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Biological control of postharvest fungal rots of rosaceous fruits

using microbial antagonists and plant extracts - a review

Article in Mycology: An International Journal On Fungal Biology · February 2016

DOI: 10.33585/cmy.68102

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 CZECH MYCOLOGY 68(1): 41–66, FEBRUARY 1, 2016 (ONLINE VERSION, ISSN 1805-1421)

Biological control of postharvest fungal rots of rosaceous

fruits using microbial antagonists and plant extracts
– a review

SHAZIA PARVEEN*, ABDUL HAMID WANI, MOHD YAQUB BHAT,

JAHANGIR ABDULLAH KOKA

Section of Mycology and Plant Pathology, Department of Botany, University of Kashmir, Hazaratbal
Srinagar, IN-190006, India; shahshazia442@gmail.com, ahamidwani@yahoo.com
*corresponding author

Parveen S., Wani A.H., Bhat M.Y., Koka J.A. (2016): Biological control of post-
harvest fungal rots of rosaceous fruits using microbial antagonists and plant ex-
tracts – a review. – Czech Mycol. 68(1): 41–66.
This article aims to give a comprehensive review on the use of microbial antagonists (fungi and
bacteria), botanicals and compost extracts as biocontrol agents against different pathogenic fungi
causing postharvest fungal rots in rosaceous fruits which shows that they can play an important role
in the biomanagement of fungi causing rot diseases. Plant extracts reported in the literature against
pathogenic fungi indicate that they can act as a good biological resource for producing safe
biofungicides. However most of the work has been done under experimental conditions rather than
field conditions. There is still a need for research to develop suitable formulations of biofungicides
from these microbial biocontrol agents and plant extracts. The review reveals that extensive ecologi-
cal research is also required in order to achieve optimum utilisation of biological resources to man-
age various postharvest diseases of fruits.

Key words: biological control, postharvest diseases, microbial pesticides, rosaceous fruits.

Article history: received 14 June 2015, revised 15 December 2015, accepted 23 December 2015,
published online 1 February 2016.

Parveen S., Wani A.H., Bhat M.Y., Koka J.A. (2016): Biologická kontrola houbo-
vých hnilob plodů růžovitých po sklizni s využitím mikrobiálních antagonistů
a rostlinných extraktů – review. – Czech Mycol. 68(1): 41–66.
Cílem článku je poskytnout komplexní přehled o využití mikrobiálních antagonistů (hub a bakte-
rií) a extraktů z rostlin a kompostu jako prostředků biologické kontroly, úcinných proti patogenním
houbám způsobujícím posklizňové hniloby plodů růžovitých; tyto prostředky mohou hrát důležitou
roli v biomanagementu houbových původců hnilob. Jak je popsáno v literatuře, rostlinné extrakty
úcinné proti patogenním houbám mohou být dobrým zdrojem pro výrobu bezpečných biofungicidů,
nicméně práce, které to dokládají, byly většinou prováděny v experimentálních podmínkách spíše
než v terénu. Stále je třeba vyvíjet vhodné biofungicidy z uvedených mikrobiálních agens a rostlin-
ných výtažků a – jak vyplývá z uvedeného přehledu – je také třeba zkoumat dostupné možnosti
v ekologických souvislostech. Tak lze dosáhnout optimálního využití biologických zdrojů pro
zamezení posklizňového poškození ovoce.

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 CZECH MYCOLOGY 68(1): 41–66, FEBRUARY 1, 2016 (ONLINE VERSION, ISSN 1805-1421)

INTRODUCTION

Rosaceous fruits such as apple, pear, peach, cherry and plum are of great eco-
nomic importance but their production is affected by several diseases especially
rot-causing fungi and bacteria developing after harvest. Fruits are highly perish-
able products during the postharvest phase, when considerable losses due to
fungi and bacteria occur. Postharvest losses in fruits in developing countries
have been estimated in the range of 10 to 30% or more (Kader 2002, Agrios 2005).
In India, postharvest diseases of fruits are responsible for causing losses up to
30% during harvest, subsequent handling and consumption (Parpia 1976).
Postharvest diseases of fruits mainly spread during sale, transport and storage
(Pierson et al. 1971, Snowdon 1990, Barkai-Golan 2001, Janisiewicz & Korsten
2002) and result in reduced food supplies, products of poorer quality, economic
hardships for growers and ultimately higher prices (Agrios 1997, Monte 2001).
Several management practices, viz. physical, chemical, regulatory (control by
regulatory agencies, plant quarantine and certification agencies), cultural and bi-
ological control methods have been used to manage postharvest diseases of
rosaceous fruits. Some of these methods, in particular the use of pesticides,
cause hazardous effects on humans and the environment. Hence strong regula-
tory actions have been imposed on their use. Additionally, the continued use of
chemicals have resulted in the appearance of pathogens which are resistant to
fungicides (Spotts & Cervantes 1986) and have resulted in various iatrogenic dis-
eases (Griffiths 1981). These health and environmental concerns have stimulated
the development of beneficial microorganisms as microbial pesticides (Droby
2006). Microbial pesticides are products used to control plant diseases consisting
of beneficial microorganisms or the metabolites they produce. Biological control
is defined as the reduction of inoculum density or disease producing activities of
a pathogen or parasite in its active or dormant state, by one or more organisms
accomplished naturally or through manipulation of the environment or host or
antagonist or by mass introduction of one or more antagonists (Baker & Cook
1974). Biological control would appear to have a significant potential in terms of
both environmental and economic issues for incorporation into organic and con-
ventional fruit production systems. Various biocontrol agents such as fungi and
bacteria have been identified for the control of postharvest diseases of many
fruits and have been marketed worldwide and obviously play an important role in
sustainable agriculture and management of plant pathogens (Wisniewski & Wil-
son 1992, Ragsdale & Sisler 1994, Montesinos 2003, Sobowale et al. 2008,
Montesinos & Bonaterra 2009, Junaid et al. 2013). The effectiveness of antagonis-
tic microorganisms depends on their ability to colonise fruit surfaces and adapt
to various environmental conditions (Wilson & Wisniewski 1989, Droby et al.
2002, Sharma 2014). Wilson & Wisniewski (1994) indicated the following charac-

