PATHOGEN QUIESCENCE IN POSTHARVEST DISEASES

Annu. Rev. Phytopathol. 1996.34:413-434. Downloaded from arjournals.annualreviews.org 

by National Medical Library-Jerusalem on 06/26/08. For personal use only. 

Annu. Rev. Phytopathol. 1996. 34:413–34 

Copyright c○ 1996 by Annual Reviews Inc. All rights reserved 

PATHOGEN QUIESCENCE IN 

POSTHARVEST DISEASES 

Dov Prusky 

Department of Postharvest Science of Fresh Produce, Agricultural Research 

Organization, Volcani Center, Bet Dagan 50250, Israel 

KEY WORDS: fruit resistance, induced and preformed resistance 

ABSTRACT 

This chapter examines the quiescence period during different stages of fungal 

attack of postharvest pathogens: quiescence during spore germination and initial 

hyphal development, during and after appressorium formation, and quiescence 

of germinated appressorium and subcuticular hyphae. The different mechanisms 

for quiescence are reviewed: factors affecting quiescence of germinated spores, 

appressoria formation and germination, and fungal colonization. Special emphasis 

is given to mechanisms of quiescence involving fungal colonization: 1. the 

pathogen’s nutritional requirements, 2. preformed antifungal compounds, 3. the 

elicitation of phytoalexins and preformed compounds, and 4. the activation of 

factors in fungal pathogenicity. 

INTRODUCTION 

Fruit and vegetable crops are exposed to a variety of microorganisms, most of 

which do not invade the plant tissue and cause disease. The life cycle of fungal 

pathogens of fruit and vegetables goes through several stages from spores 

landing on the host surface, infection, and the production of decay symptoms. 

Spores must attach to the surface, germinate, produce penetration structures or 

penetrate directly through wounds, and activate pathogenicity factors in order 

for the process of decay to develop. The pathogen must trigger pathogenicity 

factors that macerate host tissues and release the nutrients required to sustain its 

development. To be successful, a pathogen must also be able to overcome host 

defenses and initiate attack under prevailing physiological and environmental 

conditions. Since both the host and the pathogen are living entities, the conditions 

imposed by the host under which pathogenic fungi can start the parasitic 

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414 PRUSKY 

(a) 

(b) 

Figure 1 Possible stages of quiescence during fungal penetration of fruit host by (a) direct or (b) 

wound penetration pathogen. 

relationship depend on the host’s susceptibility to attack by the pathogen and 

its reaction to such attack. Disease symptoms may occur long after the initial 

stages of infection. Verhoeff (105) defined a latent, dormant, or quiescent parasitic 

relationship as a condition in which the pathogen spends long periods 

during the host’s life in a quiescent stage until, under specific circumstances, it 

becomes active. Epidemiologists might refer to the period from spore landing 

until the parasitized tissue produces new spores as a latent period (102). To 

avoid confusion, Swinburne (98) proposed the term “period of quiescence” to 

differentiate the quiescent parasitic relationship from the latent period. Quiescence 

can be enforced during the various processes of fungal attack, which 

suggests that quiescence may or could occur during any of the processes leading 

from fungal germination to colonization (Figure 1). 

Spores of Colletotrichum piperatum on the host surface of Capsicum may 

remain quiescent until they germinate in the presence of leachates of red pepper 

fruit (37), whereas germination of Botrytis cinerea may be prevented by antagonistic 

fungi (50). Quiescence can be observed at the levels of germinated spores,



POSTHARVEST PATHOGEN QUIESCENCE 415 

symptomless infections—in several Colletotrichum sp. interactions (41, 77)— 

and even in visible but nonexpanding lesions, such as in ghost spot of tomato 

caused by Botrytis cinerea (104). The occurrence and maintenance of pathogen 

quiescence on or within the host indicate a dynamic equilibrium among host, 

pathogen, and environment, without any visible symptoms (46). Postharvest 

physiological and biochemical responses of the host might trigger changes in 

that equilibrium to activate the pathogen. At the same time, the pathogen, 

which is kept at a low metabolic level during the quiescent stage, may activate 

pathogenicity factors, resulting in active parasitic development in the host 

tissues. 

THE QUIESCENT STAGE DURING PATHOGEN ATTACK 

Quiescence During Spore Germination and Hyphal Development 

Several cases of quiescence at early stages of fungal development have been 

described. Germination of conidia and appressorium formation by C. piperatum 

have been shown to be delayed on the surface of unripe peppers but not on ripe 

fruit (37). This is not a general rule, since conidia of C. musae have been 

reported to germinate on the surface of both ripe and unripe fruit, although the 

latter stimulated greater formation of appressoria (6, 82). Quiescent hyphae 

have been observed in Botrytis allii that penetrate young onion leaves but only 

develop in aging leaves (100). Similarly, hyphae of Dothiorella dominicana 

colonize the floral parts of mango trees, develop endophytically in the fruit 

pedicel, and remain quiescent until the fruit matures, at which stage the parasite 

is ready to infect through the stem end of the maturing fruit (48). In some cases, 

pathogens colonize flower parts during flowering, remain inactive until button 

abscission, then penetrate the stem end, as in the case of Diplodia natalensis in 

citrus (62). Botrytis cinerea also penetrates floral parts (petals, stigmas, styles, 

or stamens) of strawberries, raspberries, and grapes and remains dormant until it 

resumes activity and invades the fruit later in the season or during ripening (32, 

45). In other cases, hyphae of the pathogens penetrate the growing fruit directly: 

Alternaria alternata initiates infection of apricot, persimmon, and mango fruit 

by direct penetration of the fruit cuticle or through stomatal openings and then 

becomes quiescent after cuticle penetration (54, 72, 74). 

