C.musae review

Crop Protection 141 (2021) 105454
Available online 13 November 2020
0261-2194/© 2020 Elsevier Ltd. All rights reserved.
Review
Biocontrol strategies for the management of Colletotrichum species in
postharvest fruits
Xin-Chi Shi a,1
, Su-Yan Wang a,1
, Xu-Chu Duan a
, Yao-Zhou Wang b
, Feng-Quan Liu c,**
,
Pedro Laborda a,*
a
School of Life Sciences, Nantong University, Nantong, 226019, People’s Republic of China
b
Economic Development Bureau of Nantong E&T Development Area, Nantong, 226009, People’s Republic of China
c
Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base of
Ministry of Science and Technology, Nanjing, 210014, People’s Republic of China
A R T I C L E I N F O
Keywords:
Biological control
Colletotrichum
Postharvest preservation
Fruit pathogens
Anthracnose disease
A B S T R A C T
Colletotrichum is an opportunistic plant pathogen able to produce anthracnose disease in a wide range of post
harvest fruits. Although the management of Colletotrichum has been traditionally attempted using synthetic
fungicides, their toxic effects to human health, together with the appearance of resistant strains, have stimulated
the development of biocontrol strategies during last years. Here, we are reviewing for the first time all reported
biocontrol strategies for the management in vivo of Colletotrichum species in postharvest fruits. Several recently-
reported strategies showed high inhibitory activity and, in some cases, supressed completely the disease
symptoms, improving the efficacy of commercial biocontrol agents. Most strategies focused on the management
of C. acutatum, C. gloeosporioides and C. truncatum; however, other harmful clades remain completely unexplored.
Although some of the best results were obtained using yeasts, no yeast strain was commercialized for the
management of Colletotrichum, and there is a lack of information about yeast strains viability, toxicity and market
storage conditions. The conclusions achieved in this work help to understand the current state of the research
field, and reveal new insights on the development of efficient biocontrol strategies for the control of Colleto
trichum species.
1. Introduction
The genus Colletotrichum includes a number of plant pathogens of
major importance, causing diseases on a wide variety of woody and
herbaceous plants (Weir et al., 2012; Dean et al., 2012). The taxonomy
of Colletotrichum species is somehow complex, and has been subjected to
several modifications during recent years (Damm et al., 2019; Mon
gkolporn and Taylor, 2018). Currently, Colletotrichum species are clas
sified in clades (complexes of species), such as C. acutatum,
C. gloeosporioides and C. truncatum (Cannon et al., 2012). Although some
Colletotrichum species have shown high promiscuity, most clades are
commonly associated with specific hosts (Table 1).
Colletotrichum species are able to cause anthracnose disease in fruits,
and have been responsible for devastating losses in fruit storage during
recent years (Da Silva et al., 2020). The presence of Colletotrichum
species in postharvest fruits is especially important in tropical and
sub-tropical regions. Most Colletotrichum species initially establish
infection through a brief biotrophic phase, associated with large intra
cellular primary hyphae (Sudheeran et al., 2020). Then, the pathogen
switches to a necrotrophic phase, leading to brown necrotic lesions on
the fruit surface. It is known that the pathogen remains quiescent in the
host until the fruit ripens (Tian et al., 2016). Currently, C. acutatum is a
quarantine pathogen in most European countries (Feliziani and Roma
nazzi, 2016). It is estimated that 30–50% postharvest losses of dragon
fruit and papaya are due to C. gloeosporioides-caused anthracnose
(Bautista-Baños et al., 2013; Bordoh et al., 2020). A study indicated that
30% of stored avocados show body rots, predominantly caused by
C. gloeosporioides (Perkins et al., 2019). Recent occurrences of pear bitter
rot disease, caused by C. fructicola, have taken place in areas of Anhui
Province in China, with losses of 60–90% (Laborda et al., 2019).
* Corresponding author.
** Corresponding author.
E-mail addresses: fqliu20011@sina.com (F.-Q. Liu), pedro@ntu.edu.cn (P. Laborda).
1
These authors contributed equally to this work.
Contents lists available at ScienceDirect
Crop Protection
journal homepage: www.elsevier.com/locate/cropro
https://doi.org/10.1016/j.cropro.2020.105454
Received 17 August 2020; Received in revised form 2 November 2020; Accepted 4 November 2020

2
The management of Colletotrichum causing anthracnose in fruits has
been traditionally attempted using synthetic fungicides, such as man
cozeb, carbendazim, prochloraz and Tecto 60 (Chechi et al., 2019;
Sengupta et al., 2020). Although mentioned fungicides have been effi
ciently used against Colletotrichum-caused decays, their toxicity to
human health (Singh et al., 2016), together with the appearance of
fungicide-resistant strains (Tian et al., 2016), have stimulated the
development of new environmental-friendly biocontrol strategies (Car
mona-Hernandez et al., 2019; Droby et al., 2016; Dukare et al., 2019;
Zhang et al., 2018). These new strategies have been demonstrated to
show no toxicity and, in some cases, they may have better efficacy than
synthetic fungicides (Ocampo-Suarez et al., 2017a). Several bacteria,
filamentous fungi and yeasts with antifungal properties were used for
the control of Colletotrichum in postharvest fruits. Here, we are review
ing for the first time all reported biocontrol strategies for the manage
ment in vivo of Colletotrichum species in postharvest fruits. The review
was divided into 5 different sections: i) Biocontrol strategies for the
management of Colletotrichum species using bacteria, ii) Biocontrol
strategies for the management of Colletotrichum species using filamen
tous fungi, iii) Biocontrol strategies for the management of Colleto
trichum species using yeasts, iv) Commercial biocontrol agents for the
management of Colletotrichum species, and v) Conclusions and future
prospects.
2. Biocontrol strategies for the management of Colletotrichum
species using bacteria
The strategies using bacteria were directed towards the management
of C. acutatum, C. gloeosporioides and C. truncatum clades (Table 2). The
identity of the specific species, such as C. fructicola (which belongs to the
C. gloeosporioides clade), C. musae (which belongs to the
C. gloeosporioides clade) and C. nymphaeae (which belongs to the
C. acutatum clade), was also described in some references. The bacterial
biocontrol agents produced the antifungal activity via secretion of
antifungal metabolites and enzymes, or via induction of disease resis
tance in fruits. Some species, such as Bacillus subtilis, were reported to
produce both effects. All the strains belonging to the same biocontrol
species showed similar inhibitory activities and, for this reason, only the
species, and not the specific strains, were highlighted along the review.
For better understanding, this section was divided into 3 different
subsections depending on the studied pathogen.
2.1. Biocontrol strategies for the management of Colletotrichum acutatum
using bacteria
The biocontrol of C. acutatum using bacteria was studied in apple,
loquat, nectarine, peach, tamarillo and strawberry fruits.
