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Antagonistic microorganisms efficiency to suppress damage caused by

Colletotrichum gloeosporioides in papaya crop: Perspectives and challenges

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 Vol. 19, No. 2 (2020) 839-849
Revista Mexicana de Ingeniería Química
CONTENIDO
Antagonistic microorganisms efficiency to suppress damage caused by Colletotrichum
gloeosporioides in papaya crop: Perspectives and challenges
Volumen 8, número 3, 2009 / Volume 8, number 3, 2009
Eficiencia de los antagonistas microbianos para suprimir el daño ocasionado por
Colletotrichum gloeosporioides en el cultivo de papaya: Perspectivas y desafíos
213 Derivation and application of the Stefan-Maxwell equations
J.M. Silva-Jara, R. López-Cruz, J.A. Ragazzo-Sánchez, M. Calderón-Santoyo*
(Desarrollo
Tecnológico Nacional de México/Instituto y aplicación
Tecnológico de las
de Tepic. ecuaciones
Laboratorio de Stefan-Maxwell)
Integral de Investigación en Alimentos (LIIA). Avenida Tecnológico 2595, Lagos del
Country, 63175. Tepic, Nayarit; México.
Stephen Whitaker
Received: August 13, 2019; Accepted: October 24, 2019

Biotecnología / Biotechnology
Abstract
Papaya (Carica papaya 245L.) is one ofde
Modelado thelamost valued tropical
biodegradación fruits worldwide
en biorreactores due to
de lodos de its nutritional content,
hidrocarburos but petróleo
totales del its production is
drastically affected by Colletotrichum gloeosporioides, one of the main pathogens responsible for anthracnose disease. Several
intemperizados
techniques as an alternative en suelos
of conventional y sedimentos
chemical treatments for disease control have been studied. Among these techniques,
the use of antagonist microorganism has emerged as a promising, eco-friendly alternative for postharvest disease control. This
review is focused on the(Biodegradation modeling of sludge bioreactors of total petroleum hydrocarbons weathering in soil
inhibition of Colletotrichum gloeosporioides in papaya applying microbial antagonists. The main
purpose of this study, is and sediments)
to provide the results of in vivo and in vitro assays that addressed the use of microorganisms and
their activity as biocontrolS.A.
agents in papaya, considering
Medina-Moreno, its application
S. Huerta-Ochoa, to diminish crop
C.A. Lucho-Constantino, losses and suggesting
L. Aguilera-Vázquez, possible future
A. Jiménez-
researches applicable to their attractive usage. We believe that a specific compilation is helpful for groups that are in research of
González y M. Gutiérrez-Rojas
pre- and postharvest fruits management, providing useful information to create new perspectives and/or alternative in emerging
technologies. 259 Crecimiento, sobrevivencia y adaptación de Bifidobacterium infantis a condiciones ácidas
Keywords: microbial antagonists, biological control, postharvest disease, papaya, Colletotrichum gloeosporioides.
(Growth, survival and adaptation of Bifidobacterium infantis to acidic conditions)
Resumen L. Mayorga-Reyes, P. Bustamante-Camilo, A. Gutiérrez-Nava, E. Barranco-Florido y A. Azaola-
La papaya (Carica papaya L.) es uno de los frutos tropicales más apreciados a nivel mundial debido a su contenido nutricional.
Espinosa
Sin embargo, su producción es afectada drásticamente por Colletotrichum gloeosporioides, uno de los principales patógenos
265 Statistical
responsables de la antracnosis. approach
Se han to optimization
estudiado of ethanol alternativas
diversas estrategias fermentationalbytratamiento
Saccharomyces cerevisiae
químico in the para el
convencional
control de antracnosis. Entre éstas, el uso de microorganismos antagonistas ha surgido como una alternativa amigable con
presence of Valfor® zeolite NaA
el medio ambiente y eficiente para el control de enfermedades poscosecha. Esta revisión está enfocada en la inhibición de
Colletotrichum gloeosporioides en papaya
(Optimización aplicando
estadística de lamicroorganismos antagonistas,
fermentación etanólica proveyendo
de Saccharomyces los resultados
cerevisiae más importantes
en presencia de
de ensayos de inhibición in vivo e in vitro, considerando así su aplicación para disminuir las pérdidas en poscosecha, y sugiriendo
zeolita Valfor® zeolite NaA)
los posibles trabajos de investigación que requieren realizarse para hacer más atractivo su uso. Creemos que esta compilación
específica será útil a los G. Inei-Shizukawa,
grupos H. A. Velasco-Bedrán,
de investigación que trabajan G.
enF.elGutiérrez-López
manejo pre yand H. Hernández-Sánchez
poscosecha de frutas para crear nuevas
perspectivas o alternativas en el uso de tecnologías emergentes.
Palabras clave: microorganismos antagonistas, control biológico, enfermedades poscosecha, papaya, Colletotrichum gloeosporioides.
Ingeniería de procesos / Process engineering
271 Localización de una planta industrial: Revisión crítica y adecuación de los criterios empleados en