Quiescence during Appressorium Formation 

An early report on regulation of fungal attack based on the induction of appressorium 

formation described C. musae, in which anthranilic acid stimulated 

appressorium formation (96). This acid is present in banana peel leachates, and 

is rapidly degraded by conidia to active 2,3-dihydroxybenzoic acid (39). This 

compound has chelating properties and reduces the level of iron close to the 

spores. Harper and co-workers (40) concluded that iron is associated with an



416 PRUSKY 

inhibition site. Several synthetic iron-chelating agents are reported to stimulate 

germination and the formation of appressoria, which explains why chelating 

agents such as siderophores produced by bacteria on the surface of banana 

fruit greatly stimulated germination and appressorium formation by C. musae 

(57, 58). 

Spores of Colletotrichum that land on very hydrophobic surfaces such as 

fruit wax were induced to produce appressoria (68, 83). This suggests that surface 

waxes may well serve as signals for the fruit-pathogen interaction. This 

kind of signaling was demonstrated to be specific; other plant waxes could not 

induce differentiation in C. gloeosporioides, and avocado wax did not induce 

developmental processes in Colletotrichum spp. that are pathogenic to other 

plants. The fatty alcohol fraction, constituting only 5% of the whole wax, was 

the most active, with C30 and C32 as the major components. Interestingly, verylong-chain 

alcohols are present in many plant waxes (51) but they do not induce 

appressorium formation, probably because they also contain inhibitors. The addition 

of waxes from other plants inhibited the ability of avocado wax to induce 

appressorium formation by C. gloeosporiodes (68). These findings suggest that 

plant-surface lipids contain both inducers and inhibitors of spore germination 

and appressorium formation and that the balance between them might be responsible 

for the selective activation of the pathogen from its quiescent state 

and for the initiation of parasitism. 

Quiescence of Appressoria, Germinated Appressoria, and 

Subcuticular Hyphae 

The possibility that the quiescent structural stage involves structures such as 

appressoria, germinated appressoria, or subcuticular hyphae has been tested in 

several systems. In unripe banana, it was initially suggested that subcuticular 

hyphae of C. musae constitute the quiescent structure of the pathogen (90). 

However, Muirhead (61) concluded that the dark, thick-walled appressorium is 

the dormant structure of C. musae. Similarly, Brown (14, 15) described the quiescence 

of C. gloeosporioides in tangerine and suggested that the appressorium 

and not subcuticular hyphae is the quiescent structure. 

For C. gloeosporioides attacking avocado, Binyamini & Schiffmann-Nadel 

(12) suggested that the pathogen remains quiescent as appressoria on the surface 

of avocado fruit. In contrast, recent reports (83) suggest that appressoria 

of C. gloeosporioides germinate on unripe avocado fruit to produce infection 

pegs that penetrate the cuticle to the underlying epidermal cells within 72 h of 

inoculation but do not develop further until fruit ripening. This observation was 

confirmed by electron microscopy: Thin infection pegs were produced soon 

after the inoculation of immature, unripe fruit and could become physically




detached from appressoria during wax deposition on the developing avocado 

fruit (22). Similarly, it has been suggested that the quiescent stage of C. 

gloeosporioides in grape and blueberry fruit is a germinated appressorium 

(41). B. cinerea, which usually penetrates through wounds (46), penetrates 

nectarines after production of a very thin infection peg, formed from the inner 

wall of the appressorium (35). During the quiescent stage, the penetration peg 

of B. cinerea grows into the cuticle but does not breach it, remaining quiescent 

as a germinated appressorium. 

MECHANISMS FOR QUIESCENCE 

Factors Affecting Quiescence of Ungerminated and 

Germinated Spores 

The possibility that the host fruit triggers spore germination and the phenomenon 

of host specificity have been examined in several hosts. When green 

mold of citrus fruit was initiated by conidia of Penicillium digitatum in a wound 

in the fruit exocarp, germination was enhanced by nutrients in the wounded fruit, 

possibly sugars and organic acids (31). Furthermore, the mixture of volatiles released 

by the wound (possibly including CO2, ethanol, limonene, and acetaldehyde) 

specifically stimulated spore germination of P. digitatum (31). Growth 

of C. gloeosporioides and Pestalotia psidii on guavas was inhibited by extracts 

and volatiles of several dominant phylloplane fungi of the fruit (67). Regulators 

of spore germination can also be of pathogenic origin. Self-inhibition 

of germination is a common phenomenon within spp. of Colletotrichum: It 

is assumed that endogenous self-inhibitors regulate their conidial germination 

(101). Self-inhibitors have been identified in two species, C. gloeosporioides f. 

sp. jussiaea and C. graminicola (101). Inhibitors produced by C. gloeosporioides 

f. sp. jussiaea inhibited its own germination and that of C. fragariae but 

not that of 16 other Colletotrichum spp. These results confirm that specific factors 

can activate quiescent spores and modulate the initiation of the pathogen’s 

parasitic relationship with fruit. 

After the spores had germinated, the resistance of sweet cherry to infection 

by Monilinia fructicola was correlated with cuticle and cell-wall thickness 

(4, 5, 59). The quiescent period lengthened as the cuticle and cell-wall thickness 

of peaches increased. Peach cultivars that were significantly more resistant 

had a thicker and denser epidermis than did those of susceptible cultivars, 

and their resistance correlated with penetration delay and longer incubation 

periods for infection (4, 5). Similar findings were reported by Michalides and 

co-workers (59) in nectarines, where the development of quiescent infections 

in M. fructicola increased as cuticle thickness of the fruit decreased.



418 PRUSKY 

The mechanical barrier formed after fungal penetration is sometimes so thick 

as to result in a “non-activating quiescent infection.” This is the case for apricot 

fruit, which respond to M. fructicola with cell death around the infection 

point, cell-wall suberization of surrounding living cells, and the accumulation 

of phenolic compounds (107). On the other hand, resistance of plum fruit to 

Monilinia laxa is suggested to result from periderm formation, suberization, 

and gum deposition at the infection site (87). When B. cinerea penetrates 

the intact cuticle of green and senescing nectarines, plums (35), green grapes 

(42), and young tomato fruit, it causes a positive reaction for phenolics and 

callose deposition (36). Mechanical barriers set up by the host may therefore 

be sufficient to arrest infection and either delay or completely prevent the infection 

process. However, in apricots when the fruit ripened, viable hyphae of 

M. fructicola in latent infections escaped from the arrested lesions and caused 

fruit decay (107). 