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PARVEEN S., WANI A.H., BHAT M.Y., KOKA J.A.: BIOLOGICAL CONTROL OF POSTHARVEST FUNGAL ROTS

teristics of an ideal antagonist: genetic stability, efficacy at low concentrations

and against a wide range of pathogens on various fruit products, simple nutri-
tional requirements, survival in adverse environmental conditions, growth on
cheap substrates in fermenters, lack of pathogenicity to the host plant and no
production of metabolites potentially toxic to humans, resistant to the most fre-
quently used pesticides and compatible with other chemical and physical treat-
ments. Thus, biological control has been suggested as an effective, non-hazard-
ous strategy to control major postharvest decays of fruits and to improve crop
production (Janisiewicz & Korsten 2002, Dalal & Kulkarni 2013). Postharvest
biocontrol is feasible especially because harvested fruits are readily accessible to
treatment with antagonists and many postharvest pathogens infect fruits through
wounds after harvest (Janisiewicz & Jeffers 1997, Nunes et al. 2001).
In the current review, a brief overview of research that has led to comprehen-
sive understanding of various filamentous fungi, yeasts and bacteria which have
been used for postharvest biological control of rosaceous fruits is presented.
This review also gives information about various medicinal plants that have been
screened for their antifungal activity and can act as a good source for the
biomanagement of fungi causing postharvest rot diseases.

REVIEW

Biological control using fungi

Considerable research effort has been devoted to identifying yeasts and other
fungi which effectively control postharvest diseases of fruit, vegetables, and
grains (Wilson et al. 1996, Droby et al. 2002, Zhang et al. 2004, Sharma et al. 2009,
Mishra et al. 2013, Sharma 2014). Postharvest decay of fruits occurs either be-
tween flowering and fruit maturity or during harvesting, handling and storage
(Eckert & Ogawa 1988). Preharvest infections remain latent upto fruit maturity
and storage, such as infection of peaches, cherries, plums and apricots by
Monilinia sp. The majority of postharvest pathogens infect the fruit through
wounds that occur during harvest or subsequent handling (Eckert & Ogawa
1988). Most postharvest rots of several fruits could be reduced considerably by
spraying with spores of antagonistic fungi at different stages of fruit develop-
ment, or by dipping the harvested fruit in their suspensions. Experiments have
shown that several antagonistic unicellular fungi have the ability to protect many
fruits from Botrytis cinerea, Penicillium expansum, Monilinia fructicola and
Rhizoctonia rots (Agrios 1997, Karabulut & Baykal 2003). Once the antagonistic
fungal cells come into contact with the fruit surface, they also occupy the
wounds and affect the germination of pathogenic fungal spores mainly by niche
exclusion and competition for nutrients (Liu et al. 2012). Strains of Candida
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guilliermondii have been studied for the biological control of grey and blue
moulds of apple (McLaughlin et al. 1990, McLaughlin 1991). Control by Candida
guilliermondii is directly related to the spore concentration of the pathogen and
cell concentration of the antagonistic fungi (Droby et al. 1989, McLaughlin et al.
1990). Candida oleophila was approved for postharvest decay control in citrus
and apples under the trade name Aspire® (Agrios 1997, Droby et al. 1998, Lahlali
et al. 2004, Wisniewski et al. 2007). It is used for the biological control of grey
mould caused by Botrytis cinerea (Mercier & Wilson 1994), Penicillium rot
caused by Penicillium expansum (El-Neshawy & Wilson 1997, Lahlali & Jajakli
2009) and Penicillium digitatum (Lahlali et al. 2004). Kloeckera apiculata has
been used as a biocontrol agent in controlling rots caused by Penicillium
expansum, Botrytis cinerea (McLaughin et al. 1992, Karabulut & Baykal 2003,
Long et al. 2005) and Rhizopus rot of peaches (McLaughlin et al. 1992, Qing &
Shiping 2000). Another species of Candida, namely Candida sake, was approved
for the control of Penicillium expansum, Botrytis cinerea and Rhizopus
nigricans under the trade name Candifruit (Vińas et al. 1998, Janisiewicz 2010).
Cryptococcus albidus has been found effective against Mucor rot caused by
Mucor piriformis (Roberts 1990b), blue mould caused by Penicillium expan-
sum (Chand-Goyal & Spotts 1996) and grey mould caused by Botrytis cinerea
(Fan & Tian 2001). It is approved under the trade name Yield Plus in South Africa
(Mari et al. 2014). Another species of Cryptococcus, namely Cryptococcus
laurentii, have been studied for the postharvest biological control of grey mould
rot of apples (Roberts 1990a), Mucor rot of pears (Roberts 1990b), grey and blue
mould rot of pears (Zhang et al. 2003, 2005), Rhizopus rot of strawberries and
peaches (Zheng et al. 2004, Zhang et al. 2007), as well as postharvest diseases of
other fruits such as strawberries, kiwi fruits and table grapes (Lima et al. 1998).
According to Zhang et al. (2007), Cryptococcus laurentii is effective in the con-
trol of a wide range of pathogens and can be used in combination with cold stor-
age to enhance disease control. Another yeast strain, Leucosporidium scottii,
has been found effective against blue mould and grey mould of apple caused by
Penicillium expansum and Botrytis cinerea, respectively (Vero et al. 2013).
Metschnikowia pulcherrima has been reported to occur commonly on apple
and in apple cider (Clark et al. 1954, Beach 1958, 1993) and is known to control
various postharvest decays on pome fruits and grapes (De Curtis et al. 1996, Pi-
ano et al. 1997, Nigro et al. 1999, Janisiewicz et al. 2001, Spadaro et al. 2002). An-
other strain, Metschnikowia fructicola, is effective against rots caused by Botry-
tis sp., Penicillium sp., Rhizopus sp., and Aspergillus sp. It is marketed in Israel
under the trade name ‘Shemer’ (Liu et al. 2011a). A fungal antagonist, Pichia
membranifaciens, isolated from wounds of peach fruits, was evaluated for its
biocontrol capability against Rhizopus stolonifer, Monilinia fructicola and
Penicillium expansum (Chan & Tian 2005). Rhodotorula glutinis was found ef-

