biocontrol of citrus postharvest diseases

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FEATURE

Biological Control of Postharvest Diseases of Fruits andVegetables: Recent Advances

Michael E. Wisniewski and Charles L. Wilson

U.S.Department of Agriculture, Agricultural Research Service, Appalachian Fruit Research Station,Kearneysville, WV 25430

Although it is difficult to determine thefull extent of postharvest losses due to dis-eases, conservative estimates place losses tofruits and vegetables from spoilage at 24%of the harvested crop in the United States(U.S. Dept. of Agriculture, 1965) and 50%in underdeveloped, tropical countries (Cour-sey and Booth, 1972).

Fungicides are a primary means of con-trolling postharvest diseases (Eckert andOgawa, 1985). Their use worldwide is var-iable, comprising 26% of the pesticide mar-ket in Europe and Asia and 6% in the UnitedStates (Jutsum, 1988). However, as har-

vested fruits and vegetables are commonlytreated with fungicides to retard postharvestdiseases, there is a greater likelihood of di-rect, human exposure to them than to otherpesticides that are applied solely to protectfoliage.

Public and scientific concern about thepresence of synthetic chemicals in our foodsupply and in the environment has been in-creasing in the past decade. A report fromthe National Academy of Sciences (NAS)(1987) indicated particular concern about thehealth risks associated with the use of fun-gicides. As a direct result of these mountingconcerns, real or perceived, several fungi-

cides (e.g., captan and benomyl) have beenbanned by the U.S. Environmental Protec-tion Agency or voluntarily withdrawn fromthe market for some or all postharvest use.This action has the potential of greatly di-minishing our ability to control postharvestdiseases of many commodities. The NAS re-

port clearly indicated this possibility by stat-ing, For certain crops in certain regions,the loss of all oncogenic compounds-par-ticularly fungicides-would cause severeshort-term adjustments in pest control prac-tices because of the lack of economically vi-able alternatives.

Despite this situation, the trend to restrictor ban the use of current, synthetic fungi-cides for postharvest use is continuing. Arecent report inPostharvest News and Infor-mation (Rendall-Dunn, 1991) indicated thatthe European Parliament has voted in favorof a total ban on postharvest treatment of

Received for publication 10 June 1991. Acceptedfor publication 20 Sept. 1991. The cost of pub-lishing this paper was defrayed in part by the pay-

ment of page charges. Under postal regulations,this paper therefore must be hereby marked ad-vertisment solely to indicate this fact.

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fruits and vegetables with pesticides as soonas this practice becomes feasible. As a fur-ther indication of this trend, Technical In-sights, Inc., in their Twenty-five Predictionsfor theNew Century (1991), has stated thatthe Agricultural Chemical Industry as weknow it today will begin to disappear. Bio-logical products will become cost competi-tive with chemicals due to new environmental-impact taxes.

There is clearly an urgent need to developnew and effective methods of controllingpostharvest diseases that are perceived as safeby the public and pose negligible risk to hu-

man health and the environment. The use ofnonchemical techniques and nonselectivefungicide treatments have and will in the fu-ture answer a part of this need. Inoculumreduction achieved through sanitation andexclusion (Bancroft et al., 1984), the use ofnonselective fungicides (sodium carbonate,sodium bicarbonate, active chlorine, andsorbic acid), and heat treatments can signif-icantly lower the disease pressure on har-vested commodities (Eckert, 1991). Har-vesting and handling techniques that minimizeinjury to the commodity, along with storageconditions that are optimum for maintaininghost resistance (Sommer, 1985), will also

aid in suppressing disease development afterharvest. In addition to the above methods,however, considerable attention has also beenplaced on assessing the potential of biolog-ical control of postharvest diseases of fruitsand vegetables as a viable alternative to theuse of present-day, synthetic fungicides(Wilson and Wisniewski, 1989; Wilson etal., 1991). In the following report, we willreview recent advances in the use of micro-

bial antagonists to control postharvest dis-eases (especially of fruit) and to address theircommercial potential.