Bacillus cereus (Poleatewich et al., 2012), Bacillus megaterium (Pole
atewich et al., 2012), Bacillus mycoides (Poleatewich et al., 2012),
B. subtilis (Lee et al., 2012), Paenibacillus polymyxa (Kim et al., 2016),
and Serratia marcescens (Boyd-Wilson et al., 2014) were used as
biocontrol agents in apple. Although the disease incidence inhibition
(DII) when using B. cereus and B. megaterium was not indicated, it was
reported that the incidence inhibition was higher in the presence of
B. mycoides (21–34%) than in the presence of B. cereus and B. megaterium
(Poleatewich et al., 2012). Similarly, the DII of S. marcescens was 25%
(Boyd-Wilson et al., 2014). These inhibition activities were much lower
in comparison with the incidence inhibition produced by B. subtilis
(78–83%) and P. polymyxa (79%), indicating that the biocontrol ability
of the former species against C. acutatum in apple is not as good as that of
B. subtilis and P. polymyxa. Although B. megaterium showed low DII for
C. acutatum, the lesion length inhibition (LLI) was 95% (Poleatewich
et al., 2012). As mentioned below, the biocontrol yeasts were more
efficient in controlling C. acutatum in apple in comparison with the
bacterial biocontrol agents.
Bacillus subtilis was also employed for the management of C. acutatum
in peach, nectarine and tamarillo (Lee et al., 2012; Arroyave-Toro et al.,
2017). Interestingly, B. subtilis could also inhibit the disease incidence
and lesion length produced by the pathogen, with similar efficacy than
that showed in apple fruit. These results indicate that B. subtilis can
easily colonize different fruit hosts.
Bacillus amyloliquefaciens could inhibit more efficiently the disease
incidence of C. acutatum in loquat in comparison with B. cereus (Wang
et al., 2014, 2020). This result is in agreement with the modest ability of
B. cereus reducing the disease incidence of C. acutatum in apple, and
suggests that B. cereus is not a suitable biocontrol agent for the man
agement of Colletotrichum. It must be noted that the ability of
B. amyloliquefaciens to reduce the disease incidence was similar in
comparison with that produced by B. subtilis. Alijani et al. (2019) re
ported the biological control of C. nymphaeae in strawberry using
Staphylococcus sciuri, which inhibited the pathogen advancement by
72–78%.
In general, the best activities for the management of C. acutatum
were reported when using B. subtilis, P. polymyxa and
B. amyloliquefaciens. Paenibacillus polymyxa was reported to secrete
antifungal enzymes with chitinase, amylase, cellulose and protease ac
tivities (Kim et al., 2016). Bacillus subtilis EA-CB0015, which was used
for the management of C. acutatum in tamarillo, was reported to produce
antifungal lipopeptides, such as iturin A and fengycin C (Arroyave-Toro
et al., 2017). It must be remarked that the direct application of lip
opeptides and cell-free supernatant could completely inhibit the disease
incidence of C. acutatum in tamarillo, whereas the application of the
cells reduced the disease incidence only by 76%, indicating that the
cell-free supernatant is more suitable for the control of the disease in
comparison with the application of the cells. Although the antifungal
agents secreted by B. amyloliquefaciens were not studied, it was reported
that this species was able to enhance the disease resistance of loquat
fruit, increasing the activities of lytic enzymes chitinase and β-1,3-glu
canase, phenylalanine ammonia-lyase, and antioxidant peroxidase
(Wang et al., 2020).
2.2. Biocontrol strategies for the management of Colletotrichum
gloeosporioides using bacteria
The biocontrol strategies for the management of C. gloeosporioides
species using bacteria were carried out in different fruits, including
apple, avocado, chili, litchi, loquat, mango, orange, papaya, soursop,
yam, banana and pear.
Table 1
Summary of principal hosts associated with Colletotrichum complexes.
Clade Main hosts
C. acutatum Almond, apple, avocado, chili, citrus, coffee, cranberry, grape,
maple, mango, passion-fruit, grape, olive, peach, pepper,
pomegranate, Rhododendron, strawberry, tamarillo and tomato
C. boninense Almond, avocado, Eucalyptus, Euonymus japonicas, tomato,
mango and olive
C. coccodesa
Pepper, potato, tomato and onion
C. dematium Ginseng, mulberry, spinach and pepper
C. destructivum Alfalfa, legumes, sunflower and tobacco
C. dracaenophilum Buxus and bamboo
C. gloeosporioides Almond, apple, avocado, banana, cacao, cashew, chili, citrus,
coffee, cranberry, Hevea, litchi, loquat, mango, Maytenus
ilicifolia, olive, papaya, passion-fruit, pear, soursop, strawberry,
Stylosanthes, tamarillo, tea and yam
C. graminicola Maize and sorghum
C. magnum Papaya
C. orbiculare Cucumber
C. orchidearum Dendrobium, Oncidium and Philodendron
C. truncatum Bamboo, chili, papaya, pepper, soybean, strawberry and tomato
a
C. coccodes is a Colletotrichum species that is not included in any clade due to
it shows particular characteristics.
X.-C. Shi et al.

3
Table 2
Efficacy of biocontrol strategies for the management of Colletotrichum species in postharvest fruits using bacterial strains.
Pathogen clade
(species)
Fruit Antagonist Optimum concentration of
biocontrol agent
Disease incidence
inhibition (%)
Lesion length
inhibition (%)
Reference
C. acutatum Apple Bacillus cereus 107
cells/mL -a
-a
Poleatewich et al. (2012)
Apple Bacillus megaterium 107
cells/mL -a
95 Poleatewich et al. (2012)
Apple Bacillus mycoides 107
cells/mL 21–34 -a
Poleatewich et al. (2012)
Apple Bacillus subtilis 108
cells/mL 78–83 85 Lee et al. (2012)
Apple Paenibacillus polymyxa 108
cells/mL 79 47 Kim et al. (2016)
Apple Serratia marcescens 105
cells/mL 25 78 Boyd-Wilson et al. (2014)
Loquat Bacillus
amyloliquefaciens
108
cells/mL 84 57 Wang et al. (2020)
Loquat Bacillus cereus 108
cells/mL 63 73 Wang et al. (2014)
Nectarine Bacillus subtilis 108
Peach Bacillus subtilis 108
Tamarillo Bacillus subtilis 6.2 × 108
cells/mL 76b
65–68 Arroyave-Toro et al. (2017)