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PARVEEN S., WANI A.H., BHAT M.Y., KOKA J.A.: BIOLOGICAL CONTROL OF POSTHARVEST FUNGAL ROTS

fective against apple fruit decay caused by Penicillium expansum and Botrytis
cinerea (Zhang et al. 2009). It has been reported by many researchers that a mix-
ture of different fungal antagonists used in combination proved more effective in
controlling postharvest rots of many fruits than any antagonist applied alone
(Calvo et al. 2003, Janisiewicz et al. 2008). Calvo et al. (2003) reported that the
mixture of Rhodotorula glutinis and Cryptococcus albidus was more effective
against grey mould of apples. Janisiewicz et al. (2008) reported that the mixture
of antagonists Metschnikowia pulcherrima and Cryptococcus laurentii, origi-
nally isolated from apples, exhibit better biocontrol against blue mould of apple
than either antagonist applied alone. Many other yeasts, viz. Clonostachys rosea,
Candida saitoana, Cystofilobasidium infirmominiatum, Rhodosporidium
paludigenum, Pichia caribbica, P. fermentans, P. guilliermondii and P. mem-
branifaciens, have been found effective against various postharvest rot causing
pathogens of fruits (El-Ghaouth et al. 2003, Chan et al. 2007, Liu et al. 2011b, Fiori
et al. 2012, Wang et al. 2010a, Xu et al. 2013).
Trichoderma is among the most common saprotrophic fungi. Many Trichoderma
strains have been identified as having potential applications in biological control, be-
ing effective against a wide range of plant pathogenic fungi (including wood-rot
fungi) or fungus-like organisms: Armillaria, Botrytis, Colletotrichum, Dematophora,
Endothia, Fulvia, Fusarium, Chondrostereum, Fusicladium, Macrophomina,
Monilia, Nectria, Phoma, Phytophthora, Plasmopara, Pseudoperonospora,
Pythium, Rhizoctonia, Sclerotinia, Sclerotium, Venturia and Verticillium (Sawant
et al. 1995, Agrios 1997, Monte 2001, Batta 2004, Wani et al. 2009, Mishra et al. 2013,
Motlagh & Samimi 2013). Many recent studies have demonstrated the effect of vari-
ous Trichoderma species on postharvest rot diseases caused by many fungal patho-
gens (Batta 2001, 2004, Odebode 2006, Patale & Mukadam 2011, Hafez et al. 2013).
Trichoderma harzianum is used to control the fungal diseases caused by Alter-
naria alternata, Penicillium expansum (blue mould on apples), Botrytis cinerea
(grey mould on apples), damping-off diseases caused by Pythium species, and
Rhizoctonia sp. (Agrios 1997, Batta 1999, 2003, Biswas 1999, Harman & Kubicek
1998, Dutta & Das 1999, Omarjee et al. 2001). Other strains of Trichoderma, namely
T. pseudokoningii, T. koningii, T. hamatum, T. gamsii, T. atroviride, T. virens and
T. viride, are also used as biological control agents to suppress the growth of various
pathogenic fungi (Tronsmo & Raa 1977, Odebode 2006, Ngullie et al. 2010, Jagtap et
al. 2013, Shaikh & Nasreen 2013). Several commercial biocontrol products and their
formulations have been developed and approved, e.g. Trichodermil, Bio-tricho,
Supresivit, Eco-77, Trichodex (Trichoderma harzianum), Trichdermax EC, Ecohope,
Quality WG, Trichotech (T. asperellum), Trichospray, Trichopel, Trichodry, Vinevax
(T. atroviride), Remedier WP (T. gamsii), Biocure F, Bio-shield, Binab T (T. viride),
BW 240 G, BW 240 WP, G-41 technical (T. virens), Floragard (T. hamatum) (Kabaluk
et al. 2010, Bettiol et al. 2012, Woo et al. 2014).

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Tab. 1. Fungi used as biological control agents.