Biological control-A new climate

Biological control agents have had a dif-ficult time making it from the laboratory tothe marketplace. This difficulty has beenlargely due to problems of ineffectivenesswhen the biocontrol agents are subjected tothe uncontrolled environment of the fieldand to the lack of economic incentive to de-velop the technology necessary for their ef-fective use. Lack of support for widespread,sustained research in this area has been largelydue to the effectiveness and perceived safetyof chemical fungicides. However, becauseof the changing socioeconomic climate and

recent advances in genetic engineering, in-terest in biological control as a meaningfulapproach to pest and disease managementhas been rejuvenated (Jeffries and Jeger, 1990;Wilson and Wisniewski, 1989, 1992). Re-cent changes in U.S. patent laws also havecontributed to an atmosphere that is moreconducive to the development of marketablebiological control agents. Several venture-capital companies or subsidiaries of well-known agrochemical companies, with a fo-cus on biological control, have arisen in re-sponse to this new climate. Therefore, theoutlook for developing economically viable

biological control products looks very prom-ising.

Postharvest biological control-A uniqueen v iron men t

Two basic approaches are available forusing microorganisms to control postharvestdiseases: use and management of the bene-ficial microflora that already exist on fruitand vegetable surfaces or the artificial intro-duction of antagonists against postharvest

pathogens. Our knowledge of methods tomanipulate naturally occurring populationsof mixed species of microorganisms in a

beneficial manner, however, is meager (Wil-son, 1989), and the greatest use of biologicalcontrol (pre- and postharvest) has comethrough the artificial introduction of largenumbers of a known antagonist (Wilson andWisniewski, 1989).

Several factors indicate that postharvestbiological control with the use of artificiallyintroduced antagonists may prove to be aneffective technology. First, environments forthe storage of harvested commodities are oftencontrolled and maintained. This control shouldlessen the problem of introducing the bio-control agent into an unpredictable and highlyvariable environment, which previously hasbeen a limiting factor in field-released bio-control measures. Second, the ability to tar-get the biocontrol agent to the site neededfor activity is enhanced in postharvest ap-

plication. Third, the high value of harvestedcommodities may make the application ofelaborate biological control procedures morecost-effective than similar procedures in thefield. Fourth, for some commodities har-vested for fresh-market consumption, pro-tection from postharvest diseases is onlyneeded for a short duration.

Although it appears that the postharvestenvironment may be especially favorable for

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the development of biocontrol agents, a con-siderable investment of time and money isrequired to establish whether any particularorganism has commercial potential. There-fore, the isolation, screening, and selectionof potential antagonists should receive care-ful deliberation. The characteristics of anideal antagonist are listed in Table 1. Asindicated by Roberts (1991), any potentialantagonist must have the ability to colonizeand persist on the commodity at effectivelevels; be compatible with other postharvest

practices, processes, and chemicals; and beeffective under cold and, in some cases, con-trolled-atmosphere conditions. Additionally,the organism must be amenable to large-scaleproduction using low-cost substrates. Giventhese constraints, several antagonists forcontrol of postharvest diseases of fruit havebeen identified for their commercial poten-tial.

of apples and penicillium rot of oranges IC i t -rus sinensi s(L.) Osb.] when applied towounded and inoculated fruit (Fig. 1).

In addition to the above yeasts, the bac-teria Baci l l us subti l i s(Ehrenberg) Cohn andPseudomonas cepaciaBurkh. have shownpotential in controlling a wide range of rotorganisms on several commodities (Jani-siewicz and Roitman, 1988; Pusey and Wil-son, 1984; Singh and Deverall, 1984;Utkehede and Sholberg, 1986). Their activ-

ity, however, appears to rely on the produc-tion of potent antibiotics by the antagonists.This feature may be of special concern whenevaluating their commercial potential.

Table 1. Characteristics of an ideal antago-nist for the postharvest environment (adaptedfrom Wilson and Wisniewski. 1989).

Genetically stable.

Antagonistic organisms-Identificationand characterization

Effective at low concentrations.Not fastidious in its nutrient requirements.Ability to survive adverse environmental condi-

tions (including low-temperature and con-trolled-atmosphere storage).

Effective against a wide range of pathogens on avariety of fruits and vegetables.

Amenable to production on an inexpensive growthmedium.

