeted disruption of the MAK1 gene gave
increased maackiain sensitivity (to levels which were comparable to
those of naturally occurring Mak isolates)
(55). Mutants generated in this way showed a moderate reduction in pathogenicity to chickpea but were still substantially more pathogenic than naturally occurring Mak isolates.
Unlike the PDA1 experiments, chemically induced loss of the
1.6-Mb dispensable MAK1 chromosome did not result in a further reduction in pathogenicity. Transformation of a naturally occurring Mak isolate with the MAK1 gene
conferred both resistance to maackiain and increased pathogenicity to
chickpea, providing further evidence that maackiain detoxification does
contribute to pathogenicity. Taken together, these studies of pea- and
chickpea-infecting strains of N. haematococca indicate that
phytoalexin detoxification contributes to but is not the sole
determinant of pathogenicity of N. haematococca to its
legume hosts.
CONCLUSIONS AND FUTURE DIRECTIONS
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It is clear that pathogens of plants that produce antimicrobial compounds are often more tolerant of these compounds in vitro than are nonpathogens of these plants, presenting us with the tantalizing hypothesis that resistance to antimicrobial phytoprotectants may be a prerequisite for infection. This is a very simplistic but attractive notion. Obviously, other factors are needed in addition to antibiotic resistance for fungi to be successful pathogens, and the importance of toxins, components of signal transduction pathways, and other pathogenicity determinants is well established (80, 99, 138, 232). However, resistance to antifungal compounds may be a basic requirement for survival in the host plant, and there is increasing evidence to indicate that this is the case, at least for some fungus-plant interactions. This evidence has emerged largely from studies of fungal enzymes that degrade plant antibiotics and also from experiments in which plants with altered levels of antifungal secondary metabolites have been generated.
The demonstration that the root-infecting pathogen Gaeumannomyces graminis requires the saponin-detoxifying enzyme avenacinase for infection of oats has set a precedent for the involvement of saponin-detoxifying enzymes in pathogenesis (18), although the general significance of saponin detoxification for other fungal pathogens is not yet known. The increased disease susceptibility of oat variants lacking avenacins adds further support to the importance of saponin resistance for fungal pathogenesis and to the notion that saponins play a role as preformed antifungal phytoprotectants. Similarly, although the significance of degradation of cyclic hydroxamic acids by cereal and grass pathogens has not yet been tested directly, maize mutants defective in DIMBOA biosynthesis have been isolated and are more susceptible to fungal attack than the wild-type maize line (59, 81). This implies that cyclic hydroxamic acids also restrict the growth of potential pathogens and that fungal tolerance of these compounds is likely to be important for pathogenesis. It is also clear that the phytoalexin-degrading enzymes produced by pea- and chickpea-attacking isolates of N. haematococca MPVI are required for full pathogenicity, although mutants that are unable to make these enzymes show only a moderate reduction in the ability to cause disease (55, 224). There do not appear to be any reports of the isolation of phytoalexin-deficient mutants of legumes. However, the pad mutants of A. thaliana, at least one of which is likely to be specifically defective in camalexin biosynthesis, do show increased susceptibility to some fungal pathogens (71, 203), providing complementary evidence from the plant side that phytoalexins contribute to disease resistance. There are also other examples from studies of plants in which the levels of antimicrobial compounds have been altered by transformation-mediated manipulation of gene expression with associated effects on resistance to fungal pathogens (54, 78, 119). These experiments provide further evidence to indicate that antimicrobial compounds protect plants against fungal pathogens.
While there has been considerable emphasis on enzymatic degradation of antifungal compounds, nondegradative tolerance mechanisms are also likely to be important in protecting phytopathogenic fungi against host plant antifungal compounds (36, 110). For example, in addition to the production of pisatin demethylase enzymes, N. haematococca MPVI isolates that infect pea have an inducible nondegradative phytoalexin tolerance. This has been attributed to an energy-dependent mechanism that secretes pisatin from mycelium and so may involve membrane transport proteins (39, 41). Membrane transport proteins of the kind associated with multidrug resistance are known to be important for the resistance of bacterial pathogens of animals and plants to host-produced antimicrobial peptides (112, 146). Such proteins may also protect phytopathogenic fungi against plant defense compounds (48). ABC transporter genes whose products have been implicated in phytoalexin resistance have been identified in various filamentous fungi including plant pathogens (38, 113, 187, 213).
While most in vitro studies of the effects of antifungal compounds on
phytopathogenic fungi have involved individual purified compounds, many
fungi are likely to be exposed to a variety of preformed and/or induced
antifungal compounds during infection of their hosts. Resistance to
both -tomatine and phytoalexins may be required for pathogen ingress
and disease development in tomato (200). Similarly, potato
pathogens are likely to be subjected to a battery of antifungal
compounds including steroidal glycoalkaloids, phenolics, and
sesquiterpenes, some of which may have combined or synergistic
activity. The relative contributions of these various compounds to
restricting fungal growth in plants is therefore difficult to evaluate.
It is possible, for example, that the permeabilizing activity of
saponins will predispose invading fungi to the toxic effects of other
antifungal compounds such as phytoalexins.
Although the significance of some fungal enzymes that degrade host plant antifungal compounds for pathogenicity has been tested by the generation of specific mutants, it is clear from this review that many more have been characterized in some detail but their function is not yet known. For some of these enzymes, the kinetic properties and high substrate specificities for host antifungal compounds are consistent with a primary function as detoxifying enzymes. Others have less favorable properties in relation to antimicrobial substrates and may have activities toward other unidentified substrates in the plant. The contributions of these various degradative enzymes to pathogenicity on antibiotic-producing host plants will become clearer as more fungal mutants are generated by targeted gene disruption. To date, the emphasis on mechanisms of resistance of phytopathogenic fungi to antifungal secondary metabolites has been on degradative enzymes. In the future, we are likely to see a rapid expansion in our knowledge of alternative mechanisms of resistance, such as efflux systems of the kind associated with multidrug resistance, innate resistance due to insensitivity of the target site, and novel mechanisms. The manipulation of plant biosynthetic pathways to alter antibiotic profiles will also tell us more about the significance of antifungal secondary metabolites for plant defense and clearly has great potential for enhancing disease resistance for commercial purposes.
ACKNOWLEDGMENTS
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The Sainsbury Laboratory is supported by the Gatsby Charitable Foundation. John Morrissey is supported by BBSRC grant 83/PO7880.
We thank Ralph Nicholson and Charlotte Armah for providing Fig. 1B and 3, respectively. We also thank all those who have generously provided unpublished information and those who have given their critical comments on the manuscript.
FOOTNOTES
* Corresponding author. Mailing address: Sainsbury Laboratory, John Innes Centre, Colney Lane, Norwich NR4 7UH, United Kingdom. Phone: 44 1603 452571. Fax: 44 1603 250025. E-mail: osbourna{at}bbsrc.ac.uk; john.morrissey{at}bbsrc.ac.uk.
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