World Applied Sciences Journal 31 (5): 785-793, 2014
ISSN 1818-4952
© IDOSI Publications, 2014
DOI: 10.5829/idosi.wasj.2014.31.05.14534
Exploitation of Yeasts as an Alternative Strategy to
Control Post Harvest Diseases of Fruits-A Review
V. Yeka Zhimo, Dawa Dolma Bhutia, Jayanta Saha and Birendranath Panja
Department of Plant Pathology, Bidhan Chandra Krishi Viswavidyalaya,
Mohanpur, Nadia-741252, West Bengal, India
Abstract: There is an increasing concern about the environmental effects and safety of chemical pesticides
and fungicides all over the world. Microbial biocontrol agents possess a number of important advantages over
traditional chemical pesticides which make their commercial outlook particularly promising and can be
commercially developed with relative ease to control post harvest diseases of fruits. Biological control of
different plant diseases was focused primarily using bacteria or filamentous fungi and so, application of yeasts
as biocontrol agents acts as a new trend against different pathogens. Various observations suggest that
competition for space and nutrients between yeasts and pathogens, antibiosis, parasitism, induction of host
resistance and also resistance to oxidative stress are likely to be the main mechanisms of action. In order to
enhance biocontrol activity of antagonists against fungal pathogens, certain strategies, such as adding calcium
salts, carbohydrates, amino acids and other nitrogen compounds to biocontrol treatments are proposed and
can prove more beneficial than using yeasts alone. A more thorough understanding of the mechanisms of
action, interactions of fruit tissue-pathogen-biocontrol agent and effective formulation techniques are still
needed to develop these yeasts into potential candidates in the management of post harvest diseases of fruits.
Key words: Biological control
Fruits
Post-harvest diseases
INTRODUCTION
Post harvest diseases of fruits caused by pathogens
pose a major challenge throughout the fruit growing
areas of the world accounting to about 20-25% of the
harvested during postharvest handling [1-4] in developed
countries and even more exasperating in the developing
countries, where it often exceeds over 35%, due to
inadequate storage, processing and transportation
facilities [5]. A side from direct economic considerations,
diseased produce poses a potential health risk. In most
cases, fresh produce which is obviously diseased would
not be consumed. A number of fungal genera such as
Aspergillus, Penicillium, Alternaria and Fusarium are
known to produce mycotoxins under certain conditions.
Generally speaking, the greatest risk of mycotoxin
contamination occurs when diseased fruit produce is used
in the production of processed food. Losses due to
postharvest disease are affected by a great number of
factors including: commodity type, the postharvest
Yeasts
environment (temperature, relative humidity, atmosphere
composition, etc.), produce handling methods, post
harvest hygiene, produce maturity and ripeness stage,
cultivar susceptibility to postharvest diseases and
treatments used for disease control. Fungicides are
commonly used to control these post harvest decays.
However, though harvested fruits treated with fungicides
retard post harvest diseases, there is a greater likelihood
of direct human exposure to them. Synthetic chemicals
are also discouraged due to their carcinogenicity,
teratogenicity, high and acute residual toxicity,
environmental pollution and their effects on food and
side effects on humans [6-7]. Besides these, phytoxicity
and off odour effects of some fungicides have limited their
use. Development of resistance to commonly used
fungicides within populations of post harvest pathogens
has also become a significant problem. For example,
acquired resistance by Penicillium italicum and
Penicillium digitatum to fungicides used for treating
citrus fruits has been reported [8]. This calls for a new
Corresponding Author: V. Yeka Zhimo, Department of Plant Pathology,
Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, Nadia-741252, West Bengal, India.
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World Appl. Sci. J., 31 (5): 785-793, 2014
paradigm shift from the use of synthetic fungicides to a
safer and environmentally friendly alternative
for
reducing the postharvest decay in fruits and vegetables
[9-10].
In the last few years, biological control of
postharvest diseases of fruits has been developed as a
promising alternative to chemical control [11-12]. Among
the replete of bio-control approaches, the use of the
microbial antagonists like yeasts, fungi and bacteria is
quite promising and gaining popularity [2, 13- 19]. Among
the antagonistic microorganisms, natural yeasts have
been widely used as biological control agents [20].
Yeast based technologies and products (e.g Aspire®
containing Candida oleophila, Yield Plus® containing
C. albidus) for post harvest disease management of fruits
are already practiced and developed in foreign countries.
Unfortunately, no such technology or product (s) have
been developed in India although it is the major fruit
producing country in the world and very limited research
work on this aspect has been carried out.