C. acutatum (C.
nymphaeae)
Strawberry Staphylococcus sciuri 108
cells/mL -a
72–78 Alijani et al. (2019)
C. gloeosporioides Apple Amycolaptosis sp. -a
-a
94 Sadeghian et al. (2016)
Apple Bacillus subtilis 2 × 107
cells/mL >80 60 Rodríguez-Chávez et al. (2019)
Apple Paenibacillus polymyxa 108
cells/mL 84 60 Kim et al. (2016)
Avocado Bacillus atrophaeus 107
cells/mL 40 42 Guardado-Valdivia et al. (2018)
Avocado Bacillus mycoides 107
cells/mL -a
42b
Guerrero-Barajas et al. (2020)
Avocado Burkholderia spinosa 104
cells/mL -a
38 De Costa et al. (2008)
Avocado Serratia sp. -a
-a
64–73 Granada et al. (2020)
Chili Bacillus subtilis 9 × 108
cells/mL 80 64 Narasimhan and Shivakumar
(2015)
Chili Streptomyces philanthi -c
100 Boukaew et al. (2018)
Litchi Bacillus subtilis 108
cells/mL -a
-a
Wu et al. (2019)
Loquat Bacillus
methylotrophicus
104
cells/mL 0 20 He et al. (2020)
Loquat Bacillus thuringiensis 104
cells/mL 0 40 He et al. (2020)
Mango Bacillus
amyloliquefaciens
108
cells/mL 87 -a
Alvindia and Acda (2015)
Mango Bacillus licheniformis 107
cells/mL 44 82 Govender and Korsten (2006)
Mango Bacillus pumilus 106
cells/mL 94 96 Zheng et al. (2013)
Mango Bacillus subtilis 106
cells/mL 22 93d
Hernandez Montiel et al. (2017)
Mango Bacillus subtilis 106
cells/mL 80 80e
Reyes-Estebanez et al. (2020)
Mango Bacillus thuringiensis 106
cells/mL 87 88 Zheng et al. (2013)
Mango Bacillus velezensis 109
cells/mL 78 82 Reyes-Estebanez et al. (2020)
Mango Brevundimonas
diminuta
107
cells/mL -a
93 Kefialew and Ayalew (2008)
Mango Burkholderia spinosa 105
cells/mL -a
28 De Costa et al. (2008)
Mango Enterobacteriaceae sp. 107
cells/mL -a
Mango Pseudomonas
fluorescens
9 × 108
cells/mL 90 -a
Vivekananthan et al. (2004)
Mango Stenotrophomonas
maltophilia
107
cells/mL -a
Mango Stenotrophomonas
rhizophila
109
cells/mL 89 92 Hernandez Montiel et al. (2017);
Reyes-Perez et al. (2019)
Orange Bacillus
amyloliquefaciens
108
cells/mL 67 -a
Arrebola et al. (2010)
Papaya Pseudomonas putida 108
cells/mL 58 43 Shi et al. (2011)
Papaya Streptomyces violascens 106
cells/mL 100 Choudhary et al. (2015)
Soursop Bacillus atrophaeus 107
cells/mL 66 55 Guardado-Valdivia et al. (2018)
Yam Streptomyces sp. 106
cells/mL 81 88 Palayinandi et al. (2011)
C. gloeosporioides (C.
musae)
Banana Bacillus
amyloliquefaciens
108
cells/mL 90 81f
Alvindia (2013a)
Banana Bacillus subtilis 108
cells/mL -a
72 Fu et al. (2010)
Banana Bacillus subtilis 3 × 108
cells/mL -a
57h
Sangeetha et al. (2010)
Banana Bacillus velezensis 1.5 × 108
cells/mL -a
97 Damasceno et al. (2019)
Banana Burkholderia cepacia -g
56 64 Shu et al. (2017)
Banana Burkholderia spinosa 104
cells/mL -a
86–98 De Costa et al. (2008)
Banana Enterobacter cloacae 1.5 × 108
cells/mL -a
Banana Pseudomonas
fluorescens
3 × 108
cells/mL -a
57h
Banana Pseudomonas
fluorescens
3 × 108
cells/mL -a
50 Peeran et al. (2014)
Banana Pseudomonas sp. 3 × 108
cells/mL -a
57h
Banana Pseudomonas syringae 108
cells/mL -a
77 Williamson et al. (2008)
Banana Serratia marcescens 1.5 × 108
cells/mL -a
Banana Stenotrophomonas
maltophilia
1.5 × 108
cells/mL -a
Banana Streptomyces katrae -g
33 92 Shu et al. (2017)
fructicola)
Pear Lysobacter antibioticus -g
0 74 Laborda et al. (2019)
C. truncatum Chili Burkholderia arboris 108
cells/mL 90 -a
Sandani et al. (2019)
(continued on next page)
X.-C. Shi et al.

4
The management of C. gloeosporioides in apple was attempted using
B. subtilis (Rodríguez-Chávez et al., 2019), P. polymyxa (Kim et al., 2016)
and Amycolaptosis sp. (Sadeghian et al., 2016). Bacillus subtilis and
P. polymyxa could inhibit the disease incidence of C. gloeosporioides in
apple, and the inhibitory activities were similar to those described for
the control of C. acutatum (>80% incidence inhibition). The used
B. subtilis strain was found to produce lipopeptides, mainly iturin-type
compounds, and fengycin A and B, with strong antifungal activity
(Rodríguez-Chávez et al., 2019). Although the incidence inhibition was
not indicated in the reference, Amycolaptosis sp. could inhibit the
diameter of the lesion by 94% (Sadeghian et al., 2016).
The control of C. gloeosporioides in avocado was attempted using
Bacillus atrophaeus (Guardado-Valdivia et al., 2018), B. mycoides
(Guerrero-Barajas et al., 2020), Serratia sp. (Granada et al., 2020) and
Burkholderia spinosa (De Costa et al., 2008). Unfortunately, none of the
reported strategies showed high inhibitory effect. Bacillus atrophaeus
only inhibited the disease incidence by 40%, whereas the LLI was
64–73% in the presence of Serratia sp. Bacillus atrophaeus was also used
for the control of C. gloeosporioides in soursop, showing higher incidence
inhibition (66%) in comparison with that reported in avocado (Guar
dado-Valdivia et al., 2018). Several genes involved in the production of
surfactin, bacillomycin and iturin were identified in the genome of
B. atrophaeus, suggesting that these antibiotics may be involved in the
antifungal activity. Bacillus mycoides was studied for the control of
C. acutatum in apple and C. gloeosporioides in avocado (Poleatewich
et al., 2012; Guerrero-Barajas et al., 2020), and showed low inhibitory
activities in both cases, suggesting that this species is not a suitable
biocontrol agent for the management of Colletotrichum species.
Bacillus subtilis and Streptomyces philanthi were used for the control of
C. gloeosporioides in chili. The efficacy of B. subtilis to reduce the disease
incidence and lesion length was similar to that reported using the same
bacteria in apple (80%) (Narasimhan and Shivakumar, 2015). Interest
ingly, S. philanthi could completely inhibit (100%) the disease incidence
(Boukaew et al., 2018), indicating that S. philanthi is a very powerful
agent for the management of C. gloeosporioides. The application of
S. philanthi was not performed via cell colonization but via treatment
with S. philanthi-produced volatile organic compounds (VOCs), which
were mainly composed of antifungal acetophenone.