Biocontrol agent Disease References

Candida guilliermondii Blue mould (Penicillium expansum) McLaughlin et al. (1990)
Grey mould (Botrytis cinerea) McLaughlin et al. (1992)
Candida oleophila Penicillium rot (Penicillium expansum) El-Neshawy & Wilson (1997)
Grey mould (Botrytis cinerea) Mercier & Wilson (1994)
Candida saitoana Grey mould of apple (Botrytis cinerea) El-Ghaouth et al. (2003)
Candida sake Penicillium rot (Penicillium expansum) Vińas et al. (1996)
Grey mould (Botrytis cinerea) Vińas et al. (1998)
Rhizopus rot (Rhizopus nigricans) Vińas et al. (1998)
Botrytis bunch rot (Botrytis cinerea) Calvo-Garrido et al. (2013)
Clonostachys rosea Fusarium dry rot (Fusarium avenaceum, Jima (2013)
Fusarium caeruleum)
Grey mould (Botrytis cinerea) Reeh (2012)
Cryptococcus albidus Mucor rot (Mucor piriformis) Roberts (1990b)
Grey mould (Botrytis cinerea) Fan & Tian (2001)
Blue mould (Penicillium expansum) Chand-Goyal & Spotts (1996),
Calvo et al. (2003)
Cryptococcus flavus Mucor rot (Mucor piriformis) Roberts (1990b)
Cryptococcus laurentii Bitter rot (Glomerella cingulata) Blum et al. (2004)
Mucor rot (Mucor piriformis) Roberts (1990b)
Grey mould (Botrytis cinerea) Chand-Goyal & Spotts (1997),
Zhang et al. (2005),
Zhang et al. (2007)
Blue mould (Penicillium expansum) Zhang et al. (2003),
Zhang et al. (2007)
Rhizopus rot (Rhizopus stolonifer) Zhang et al. (2007)
Cystofilobasidium Penicillium rot of apple Liu et al. (2011b)
infirmominiatum (Penicillium expansum)
Epicoccum nigrum Brown rot of stone fruits (Monilinia laxa) Madrigal et al. (1994),
Foschi et al. (1995)
Kloeckera apiculata Grey mould (Botrytis cinerea) McLaughlin et al. (1992)
Rhizopus rot (Rhizopus stolonifer) McLaughlin et al. (1992),
Qing & Shiping (2000)
Leucosporidium scottii Blue mould of apple (Penicillium expansum) Vero et al. (2013)
Grey mould of apple (Botrytis cinerea) Vero et al. (2013)
Metschnikowia fructicola Apple rot (Penicillium expansum) Liu et al. (2011a)
Metschnikowia pulcherrima Blue mould (Penicillium expansum) Spadaro et al. (2002),
Janisiewicz et al. (2001)
Grey mould (Botrytis cinerea) Spadaro et al. (2002)
Penicillium roqueforti and Black rot disease (Aspergillus niger) Khokhar et al. (2013)
Penicillium viridicatum
Pichia caribbica Rhizopus rot of peach (Rhizopus stolonifer) Xu et al. (2013)
Pichia fermentans Apple and peach decay (Monilinia fructicola Fiori et al. (2012)
and Botrytis cinerea)

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PARVEEN S., WANI A.H., BHAT M.Y., KOKA J.A.: BIOLOGICAL CONTROL OF POSTHARVEST FUNGAL ROTS

Biocontrol agent Disease References

Pichia guilliermondii Grey mould (Botrytis cinerea) Wisniewski et al. (1991a)
Pichia membranifaciens Penicillium expansum (peach) Chan et al. (2007)
Apple fruit decay (Penicillium expansum, Chan & Tian (2005)
Monilinia fructicola, Rhizopus stolonifer)
Rhodosporidium Pear fruit decay (Alternaria alternata, Wang et al. (2010a)
paludigenum Penicillium expansum)
Rhodotorula glutinis Apple fruit decay (Penicillium expansum, Zhang et al. (2009)
Botrytis cinerea)
Trichoderma atroviride Phomopsis sp. Das et al. (2014)
Trichoderma hamatum Fungal diseases (Phytophthora palmivora, Ha (2010),
Rhizoctonia solani, Fusarium spp., Ngullie et al. (2010)
Sclerotium rolfsii, Pythium sp.)
Trichoderma harzianum Grey mould (Botrytis cinerea) Batta (1999, 2003)
Blue mould (Penicillium expansum) Batta (2004)
Trichoderma koningii Alternaria diseases (Alternaria alternata) Odebode (2006),
Shaikh & Nasreen (2013)
Trichoderma pseudokoningii Brown rot (Monilinia laxa) Tronsmo & Raa (1977)
Trichoderma viride Fruit rots (Colletotrichum gloeosporioides) Ngullie et al. (2010),
Jagtap et al. (2013)

Biological control using bacteria

Several bacteria have been identified to play an important role as biological con-
trol agents in controlling disease caused by many plant pathogenic fungi (Pusey &
Wilson 1984, Pratella et al. 1993, Smilanick et al. 1993, Frances et al. 2006, Pal &
Garderner 2006, Sreevidya & Gopalakrishnan 2012, Mishra et al. 2013). Among dif-
ferent bacteria used as biological control agents, an isolate of Burkholderia cepacia
provided biological control of blue mould and grey mould of Golden Delicious ap-
ples (Janisiewicz & Roitman 1988). A saprophytic strain of Pseudomonas syringae
marketed under trade name BiosaveTM, provided biological control against grey
mould, blue mould and Mucor rot on pear and apple (Janisiewicz & Marchi 1992,
Jeffers & Wright 1994, Mari et al. 2014). On pears it was reported to be the most ef-
fective postharvest treatment against various diseases in an integrated management
programme (Sugar 2006). Another species of Pseudomonas, namely Pseudomonas
fluorescens, has been reported to control grey mould caused by Botrytis sp. (Mikani
et al. 2008). Strains of Pantoea agglomerans were reported to be effective against
rots caused by Botrytis cinerea, Rhizopus stolonifer, Penicillium expansum,
Penicillium digitatum and Penicillium italicum (Nunes et al. 2001, Teixidó et al.
2001, Frances et al. 2006, Kotan et al. 2009, Trias et al. 2010). Bacillus subtilis ap-
plied to wounded apples reduced fruit rot caused by Botrytis cinerea, Alternaria
alternata, Penicillium expansum and P. malicorticis (Leibinger et al. 1997, Wang et
al. 2010b). It has been reported that the postharvest brown rot of stone fruits can

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also be controlled by the application of Bacillus subtilis and Pseudomonas sp.