The objective of this review is to critically assess the
use of yeasts as microbial antagonists for controlling
postharvest diseases of fruits, in order to reduce the use
of chemical agents that may be harmful to humans and the
environment.
sustain many of the pesticides used in the post-harvest
environment and can grow rapidly on cheap substrates in
fermenters and are therefore easy to produce in large
quantities. The suggested modes of action of biocontrol
yeasts are not likely to constitute any hazard for the
consumer. Furthermore, yeast cells contain high amounts
of vitamins, minerals and essential amino acids and
several reports on the beneficial effect of yeast addition
in both food and feed can be found in the literature
[21-23].
Mechanisms of Yeasts in Biological Control:
The mechanism by which the yeasts inhibits the target
pathogen is not clear and still incomplete due to the
difficulties encountered during the study of the complex
interactions between host, pathogen, antagonist and
other microorganisms present making it extremely
difficult to construct experiments that can exclude all
other possible mechanisms in the complex biocontrol
environment. However, several modes of action have
been suggested and so far no one single mechanism has
been shown to be responsible for the whole biocontrol
effect [15].
Competition for Space and Nutrition: Competition for
space and nutrients is the primary mechanism of action of
most of the biocontrol agents. Rapid colonization of fruits
by biocontrol agents is critical for decay control and
manipulations leading to improved colonization enhance
biocontrol [24]. They should be able to grow more rapidly
than the pathogen and should have the ability to survive
even under conditions that are unfavorable to the
pathogen. The biocontrol activity of some yeasts increase
with their increasing concentrations and decreasing
concentrations of pathogens. For example, Candida
saitona was effective at a concentration of 107 CFU/ml for
controlling Penicillium expansum on apples fruits and
less effective when concentrations were decreases [25].
In another study, it was reported that for Candida
saitona, a concentration of 108 CFU/ml was better in
controlling Penicillium expansum on apples [26].
This qualitative relationship, however, is highly
dependent on the ability of the antagonists to multiply
and grow at the wound site. This was demonstrated by
using a mutant of Pichia guilliermondii, which lost its
biocontrol activity against Penicillium digitatum on
grapefruit and against Botrytis cinerea on apples, even
when applied to the wounds at concentrations as high as
10 10 CFU/ml [14]. The cell population of this mutant
remained constant at the wound sites during incubation
What are yeasts?: Yeasts are a heterogenous group of
fungi that superficially appear to be homogeneous.
They grow in a conspicuous unicellular form that
reproduces by fission, budding, or a combination of both.
True
yeasts reproduce sexually,
developing
ascospores or basidiospores under favourable conditions.
The majority of ascomycetous and basidiomycetous
yeasts isolated in laboratories go unrecognized because
most of them are heterothallic. In most instances, only one
of the mating types is isolated and therefore no asci or
basidia are produced. Yeast-like fungi (imperfect yeasts)
reproduce only by asexual means. The identification of
these fungi is based upon a combination of morphological
and biochemical criteria. Morphology is primarily used to
establish the genera, whereas biochemical assimilations
are used to differentiate the various species. Several
important properties of yeasts make them stand out
among others for biological control purposes:
(i)Yeasts do not produce allergenic spores or
mycotoxins as many mycelial fungi do or antibiotic
metabolites as possibly produced by bacterial antagonists
(ii). They generally have simple nutritional requirements
and are able to colonize dry surfaces for long periods of
time. . (iii) They rapidly utilize available nutrients and can
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World Appl. Sci. J., 31 (5): 785-793, 2014
period, while that of the wild type increased 10- to 20-fold,
within 24 h hours. Competition for nutrients has been
suggested as the mode of action of several yeasts like
Pichia guilliermondii against Penicillium digitatum [27],
Candida guilliermondii, Cryptococcus laurentii and
Metschnikowia pulcherima against Botrytis cinerea and
Penicillium expansum [13, 28- 31]. It was demonstrated
that addition of exogenous nutrients reduced the
efficacy of P. guilliermondii against P. digitatum [27].
The antagonistic yeasts Candida lauretii and
Sporobolomyces roseus had stronger sugar consumption
than the pathogen B. Cinerea by blocking fungus
conidial germination due to the deprivation of nutrients
[32]. However, no differences in sugar consumption were
observed between yeasts with and without biocontrol
activity, suggesting that additional factors are part of the
inhibiting mechanisms. In fruit wounds, competition for
nutrients is probably extended to other nutrients, such as
nitrogen compounds present in low concentration. Both
organic and inorganic sources of nitrogen can be utilized
by yeast for growth. Amino acids, amines and urea are all
suitable sources of nitrogen for all yeasts, as inorganic
ammonium salts while nitrate utilization is confined to a
certain species or genera of yeasts and this is a valuable
diagnostic character used for identification purposes
too. Although very few species can hydrolyse
proteins extracellularly, short peptides can be transported
into the cell and utilized intracellularly [33]. In a tissue
culture plate system with membrane inserts separating
the organism, Janisiewicz et al., [34] were able to show
that the yeast Aureobasidium pullulans consumes the
amino acids and inhibits germination of P. expansum in
apple juice. A non-destructive method using tissue
culture plates: a defusing membrane at the lower end of
cylindrical inserts to o study the competition for nutrients
separated from the competition for space has been
developed [34].
registered for use on food or feed. Moreover, similar
problems with resistant pathogen strains, as experienced
today with fungicides, would probably rapidly occur if a
one-substance effect was the only mechanism involved.
