Exploitation of natural products as an alternative strategy to control postharvest fungal rotting of fruit and vegetables

Postharvest Biology and Technology 32 (2004) 235–245

Review

Exploitation of natural products as an alternative strategy to control postharvest fungal rotting of fruit and vegetables Pramila Tripathi∗ , N.K. Dubey Department of Botany, Banaras Hindu University, Varanasi 221005, India Received 7 February 2003; accepted 7 November 2003

Abstract Chemical fungicides provide the primary means for controlling postharvest fungal decay of fruit and vegetables. Continuous use of fungicides has faced two major obstacles—increasing public concern regarding contamination of perishables with fungicidal residues, and proliferation of resistance in the pathogen populations. The ultimate aim of recent research in this area has been the development and evaluation of various alternative control strategies to reduce dependency on synthetic fungicides. Several non-chemical treatments have been proposed for fungal decay control. Although these approaches have been shown to reduce postharvest rots of fruit and vegetables, each has limitations that can affect their commercial applicability. When used as stand-alone treatments, none of the non-chemical control methods has been clearly shown to offer a consistently economic level of disease control that warrants acceptance as an alternative to synthetic fungicides. Recently, the exploitation of natural products to control decay and prolong storage life of perishables has received more and more attention. Biologically active natural products have the potential to replace synthetic fungicides. This review deals with exploitation of some natural products such as flavour compounds, acetic acid, jasmonates, glucosinolates, propolis, fusapyrone and deoxyfusapyrone, chitosan, essential oils and plant extracts for the management of fungal rotting of fruit and vegetables, thereby prolonging shelf life. © 2003 Elsevier B.V. All rights reserved. Keywords: Postharvest diseases; Jasmonates; Essential oils; Plant extracts; Flavour compounds; Natural products; Glucosinolates; Fusapyrone; Propolis; Chitosan

1. Introduction Considerable postharvest losses of fruit and vegetables are brought about by decay caused by fungal plant pathogens. Fruit, due to their low pH, higher moisture content and nutrient composition are very susceptible to attack by pathogenic fungi, which in ∗

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addition to causing rots may also make them unfit for consumption by producing mycotoxins (Phillips, 1984; Moss, 2002). Eckert and Ratnayake (1983) estimated that out of 100,000 species of fungi, less than 10% are plant pathogens and more than 100 species of fungi are responsible for the majority of postharvest diseases. International agencies that monitor world food resources have acknowledged that one of the most feasible options for meeting future food needs is reduction of postharvest losses (Kelman, 1984).

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Although it is very difficult to determine the full extent of postharvest losses due to decay, which varies widely with commodity, production area and season, it is well known that these losses are significant (Eckert, 1975; Burchill and Maude, 1986; Pathak, 1997), and conservative estimates place losses of perishable commodities at 50% in under-developing and tropical countries (Coursey and Booth, 1972; Jeffries and Jeger, 1990).

2. Synthetic chemicals and postharvest diseases Fungicides are the primary means of controlling postharvest diseases. Their world-wide use is variable, comprising 26% of the plant protection market in Europe and Asia and 6% in the US (Jutsum, 1988). About 23 million kg of fungicides are applied to fruit and vegetables annually, and it is generally accepted that production and marketing of these perishable products would not be possible without their use (Ragsdale and Sisler, 1994). However, as harvested fruit and vegetables are commonly treated with fungicides to retard postharvest diseases, there is a greater likelihood of direct human exposure to them than to chemicals that are applied solely to protect foliage. Further, the use of synthetic chemicals to control postharvest deterioration has been restricted due to their carcinogenicity, teratogenicity, high and acute residual toxicity, long degradation period, environmental pollution and their effects on food and other side-effects on humans (Lingk, 1991; Unnikrishnan and Nath, 2002). As well, phytotoxic and off-odour effects of some prevalent fungicides have limited their use. One problem with these synthetic chemicals is that as their potency has been enhanced, so has been their side-effects, and also their cost (Tyler, 1992; Castro et al., 1999; Falandysz, 2000; Kast-Hutcheson et al., 2001; Sorour and Larink, 2001). In addition, synthetic fungicides can leave significant residues in treated commodities (Parmar and Devkumar, 1993; Fernandez et al., 2001; Dogheim et al., 2002; Zahida and Masud, 2002). Development of resistance to commonly used fungicides within populations of postharvest pathogens has also become a significant problem (Reimann and Deising, 2000; Dianz et al., 2002). For example, many synthetic fungicides are currently used to control blue mould rot of citrus fruit. However, acquired resistance