Quiescence at the Level of Appressorium Formation 

Signals from the plant induce germination of fungal spores and appressorium 

formation (43). Appressorium formation in C. gloeosporioides was induced 

specifically by the surface wax of its host (68, 83). The molecular events triggered 

in the fungus by chemical signals from the host are not known. Hwang 

and co-workers (44) described one gene, cap20, whose expression is induced 

uniquely by the host wax during appressorium formation. This gene is not 

expressed by the host wax under non-appressorium-forming conditions, suggesting 

that cap20 is likely involved in appressorium formation. Disruption 

of cap20 resulted in conidia of C. gloeosporioides that germinated normally 

and differentiated into appressoria when treated with wax. This disruption did 

not seem to affect appressorium formation, but the appressoria formed may not 

be fully functional in infection since the mutants failed to infect avocado fruit 

(44). This is the first clear demonstration of a functional role for appressorium 

formation in the initiation of fruit pathogenesis, and it indicates that several 

steps occur during the activation of this quiescent infection. The genes that 

turn on the processes of fungal differentiation necessary for infection are just 

starting to be identified. 

Appressorium Quiescence 

Constitutive and exogenous factors may affect appressorium dormancy (61). 

Constitutive dormancy might be affected by factors that either induce or restrict 

appressorium development. Dark, thick-walled appressoria of C. musae, usually 

quiescent in green bananas, were induced in distilled water and germinated 

in the absence of an external stimulus, suggesting that constitutive dormancy is 

either nonexistent or transitory in these species (61). Exogenous dormancy is




more likely due to deprivation of one or more factor(s) required for germination 

or to the presence of a germination inhibitor. Inhibitors of appressorium 

germination may be volatile or nonvolatile and could originate from the host, 

acting as a single factor for fungal initiation of attack, or they could be produced 

by epiphytic microorganisms. A strain of B. subtilis has been used to control 

C. gloeosporioides in avocado by affecting spore and appressorium germination 

(52). However, the lack of appressorium germination may result from the 

lack of a germination-triggering factor that only appears during specific periods 

during life of the fruit. 

Swinburne (97) reported that antifungal compounds of host origin inhibited 

appressorium germination. Antifungal compounds elicited by C. musae 

in green bananas may result in quiescence of the appressoria. On the other 

hand, several enhancers of appressorium germination of host origin have been 

reported. Soluble nutrients from the fruit stimulated appressorial germination, 

hence, were suggested to be factors able to terminate dormancy in vivo (26, 90). 

If appressorial dormancy were terminated naturally by an increase in nutrient 

solutions, artificial application of nutrients to dormant appressoria should have 

a similar effect. However, ripe fruit extracts applied to dormant appressoria 

of C. musae on green banana peel were ineffective in enhancing germination 

(61), which suggests that dormancy is not broken naturally by nutrients applied 

exogenously. Nutrients moving outwards through the cuticle might, however, 

reach the cytoplasm of the appressoria more effectively. 

Flaishman & Kolattukudy (34) advanced a novel explanation for the induction 

of appressorium formation: Ethylene produced by the host specifically 

at ripening acts as a signal to terminate appressorial dormancy on the fruit 

surface. Ethylene at concentrations of less than 1 µl/liter, i.e. much lower 

than the concentration produced during fruit ripening, induced both germination 

and appressorium formation in C. gloeosporioides and C. musae, but not 

in Colletotrichum species that infect nonclimacteric fruit. When spores of C. 

gloeosporioides were placed on oranges, a nonclimacteric fruit that does not 

produce significant amounts of ethylene after harvest, formation of multiple 

appressoria was not observed; nor did C. gloeosporioides cause any decay 

problems unless the fruit were de-greened. Exposure to 25 µl/liter ethylene, 

a treatment used for de-greening, caused formation of multiple appressoria 

and infection of tangerines (14, 15). On the other hand, on transgenic tomato 

fruit, which are incapable of producing ethylene, the spores of C. gloeosporioides 

(nonhost in tomato) did not germinate, but upon exposure to exogenous 

ethylene, the spores germinated, formed multiple appressoria, and produced 

infection lesions (34). This suggests that the ripening hormone times fungal 

infection. Because a cascade of significant events occurs after exposure of



420 PRUSKY 

climacteric fruit to ethylene, it is unclear whether ethylene is the only factor 

timing the infection. For example, when unripe avocado fruit (climacteric fruit) 

were treated with 27 µl/liter ethylene, there was no immediate effect on decay 

symptoms and the fruit started to decay about 21 days later; ethylene-treated 

avocado fruit developed symptoms only 2–3 days before untreated fruit (D 

Prusky, C Wattad, I Kobiler, unpublished). This indicates that even if ethylene 

does have a morphological effect on the pathogen in vitro, it might not behave 

as a single signal for initiation of fungal decay unless the fruit has ripened and 

other changes have occurred in the peel. 

Quiescence During Hyphal Penetration and 

Fungal Colonization 

The resistance of fruit and vegetables to colonization by the pathogen has been 

studied more closely than other aspects of quiescence. Quiescence at the colonization 

stage includes the inhibition of colonization initiated from germinated 

appressoria and from hyphae of germinated spores that do not produce appressoria. 

Early reports by Verhoeff (105) and Swinburne (98) postulated that significant 

physiological changes occur in the host and in the pathogen during fruit 

ripening to activate quiescent infections (47, 90). Resistance mechanisms were 

grouped (98) into four hypotheses: (a) host effects and nutritional requirements 

of the pathogen, (b) preformed antifungal compounds, (c) inducible antifungal 

compounds, and (d) activation of fungal pathogenicity factors. 