Parasitism: Parasitism by yeasts has been suggested
as a fungus-inhibiting mechanism. The yeast Pichia
guilliermondii inhibits B. cinerea and adheres strongly
to the fungal mycelium [37]. It has also been shown that
P. anomala strain K has a strong production of
ß-1,3-glucanase enzyme that degrades the fungal cell wall
[38]. Aureobasidium pullulans
in apple wounds
produces extracellular exochitinase and -1,3-glucanase
which could play a role in the biocontrol activity [39].
Induction of Host Resistance: The characteristic defense
response in fruit includes production of inhibitors of cell
wall-degrading enzymes of the pathogen, activity of
antifungal compounds (such as phenolic compounds
and
phytolaexins),
active oxygen species and
reinforcement of the cell wall of the host [40]. The
resistance induction is due to the antagonist ability
to elicit host plant defense responses. It involves
several chemical or biochemical reactions in the host
tissue, including changes of tissue structure and
production of pathogenesis-related proteins, which
can be expressed locally or systemically [41-42].
P. guillermondii has been shown to stimulate the
production of ethylene in grapefruit [37]. Candida famata
(F35) stimulates the production of the phytoalexins,
scoparone and scopoletin in the wound site of oranges
[43]. Candida oleophila was found to induce resistance
to P. digitatum when applied in the surface of both
wounded and unwounded grapefruit [44]. Some Candida
strains are able to cause chemical and osmotic changes in
apple tissues and thus favouring antagonist settlement
[25]. P. guilliermondii strain has been shown to stimulate
the production of ethylene, a hormone in grapefruit able
to activate the phenylalaninammoniumlyase, an enzyme
involved in the synthesis of phenols, phytoalexins and
lignins [37]. Accumulation of phytoalexins, i.e., scoparon
and scopoletin has been observed in citrus fruits treated
with yeast cells [45].
Antibiosis: Production of antibiotic substances is a
commonly suggested mode of action for bacterial
biocontrol agents [35]. It has been shown that the yeast
Pseudozyma flocculosa produces extracellular fatty acids
that are detrimental to powdery mildew [36]. Biocontrol
agents producing antibiotic metabolites could be effective
against a wide range of target organisms, including
pathogens that have occurred prior to the application of
the biocontrol agent, as well as against latent infections.
However, given the current debate about the antibiotic
resistance of human pathogens it is doubtful that an
antibiotic-producing
biocontrol
agent would be
Resistance to Oxidative Stress: Resistance to oxidative
stress is another suggested mode of action of some
yeast. A model system consisting of two yeasts with
higher (Cryptococcus laurentii LS-28) or lower
(Rhodotorula
glutinis LS-11) antagonistic activity
against the postharvest pathogens Botrytis cinerea and
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Commercially Available Yeast Biocontrol Products:
There are currently three commercial yeast biocontrol
products available on the market for combating
post-harvest decays in fruit. Aspire® (Ecogen, Inc.,
Langhorne, Pa) is based on the yeast Candida oleophila
and is used as a spray or dip against post-harvest
diseases on pome and citrus fruits [15, 65]. The product
was introduced commercially in the United States in 1996.
The commercial product Yield Plus® with Cryptococcus
albidus as the active antagonist was introduced
commercially on the South African market in 1997 by
Anchor Yeast. Yield Plus® is used as a biocontrol
product against Botrytis, Penicillium and Mucor on
apples and pears and is also under evaluation for other
crops (Lisa Picard, Anchor Yeast, Cape Town, South
Africa, pers. comm.). The recent product Shemer®,
registered in Israel, is based on a newly identified yeast
Metschnikowia fructicola [66] and is effective against a
wide range of pathogens of grape, strawberry and sweet
potato.
Penicillium expansum was analysed and found that
Cryptococcus laurentii LS-28 exhibited faster and greater
colonization of wounds than Rhodotorula glutinis LS-11
[46]. In contrast to LS-28, the number of LS-11 cells
dropped 1 and 2 h after application and then increased
only later. In vitro, LS-28 was more resistant to
ROS-generated oxidative stress. The combined
application of biocontrol yeasts and ROS-deactivating
enzymes in apple wounds prevented the decrease in
number of LS-11 cells mentioned above and enhanced
colonization and antagonistic activity of both biocontrol
yeasts against B. cinerea and P. expansum.