Bacillus amyloliquefaciens was used for the control of
C. gloeosporioides in mango and orange, showing higher incidence in
hibition activity in mango (87%) than in orange (67%) (Alvindia and
Acda, 2015; Arrebola et al., 2010). The incidence inhibition in mango
was similar to that reported for the inhibition of C. acutatum by
B. amyloliquefaciens in loquat fruit (84%) (Wang et al., 2020). Bacillus
amyloliquefaciens was reported to produce lipopeptide iturin A, which
was identified as the main agent producing the antifungal activity (Yan
et al., 2020). This result suggests that, considering the total inhibitory
activity, the ability of Bacillus species to induce disease resistance in
fruits is not as important as the secreted antifungal lipopeptides.
Apart from B. amyloliquefaciens, several Bacillus species were used for
the management of C. gloeosporioides in mango, including B. licheniformis
(Govender and Korsten, 2006), B. pumilus (Zheng et al., 2013), B. subtilis
(Hernandez Montiel et al., 2017; Reyes-Estebanez et al., 2020),
B. thuringiensis (Zheng et al., 2013) and B. velezensis (Reyes-Estebanez
et al., 2020). All the species could efficiently inhibit the disease inci
dence (>78%), with the exception of B. licheniformis that showed low
inhibitory activity (44%). The reports when using B. subtilis were slightly
contradictory. In this sense, B. subtilis ATCC55614 was reported to
inhibit the disease incidence by 77% (Hernandez-Montiel et al., 2017);
however, B. subtilis RBM01 inhibited the disease incidence by 22%, and
the lesion length by 93% (Reyes-Estebanez et al., 2020). This difference
can be explained considering that the results obtained with ATCC55614
were measured 5 days after inoculation, whereas the results with
RBM01 were measured after 10 days. It must be remarked that the re
sults obtained with ATCC55614 were similar to those obtained with
other B. subtilis strains described in this review. Bacillus pumilus and
B. thuringiensis, which showed the highest inhibitory activity (94 and
87%, respectively), were reported to produce antifungal VOCs, such as
2-nonanone, 2-decanone and β-benzeneethanamine (Zheng et al., 2013).
The management of C. gloeosporioides in mango was also attempted
using Brevundimonas diminuta (Kefialew and Ayalew, 2008), B. spinosa
(De Costa et al., 2008), Enterobacteriaceae sp. (Kefialew and Ayalew,
2008), Pseudomonas fluorescens (Vivekananthan et al., 2004), Steno
trophomonas maltophilia (Kefialew and Ayalew, 2008) and Steno
trophomonas rhizophila (Hernandez-Montiel et al., 2017). Pseudomonas
fluorescens and S. rhizophila could inhibit the disease incidence by 90%
and 89%, respectively. The antifungal effect of P. fluorescens was mainly
attributed to the ability of this bacterium to enhance the disease resis
tance of mango, inducing the expression of lytic enzymes chitinase and
β-1,3-glucanase (Vivekananthan et al., 2004).
The management of C. gloeosporioides in papaya was carried out
using Pseudomonas putida and Streptomyces violascens. The inhibitory
activity in disease incidence obtained with P. putida was low (58%) (Shi
et al., 2011), whereas S. violascens could completely inhibit the symp
toms (Choudhary et al., 2015). Only 2 bacterial strains could completely
inhibit the growth of C. gloeosporioides (in mango and in papaya), and
both of them belonged to the Streptomyces genus, indicating that Strep
tomyces species are especially suitable for the management of this
pathogen. Another Streptomyces strain, Streptomyces sp. MJM5763, was
used for the control of C. gloeosporioides in yam, providing again high
inhibitory activity (DII: 81%; LLI: 88%) (Palayinandi et al., 2011).
Bacillus subtilis combined with hot air treatment reduced
C. gloeosporioides-caused rot in litchi fruit (Wu et al., 2019). The treat
ment effectively enhanced the activity of antioxidants peroxidase,
catalase, and superoxide dismutase, and of disease-defence enzyme
phenylalanine ammonia-lyase, chitinase and β-1,3-glucanase in litchi
fruit. Bacillus methylotrophicus and B. thuringiensis were used for the
control of C. gloeosporioides in loquat, showing modest antifungal ac
tivities (He et al., 2020). Although the disease incidence was slightly
reduced after 48 h, no inhibition in disease incidence was observed at
Table 2 (continued)
Pathogen clade
(species)
Fruit Antagonist Optimum concentration of
biocontrol agent
Disease incidence
inhibition (%)
Lesion length
inhibition (%)
Reference
Chili Burkholderia gladioli 108
cells/mL 75 -a
Sandani et al. (2019)
Chili Burkholderia rinojensis 108
cells/mL 100 Sandani et al. (2019)
Chili Pseudomonas
aeruginosa
108
cells/mL 100 Sandani et al. (2019)
a
Not indicated.
b
The cell-free supernant completely inhibit the disease incidence.
c
Application of VOCs.
d
After 10 days at 28 ◦
C.
e
After 5 days at 28 ◦
C.
f
Simultaneous treatment with hot water.
g
The cell-free supernatant was used.
h
Simultaneous application of B. subtilis, P. fluorescens and Pseudomonas sp.
X.-C. Shi et al.

5
extended periods. This result is contrary with the high efficiency of
B. thuringiensis for the control of the same pathogen in mango.
Still inside the C. gloeosporioides clade, several biocontrol strategies
have been directed towards the control of C. musae, the species typically
associated with banana anthracnose. These strategies have employed a
wide range of biocontrol agents, including B. amyloliquefaciens (Alvin
dia, 2013a), B. subtilis (Sangeetha et al., 2010; Fu et al., 2010; Peeran
et al., 2014), B. velezensis (Damasceno et al., 2019), Burkholderia cepacia
(Shu et al., 2017), B. spinosa (De Costa et al., 2008), Enterobacter cloacae
(Damasceno et al., 2019), P. fluorescens (Sangeetha et al., 2010), Pseu
domonas sp. (Sangeetha et al., 2010), Pseudomonas syringae (Williamson
et al., 2008), S. marcescens (Damasceno et al., 2019), Stenotrophomonas
maltophilia (Damasceno et al., 2019) and Streptomyces katrae (Shu et al.,
2017). The best inhibitory activities were observed when using
B. amyloliquefaciens (DII: 90%; LLI: 81%), B. velezensis (LLI: 97%),
B. spinosa (LLI: 86–98%) and Streptomyces katrae (DII: 33%; LLI: 92%),
whereas the other bacterial strains only showed modest activity. Bacillus
velezensis showed higher performance in comparison with fungicide
Tecto SC (Damasceno et al., 2019).
Interestingly, although B. spinosa did not provide good inhibitory
activity against C. gloeosporioides in avocado and mango, it could suc
cessfully inhibit C. musae in banana. Bacillus amyloliquefaciens showed
interesting activities inhibiting the incidence of C. musae in banana, of
C. gloeosporioides in mango and orange, and C. acutatum in loquat,
indicating its capacity of colonizing diverse fruit hosts.