by Penicillium italicum and Penicillium digitatum to fungicides used on citrus fruit has become a matter of much concern in recent years (Fogliata et al., 2001). The side-effects of synthetic fungicides means that alternative strategies need to be developed for reducing losses due to postharvest decay that are perceived as safe by the public and pose negligible risk to human health and environment (Wilson et al., 1999). The use of non-chemical methods and non-selective fungicide treatments may provide a part of this need. Inoculum reduction achieved through sanitation and exclusion (Bancroft et al., 1984), the use of non-selective fungicides (sodium carbonate, sodium bicarbonate, active chlorine and sorbic acid) and physical treatments such as heat therapy, low temperature storage, hot water treatments and radiation can significantly lower the disease pressure on harvested commodities (Eckert, 1991; Lurie, 2001). Harvesting and handling techniques that minimise injury to the commodity, along with storage conditions that are optimum for maintaining host resistance (Sommer, 1985) will also aid in suppressing disease development after harvest. However, none of these treatments are consequently effective, and many cause damage to the commodities.

3. Biocontrol agents in management of postharvest diseases Considerable attention has also been given to the potential of biological control of postharvest diseases of fruit and vegetables as a viable alternative to the use of present day synthetic fungicides (Wilson and Wisniewski, 1989; Wilson et al., 1999; Pang et al., 2002). Microbial antagonists have been reported to protect a variety of harvested perishable commodities against a number of postharvest pathogens (Wisniewski et al., 2001). However, decreasing efficacy and lack of consistency when these methodologies are applied as stand-alone treatments under commercial conditions (Droby et al., 2001) is limiting their use. These drawbacks in alternative methods have increased interest in developing further alternative control methods, particularly those which are environmentally sound and biodegradable. Thus, replacement

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of synthetic fungicides by natural products (particularly of plant origin), which are non-toxic and specific in their action, is gaining considerable attention. This review deals with exploitation of natural products such as flavour compounds (e.g. acetaldehyde, benzaldehyde, hexanal, etc.) acetic acid, jasmonates, glucosinolates, propolis fusapyrone and deoxyfusapyrone, chitosan, essential oils, active principles of some plants, and plant extracts in the management of decay of fruit caused by plant pathogenic fungi. 3.1. Flavour compounds Fruit and vegetables have a number of constitutive and inducible compounds that are antimicrobial and such compounds have not been fully explored as biological control agents for postharvest disease (Culter et al., 1986). Such compounds could be extracted and applied to other harvested perishables. The flavour compounds are secondary metabolites having unique properties of volatility, and fat and low-water solubility. Being volatile, not very water soluble, and easily adsorbed, they are very useful in postharvest protection. Many such compounds would be harmless in mammalian systems and there would be less chance of any off-odours in treated perishables. Many volatiles express their effects at very low concentration. As potential fungicides, their natural occurrence as part of the human diet, their ephemeral nature, and their biodegradability suggest low toxic residue problems. Wilson et al. (1987) found that a number of fruit volatiles produced by peaches as they ripen are highly fungicidal. Acetaldehyde has been used as a fumigant to control the green peach aphid on head lettuce (Stewart et al., 1980). Shaw (1969) suggested that rot resistance of strawberries in high CO2 storage was due to the production of high levels of acetaldehyde and ethyl acetate by the fruit in response to these conditions. Prasad and Stadelbacher (1973) controlled Botrytis cinerea with acetaldehyde vapour. Acetaldehyde has been tested against decay micro-organisms commonly found on strawberry fruit such as B. cinerea and Rhizopus stolonifer (Avissar and Pesis, 1991). In addition, acetaldehyde has also been reported to inhibit postharvest micro-organisms such as Erwinia carotovora, Pseudomonas fluorescens, Monilinia fructicola (Aharoni and Stadelbacher, 1973), Penicillium spp. (Stalelbacher and Prasad,