HOST EFFECTS AND NUTRITIONAL REQUIREMENTS OF THE PATHOGEN Because 

fruit undergo profound biochemical changes during ripening, several authors 

(90, 105) have hypothesized that pathogen activation is triggered by nutrient 

availability. Generally, changes in sugar concentrations occur in parallel with 

a cascade of processes induced during ripening. But this correlation has not 

been proven to be causally involved. In some cases, infusion of sucrose or 

fructose into apple fruit via the petiole accelerated the onset of susceptibility to 

Botryosphaeria ribis (91), but the treatment also removes other factors (antifungal 

compounds). However, a similar infusion with sucrose, at concentrations 

that sustain maximal growth of A. alternata in vitro, did not enhance the susceptibility 

of resistant mango fruit tissue. Furthermore, the main increase in total 

soluble solids, up to 14%, in the peel and flesh of ripening mango fruit occurred 

13 days after harvest, whereas symptoms of A. alternata appeared 5 days later 

(30). No changes in acidity were detected in the peel of unripe resistant or ripe 

Alternaria-susceptible fruit. In contrast, Palejwa et al (66) suggested that the 

low susceptibility of unripe mango fruit to attack by the saprophyte Penicillium 

cyclopium might be due to their high acid and low sugar contents, in addition 

to the presence of phenolics (66).




Opposing experimental results were also obtained when a similar development 

of decay by C. gloeosporioides occurred in the flesh of both unharvestedunripe 

and ripe avocado fruit. These results suggest that resistance is not 

attributable to the lack of a substrate for fungal growth. Thus the biochemical 

changes occurring in fruit flesh during ripening do not confer the susceptibility 

observed in unripe fruit (49, 71). 

Cruickshank & Wade (24) suggested that fruit volatiles (ethanol and acetaldehyde) 

produced during the ripening of apricots could transform mycelium of 

M. fructicola from latent into invasive, since the volatiles were produced in parallel 

with symptom development. However, when infected green apricots were 

exposed to the same volatiles, a limited growth of the fungus was observed but 

there was no invasion of the fruit. Exogenous ethylene is significant in activating 

quiescent mycelia of Diplodia natalensis in the stem end of necrotic tissue; 

it enhanced the activities of two enzymes involved in stem-end fruit abscission, 

exo-polyglacturonase and cellulase, enabling fungal penetration and the occurrence 

of stem-end rots (17). Since oranges do not produce significant amounts 

of ethylene after harvest, other factors such as tissue senescence may activate 

naturally occurring Diplodia infections. Whether the biochemical processes 

that occur during ripening confer fruit susceptibility has not been shown conclusively 

from these or other data obtained from various other fruit-pathogen 

systems. 

PREFORMED ANTIFUNGAL COMPOUNDS It is difficult to conduct critical tests 

on the role of preformed compounds [phytoanticipins (103)] in disease resistance, 

primarily because of problems in accurately assessing the quantities of 

inhibitory compounds that may contact the invading pathogen, in determining 

the in vivo biological activity of these compounds, and in relating changes in 

their concentration to fruit resistance (88). In several systems studied, changes 

in concentrations of inhibitory compounds did not coincide with changes in 

susceptibility (89), and infusion of fruit with antifungal substances did not always 

improve their resistance to rotting (91). Dopamine, for example, was 

isolated from the peel of unripe banana in concentrations that inhibited C. 

musae in vitro; it was therefore presumed to be a possible preformed antifungal 

compound. However, changes in its concentration were not synchronized with 

changes in decay development (60). Few cases have shown the importance of 

preformed antifungal compounds. 

The tomato system The involvement of preformed inhibitors in quiescent 

infection by B. cinerea was suggested in tomato fruit (95). The saponin, 

α-tomatine, present in high concentrations in the peel of green tomatoes, 

is inhibitory to the fungus at concentrations present in the peel. However,



422 PRUSKY 

although the lesions did not develop further after ripening, tomatine was not 

detected in mature fruit. The potent antifungal properties associated with many 

saponins has given rise to considerable speculation about their possible function 

as preformed determinants of resistance of plants to attack by saponin-sensitive 

fungi (64, 65). Strong evidence for a functional role of preformed tomatine in 

disease resistance came from the use of genetically related strains of pathogen 

with differing abilities to tolerate or degrade a plant antifungal compound (10, 

25). DeFago and coworkers induced mutants of Nectria haematococca that 

were more tolerant to α-tomatine and demonstrated that these mutants were 

now pathogenic on green tomato fruit, which contain high concentrations of 

α-tomatine (25). The wild-type strains were pathogenic only on ripe fruit, 

which contain little or no α-tomatine. 

A different approach was followed by Osbourn and co-workers. They noted 

that the resistance of oat to Gaeumannomyces graminis var. avenae has been attributed 

to the presence in the roots of the fungitoxic saponin, avenacin, whereas 

oat varieties lacking avenacin in their roots were susceptible to the pathogen 

(65). α-Tomatin and avenacin can be detoxified by terminal deglucosylation 

by avenacinase and tomatinase produced by specific pathogens (63, 64). The 

gene encoding the enzyme that detoxifies saponins, avenacinase, has recently 

been cloned and an avenacinase-minus mutant generated (13). This mutant 

was unable to infect the saponin-containing host, but retained full pathogenicity 

to attack the non-saponin-containing host. This is the first genetic proof of a 

plant-fungus interaction to determine the importance of saponin detoxification 

for fungal attack and the enzyme can therefore be regarded as a determinant 

of host range (13). The recent cloning of the gene encoding for tomatinase 

should clarify whether degradation of α-tomatine by the enzyme is necessary 

and sufficient to parasitize tomato (64, 86), and it should further support the 

role of the preformed compounds in disease resistance. 

The mango system In mangos, a mixture of antifungal compounds consisting 

of 5-12-cis-heptadecenyl resorcinol and 5-pentadecenyl resorcinol was found 

at fungitoxic concentration in the peel of unripe mango fruit that were resistant 

to A. alternata (28, 29). A new substituted resorcinol, hitherto not reported, was 

also recently detected (R Reved, I Kobiler, A Dinoor, D Prusky, unpublished). 