(Pusey & Wilson 1984, Smilanick et al. 1993). Bacillus pumilus and Bacillus
amyloliquefaciens are reported to control grey mould in pears and tomatoes caused
by Botrytis cinerea (Mari et al. 1996). Another species of Bacillus, namely Bacillus
licheniformis, has been reported to control grey mould caused by Botrytis mali
(Jamalizadeh et al. 2008). Rahnella aquatilis has been studied as a possible
biocontrol agent against plant pathogenic fungi, viz. Penicillium expansum, Botry-
tis cinerea and Alternaria alternata, which produce postharvest spoilage in apple
fruits (Nunes et al. 2001, Calvo et al. 2007).

Tab. 2. Bacteria used as biological control agents.

Biocontrol agent Disease References

Bacillus amyloliquefaciens Grey mould (Botrytis cinerea) Mari et al. (1996)
Bacillus licheniformis Grey mould (Botrytis mali) Jamalizadeh et al. (2008)
Bacillus pumilus Grey mould (Botrytis cinerea) Mari et al. (1996)
Bacillus subtilis Brown rot (Monilinia sp.) Pusey et al. (1986)
Apple fruit rot (Botrytis cinerea, Leibinger et al. (1997)
Penicillium expansum)
Apple ring rot Liu et al. (2009)
(Botryosphaeria berengeriana)
Alternaria diseases (Alternaria alternata) Wang et al. (2010b)
Burkholderia cepacia Blue mould (Penicillium expansum) Janisiewicz & Roitman (1988)
Mucor rot (Mucor piriformis) Janisiewicz & Roitman (1988)
Grey mould (Botrytis cinerea) Janisiewicz & Roitman (1988)
Burkholderia gladioli Phytopathogenic fungi (Botrytis cinerea, Elshafie et al. (2012)
Penicillium expansum, Penicillium digitatum,
Aspergillus flavus, Aspergillus niger, Phyto-
phthora cactorum, Sclerotinia sclerotiorum)
Enterobacter cloacae Fusarium dry rot (Fusarium sambucinum) Al-Mughrabi (2010)
Pantoea agglomerans Penicillium rot (Penicillium expansum) Nunes et al. (2001), Teixidó et al.
(2001), Frances et al. (2006)
Rhizopus rot (Rhizopus nigricans) Nunes et al. (2001)
Brown rot (Monilinia laxa) Bonaterra et al. (2003)
Soft rot (Rhizopus stolonifer) Bonaterra et al. (2003)
Pantoea vagans Disease of apple and pears (Erwinia amylovora) Smits et al. (2010)
Pseudomonas fluorescens Grey mould (Botrytis spp.) Mikani et al. (2008)
Pseudomonas syringae Blue mould (Penicillium expansum) Janisiewicz (1987),
Zhou et al. (2001)
Grey mould (Botrytis cinerea) Zhou et al. (2001)
Mucor rot (Mucor piriformis) Janisiewicz & Marchi (1992),
Jeffers & Wright (1994)
Rahnella aquatilis Penicillium rot (Penicillium expansum) Calvo et al. (2007)
Grey mould (Botrytis cinerea) Calvo et al. (2007)

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PARVEEN S., WANI A.H., BHAT M.Y., KOKA J.A.: BIOLOGICAL CONTROL OF POSTHARVEST FUNGAL ROTS

Mechanisms of action of microbial antagonists against postharvest pathogens

Knowledge of the mechanism of action is a key factor to achieve an efficient in-
hibition of pathogens in their hosts. The mechanisms of action involved in the
biocontrol process can permit establishment of optimum conditions for interac-
tion between the pathogen and the biological control agent and is important in im-
plementing a biological control strategy in a particular pathosystem (Cook 1993,
Handelsman & Stabb 1996). Several mechanisms have been suggested to operate
in postharvest biocontrol, including antibiosis, induced resistance, mycopara-
sitism, cell-wall degradation, competition for space, and limited resources.
Several strains of antagonistic fungi use a single mechanism to inhibit the
growth of pathogenic fungi, while some strains are reported to use multiple
mechanisms. The most effective biological control agent studied antagonise
a plant pathogen using multiple mechanisms utilising both antibiosis and induc-
tion of host resistance to suppress the disease-causing microorganisms, such as
in Pseudomonas (Janisiewicz & Roitman 1988, Junaid et al. 2013); it is reported
that Pseudomonas produces antibiotic 2,4-diacetylphloroglucinol and also in-
duces host defences (Iavicoli et al. 2003).
Antibiosis is a direct toxic effect on the pathogen by antibiotic substances re-
leased by the antagonist. Trichoderma harzianum and Clonostachys rosea (for-
merly Gliocladium roseum) control anthracnose of fruits through antibiosis
(Živković et al. 2010). Pyrrolnitrin can be the main mode of action of Pseudomo-
nas cepacia in controlling Botrytis cinerea and Penicillium expansum on ap-
ples and pears (Janisiewicz & Roitman 1988). Bacillus subtilis may control
Monilinia fructicola by the production of iturine (Pusey & Wilson 1984), grey
mould by the production of cyclolipopeptides like fengecins (Ongena et al. 2005).
A yeast-like antagonist, Aureobasidium pullulans, controls anthracnose caused
by Colletotrichum acutatum by antibiosis (b-1,3-glucanase and chitinase) and
hyperparisitism (Hartati et al. 2015).
Competitive exclusion of the pathogen from sites of infection by better use of
nutrients and colonisation than the pathogen is also a common mechanism that
can accompany other mechanisms, and is considered as the major modes of ac-
tion by which microbial agents control pathogens causing postharvest decay of
pome fruits (Sharma et al. 2009). Competition for nutrients was suggested to play
a role in the biocontrol of Penicillium digitatum by Debaryomyces hansenii
(Droby et al. 1989) and of Botrytis cinerea by Cryptococcus sp. (Filonow et al.
1996). Preemptive exclusion of fungal infection sites by the antagonist was ob-
served in Candida oleophila and Cryptoccocus laurentii, which control Botrytis
cinerea (Roberts 1990a, Mercier & Wilson 1995).
Inhibition of plant pathogens by Pantoea agglomerans is dependent on the
strain and has been attributed to production of an acidic environment (Riggle