Alvindia (2013b) studied the ability of B. amyloliquefaciens DGA14 to
reduce the incidence of C. musae under different treatment conditions.
Combination of DGA14 and hot water inhibited mycelium growth by
83% as compared to 67% by DGA14 and 38% by hot water, as single
treatments. In agreement, the in vivo treatment of the fruits with DGA14
and hot water reduced the incidence by 91%, whereas the treatment
with DGA14 only reduced the inhibition by 70%.
The cell-free supernatant of Lysobacter antibioticus efficiently reduced
the lesion length of C. fructicola in pear by 74% (Laborda et al., 2019).
The activity was attributed to p-aminobenzoic acid, which showed a
mode of action based on cytokinesis inhibition (Laborda et al., 2018).
This is the only biocontrol strategy for the management of Colletotrichum
in pear fruit that was reported until date.
truncatum using bacteria
Sandani et al. (2019) described the use of Burkholderia arboris, Bur
kholderia gladioli, Burkholderia rinojensis and Pseudomonas aeruginosa for
the control of C. truncatum in chili. All species could efficiently inhibit
the disease incidence of C. truncatum, obtaining the complete inhibition
when using B. rinojensis and P. aeruginosa. The antifungal agents
involved in the activity of these species were not studied.
species using filamentous fungi
As in the case of the biocontrol strategies using bacteria, filamentous
fungi were also used for the management of C. acutatum,
C. gloeosporioides and C. truncatum. The biocontrol of Colletotrichum
species was attempted using different filamentous fungi, including
Aureobasidium pullulans, Clonostachys byssicola, Curvularia pallescens,
Epicoccum dendrobii and Trichoderma species (Table 3). In contrast with
the bacterial biocontrol agents, most filamentous fungi were reported to
produce the antifungal activity via colonization of Colletotrichum hyphae
and subsequent competition for space. The strategies were used for the
management of Colletotrichum species in apple, lemon and banana.
Aureobasidium pullulans was used for the management of C. acutatum
in apple; however, the strategy showed low inhibitory activity (44%) (Di
Francesco et al., 2015; Mari et al., 2012). This inhibition was much
lower in comparison with the inhibition produced by bacteria, such as
B. subtilis and P. polymyxa, and yeasts in the same fruit.
It must be remarked that Trichoderma harzianum could completely
inhibit the advancement of C. gloeosporioides in lemon (Oliveri et al.,
2015). As far as we know, this is the only strategy for the management of
C. gloeosporioides in lemon fruit that was reported. Epicoccum dendrobii
was able to enter the internal tissues of apple fruit via stomatal cells, and
inhibited conidial germination and appressorium formation of
C. gloeosporioides (Bian et al., 2020). The antifungal activity of
E. dendrobii was found to be higher when the biocontrol agent was
applied prior to infection than post infection. In preventive applications,
E. dendrobii could completely inhibit the pathogen advancement,
Table 3
Efficacy of biocontrol strategies for the management of Colletotrichum species in postharvest fruits using filamentous fungi.
Pathogen clade
(species)
Fruit Species Optimum concentration of
biocontrol agent (cells/mL)
Disease incidence
inhibition (%)
Lesion length
inhibition (%)
Reference
C. acutatum Apple Aureobasidium
pullulans
108
cells/mL 44b
-a
Di Francesco et al. (2015);
Mari et al. (2012)
C. gloeosporioides Apple Epicoccum dendrobii 105
cells/mL 100 Bian et al. (2020)
Lemon Trichoderma
harzianum
106
spore/mL 100 Oliveri et al. (2015)
musae)
Banana Clonostachys
byssicola
106
spore/mL -a
68 Alvindia and Natsuaki
(2008)
Banana Curvularia pallescens 106
spore/mL -a
(2008)
Banana Trichoderma
harzianum
109
spore/mL -a
88c
Banana Trichoderma
harzianum
106
spore/mL -a
(2008)
Banana Trichoderma
harzianum
106
spore/mL 92d
-a
Alvindia (2013a)
Banana Trichoderma koningii 109
spore/mL -a
60c
Banana Trichoderma
pseudokoningii
109
spore/mL -a
88c
Banana Trichoderma reseei 109
spore/mL -a
59 Sangeetha et al. (2009)
Banana Trichoderma virens 109
spore/mL -a
Banana Trichoderma viride 109
spore/mL -a
Banana Trichoderma sp. 108
spore/mL -a
50 Oliveira et al. (2016)
a
Not indicated.
b
Application of VOCs.
c
At 1 ◦
C.
d
Treatment with sodium bicarbonate.
X.-C. Shi et al.

6
demonstrating higher ability for the control of C. gloeosporioides in apple
in comparison with the bacterial strains Amycolaptosis sp., B. subtilis and
Paenibacillus polymyxa.
Filamentous fungi have been extensively used for the management of
C. musae in banana. In this field, Cl. byssicola and Cu. pallescens reduced
the symptoms by 68 and 41%, respectively (Alvindia and Natsuaki,
2008), and similar inhibitory activities were found when using Tricho
derma species. The highest inhibitory activity was detected with
T. harzianum and T. pseudokoningii, with 88% inhibition (Sangeetha
et al., 2009). Interestingly, Alvindia reported a suitable combination to
improve the inhibitory effect of T. harzianum by adding sodium bicar
bonate, which showed 92% incidence inhibition (Alvindia, 2013a).
When comparing the LLI produced by bacteria and filamentous fungi, it
can be observed that the bacterial strategies, such as the ones with
B. velezensis (97%) or B. spinosa (86–98%) (Table 2), showed higher
inhibitory activity in comparison with the strategies with filamentous
fungi.
using yeasts
As in the strategies with bacteria and filamentous fungi, some stra
tegies using yeasts were directed towards the management of
C. acutatum, C. gloeosporioides and C. truncatum, whereas some reports
focused on the control of Colletotrichum coccodes and Colletotrichum
dianesei species, which are not included in any clade (Table 4). Three
mechanisms have been related to the antifungal activity of yeasts against
Colletotrichum species, including secretion of antifungal metabolites and
enzymes, competition for nutrients and space, and induced resistance. In
this sense, yeasts provide a combination of the antifungal mechanisms
showed by both bacteria and filamentous fungi together.
Numerous biocontrol strategies for the management of Colleto
trichum species using yeasts were reported. For better understanding,
this section was divided into 4 different subsections depending on the
studied pathogen.