In their book on biological control, Cookand Baker (1983) presented only one ex-

ample of the biological control of a post-harvest disease of a fruit or vegetable. Thiswas the biological control of botrytis rot ofstrawberry (Fragaria ananassa) with Tr i-choderma sp. (Tronsmo and Dennis, 1977).Since that time, there has been a wealth ofresearch conducted in this area, mostly onfruit diseases, and several antagonists havebeen identified. The topic has also been thesubject of several reviews (Janisiewcz, 1988a;Jeffries and Jeger, 1990; Wilson and Pusey,1985; Wilson and Wisniewski, 1989, 1991;Wilson et al., 1991).

Amenable to a formulation with a long shelf life.Easy to dispense.Does not produce metabolites that are deleterious

to human health.Resistant to pesticides.Compatible with commercial processing proce-

dures.Nonpathogenic to host commodity.

In general, the mode of action of many ofthe antagonists that have been identified foruse in controlling postharvest diseases is

poorly understood. In the absence of the pro-duction of antibiotics, it appears that the modeof action involves a complex syndrome ofcharacters (Droby et al., 1989, 1991; Wis-niewski et al., 1989, 1991), including nu-

trient competition, site exclusion, attachmentof the antagonist to the pathogen, inducedresistance, and, perhaps, direct parasitism.Undoubtedly, many of the evolving conceptsfor biocontrol of plant diseases also wouldapply to the postharvest arena. Additionally,as Baker (1987) has indicated, many undis-cerned mechanisms have evolved and arefunctioning in the natural world. As researchon biological control of postharvest diseasescontinues, our knowledge likely will in-crease rapidly by drawing from and buildingon the base of information developed in otherareas of biocontrol and phylloplane research.This base of knowledge should allow the de-

velopment of more reliable procedures forthe effective application of known antago-nists and also provide a rationale for effi-ciently selecting other effective antagonists(Wilson and Wisniewski, 1989).

Table 2. Reports of postharvest biological control.

Commodity Disease Biocontrol agent Reference

Apple

Microbial antagonists have been reportedto control several rot pathogens on diversecommodities (Table 2). Of particular interest

among these antagonists are yeasts and yeast-like organisms, such as Pichia guill iermon-di iWickerham, isolated and developed byWilson and Chalutz (1989) and subsequent co-workers (Droby et al., 1989, 1991; Mc-Laughlin et al., 1990a, Wisniewski et al.,1991), for control of postharvest rots of cit-rus and other fruits; Acremonium breve(Su-kapure and Thiramalachar) W. Gams, isolatedby Janisiewicz (1988b); and several speciesof Cryptococcus, isolated by Roberts (1990a,1990b), for control of postharvest rots of ap-ple (M alus domesticaBorkh.) and pear (Py-rus communi sL.). As indicated by Janisiewicz(1988a), yeasts can colonize a surface for

long periods under dry conditions, produceextracellular polysaccharides that enhancetheir survivability and restrict both coloni-zation sites and the flow of germination cuesto fungal propagules, use available nutrientsrapidly and proliferate, and are impactedminimally by pesticides. These are featuresthat can greatly enhance the effectiveness ofany antagonist that is identified for its po-tential use in the postharvest environment.The effectiveness of the yeastPichiu guil-liermondii, previously classified asDebar-yomyces hansenii (McLaughlin et al., 1990a),is highly effective in controlling botrytis rot

Blue moldBlue moldBlue moldBlue moldGray mold

Pseudomonas syringaePseudomonas cepaciaCryptococcus spp.

Pichia guilliermondiiPichia guilliermondii

Citrus

Citrus

Gray moldGray mold

Gray moldGray moldMucor rotGreen mold

Pseudomonas cepaciaC. laurentii

C. flavus, C. albidusAcremonium brevePseudomonas cepaciaPichia guilliermondii

Pear

Green moldBlue moldSour rotSour rotSour rotStem end rotBlue moldGray moldGray moldMucor rot

Janisiewicz, 1987Janisiewicz and Roitman, 1988Roberts, 1991McLaughlin et al., 1990bWisniewski et al., 1988;

McLaughlin et al., 1990bJanisiewicz and Roitman, 1988Roberts, 1990a

Roberts, 1991Janisiewicz, 1988bJanisiewicz and Roitman, 1987Chalutz and Wilson, 1990; Wilson

and Chalutz, 1989Singh and Deverall, 1984Chalutz and Wilson. 1990Chalutz and Wilson; 1990Singh and Deverall, 1984De Matos, 1983Singh and Deverall, 1984Janisiewicz and Roitman, 1988Janisiewicz and Roitman. 1988Mao and Cappellini, 1986Roberts, 1990b

Nectarine

PeachPeachApricotPlumCherry

Grape

Tomato

StrawberryPineapple

Brown rot

Brown rotRhizopus rotBrown rotBrown rotAlternaria rotBrown rotGray moldGray moldRhizopus rotGray moldAlternaria rotGray moldPenicillium rot

Bacillus subtilisPichia guilliennondiiPichia guilliermondiiB. subtilisTrichodenna sp.