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1974), and various species of yeast (Barkai-Golan and Aharoni, 1976) commonly found on fruit and vegetables. Some plant volatiles, e.g. acetaldehyde, benzaldehyde, cinnamaldehyde, ethanol, benzyl alcohol, nerolidol, 2-nonanone have also been found to have antifungal activity against the fruit and vegetable pathogens P. digitatum, R. stolonifer, Colletotrichum musae and Ervinia caratovora during in vitro trials (Utama et al., 2002). Benzaldehyde has been used in the laboratory to fumigate peaches and to protect them against Rhizopus rot, and it totally inhibited spore germination of B. cinerea at 25 ␮l l−1 and germination of M. fructicola at 125 ␮g l−1 (Wilson et al., 1987). (E)-2-Hexenal, another ubiquitous volatile (Hatanaka, 1993), is strongly antifungal in nature and its activity has been reported by a number of workers against B. cinerea (Hamilton-Kemp et al., 1992; Fallik et al., 1998). Archbold et al. (1999) showed it to be an efficient fumigant in controlling mold on seedless table grapes. Hexenel vapour inhibited hyphae growth of Penicillium expansum and B. cinerea in vitro and on apple slices (Song et al., 1996). This raises the possibility of developing a system for treating apple slices with hexenel in modified atmospheres and packages. Hexenel vapours have a number of attributes that may be important in consumer demand for more natural control measures for fruit diseases with fewer toxic residues. Six carbon (C6 ) aldehydes have been found to inhibit the hyphal growth of Alternaria alternata and B. cinerea (Hamilton-Kemp et al., 1992). These aldehydes, with or without double bonds, are dominant compounds released by plant material through the lipoxygenase pathway after tissue damage (Vick and Zimmerman, 1987). They are also important precursors for the formation of C6 alcohols and C6 esters, which are among the most abundant volatile components in apple, pear, and banana, and contribute to typical fruity odours (Paillard, 1986, 1990). This suggests that hexenal and similar aldehydes may have a use as antifungal agents with fruit such as pears, strawberries, bananas, pineapples and melons. Use of these aldehydes in packaging of highly processed products of these commodities also seems to be a possible future option. However, practical doses of these compounds still need to be worked out, particularly in relation to any mammalian toxicity that might occur.

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3.2. Acetic acid Effective surface sterilisation by suitable chemicals may lead to extended storage or shelf life of some fruit. Acetic acid fumigation offers promise as a method for surface-sterilising a wide range of fruit and possibly vegetables. Acetic acid is a metabolic intermediate that occurs naturally in many fruit (Nursten, 1970).The inhibitory effect of acetic acid on micro-organisms is greater than that due to pH alone and the undissociated acetic acid can penetrate the microbial cell to exert its toxic effect (Banwart, 1981). Sholberg and Gaunce (1995) showed that low concentrations of acetic acid in air were extremely effective for control of B. cinerea conidia on apple fruit without phytotoxic effect. Fumigation with acetic acid protected grapes from spoilage for up to 2 months in modified atmosphere packaging at 0 ◦ C, and presents a possible alternative for extending shelf life of grapes (Moyls et al., 1996). Acetic acid vapour is also a potential replacement for sulphur dioxide currently used to control decay in stored table grapes. Sholberg and Gaunce (1995) have suggested that acetic acid vapour initially sterilises the fruit surface, killing surface borne spores. There are several advantages in using acetic acid fumigation. It is a natural compound found throughout the biosphere, posing little or no residual hazard at the low levels required to kill fungal spores. In addition, it is inexpensive, compared to other fumigants such as acetaldehyde, and can be used in relatively low concentrations, and it can be used to treat produce in air-tight storage rooms or containers without requiring handling of the produce. Acetic acid has been shown to be an effective fumigant for commercial use on apricot and plums (Liu et al., 2002), grapes (Sholberg et al., 1996) and sweet cherries (Sholberg, 1998; Chu et al., 1999, 2001). The use of vinegar is even safer and still effective (Sholberg et al., 2000). 3.3. Jasmonates Jasmonic acid (JA) and methyl jasmonates (MJ) collectively referred to as jasmonates, are naturally occurring plant growth regulators that are widely distributed in the plant kingdom, and are known to regulate various aspects of plant development and responses to environmental stresses (Sembdner and Parthier, 1993; Creelman and Mullet, 1995, 1997). Jasmonates are a