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& Klos 1972, Beer et al. 1984), competition for nutrients (Goodman 1967), pro-
duction of herbicolin or other antibiotics (Ishimaru et al. 1988, Vanneste et al.
1992, Kearns & Hale 1996), preemptive colonisation (Wilson et al. 1992, Kearns
& Hale 1996), parasitism of the pathogen (Bryk et al. 1998) and induction of plant
defense response (Slade & Tiffin 1984).
Attachment alone or in combination with secretion of cell-wall degrading en-
zymes has been proposed as the viable mechanism operating in the biocontrol of
Botrytis cinerea by Pichia guilliermondii (Wisniewski et al. 1991a). It is re-
ported that Pichia guilliermondii and Candida saitoana cells have the ability to
attach to the hyphae of Botrytis cinerea and cause degradation of the cell wall at
the attachment sites (Wisniewski et al. 1991b, El-Ghaouth et al. 1998). The antag-
onistic activity of Aureobasidium pullulans against Botrytis cinerea, Rhizopus
stolonifer, Penicillium expansum and Aspergillus niger was found to be the re-
sult of antibiosis in conjugation with attachment of microbial antagonist to the
hyphae of pathogenic fungi (Castoria et al. 2001).
Several hyperparasites, especially abundant among fungi like Pichia and
Trichoderma, interact directly and degrade the fungal cell or exert antagonism
through antimicrobial compounds, develop hyperparasitism [involving trophic
growth of the biocontrol organism towards the pathogenic fungi, causes coiling,
attack and dissolution of the cell wall and membrane of the pathogenic fungi by
the activity of enzymes (Tewari 1996)], or directly attach to the pathogen cells, in-
terfere with pathogen signals, or induce resistance in the plant host (Harman
2006).
Some bacteria and fungi are able to induce defense responses in plants, by
producing either elicitors (e.g. cell-wall components) or messenger molecules
(e.g. salicylic acid) (Spadaro & Gullino 2004). Induction of host defence reactions
was proposed to be the mechanism in the biocontrol of Botrytis cinerea by
Candida saitoana (El-Ghaouth et al. 1998) and of Penicillium digitatum by
Verticillium lecanii (Benhamou & Brodeur 2000).

Biological control using botanicals

Much work has been carried out to evaluate the antimicrobial efficacy of vari-
ous medicinal plant extracts against phytopathogenic fungi. It has been reported
that they play an important role in controlling diseases of plants caused by these
fungi (Hossain et al. 1993, Anwar et al. 1994, Jacob & Sivaprakasan 1994, Arya et
al. 1995, Karade & Sawant 1999, Datar 1999, Anwar & Khan 2001, Lin et al. 2001,
Okemo et al. 2003, Choi et al. 2004, Mares et al. 2004, Khalil et al. 2005, Abd-El-
Khair & Haggag 2007, Ogbebor et al. 2007, Perez-Sanchez et al. 2007, Baka 2010,
Znini et al. 2011, Raji & Raveendran 2013, Parveen et al. 2013, 2014, Ekwere et al.
2015, Nweke 2015). Dababneh & Khalil (2007) studied the effect of five different

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PARVEEN S., WANI A.H., BHAT M.Y., KOKA J.A.: BIOLOGICAL CONTROL OF POSTHARVEST FUNGAL ROTS

medicinal plant extracts, viz. Crupina crupinastrum, Teucrium polium,

Achillea santolina, Micromeria nervosa and Ballota philistaea, against four
pathogenic fungi, viz. Fusarium oxysporum, Rhizoctonia solani, Penicillium
sp. and Verticillium sp. Webster et al. (2008) screened 14 plants for their
antifungal activity against various pathogenic fungi and concluded that Fragaria
virginiana, Epilobium angustifolium and Potentilla simplex show a promising
antifungal potential. Bobbarala et al. (2009) reported the antifungal activity of 49
different plant extracts against Aspergillus niger. Among the 49 plants used, 89%
showed antifungal activity, while 11% were not effective. Satish et al. (2009) re-
ported the antifungal potential of 46 plants against eight species of Fusarium,
viz. F. equiseti, F. moniliforme, F. semitectum, F. graminearum, F. oxysporum,
F. proliferatum, F. solani and F. lateritium. Taskeen-Un-Nisa et al. (2010, 2011)
reported the antimycotic activity of some plant extracts including onion (Allium
cepa), garlic (Allium sativum) and mint (Mentha arvensis), against Alternaria
alternata, Rhizopus stolonifer and Fusarium oxysporum. Gatto et al. (2011)
studied the in vitro and in vivo activity of extracts from nine herbaceous species,
viz. Borago officinalis, Orobanche crenata, Plantago lanceolata, Plantago coro-
nopus, Sanguisorba minor, Silene vulgaris, Sonchus asper, Sonchus oleraceus
and Taraxacum officinale, against some postharvest fungal rot causing patho-
gens (Monilinia laxa, Botrytis cinerea, Penicillium expansum, Penicillium
digitatum, Penicillium italicum, Aspergillus carbonarius and Aspergillus
niger) and reported that the extract of Sanguisorba minor completely inhibited
the spore germination of Monilinia laxa, Penicillium digitatum, Penicillium
italicum and Aspergillus niger. Parveen et al. (2013, 2014) reported the
antifungal activity of five different plant extracts, viz. Artemisia absinthium,
Rumex obtusifolius, Taraxacum officinale, Plantago lanceolata and Malva
sylvestris, against some rot-causing fungal pathogens, Alternaria alternata,
Penicillium expansum, Aspergillus niger and Mucor piriformis. Essential oils
have been extracted from various plants and evaluated for their efficacy against
a number of pathogenic fungi causing postharvest rots of rosaceous fruits
(Pandey et al. 1982, Edris & Farrag 2003, Nakamura et al. 2004, Chuang et al.
2007, Tzortzakis & Economakis 2007, Soylu et al. 2010, Znini et al. 2011, 2013).
Znini et al. (2013) extracted an essential oil from the plant Warionia saharae and
reported its antifungal activity against three apple phytopathogenic fungi, viz.
Alternaria species (Alternaria rot), Penicillium expansum (blue mould), and
Rhizopus stolonifer (Rhizopus rot). The extracts of these plants used by differ-
ent researchers against pathogenic fungi show promising antifungal activity
which indicates that these plants can act as a good biological resource for pro-
ducing safe biofungicides.