4.1. Biocontrol strategies for the management of Colletotrichum acutatum
using yeasts
The biocontrol of C. acutatum using yeasts was carried out in apple,
avocado and loquat. All yeasts used for the management of C. acutatum
in apple, including Candida pyralidae (Mewa-Ngongang et al., 2019),
Cryptococcus laurentii (Conway et al., 2005), Metchnikowia pulcherrima
(Conway et al., 2005; Janisiewicz et al., 2003) and Pichia kluyveri
(Mewa-Ngongang et al., 2019), allowed the complete inhibition of the
pathogen. It is must be noted that no bacteria or filamentous fungi could
achieve the complete inhibition of C. acutatum in apple, demonstrating
the suitability of yeasts for the management of Colletotrichum. Sodium
bicarbonate was used in the treatment with C. laurentii and
M. pulcherrima, and improved the antifungal activity (Conway et al.,
2005). This result is in agreement with the above-mentioned strategy
based on the combination of T. harzianum and sodium bicarbonate to
improve the antifungal activity against C. musae in banana (Alvindia,
2013b). Candida pyralidae and P. kluyveri were reported to produce
antifungal VOCs, such as phenethyl acetate (Mewa-Ngongang et al.,
2019). As in the case of S. philanthi-produced acetophenone (Nar
asimhan and Shivakumar, 2015), most active VOCs consisted of ester
structures.
Wickerhamomyces anomalus and Candida intermedia were used for the
management of C. acutatum in avocado, with the former one showing the
best DII and LLI (75 and 55%, respectively) (Campos-Martinez et al.,
2016). The incidence inhibition of W. anomalus against C. acutatum in
avocado was not as high as the one showed by W. anomalus against
C. gloeosporioides in the same fruit (88%), indicating that this species in
more suitable for the management of C. gloeosporioides than for the
management of C. acutatum.
On the other hand, Pichia membranaefaciens and Pichia guilliermondi
were employed for the control of C. acutatum in loquat, and inhibited the
disease incidence by 64 and 55%, respectively (Cao et al., 2008, 2009;
Liu et al., 2010). These incidence inhibitions were lower in comparison
with that obtained using B. amyloliquefaciens (84%) (Wang et al., 2020).
gloeosporioides using yeasts
The control of C. gloeosporioides species using yeasts has been carried
out in avocado, citrus, grape, mango, olive, papaya and banana.
Campos-Martínez et al. (2016) used C. intermedia and W. anomalus
for the management of C. gloeosporioides in avocado. The highest inci
dence inhibiton (88%) was achieved when using W. anomalus. This in
hibition is higher than those obtained with bacteria, demonstrating the
ability of W. anomalus to control C. gloeosporioides.
Pichia membranaefaciens was used for the management of
C. gloeosporioides in citrus fruit, with 82% incidence inhibition after 15
days (Zhao et al., 2018). The P. membranaefaciens treatment increased
phenylalanine ammonia-lyase activity, which induced the accumulation
of lignin, and maintained the concentration of pectin and cellulose in
citrus fruit, enhancing cellular integrity. The addition of chitosan in the
P. membranaefaciens treatment enhanced the inhibitory activity,
achieving 80% inhibition after 19 days (Zhou et al., 2016).
Liu et al. (2018) reported the control of C. gloeosporioides in grape
using Saccharomyces cerevisiae, obtaining 80% incidence inhibition. It
was reported that S. cerevisiae produced antifungal VOCs, and proteins
with β-1,3-glucanase and chitinase activities.
The biocontrol of C. gloeosporioides in mango was studied using
Candida membranaefaciens (Kefialew and Ayalew, 2008), Cryptococcus
diffluens (Hernandez-Montiel et al., 2017), Cryptococcus laurentii (Bau
tista-Rosales et al., 2014), Debaryomyces hansenii (Hernandez-Montiel
et al., 2017), Debaryomyces nepalensis (Zhou et al., 2018), M. pulcherrima
(Tian et al., 2018), Meyerozyma caribbica (Bautista-Rosales et al., 2014;
Aguirre-Güitrón et al., 2019), Meyerozyma guilliermondii (Lopex-Cruz
et al., 2020), Papiliotrema aspenensis (Konsue et al., 2020), Pseudozyma
hubeiensis (Konsue et al., 2020), Rhodotorula minuta (Hernandez-Montiel
et al., 2017) and Torulaspora indica (Konsue et al., 2020). The highest
inhibitory activities were observed when using D. hansenii (LLI: 91%),
D. nepalensis (LLI: 93%), M. pulcherrima (DII: 100%), Meyerozyma guil
liermondii (DII: 89%; LLI: 94%) and P. aspenensis (LLI: 94%). Some yeast
species, such as T. indica and P. hubeiensis, did not show any inhibitory
activity. Among all bacterial and yeast biocontrol agents, M. pulcherrima
was the only one that could inhibit completely the disease incidence.
The treatment of mango fruit with M. pulcherrima promoted the activ
ities of lytic enzymes β-1,3-glucanase and chitinase, enhancing the dis
ease resistance of the fruit (Tian et al., 2018; Shao et al., 2019). As
indicated in Table 4, M. pulcherrima also produced the complete inhi
bition of C. acutatum in apple, demonstrating that M. pulcherrima is a
powerful biocontrol agent for the management of Colletotrichum species.
The antifungal mechanism of P. aspenensis DMKU-SP67, which was used
for the control of C. gloeosporioides in mango, consisted of the production
of antifungal VOCs, biofilm formation and siderophore production
(Konsue et al., 2020). DMKU-SP67 provided similar efficacy in com
parison with benomyl.
For the management of C. gloeosporioides in olive, Pesce et al. (2018)
screened a number of yeast species, including Candida tropicalis, Cryp
tococcus albidus, Pichia kudriavzevii, P. membranaefaciens, Saccharomyces
chevalieri, Torulaspora delbrueckii and W. anomalus. In this case, the
highest inhibitory activity was detected when using C. tropicalis and
W. anomalus, with 90% LLI in both cases. Wickerhamomyces anomalus
was reported to secrete proteins with chitinase and β-1,3-glucanase ac
tivities. Although P. membranaefaciens was employed in the manage
ment of C. gloeosporioides in olive and C. acutatum in loquat, it showed
modest activities in both cases.
Taken together, W. anomalus was successfully used for the control of
X.-C. Shi et al.

7
Table 4
Efficacy of biocontrol strategies for the management of Colletotrichum species in postharvest fruits using yeasts.