Several lines of evidence suggest that the preformed substituted resorcinols 

might be involved in the resistance of mango fruit to fungal development: (a) 

5-Substituted resorcinols occur at fungitoxic concentrations in the peel of unripe 

fruit of several mango cultivars and decrease to nontoxic concentrations in ripening 

fruit at the same time as symptoms of decay appear in inoculated fruit; (b) 

concentrations of the 5-substituted resorcinols decreased faster during ripening 

in susceptible than in resistant cultivars; (c) delayed reduction in concentrations




of the antifungal compound was correlated with delayed decay development; 

and (d) the flesh of unripe fruit, containing subfungitoxic concentrations of 

the preformed antifungal compounds, was susceptible to Alternaria attack. 

These observations suggest, but do not conclusively prove, that the resistance 

of unripe mango fruit is attributable to fungitoxic concentrations of the antifungal 

resorcinols present in the peel and that act on the germinated hyphae of 

A. alternata. 

The avocado system The resistance of unripe avocado fruit to the quiescent 

germinated appressoria of C. gloeosporioides is correlated with the presence of 

high concentrations of preformed antifungal compounds. The major antifungal 

compound has been shown to be 1-acetoxy-2-hydroxy-4-oxo-heneicosa-12,15diene 

(79); the amount of this compound decreased tenfold, to subfungitoxic 

concentrations, during fruit ripening. A second antifungal compound was subsequently 

purified from unripe avocado fruit and identified as 1-acetoxy-2,4dihydroxy-n-heptadeca-16-ene 

(80). This monoene was less fungitoxic than 

the diene, its concentration in the peel of unripe fruit was about half that of the 

diene, and it decreased as decay symptoms appeared. Thus the diene appears to 

account for most of the antifungal activity. Cultivars that were more susceptible 

to decay showed a faster decrease in both compounds during ripening. These 

observations are all consistent with the view that activation of fungus development 

depends on a threshold concentration of the antifungal diene present in 

unripe fruit. Other, less active antifungal compounds have also been found in 

avocado fruit (9). 

Because disease susceptibility in avocado fruit is correlated with decreased 

concentrations of the preformed antifungal compound, the mechanism controlling 

this reduction may predispose fruit to activation of quiescent infection by 

Colletotrichum. The antifungal diene serves as a substrate for oxidation by 

lipoxygenase. Several experimental findings (70, 78) indicate that lipoxygenase 

can degrade the antifungal diene and induce decay susceptibility in ripening 

fruit: (a) The apparent specific activity of the enzyme increased by 80% during 

fruit ripening; (b) avocado lipoxygenase oxidized the antifungal diene in vitro; 

(c) treatments with the nonspecific inhibitor α-tocopherol acetate or with the 

specific inhibitor of lipoxygenase 5,8,11,14-eicosatetraynoic acid inhibited enzyme 

activity in vitro and delayed decay development by C. gloeosporioides; 

and (d) treatment with methyl jasmonate, which enhances peroxidation processes, 

increased lipoxygenase activity and enhanced diene decrease and fruit 

susceptibility (R Ardi, I Kobiler, B Jacoby, D Prusky, unpublished). 

Lipoxygenase activity in unripe and ripening avocado fruit is reported to be 

affected by an endogenous inhibitor, epicatechin, present in the peel of avocado 

(77, 81): This flavan-3-ol competitively inhibited lipoxygenase activity



424 PRUSKY 

and decreased in concentration during fruit ripening, thus permitting lipoxygenase 

activity. The concentration of epicatechin in fruit of a highly susceptible 

cultivar decreased in parallel with a decrease in fruit softening during ripening, 

and symptom expression occurred when the epicatechin concentration was at 

its lowest. In a resistant cultivar in which the quiescent infection was activated 

and expressed symptoms later than in a susceptible cultlivar, the initial 

concentration of epicatechin was much higher, and a considerable amount of 

epicatechin remained in the peel of soft, ripe fruit. Activation of quiescent 

infections was thus related to the period required for complete reduction of epicatechin 

in softening fruit. This finding indicates that quiescent infections of C. 

gloeosporioides in avocado might be regulated initially by epicatechin acting 

as an inhibitor of lipoxygenase activity and consequently delaying degradation 

of the antifungal diene (77). 

The citrus system Citrus fruit are resistant to wound pathogens during fruit 

growth despite the presence of a significant amount of inoculum of Penicillium 

and the occurrence of natural wounding in the orchard. It has been suggested 

that the resistance of young mature green lemons is related to the presence 

of a preformed monoterpene aldehyde, citral, that decreases in older yellow 

fruit, enabling decay to develop rapidly (85). Cautious correlations between 

the levels of resistance of fruit after harvest and the in vivo concentrations 

of preformed inhibitory compounds suggest the possible involvement of these 

compounds in quiescence of pathogens. 

ELICITATION OF PHYTOALEXINS AND PREFORMED COMPOUNDS The resistance 

of Bramley’s Seedling apples to Nectria galligena is the result of induced 

phytoalexin formation. Nectria galligena is a pathogen that invades wounds 

and lenticels of apple fruit before harvest (95), but fruit rotting does not become 

severe until after harvest. Limited colonization takes place following the initial 

invasions and the synthesis of benzoic acid in the necrotic tissue has been 

observed (94). The elicitor of benzoic acid synthesis is a protease produced by 

the pathogen (95). Two other apple pathogens that induce quiescent infections, 

Diaporthe perniciosa and Gloeosporium perennans, also secrete proteases in 

vivo. In the case of Penicillium expansum, B. cinerea, Phytophthora cactorum, 

Sclerotinia fructigena, and Aspergillus niger, no protease was produced in 

infected tissue. Consequently, these organisms can rot immature fruit without 

inducing the accumulation of benzoic acid (16, 95). Benzoic acid is toxic only 

as an undissociated molecule, but its fungitoxic activity decreases significantly 

as a result of the increase in pH during fruit ripening (18). This, in conjunction 

with increasing sugar concentrations, enables the pathogen to degrade benzoic 

acid and resume active growth. The secretion of proteases followed by the 

induction of benzoic acid has been suggested to be the basis for quiescent 

infection of this cultivar.