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Tab. 3. Biological control of rot causing fungal pathogens by using botanicals.

Plant extract Fungal pathogens References

Aframomum melegueta Botryodiplodia theobromae, Fusarium Okigbo & Ogbonnaya (2006)
oxysporum, Aspergillus niger
Allium cepa Aspergillus niger, Fusarium oxysporum, Taskeen-Un-Nisa (2010, 2011)
Rhizopus stolonifer, Penicillium chrysogenum
Allium sativum Penicillium sp., Aspergillus candidus, Magro et al. (2006),
Fusarium culmorum, Aspergillus niger, Taskeen-Un-Nisa (2010, 2011),
Fusarium oxysporum, Rhizopus stolonifer, Hadi & Kashefi (2013)
Penicillium chrysogenum
Annona reticulata Rhizopus stolonifer, Colletotrichum Bautista-Bańos et al. (2000)
gloeosporioides
Anthemis nobilis (currently Penicillium sp., Aspergillus candidus, Magro et al. (2006)
Chamaemelum nobile) Fusarium culmorum, Aspergillus niger
Artemisia absinthium Alternaria alternata (Alternaria rot), Parveen et al. (2013, 2014)
Penicillium expansum (Penicillium rot),
Mucor piriformis (Mucor rot), Aspergillus
niger (Black mould rot)
Borago officinalis Monilinia laxa, Botrytis cinerea, Gatto et al. (2011)
Penicillium expansum, Penicillium
digitatum, Penicillium italicum, Aspergillus
carbonarius, Aspergillus niger
Cinnamomum verum Penicillium sp., Aspergillus candidus, Magro et al. (2006)
Fusarium culmorum, Aspergillus niger
Curcuma longa Colletotrichum gloeosporioides Imtiaj et al. (2005)
(anthracnose diseases of fruits)
Datura innoxia and Datura Alternaria solani, Fusarium oxysporum Jalander & Gachande (2012)
stramonium
Dittrichia viscosa Penicillium digitatum, Penicillium Mamoci et al. (2011)
expansum, Botryotinia fuckeliana,
Aspergillus sp., Monilinia laxa, Monilinia
fructigena
Ferula communis Identical to the pathogens of Dittrichia viscosa Mamoci et al. (2011)
Hypochaeris radiata Paecilomyces lilacinus, Mucor sp., Senguttuvan et al. (2013)
Trichoderma viride, Verticillium lecanii,
Candida albicans, Fusarium sp.,
Penicillium sp., Aspergillus fumigatus,
Aspergillus niger
Lavandula stoechas Penicillium sp., Aspergillus candidus, Magro et al. (2006)
Fusarium culmorum, Aspergillus niger
Malva sylvestris Alternaria alternata, Penicillium expansum, Magro et al. (2006),
Mucor piriformis, Aspergillus candidus, Parveen et al. (2013, 2014)
Fusarium culmorum, Aspergillus niger
Mentha arvensis Aspergillus niger, Fusarium oxysporum, Taskeen-Un-Nisa (2010, 2011)
Rhizopus stolonifer, Penicillium chrysogenum
Mentha cordifolia Colletotrichum gloeosporioides (anthracnose Bussaman et al. (2012)
disease)

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PARVEEN S., WANI A.H., BHAT M.Y., KOKA J.A.: BIOLOGICAL CONTROL OF POSTHARVEST FUNGAL ROTS