Pathogen clade
(species)
Disease incidence
inhibition (%)
Lesion length
inhibition (%)
Reference
Colletotrichum sp. Pepper Rhodotorula glutinis 108
cells/mL -a
85 De Franca et al. (2015)
C. acutatum Apple Candida pyralidae 108
cells/mL 100 Mewa-Ngongang et al. (2019)
Apple Cryptococcus laurentii 3 × 107
cells/mL 100b
Conway et al. (2004, 2005)
Apple Metchnikowia
pulcherrima
3 × 107
cells/mL 100b
Conway et al. (2004, 2005)
Apple Metchnikowia
pulcherrima
3 × 107
cells/mL 100 Janisiewicz et al. (2003)
Apple Pichia kluyveri 108
cells/mL 100 Mewa-Ngongang et al. (2019)
Avocado Candida intermedia 4 × 107
cells/mL 50 -a
Campos-Martínez et al. (2016)
Avocado Wickerhamomyces
anomalus
4 × 107
cells/mL 75 55 Campos-Martínez et al. (2016)
Loquat Pichia guilliermondii 108
cells/mL 55 38 Liu et al. (2010)
Loquat Pichia
membranaefaciens
108
cells/mL 64c
30c
Cao et al. (2008, 2009)
C. coccodes Tomato Saccharomyces
cerevisiae
-a
100 Heling et al. (2017)
C. dianesei Mango Cystobasidium
calyptogena
106
cells/mL 0 0 Chanchalchaovivat et al. (2007)
Mango Pichia kudriavzevii 106
Mango Saccharomyces
cerevisiae
106
C. gloeosporioides Avocado Candida intermedia 4 × 107
cells/mL 50 -a
Campos-Martínez et al. (2016)
Avocado Wickerhamomyces
anomalus
4 × 107
cells/mL 88 36 Campos-Martínez et al. (2016)
Citrus Pichia
membranaefaciens
108
cells/mL 82d
88 Zhao et al. (2018)
Citrus Pichia
membranaefaciens
108
cells/mL 80e
33 Zhou et al. (2016)
Grape Saccharomyces
cerevisiae
108
cells/mL 80 40 Liu et al. (2018)
Mango Candida
membranaefaciens
107
cells/mL -a
Mango Cryptococcus diffluens 106
spore/mL -a
49 Hernandez Montiel et al. (2017)
Mango Cryptococcus laurentii 107
cells/mL -a
76 Bautista-Rosales et al. (2014)
Mango Debaryomyces
hansenii
106
spore/mL 56 91 Hernandez Montiel et al. (2017)
Mango Debaryomyces
nepalensis
108
cells/mL -a
93 Zhou et al. (2018)
Mango Metchnikowia
pulcherrima
108
cells/mL 100f
Tian et al. (2018)
Mango Meyerozyma caribbica 107
cells/mL 53 24 Aguirre-Güitrón et al. (2019)
Mango Meyerozyma caribbica 107
cells/mL 69 69 Bautista-Rosales et al. (2013)
Mango Meyerozyma
guilliermondii
108
cells/mL 89 94 Lopez-Cruz et al. (2020)
Mango Papiliotrema
aspenensis
108
cells/mL -a
94 Konsue et al. (2020)
Mango Pseudozyma hubeiensis 108
cells/mL -a
Mango Rhodotorula minuta 106
spore/mL -a
82 Hernandez Montiel et al. (2017)
Mango Torulaspora indica 108
cells/mL -a
Olive Candida tropicalis 108
cells/mL 90 47 Pesce et al. (2018)
Olive Cryptococcus albidus 108
Olive Pichia kudriavzevii 108
Olive Pichia
membranaefaciens
108
Olive Saccharomyces
chevalieri
108
Olive Torulaspora
delbrueckii
108
Olive Wickerhamomyces
anomalus
108
Papaya Anthracocystis
grodzinskae
108
cells/mL -a
94b
Silva Ferreira et al. (2018)
Papaya Candida oleophila 2 × 108
cells/mL 54 88b
Gamagae et al. (2004)
Papaya Cryptococcus magnus 108
cells/mL -a
-a
De Capdeville et al. (2007)
Papaya Debaryomyces
hansenii
106
cells/mL 50g
83g
Hernandez-Montiel et al. (2017)
Papaya Debaryomyces
hansenii
104
cells/mL 40g
66g
Hernandez-Montiel et al. (2017)
Papaya Meyerozyma
guilliermondii
108
cells/mL -a
41 Lima et al. (2013)
Papaya Wickerhamomyces
anomalus
108
cells/mL -a
30 Lima et al. (2013)
Banana Candida inconspicua 108
cells/mL -a
48 Vilaplana et al. (2020)
(continued on next page)
X.-C. Shi et al.

8
C. gloeosporioides in olive, and C. gloeosporioides and C. acutatum in
mango, indicating the capacity of this yeast to colonize different fruit
hosts. However, W. anomalus showed only modest activity for the con
trol of C. gloeosporioides in papaya (30% LLI) (Lima et al., 2013).
Apart from W. anomalus, several yeasts, such as Anthracocystis
grodzinskae (Silva Ferreira et al., 2018), Candida oleophila (Gamagae
et al., 2004), Cryptococcus magnus (De Capdeville et al., 2007),
D. hansenii (Hernandez-Montiel et al., 2018) and M. guilliermondii (Lima
et al., 2013), were studied for the control of C. gloeosporioides in papaya.
Debaryomyces hansenii provided similar LLI for C. gloeosporioides in
papaya (83%) in comparison with that obtained in mango. Debar
yomyces hansenii showed various antifungal mechanisms, including
antifungal VOCs production, β-1,3-glucanase and protease activity, and
competition for nutrients. D. hansenii was more efficient for the control
of C. gloeosporioides in papaya than Tecto 60. As it can be seen in Table 4,
the efficacy of D. hansenii was highly dependent on the cell concentra
tion, detecting higher inhibitory activity when applying 106
cells/mL
than when applying 104
cells/mL. The incidence inhibitions produced
by A. grodzinskae (88%) and C. oleophila (94%) were higher than that
produced by D. hansenii. The optima biocontrol efficacy for
A. grodzinskae was found when combining the yeast with sodium bi
carbonate (Silva Ferreira et al., 2018). Similarly, the combined appli
cation of sodium bicarbonate in wax formulation and C. oleophila
provided the highest efficacy (Gamagae et al., 2004).
Although M. guilliermondii was successfully used for the control of
C. gloeosporioides in mango, the inhibitory activity was low in papaya
(Lopez-Cruz et al., 2020; Lima et al., 2013). Hassan et al. (2013) used
five non-identified yeast strains that showed in vivo antifungal activities
against C. gloeosporioides causing anthracnose in papaya.
A number of biocontrol yeasts were studied for the management of
C. musae in banana, including Candida inconspicua (Vilaplana et al.,
2020), Candida musae (Lassois et al., 2008), C. tropicalis (Zhimo et al.,
2016, 2017), Pichia anomala (Lassois et al., 2008), Saccharomyces bou
lardii (Heling et al., 2017) and S. cerevisiae (Zhimo et al., 2016, 2017;
Heling et al., 2017). Among all studied yeasts, C. tropicalis showed the
highest inhibitory activity, with 96% LLI. This result was similar to that
reported for some bacterial biocontrol agents, such as B. velezensis (97%)
and B. spinosa (98%). Candida tropicalis could easily colonize banana
wounds, remained stable in the inoculation site, and showed a mode of
action based on competition for nutrients and space. The highest
inhibitory activity was observed when the C. tropicalis treatment was
carried out 36 h before the pathogen inoculation. As above mentioned,
C. tropicalis could also successfully inhibit the growth of
C. gloeosporioides in olive, which highlights its ability to colonize
different fruit hosts. In contrast with the high inhibitory activity showed
by S. cerevisiae for the control of C. gloeosporioides in grape, S. cerevisiae
showed low inhibitory activity for the management of C. musae in
banana.
truncatum using yeasts
Chanchalchaovivat et al. (2007) reported the management of Colle
totrichum capsici, which belongs to the C. truncatum clade, in chili. Four
different yeasts, including Candida musae, Candida quercitrusa, Issatch
enkia orientalis and P. guilliermondii, were employed in this regard.