B. subtilisPseudomonas cepaciaPseudomonas cepaciaPseudomonas gladioliC. laurentii,

C. flaws, C. albidusB. subtilis

B. subtilisEnterobacter cloacaeB. subtilisB. subtilisE. aerogenesB. subtilisTrichoderma harzianum

Pichia guilliermondiiPichia guilliermondiiPichia guilliermondiiPichia guilliermondiiTrichoderma sp.Attenuated strains

ofPenicillium sp.

Pusey and Wilson, 1984

Pusey and Wilson; 1984Wilson et al., 1987Pusey and Wilson, 1984Pusey and Wilson, 1984Utkhede and Sholberg, 1986Utkhede and Sholberg, 1986Dubos, 1984Chalutz et al., 1988Chalutz et al., 1988Chalutz et al., 1988Chalutz et al., 1988Tronsmo and Dennis, 1977Tong-Kwee and Rohrbock, 1980

Potato Soft rot Pseudomonas putida Colyer and Mount, 1984

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Fig. 1. Biological control of gray mold (Botrytis cinerea Pers.:Fr) on apple (la) and green mold [Penicillium digitatum (Pers.:Fr) Sacc.] on oranges (lb)with the use of the antagonistic yeastPichia guilliermondii (strain 87). Photographs were taken 1 week after wounding and application of the yeast andpathogen to the wound site.

Postharvest biological control-Commercialization

Commercialization of an antagonist re-quires the integration of biological controlmeasures with current handling practices.Pusey et al. (1986, 1988) were able to in-corporate the antagonist B. subtilis into thefruit wax used commercially to treat peaches

on the packing line. In these pilot tests, theuse of the antagonist gave a level of protec-tion similar to that obtained with wax plusthe fungicide methyl 1-(butylcarbamoyl)-2-

benzimi-clazolecarbamate (benomyl).McLaughlin et al. (1990b) demonstrated

that the addition of 2% calcium chloride tothe yeast suspension greatly enhanced theability of the yeastP. guilliermondii to con-

trol postharvest diseases of apples. This al-lowed a significant reduction in the amountof yeast biomass needed to achieve control.Further, initial pilot tests ofP. guilliermon-dii on citrus (Hofstein et al., 1991) have in-dicated that biocontrol activity of the yeastcan be significantly enhanced with the ad-dition of 10% of the normally recommendedrate of the fungicide thiabendazole. These

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reports suggest that biocontrol procedures canbe integrated into the commercial post-harvest operation.

As Wilson and Wisniewski (1992) haveindicated, the application of antagonistic mi-croorganisms to food that is to be consumed

presents special problems. Public reaction tothe application of living fungicides to foodis yet to be determined. The use of antago-nists that produce antibiotics as their prin-cipal mode of action will also raise additionalconcern. The potential exists that exposure

of human and animal pathogens to such an-tibiotics may cause resistance to develop to

potentially effective therapeutic compounds.Possible pathogenicity to man and other an-imals, as well as a wide range of harvestedcommodities, must be considered. In select-ing antagonists as biological control agentson food, attention should be given to these

potential problems. However, microorgan-isms have been used since ancient times to

pickle and ferment foods to preserve them(Gilliland, 1985). Among the wide array ofantagonists available, selection of safe andeffective biocontrol agents should be possi-

ble.

The publics demand for reduced pesti-cides in our food and the environment hascaused an energetic debate over the safenessof our present control practices for post-harvest diseases. As researchers, we havethe challenge and opportunity to develop safeand effective alternatives to present-day syn-thetic fungicides. The climate for support of

biological control research is now excellent.There is every indication that significant ad-vances will be made and commercially avail-able products will be available for postharvestuse in the near future.

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