class of olypines derived from oxygenase-dependent oxidation of fatty acids. Several lines of evidence suggest that jasmonates play an important role as signal molecules in plant defence responses against pathogen attack. Jasmonic acid accumulates in plant tissues or in cell cultures treated with elicitors of plant defence mechanisms (Gundlach et al., 1992; Doares et al., 1995; Nojiri et al., 1996). Several jasmonates have been shown to activate genes encoding antifungal proteins such as thionin (Andresen et al., 1992), osmotin (Xu et al., 1994), a novel ribosome inactive protein RIP (Chaudhry et al., 1994), and several other genes involved in phytoalexin biosynthesis (Creelman et al., 1992; Gundlach et al., 1992). Recently, it was reported that MJ can be applied effectively, as a postharvest treatment, to suppress grey mold rot caused by B. cinerea in strawberry (Moline et al., 1997). Droby et al. (1999) found that postharvest application of jasmonates reduced decay caused by the grey mold, P. digitatum either after natural or artificial inoculation of “Marsh Seedless” grapefruit. The volatility of MJ allows treatments to be applied without immersing fruit in water. Methyl jasmonate has a pleasant aroma and its chemical properties result in surface binding to polymeric materials, which may prolong MJ presence in storage rooms or fumigation chambers. Jasmonic acid, being more soluble in water, is suitable for use in solution as a drench or dip. When applied at low concentrations, jasmonates are potential postharvest treatments to enhance natural resistance and to reduce decay in fruit. Since they are naturally occurring compounds and are given in low doses, jasmonates may provide a more environment-friendly means of reducing the current chemical usage. 3.4. Glucosinolates Among natural substances with potential antimicrobial activity are the glucosinolates, a large class of approximately 100 compounds produced by the Crucifereae, with well-documented activity (Fenwick et al., 1983). Hydrolysis of glucosinolates produces dglucose, sulphate ion and a series of compounds such as isothiocyanate (ITC), thiocyanate and nitrile. The antifungal activity of six glucosinolates has been tested on several postharvest pathogens, both in vitro (Mari et al., 1993) and in vivo (Mari et al., 1996) with encour-

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aging results. In particular, glucoraphenine ITC was active against Monilinia laxa in artificially-inoculated pears. Allyl-isothiocyanate (AITC), a naturally occurring flavour compound in mustard and horseradish, has a well-documented antimicrobial activity (Ishiki et al., 1992; Delaquis and Mazza, 1995). This volatile substance can be employed successfully in modified atmosphere packaging or as a gaseous treatment before storage. Exposure of pear fruit to an AITC-enriched atmosphere resulted in good control of blue mould, including a TBZ-resistant strain on pears (Mari et al., 2002).The use of AITC, produced from purified sinigrin or from Brassica juncea, against P. expansum appears very promising as an economically viable alternative with moderately low impact on the environment (Mari et al., 2003). 3.5. Propolis Propolis is natural resinous substance obtained from leaf buds and bark of poplar and conifer trees. Propolis contains protein, amino acids, vitamins, minerals and flavonoids (Moreira, 1986; Walker and Crane, 1987; Stangaciu, 1997). It has antibiotic activity, antibacterial and antifungal activity (Tosi et al., 1996). Propolis has been found to inhibit the postharvest pathogens B. cinerea and P. expansum (Lima et al., 1998). 3.6. Fusapyrone and deoxyfusapyrone An antifungal metabolite named fusapyrone has been purified and characterised from cultures of Fusarium semitectum isolated from soil. The inhibitory activity of fusapyrone against growth of B. cinerea has been assayed in vitro and in vivo on grapes. Significant inhibition of conidia germination of B. cinerea has been recorded and grapes treated with 100 ␮g ml−1 of fusapyrone inhibited the development of grey mould on damaged grapes (Altomare et al., 1998). Low toxicity towards animals and absence of phytotoxic effects of fusapyrone have promoted its use in control of B. cinerea on grapes and other crops (Altomare et al., 2000). 3.7. Chitosan Chitosan is soluble form of chitin. Chitosan and its derivatives have plant protective and antifungal