Phytoalexins are induced at the initial stage of infection in peppers. The capsicannol 

phytoalexins, 1-deoxycapsidion and endesmadienol, were associated 

with the induction of quiescence in fruit of Capsicum annuum infected with 

Glomerella cingulata (7). When harvested unripe fruit were inoculated with G. 

cingulata, capsicannol readily accumulated (98). In ripening fruit, both capsicannol 

and capsidiol accumulated but when lesion expansion occurred, both 

compounds were absent. It has been suggested that these compounds also accumulate 

at the sites of arrested lesions of B. cinerea, but not in progressive lesions 

(8). A series of compounds also accumulated in arrested lesions in banana: Resistance 

of green bananas to C. musae was associated with a growing necrotic 

reaction within the peel (20), and five antifungal compounds not present in 

healthy tissue were isolated (19). In some cases, the induction of antifungal 

compounds during fungal penetration can lead to the final localization of the 

pathogen by an antimicrobial barrier. Stange and co-workers (92) reported that 

“wound gum” accumulated in injured citrus exocarp: A predominantly antifungal 

compound, identified as 3-[4-hydroxy-3-(methyl-2-butenyl)phenyl]-2- 

(E)-propenal, increased in concentration as a function of time, resulting in the 

complete quiescence of the invading pathogen. 

Challenge inoculation in unripe fruit also induces preformed antifungal compounds 

(76). Induction of higher concentrations of preformed antifungal compounds 

occurred in response to challenge inoculation of unripe, but not of 

ripe, fruit. Inoculation of unripe avocado fruit with C. gloeosporioides doubled 

the amount of the preformed antifungal diene 1 day after the challenge, 

and the effect remained for 3 days, suggesting persistence of the elicitor (82). 

However, the level of the induced compound decreased before symptoms of 

disease occurred. Interestingly, inoculation of unripe avocado fruit with spores 

of a nonpathogenic mutant of Colletotrichum magna also induced a significant 

increase in concentrations of the antifungal diene, with longer persistence 

of the elicitors, without developing symptom expression (73). This effect of 

a nonpathogenic strain was used to delay the activation period of wild-type 

C. gloeosporioides, by co-inoculating fruit with both strains (73). The induction 

of preformed antifungal compounds by two different Colletotrichum spp. 

suggests that nonspecific eliciting factors are probably present in the hyphae of 

both pathogen species (73). Elicitors from the cell wall of Glomerella cingulata 

may also enhance host reaction and protect pepper fruit from B. cinerea (8). 

Other preformed inducible compounds are the polyacetylenes, falcarindiol 

and falcarinol, which have been hypothesized to affect resistance of carrot 

roots (38). These compounds are compartmentalized in extracellular oil droplets, 

mainly within the root periderm and pericyclic area in carrot. Continuous 

contact of the tissue with organisms in the rhizosphere or with other organisms 

may result in induction of significantly higher concentrations of the preformed



426 PRUSKY 

compound. These results suggest that all of the inducible compounds can be 

elicited during the quiescent period. However, only those that remain active 

for considerable fractions of the lifetime of the fruit can really be considered to 

affect quiescence. 

ACTIVATION OF FUNGAL PATHOGENICITY FACTORS Simmonds (90) hypothesized 

that quiescent infections are attributable to failure of the pathogen to produce 

adequate amounts of pathogenicity factors, such as pectolytic enzymes, 

until the ripening process leads to suitable changes in the cell-wall structure. 

Many lines of evidence suggest that cuticular penetration of C. gloeosporioides 

into the host is associated with the induction of production of extracellular cutinase 

(27). Cutinase was target secreted by the infection peg of an appressorium 

of Colletotrichum spores (69). The inhibition of cutinase production could 

result in a delay in the penetration of germinating fungal appressoria into the 

host. No natural inhibitors of cutinase have been detected to date. 

Theoretically, an inadequate pectolytic enzyme potential could be caused in 

several ways (98): (a) Pathogen enzymes are not all constitutive and may require 

induction by proper substrates (11); (b) enzymes of the pathogen might be 

produced but are blocked by cation cross-linking; (c) enzymes of the pathogen 

might be inhibited or inactivated by substances present in higher quantities in 

immature fruit. 

The first hypothesis, supported by Simmonds (90) and Verhoeff (105), fails to 

explain a simple experiment in which C. gloeosporioides and A. alternata macerated 

(within 1 day) the mesocarp of peeled fruit of unharvested or freshly harvested 

unripe avocado and mango fruit before any of the physiological changes 

that take place during ripening occur. Infection of the peel (pericarp) of the 

same unripe fruit resulted in a quiescent infection for 14–20 days later (30, 

49). This simple experiment underscores the difference in tissue susceptibility 

between the peel (pericarp) and the flesh (mesocarp) of unripe avocado and 

mango fruit and indicates that the biochemical changes in the flesh during fruit 

ripening are not directly related to activation of quiescent infections in the peel. 

Fruit-cell-wall degrading enzymes may also behave as specific activators of 

fungal pathogenicity factors and hence activate quiescence. Expression of the 

tomato polygalacturonase (PG) during the fruit climacteric is temporally correlated 

with the susceptibility of the fruit to fungal infection (56). The severity 

of postharvest diseases caused by A. alternata and R. stolonifer in transgenic 

tomato fruit lines is a function of the level of polygalacturonase expressed by 

the plant, suggesting that developmentally regulated plant genes act as biochemical 

determinants of susceptibility (56). Furthermore polyglacturonasesolubilized 

pectic polysaccharides from tomato may act as signal molecules 

that specifically induce toxin production of A. alternata f. sp. lycopersici




(AAL) on resistant isolines. The PG-solubilized signals induced significantly 

increased toxin production by the AAL-toxin–producing pathogen and by the 

saprophytic nontoxin-producing isolate of A. alternata (RM Martin, DJ Nevins, 

DG Gilchrist, unpublished data). This indicates that a highly evolved and complementary 

signaling process might be invoked by the plant and the pathogens 

in order to activate infection by the pathogens. 