Plant extract Fungal pathogens References

Mentha piperita Penicillium sp., Aspergillus candidus, Magro et al. (2006),
Fusarium culmorum, Aspergillus niger, Hadi & Kashefi (2013)
Fusarium oxysporum
Ocimum gratissimum Botryodiplodia theobromae, Fusarium Amandioha (2001),
oxysporum, Aspergillus niger, Rhizopus Okigbo & Ogbonnaya (2006)
oryzae
Orobanche crenata Identical to the pathogens of Borago officinalis Gatto et al. (2011)
Piper sarmentosum Colletotrichum gloeosporioides (anthracnose Bussaman et al. (2012)
disease)
Plantago coronopus Identical to the pathogens of Borago officinalis Gatto et al. (2011)
Plantago lanceolata Identical to the pathogens of Artemisia Parveen et al. (2013, 2014)
absinthium
Rumex obtusifolius Identical to the pathogens of Artemisia Parveen et al. (2013, 2014)
absinthium
Sanguisorba minor Identical to the pathogens of Borago officinalis Gatto et al. (2011)
Silene vulgaris Identical to the pathogens of Borago officinalis Gatto et al. (2011)
Sonchus asper and Identical to the pathogens of Borago officinalis Gatto et al. (2011)
Sonchus oleraceus
Taraxacum officinale Alternaria alternata (Alternaria rot), Gatto et al. (2011),
Penicillium expansum (Penicillium rot), Parveen et al. (2013, 2014)
Mucor piriformis (Mucor rot), Aspergillus
niger (Black mould rot), Monilinia laxa,
Botrytis cinerea, Penicillium italicum,
Penicillium digitatum
Tagetes erecta Colletotrichum gloeosporioides (anthracnose Imtiaj et al. (2005)
diseases of fruits)
Warionia saharae Alternaria alternata (Alternaria rot), Znini et al. (2013)
Penicillium expansum (Penicillium rot),
Rhizopus stolonifer (Rhizopus rot)
Zingiber officinale Colletotrichum gloeosporioides (anthracnose Imtiaj et al. (2005)
diseases of fruits)

Control using compost extracts

Compost extracts from plant materials have been used as a biological control
agent for different postharvest pathogens, such as Plasmopara viticola,
Uncinula necator, Pseudopeziza tracheiphila, Botrytis cinerea, and Sclerotium
rolfsii (Weltzien 1989, Zmora-Nahum et al. 2008). Chakroune et al. (2008) found
that compost extracts from palm were very effective in managing Fusarium
oxysporum f. sp. albedinis. Exadaktylou & Thomidis (2010) used compost ex-
tracts from a seagrass species, Posidonia oceanica, and the organic fertiliser
Cofuna 3, made from bagasse (fibrous matter that remains after sugarcane or sor-
ghum stalks are crushed to extract their juice) and found them effective against
the postharvest fruit rots of peach caused by Monilinia sp., Penicillium sp. and
Rhizopus sp. They found that fruits treated with an extract from Cofuna 3

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showed relatively fewer symptoms of rotting for all fungi tested than Posidonia
oceanica. It was shown that compost extracts rich in lignocellulosic substances
are most effective in inhibiting the growth of several species of Fusarium
(Znaidi 2002). There are very few reports on the use of compost extracts to con-
trol pathogens that cause postharvest fruit rots. They are mostly used for control-
ling soil-borne plant pathogens (Mokhtar & El-Mougy 2014).

DISCUSSION AND CONCLUSION

Biological control using microorganisms associated with plants is an efficient

and effective approach to control diseases and is considered environmentally
friendly. The first step is to screen potential biological control agents (BCA),
while the main screening strategy used by many scientists is based on in vitro an-
tagonistic activity.
A successful biocontrol agent is generally equipped with several mechanisms
which often work in concert, and may be crucial in controlling disease develop-
ment. It involves a complex interaction between host, pathogen, antagonists and
environment (Droby et al. 2009, Nunes 2012). A bacterial biocontrol agent of the
genus Bacillus uses nutrient and space competition, induced resistance, produc-
tion of diffusible antibiotics, volatile organic compounds, toxins, and cell-wall
degrading enzymes such as chitinase and b-1,3-glucanase (Nunes 2012). Numer-
ous studies have reported a range of antifungal compounds produced by differ-
ent biological control agents. Among them, lipopeptides from the fengycin, iturin
and surfactin families are regarded as key factors in biological control activity
(Santoyo et al. 2012).
Information on the mechanisms of action by which biological control agents
suppress postharvest diseases is still not fully known mainly due to difficulties
encountered during the study of complex interactions between host, pathogen
and biological control. However several possible mechanisms have been men-
tioned, which include production of antibiotics, lytic enzymes, direct parasitism,
induction of resistance in the host tissue, and competition for nutrients and
space. Spadaro & Gullino (2004) provided the major characteristics of an effi-
cient antagonist or biological control agent, including genetic stability, efficiency
at low levels and against a range of pathogens on various fruits, growth on cheap
substrates in fermenters, survival in adverse environmental conditions, lack of
pathogenicity on the host, and no production of metabolites toxic to humans.
Based on these traits, yeasts seem to be excellent candidates for the biological
control of pathogenic fungi. Moreover, characteristics inherent to yeasts, such as
fast growth, fruit surface colonisation and the deprivation of nutrients from

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pathogens (through competition) have placed these organisms among the most
suitable biocontrol agents (Richard & Prusky 2002).
Botanicals are also effective in controlling postharvest rot of fruit. Plants
provide a wide range of secondary metabolites, i.e. essential oils which have
antimicrobic, allelopathic, bioregulatory and antioxidant properties. The family
Brassicaceae is well documented for their antimicrobial activity and production
of glucosinolates.
Since significant progress has been made in different aspects of the biological
control of various plant diseases including postharvest rots, but this area still
needs more attention to solve the existing problems. In order to have more
effective biological control strategies in future, a better understanding of the
biocontrol agent and its interaction with the microorganism is needed. Microbial
biological control agents have their limitation, which may restrict their use under
certain circumstances. Microbial biological control agents have been criticised
mainly for not providing such a consistent or broad-spectrum control as syn-
thetic fungicides. Some biocontrol agents can be toxic or cause environmental
contamination, so the key success of this technology for disease control is re-
lated to the biosafety and environmental impact of biocontrol agents. It is impor-
tant to carry out more research studies on less known aspects of biological con-
trol including development of novel formulations from microbial agents and
bioagents of plant origin reported by several researchers, their impact on the en-
vironment, and mass production to make new biocontrol products effective, sta-
ble, safer and cost effective. The approach would undoubtly encourage environ-
mentally friendly products to reach the market and would lead us towards a sus-
tainable agricultural system in the future.

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