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properties. They can trigger defensive mechanisms in plants against pathogenic attacks at very low concentrations. They can also be used in solution, powder form or as wettable coatings of seeds and fruit (Choi et al., 2002). Chitosan has been used as an alternative control agent against blue mould in harvested ‘Red Delicious’ apple fruit and has been shown to induce resistance in the fruit rather than merely inhibiting the pathogen directly (Capdeville et al., 2002). 3.8. Essential oils The general antifungal activity of essential oils is well documented (Reuveni et al., 1984; Deans and Ritchie, 1987; Alankararao et al., 1991; Baruah et al., 1996; Gogoi et al., 1997; Pitarokili et al., 1999; Meepagala et al., 2002) and there have been some studies on the effects of essential oils on postharvest pathogens (Bishop and Thornton, 1997). The advantage of essential oils is their bioactivity in the vapour phase, a characteristic that makes them attractive as possible fumigants for stored product protection. These essential oils are thought to play a role in plant defence mechanisms against phytopathogenic micro-organisms (Mihaliak et al., 1991). Most of the essential oils have been reported to inhibit postharvest fungi in in vitro conditions (Bishop and Reagan, 1998; Singh and Tripathi, 1999; Bellerbeck et al., 2001; Hidalgo et al., 2002). However, the in vivo efficacy and practical activity of only a few of the essential oils have been studied. Some of the essential oils have been reported to protect stored commodities from biodeterioration. There are also some reports on essential oils in enhancing storage life of fruit and vegetables by controlling their fungal rotting. Dubey and Kishore (1988) found that the essential oils from leaves of Melaleuca leucadendron, Ocimum canum and Citrus medica were able to protect several stored food commodities from biodeterioration caused by Aspergillus flavus and Aspergillus versicolor. These oils were active at between 500 and 2000 ␮g ml−1 . The potential of using essential oils by spraying or dipping to control postharvest decay has been examined in fruit and vegetables (Tiwari et al., 1988; Smid et al., 1994; Dixit et al., 1995). Thymol is an essential oil component from thyme (Thymus capitatus) and has been used as medicinal drug, food preservative, and beverage ingredient (Jain,

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1985; Mansour et al., 1986). Fumigation of sweet cherries with thymol was effective in controlling postharvest grey mold rot caused by B. cinerea (Chu et al., 1999), and brown rot caused by M. fructicola (Chu et al., 2001). Fumigation with thymol at 30 mg l−1 reduced the incidence of grey mold rot from 35% in untreated fruit to 0.5%. Liu et al. (2002) also found that thymol was more effective for controlling brown rot symptoms on apricots, and fumigation of plums with relatively low concentrations such as 2 or 4 mg l−1 can greatly reduce postharvest decay without causing any phytotoxicity. The US Food and Drug Administration lists thymol, thymol essential oil and thyme (spice) as food for human consumption, as well as food additives. Thymol was initially registered as a pesticide in the US in 1964. Recently, carvone, a monoterpene, isolated from the essential oil of Carum carvi has been shown to inhibit sprouting of potatoes during storage and it also exhibited fungicidal activity in protecting the potato tubers from rotting without altering taste and quality of the treated commodity, and without exhibiting mammalian toxicity (Hartmans et al., 1995; Oosterhaven, 1995). It has been introduced under the trade name TALENT in The Netherlands. The essential oil of Salvia officinalis has also shown practical potency in enhancing the storage life of some vegetables by protecting them from fungal rotting (Bang, 1995). Treatment of oranges with the essential oils of Mentha arvensis, O. canum and Zingiber officinale has been found to control blue mold, thereby enhancing shelf life (Tripathi, 2001).The fungitoxic potency of the essential oils may be due to synergism between their components. Thus, there would be negligible chance of development of resistant races of fungi after application of essential oils to fruit and vegetables. Although the fungitoxic properties of the volatile constituents of higher plants have been reported, little attention has been paid to the fungitoxicity of these substances when combined. This information is desirable since the fungitoxic potency of most of the fungicides has been reported to be enhanced when combined (Levy et al., 1986; Gullino and Garibaldi, 1987; Migheli et al., 1988; Pandey and Dubey, 1997). The enhancement of fungitoxic potential of mixtures of the oils may be due to the joint action of two or more substances present in the oils (Scardavi, 1966). This syn-