The presence of blocked cross-linked bonds in the cell-wall pectin may affect 

enzymatic degradation. The configuration of the polygalacturonic chain allows 

spaces for a series of cations to bind between carboxyl groups. The formation of 

cation cross bridges between pectic acid may make the cell wall less accessible 

to enzymes produced by fungal pathogens that cause decay (99). Increasing 

the Ca 2+ content of apples by means of preharvest sprays and postharvest dips 

reduces postharvest decay. Such treatments were found to increase significantly 

the number of salt bridges and consequently the structural integrity of the cell 

wall, thus reducing the vulnerability of the cell walls to maceration (23). 

The inactivation of pectic enzymes by inhibitors has been proposed as a hypothetical 

mean of modulating fungal pathogenicity. According to Byrde and 

co-workers (21), polyphenols and tannins may account for this inactivation. 

However, several of the compounds are localized within vessels and are not 

therefore generally available to the attacking pathogen. It was recently shown 

that there is a close relationship between changes in the level of the flavan-3-ol, 

epicatechin, present in the peel of avocado fruit and the inhibition of pectolytic 

enzymes by C. gloeosporioides. Purified polygalacturonase and pectate lyase 

produced by C. gloeosporioides were also inhibited in vitro by epicatechin 

(75, 108). At 20 µg/ml, epicatechin reduced the maceration capability of the 

enzymes by 64%. Since the flavan is present in unripe fruit at much higher concentrations 

(about 350 µg/g fresh weight) than the inhibitory concentrations, 

epicatechin may contribute to the quiescence of C. gloeosporioides by inhibiting 

the activity of pathogenicity factors. The importance of pectate lyase (PL) 

as a pathogenicity factor during the activation of quiescent infections has been 

demonstrated in two experiments: (a) Antibodies produced against purified PL 

of C. gloeosporiodes, incubated with spores of C. gloeosporioides, inhibited anthracnose 

development in ripe fruit (C Wattad, D Kobiler, A Dinoor, D Prusky, 

unpublished); and (b) development of a nonsecreting PL mutant was nonpathogenic 

on susceptible avocado, indicating that even when concentrations of 

antifungal compounds decreased, PL production is required for infection (109). 

Another class of inhibitors of cell-wall-degrading enzymes comprises the 

polygalacturonase inhibitory proteins (PGIP) present in infected and uninfected 

plant tissue (1, 3). Purified pear PGIPs inhibited various fungal PGs, including 

that of B. cinerea, but did not affect endogenous PG activity in pear fruit (2). In



428 PRUSKY 

pears, PGIP activity was observed throughout development (4–14 weeks after 

anthesis), and changes in susceptibility to decay development after fruit ripening 

were accompanied by a decrease in the PG inhibitor content of Bartlett pear fruit. 

PGIPs from different plant species are likely to differ in their inhibition kinetics 

and target specificity (2, 3). The molecular characterization of PGIP from pear 

was recently reported (93). The expression of polygalacturonase inhibitor is 

regulated in a tissue-specific manner. mRNA in PGIP was approximately 100fold 

more abundant in fruit than in flowers and was not detectable in pear leaves. 

Specific activity of PGIP in fruit was 200-fold higher than in flowers and 1400fold 

higher than in leaves. Labavitch and co-workers suggested that the PGIP 

promoter in pear may affect a fruit-specific expression of the gene, resulting in 

the inhibition of B. cinerea (93). Recently, a new protein inhibitor that may be 

involved in the inhibition of the enzymes necessary for microbial development 

was isolated from cabbage (55). This inhibitor significantly inhibited growth 

of B. cinerea by blocking chitin synthesis and resulting in cytoplasmic leakage. 

The characterization of protein inhibitor from pear (93) and from other plants 

(33) should lead to expression of PGIPs in transgenic plants and possibly delay 

in the development of decay. Following a similar idea, it might be possible to 

select avocado cultivars with intrinsically higher concentrations of epicatechin 

that will remain resistant by inhibiting the pathogenicity factors produced by 

C. gloeosporioides. 

Activation of quiescent infections may also occur through the activation of 

specific fungal pathogenicity factors that detoxify preformed resistant compounds 

(63). Antifungal saponins occur in many plant species and provide 

a preformed barrier to attack by fungi (63, 106). Arneson & Durbin (10) 

demonstrated that fungi that are not normally pathogenic on plants producing 

α-tomatine are more sensitive to α-tomatine than are pathogens of these plants. 

Most tomato pathogens produce enzymes that specifically degrade α-tomatine, 

and these enzymes may be important for tomato pathogens (10,106). Since 

saponins have been implicated as preformed resistance determinants that protect 

fruit against attack by saponin-sensitive fungi, the activation of this specific 

enzyme during fruit ripening could result in the activation of quiescent infection 

in fruit where saponins determine their resistance. 

SUMMARY 

The various hypotheses advanced over the years to explain quiescent infection 

and the diversity of hosts that induce quiescence in pathogens point to the involvement 

of several mechanisms. In grapes, for example, a two-component 

system has been described: the presence of proanthocyanidins that are located 

in the skin of the grapes, which inhibit macerating enzymes produced by the 

fungus (42), and production of the stilbene resveratrol (53). Immature grapes




synthesize large amounts of resveratrol, but as they mature this capability 

steadily decreases and the fruit become more susceptible. In the avocado 

system, a two-component factor may also affect resistance: the presence of 

a preformed antifungal compound and the inhibition by epicatechin of the 

activity of pectate lyase produced by the pathogen (77). In both grape and 

avocado, after the host barriers decline, the pathogenicity factors produced by 

the activating fungus result in decay development. In each host-parasite interaction, 

therefore, several mechanisms may be operating simultaneously or even 

sequentially, resulting in fungal quiescence. 