To summarize, the activity of a biocontrol agent
seems to be primarily dependent on its ability to rapidly
colonize the wound site and compete for nutrients, but
may also depend on its ability to attach firmly to hyphae
of the pathogen, produce cell wall degrading enzymes
or volatile compounds, or induce host resistance.
An example: it has been demonstrated that direct
attachment, competition for nitrogen and carbon sources,
secretion of hydrolytic enzymes and induction of host
resistance play a role in the biocontrol mechanisms of
P. guilliermondii M8 against B. cinerea [47].
Combination of Some Safe Compounds with Yeasts:
Biological means cannot at the moment solve all the
problems of postharvest rots during fruit storage and
they must be considered instruments to be used in
combination with other methods in an integrated vision
of disease management. For example, biocontrol agents
can be combined with waxes and fungicides applied not
only in post but also in pre-harvest [67]. In order to
enhance biocontrol activity of antagonists against fungal
pathogens, certain strategies, such as adding calcium
salts, carbohydrates, amino acids and other nitrogen
compounds to biocontrol treatments, are proposed
[68-71]. Many researchers have shown that calcium
plays an important role in the inhibition of postharvest
decay of fruits [72-73]. Postharvest calcium treatment of
apples provided broad-spectrum protection against the
postharvest pathogens of Penicillium expansum and
Botrytis cinerea [74]. The addition of CaCl2 (2% w/v) to
the formulation of the yeast biocontrol agent, Candida
oleophila, enhanced the ability of this yeast to protect
apples against postharvest decay [75]. The efficacy of
controlling grey mould and blue mould rots in apples was
enhanced when Trichosporon sp., even at a low
concentration of 10 5 CFU mL ,1 was applied in the
presence of CaCl2 (2% w/v) in an aqueous suspension
[76]. However, application of 68 mM CaCl 2 to grapefruit
reduced the incidence of green mold decay by 43%
and in combination with an antagonist P. guilliermondi
strain US-7 by 97% [77]. Other compounds like
sodium bicarbonate and ammonium molybdate exhibit
Yeasts as a Biological Control Candidate in the
Management of Post Harvest Diseases: Yeasts are
particularly attractive as biological control candidates
and are encouraged by the fact that these microorganisms
are frequently associated with foods and might be more
acceptable to consumers than exotic bacteria [48] and also
there is considerable information available with respect
to techniques for genetic manipulation, production and
storage of yeast cells [49]. Moreover, yeasts as a major
component of the epiphytic microbial community on the
surfaces of fruits and vegetables [50], may be a more
effective biocontrol agent because they are
phenotypically adapted to this niche and, thus, are able
to more effectively colonize and compete for nutrients
and space on fruit surfaces. In the last two decades,
several scientific studies have demonstrated the
efficiency of yeasts as biocontrol agents against a wide
variety of phytopathogens [51-60]. Among yeasts,
Candida spp. have been found to be highly effective
against different fungal pathogens [25], Hanseniaspora
uvarum against Rhizopus stolonifer and Botrytis
cinerea [61], Cryptococcus spp. against grey mould,
blue mould and Mucor rot [62]. Yeast strains from species,
Pichia guilliermondii, Debaryomyces hansenii and
Kloeckera apiculata have been shown to have the
ability to control post-harvest diseases of several fruits
[25, 63-64].
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World Appl. Sci. J., 31 (5): 785-793, 2014
broad-spectrum antifungal activity [78-79]. Chitosan and
its derivatives, including glycolchitosan, were also
reported to inhibit fungal growth and to induce hostdefense responses in plants and harvested commodities
[80]. Combining 0.2% glycolchitosan with the antagonist
Candida saitoana was more effective in controlling green
mould of oranges and lemons, caused by P. digitatum
and gray and blue molds of apples than either treatment
alone [81]. The addition of ammonium molybdate to the
yeast Candida sake, significantly enhanced its biocontrol
efficacy in controlling postharvest decay in pear fruits
[82]. However, there was little reported use of sodium
bicarbonate as an additive to improve the efficacy of
yeasts against fungal diseases in fruits.
field crop or soil-borne diseases, successful commercial
control of postharvest diseases of fruit and vegetables
must be extremely efficient, in the range of 95-98%. As of
today, such levels of control can be reliably reached by
bio- fungicides only when supplemented with low levels
of synthetic chemical fungicides. A more thorough
understanding of the microbial ecology of fruit surfaces
will help us figure out which problems to work on, how to
approach them, when and where to apply the biocontrol
agent and predict situations in which biocontrol would
not be expected to work.
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