ergism would be beneficial in postharvest protection because the pathogen would not easily produce resistance against the components. However, more work on synergistic action of plant products in in vitro and in vivo conditions is required. The literature is also silent on the mode of action of the essential oils when used as postharvest fungitoxicants. 3.9. Plant extracts The preservative nature of some plant extracts has been known for centuries and there has been renewed interest in the antimicrobial properties of extracts from aromatic plants. Some plants extracted in different organic solvents have shown inhibitory action against different storage fungi (Singh et al., 1993; Mohamed et al., 1994; Hiremath et al., 1996; Kapoor, 1997; Radha et al., 1999; Rana et al., 1999). However, active principles of some of plants have been isolated phytochemically and have shown strong inhibitory action against postharvest fungi. Four compounds, irilin A, irilin B, the flavonone dihydrowogonin and sesquiterpene pygmol, were isolated from dichloromethane extract of the aerial parts of Chenopodium procerum. The latter three compounds inhibited the growth of the plant pathogenic fungus Cladosporium cucumerinum (Bergeron et al., 1995). A naturally occurring compound isolated from the flavedo tissue of “Star Ruby” grapefruit (Citrus paradisi) identified as 7-geranoxy coumarin exhibited antifungal activity against P. italicum and P. digitatum during in vitro and in vivo tests (Agnioni et al., 1998). In vitro inhibition of Botryodiplodia theobromae causing Java black rot in sweet potato was induced by phenolic compounds, chlorogenic acid giving the highest in vitro inhibition followed by pyrogallol, pyrocatechol, phenol and resorcinol. Mohapotra et al. (2000) concluded that low concentrations of phenols (3–5 ␮g ml−1 ) are required by the fungus during normal metabolism but higher concentrations (approximately 20 ␮g ml−1 ) are inhibitory to growth. The aqueous extract of Acacia nilotica showed pronounced antifungal activity against P. italicum and enhanced the shelf life of oranges for 6 days. The phytochemical investigation of a methanolic extract of A. nilotica resulted in the isolation of six compounds, sitosterol, ␣-amyrin, naringenin-5-methyl ether, kaempferol, kaempferol-3-O-rhamnoside and

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myrecetine-3-O-rhamnoside. Of these compounds, kaempferol has shown antifungal activity against P. italicum (Tripathi et al., 2002). Investigation on the mode of action and practical applicability of such plant products is required so as to recommend their formulation in control of postharvest diseases.

4. Conclusion Encouraging results on the use of natural products to control postharvest fungal rotting indicate that we should be able to develop natural fungicides that would be as effective as synthetic fungicides, and presumably safer for man and the environment. Although about 10,000 secondary plant metabolites have been chemically defined for their role as anti-pathogenic chemicals, the total number of plant chemicals available could amount to 400,000 or more (Ahmed, 1987). Many of these substances can play a fundamental role in host–pathogen interaction. Biological compounds because of their natural origin are comparatively biodegradable and most of them are almost non-residual in nature (Beye, 1978). Several plants have thousands of years of history and their non-toxicity, at least at an oral level, is proven. This safety feature is very important in formulations of such products for commercial purposes because it has an impact on the cost of development and registration of a new pesticide product. The research and development costs of botanical fungicides from discovery to marketing is much less compared to that of chemical fungicides. Most chemical fungicides have a long 7–10 years development period and registration time frame, with high registration costs. This expense is in large part due to the concern over possible high animal toxicities of such materials that necessitate long-term toxicological testing on experimental animals. Biologicals, because of their target specificity, typically require only short-term toxicological tests (Carlton, 1988; Satyanarayan and Sharma, 1993). Although the exploitation of natural products to protect the postharvest decay of perishable products is in its infancy, these products have the potential to be safe fungicides and will replace the synthetic ones. A consolidated and continuous search of natural products may yield safer alternative control measures comparable to azadirachtin and pyrethryoids which are being

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used in different parts of the world as ideal natural fungicides. Proper organoleptic tests are also necessary before any recommendation. The product should be effective even for short duration treatments due to the limited postharvest life of fruit. The treatment should not have an effect on quality parameters such as acidity, flavour and aroma. The lowest suitable dose of the chemicals for practical application should also be determined. Keeping in view the merits of the botanicals as postharvest fungitoxicants, the products which are found efficacious during in vitro testings, should be properly tested for their practical potency based on in vivo trials, organoleptic tests and safety limit profile.

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