Although many data supporting the involvement of preformed antifungal 

compounds in quiescence constitute correlative evidence, the role in resistance 

is not proven; experiments that modulated the mechanism of resistance affected 

the quiescence period. The fact that delaying the decrease of the antifungal 

diene in avocado by means of antioxidant treatments (70) and high CO2 concentrations 

(84) led to predicted changes in fruit resistance constitutes evidence 

that the preformed compound is an important agent affecting quiescence of C. 

gloeosporioides during colonization stages in avocado (77). Furthermore, the 

possibility of inducing preformed compounds by nonpathogenic strains of Colletotrichum 

indicates the importance of such elicitation in inducing resistance 

and possible biological modulation of quiescence during fungal colonization. 

The activation of quiescent infection may result not only from a reduction of 

inducible or preformed host barriers, but also from the production of specific 

host signals, such as ethylene, that activate genes initiating the germination of 

appressoria and triggering fungal pathogenicity factors. If studies on the preformed 

α-tomatine suggest that saponin-degrading enzymes may have a more 

general role in pathogenicity, then these enzymes may become attractive targets 

for disease control strategies involving inhibitors (64, 86). The extracellular 

location of the enzymes should facilitate approaches involving the use of chemicals 

or the expression of saponinase inhibitors in genetically engineered plants, 

since the inhibitors would not need to penetrate the fungal hyphae (64). Quiescence 

could also be modulated during the early stages of germination, as in 

the case of the antagonistic effect of B. subtilis (52) on Colletotrichum, or by 

using analogs of germination self-inhibitors that could facilitate the biological 

control of those pathogens (101). Modulation of the quiescence mechanisms 

by biological, physical, and chemical means should provide new options in the 

control of postharvest decay and in the reduction of pesticide use. 

ACKNOWLEDGMENTS 

I would like to thank NT Keen, R Barkai Golan, and I Kobiler for their useful 

remarks while reviewing the manuscript and R Martin and R Ardi for supplying 

unpublished results.



430 PRUSKY 

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Annual Review of Phytopathology 

Volume 34, 1996 

CONTENTS 

PLANT PATHOLOGY: A Discipline at a Crossroads, Albert R. 

Weinhold 1 

HELEN HART, REMARKABLE PLANT PATHOLOGIST 

(1900–1971), Roy D. Wilcoxson 13 

DR. GOTTHOLD STEINER (1886–1961): VERSATILE 

NEMATOLOGIST, Robert P. Esser 25 

THE RED QUEEN HYPOTHESIS AND PLANT/PATHOGEN 

INTERACTIONS, Keith Clay, Paula X. Kover 29 

THE ROLE OF PLANT CLINICS IN PLANT DISEASE DIAGNOSIS 

AND EDUCATION IN DEVELOPING COUNTRIES, Reuben Ausher, 

Israel S. Ben-Ze'ev, Robert Black 51 

DWARF BUNT: Politics, Identification, and Biology, D. E. Mathre 67 

FUNGAL TRANSMISSION OF PLANT VIRUSES, R. N. Campbell 87 

EPICHLOË SPECIES: Fungal Symbionts of Grasses, Christopher L. 

Schardl 109 

FASTIDIOUS XYLEM-LIMITED BACTERIAL PLANT 

PATHOGENS, Alexander H. Purcell, Donald L. Hopkins 131 

BACTERIAL AVIRULENCE GENES, Jan E. Leach, Frank F. White 153 

CHEMORECEPTION IN PLANT PARASITIC NEMATODES, Roland 

N. Perry 181 

NEMATODE MANAGEMENT IN SUSTAINABLE AND 

SUBSISTENCE AGRICULTURE, J. Bridge 201 

HELPER-DEPENDENT VECTOR TRANSMISSION OF PLANT 

VIRUSES, Thomas P. Pirone, Stéphane Blanc 227 

BIOLOGY AND EPIDEMIOLOGY OF RICE VIRUSES, Hiroyuki 

Hibino 249 

MOLECULAR BIOLOGY OF RICE TUNGRO VIRUSES, Roger Hull 275 

PLANT VIRUS GENE VECTORS FOR TRANSIENT EXPRESSION 

OF FOREIGN PROTEINS IN PLANTS, Herman B. Scholthof, Karen- 

Beth G. Scholthof, Andrew O. Jackson 299 

ROOT SYSTEM REGULATION OF WHOLE PLANT GROWTH, R. 

M. Aiken, A. J. M. Smucker 325 

OZONE AND PLANT HEALTH, Heinrich Sandermann Jr 347 

MORPHOGENESIS AND MECHANISMS OF PENETRATION BY 

PLANT PATHOGENIC FUNGI, K. Mendgen, M. Hahn, H. Deising 367 

MICROBIAL ELICITORS AND THEIR RECEPTORS IN PLANTS, 

Michael G. Hahn 387 

PATHOGEN QUIESCENCE IN POSTHARVEST DISEASES, Dov 

Prusky 413 

GENETICS OF RESISTANCE TO WHEAT LEAF RUST, J. A. Kolmer 435 

RECOMBINATION AND THE MULTILOCUS STRUCTURE OF 

FUNGAL POPULATIONS, Michael G. Milgroom 457 

QTL MAPPING AND QUANTITATIVE DISEASE RESISTANCE IN 

PLANTS, N. D. Young 479 

BREEDING DISEASE-RESISTANT WHEATS FOR TROPICAL 

HIGHLANDS AND LOWLANDS, H.J. Dubin, S. Rajaram 503 

CHANGING OPTIONS FOR THE CONTROL OF DECIDUOUS 

FRUIT TREE DISEASES, Turner B. Sutton 527



RESISTANCE TO PHENYLAMIDE FUNGICIDES: A Case Study with 

Phytophthora infestans Involving Mating Type and Race Structure, U. 

Gisi, Y. Cohen 549 

STATUS OF CACAO WITCHES' BROOM: Biology, Epidemiology, and 

Management, LH Purdy, RA Schmidt 573

PATHOGEN QUIESCENCE IN POSTHARVEST DISEASES

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