Interestingly, P. guilliermondii, which showed the highest activity, could
reduce the disease incidence by 93%. By comparing the biocontrol
strategies of C. trucatum in chili using bacteria and yeasts, it can be
observed that the complete inhibition was only obtained when using
bacteria, particularly with B. rinojensis and Pseudomonas aeruginosa,
which indicates that these bacteria are more efficient. The specific
mechanisms involved in the antifungal activity of bacteria and yeasts
were not indicated.
4.4. Biocontrol strategies for the management of Colletotrichum coccodes
and Colletotrichum dianesei using yeasts
Saccharomyces cerevisiae transformants expressing a cecropin A-
based peptide were used for the management of C. coccodes causing
anthracnose in tomato fruit (Jones and Prusky, 2002). Mentioned
transformants could completely inhibit the disease incidence. As far as
we know, only this biocontrol strategy was reported for the management
of C. coccodes. Similarly, only one report can be found in the literature
related to the biocontrol of C. dianesei in mango (Tuao Gava et al., 2018).
In this report, Cystobasidium calyptogena, P. kudriavzevii and S. cerevisiae
were screened. Cystobasidium calyptogena and P. kudriavzevii showed no
inhibitory activity against C. coccodes, whereas S. cerevisiae could inhibit
the disease incidence and lesion length by 39 and 34%, respectively.
This result is in agreement with the modest antifungal activities showed
Table 4 (continued)
Pathogen clade
(species)
Disease incidence
inhibition (%)
Lesion length
inhibition (%)
Reference
musae)
Banana Candida musae 108
cells/mL -a
54 Lassois et al. (2008)
Banana Candida tropicalis 108
cells/mL -a
96 Zhimo et al. (2016, 2017)
Banana Pichia anomala 108
cells/mL -a
-a
Lassois et al. (2008)
Banana Saccharomyces
boulardii
6.3 g/L -a
cerevisiae
5.5 g/L -a
cerevisiae
108
cells/mL -a
67 Zhimo et al. (2016, 2017)
C. truncatum (C.
capsici)
Chili Candida musae 5 × 108
cells/mL 83 49 Chanchalchaovivat et al. (2007,
2008); Nantawanit et al. (2010)
Chili Candida quercitrusa 5 × 108
Chili Issatchenkia orientalis 5 × 108
Chili Pichia guilliermondii 5 × 108
a
Not indicated.
b
Treatment with sodium bicarbonate.
c
After 4 days and simultaneous application of jasmonic acid.
d
After 15 days.
e
In combination with chitosan after 19 days.
f
Metchnikowia pulcherrima was inoculated 24 h earlier than the pathogen, and the fruit was storage at 15 ◦
C.
g
Treatment with sodium bicarbonate and wax.
X.-C. Shi et al.

9
by S. cerevisiae against C. musae in banana fruit. Pichia kudriavzevii did
not show any inhibitory activity for the management of C. dianesei in
mango, and low inhibitory activity for the management of
C. gloeosporioides in olive.
5. Commercial biocontrol agents for the management of
Colletotrichum species
According to Greenbook, there are 2 biocontrol agents recommended
for the management of Colletotrichum species: Serenade ASO and Dou
bleNickel55. Serenade ASO, which is commercialized by Bayer, contains
B. subtilis QST713; whereas DoubleNickel55 contains
B. amyloliquefaciens D747, and is commercialized by Certis. As it can be
observed in Table 2, both B. subtilis and B. amyloliquefaciens have been
used in different fruits; however, in general, these species did not show
the highest inhibitory activities, indicating that more efficient biocon
trol strategies have been developed during last years.
On the other hand, T. harzianum T-39, which is commercialized by
Trichodex, is a biocontrol agent suggested for the management of
Botrytis cinerea in postharvest fruits. Despite this fact, Freeman et al.
(2004) reported that this biocontrol agent was also efficient for the
management of C. acutatum in strawberry. The obtained results indi
cated that the disease incidence was reduced by 51%. By comparing all
reported strategies for the control of C. acutatum with this strategy using
T-39, it can be observed that most strategies using other bacterial and
yeast biocontrol agents showed better inhibitory activities for the
management of C. acutatum in fruit in comparison with T-39 (Tables 2
and 4). As it can be observed in Table 4, some recently reported stra
tegies using yeasts could completely inhibit the advancement of this
pathogen.
It is remarkable that, although some of the best inhibitory results
were obtained using yeasts, no yeast strain was commercialized for the
management of Colletotrichum species.
6. Conclusions and future prospects
In summary, a number of strategies have been reported during recent
years able to suppress Colletotrichum-caused diseases in postharvest
fruits, with some of them showing higher inhibitory activities in com
parison with the commercial biocontrol agents. The reported strategies
could cover a number of different fruits; however, most strategies
focused on the study of species from the C. acutatum, C. gloeosporioides
and C. truncatum clades, whereas the C. boninense and C. magnum clades,
which have been also found causing anthracnose in postharvest fruits
(Damm et al., 2019; Chung et al., 2020), remain completely unexplored.
The commercialized species B. subtilis and B. amyloliquefaciens have been
thoroughly studied in different fruits against different pathogens; how
ever, other antagonists with higher antifungal activity were only
examined against few pathogens in few fruits, resulting in a lack of
knowledge about their antifungal spectrum and their ability to colonize
different fruits.
Apart from data demonstrating the efficacy of biocontrol agents,
these need to be safe. Toxicity studies have developed as a requisite for
all new biocontrol products that reach the market (Ocampo-Suarez
et al., 2017b). Some studied biocontrol agents, such as Pichia kudriav
zevii, are known as nosocomial pathogens and may cause neonate deaths
(Nagarathnamma et al., 2017). Thus, many researchers may be gener
ating valuable information in terms of disease control, but those results
will not be suitable for practical use.
In general, there is a lack of information about the specific mecha
nisms involved in the antifungal activity and, specially, about how
relevant is each mechanism in the total antifungal activity. In order to
explore the full potential of the newly reported microbial antagonists,
preliminary research goals should be focused on its inhibition mecha
nism and molecular analysis, microbial viability, toxicity and market
storage conditions.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
This study was supported by the National Natural Science Founda
tion of China (81803407 and 32050410290), the Nantong Applied
Research Program (MS12017023-8), and the Natural Science Research
Project of Jiangsu Higher Education Institutions (18KJB180023).
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