1 Introduction
esta decisión fungicides, resulting in economic losses (Chávez-
Magdaleno
(Plant site selection: Critical review and adequation this2018;
et inal.,
criteria used decision)Hernández-Lópezet al.,
J.R. Medina, R.L. Romero y G.A. Pérez 2018, Ramos-Guerrero et al. 2020). More than
50% of waste of fresh fruits and vegetables are
Papaya (Carica papaya L.) is one of the main tropical
caused by Colletotrichum species (Paull et al.,
fruits produced in Mexico (Carballo-Sánchez et al.,
1997; Awang et al., 2011; Chávez-Magdaleno et
2016), but it can be infected with, anthracnose,
al., 2018). This disease is associated to the fungus
one of the main diseases that affects it. In recent
Colletotrichum gloeosporioides that causes deep
years, anthracnose prevalence in crops and postharvest
rounded stains, soaked with water in orange-pink
production of papaya and other tropical fruits,
zones formed due to the conidia mass that covers
has grown in Mexico despite the treatments with
* Corresponding author. E-mail: mcalderon@ittepic.edu.mx
Tel. 33-33-45-52-00, Ext. 1312
https://doi.org/10.24275/rmiq/Bio788
issn-e: 2395-8472

Publicado por la Academia Mexicana de Investigación y Docencia en Ingeniería Química A.C. 839
 Silva-Jara et al./ Revista Mexicana de Ingeniería Química Vol. 19, No. 2 (2020) 839-849

the center of the lesion and sometimes, a pattern

of concentrically rings. Another species of this
fungus is Colletotrichum truncatum, also known as
Colletotrichum capsici; this fungus causes lesions
with color from brown to black, with spore mass
in gray color and plenty of concentrically rings
(Tapia-Tussell et al., 2008; Torres-Calzada et al.,
2013). Furthermore, it causes cell damage, and
the production of acervuli is associated with dark
sunken areas on the surface of fruit with diameter
of about 4.2 cm. This pathogen infects the host
fruit through a subcuticular intramural infection,
causing anthracnose in 72 hours, and producing
acervuli in 96 hours after inoculation, completing
Fig. 1. Anthracnose symptoms in papaya (Carica
its life cycle (Rojo-Báez et al., 2016). Recently,
papaya L.).
Colletotrichum magnum was identified in papaya Fig. 1. Anthracnose symptoms in papaya (Carica papaya L.)
infected with anthracnose; colonies exhibiting white-
orange color with acervuli, unicellular cylindrical
conidia with rounded edges were isolated (Tapia-
Tussell et al., 2016). Also, Colletotrichum fructicola
has been first evidenced as a phytopathogen for
papaya in Oaxaca, Mexico, with lesions characterized
by sunken and irregular edges, presenting white
to gray sporulation at the center. Even if these
characteristics are similar to C. gloeosporioides
species, identification through molecular techniques,
revealed different species (Marquez-Zequera et al.,
2018).
Biological control agents (BCA) emerged as
an alternative for chemical fungicides, promoting
a sustainable, eco-friendly treatment. In literature,
the first report of BCA was Trichoderma spp. as Fig. 2. Life cycle of Colletotrichum gloeosporioides
an antagonist microorganism against the strawberry Fig.(Sharma
2. Lifeand
cycle of Colletotrichum
Kulshrestha, 2015) gloeosporioides (Sharma
pathogen Botrytis rot (Tronsmo and Denis, 1977).
Since then, numerous antagonists were isolated media for growth and sporulation, e.g. potato dextrose
and identified as BCA. In this review, we agar (PDA) or malt extract agar. Anthracnose caused
collect information of BCA against the pathogen by C. gloeosporioides infects fruits, like avocado,
Colletotrichum gloeosporioides, the main pathogen apple, mango, papaya, strawberry, and many others.
responsible for papaya anthracnose. Symptoms of infection by this pathogen are expressed
as small, dark lesions that appear on leaves, fruits, and
flowers, which produce concentric ring patterns, as
2 Colletotrichum gloeosporioides depicted in Figure 1 (Sharma and Kulshrestha, 2015).

2.1 Life cycle

Colletotrichum gloeosporioides is a fungal pathogen
that belongs to the order Melanconiales. It can C. gloeosporioides follows two routes: pathogenic and
infect different crops, from seeds to trees, and cause saprophytic. Pathogenic germination takes place on
postharvest diseases, such as anthracnose. Optimal plants or hydrophobic surfaces, with fast mitosis and
conditions for C. gloeosporioides growth are 25-28°C development of a single germ tube. This process is
and pH 5.8-6.5. This pathogen grows when conditions initiated immediately and results in the formation of
of humidity are suitable, but in dry seasons, it does appressoria (Barhoom and Sharon, 2004). Figure 2
not develop. It has been isolated in various growing depicts this process.

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Fig. 3. Antagonist mechanisms of action.

2.2 Anthracnose disease spreading species screening. Currently, the list of Colletotrichum
Fig. 3. Antagonist mechanisms
Some fungi are capable to displace short distances
of has
names in use action
a total of 66 species, and 20
were recently added but considered as doubtful. Thus,
on their own. Fungal spores spread by wind driven this demands the increasing reliance on molecular
rain, irrigation water, insects, mammals, soil water, methods for species definition. Finally, because carbon
and humans as carriers (LeClair et al., 2015). and nitrogen are the most important and essential
When fungal spores are transferred to new host elements, besides others, for their sources and
plants, they attach to them and begin the infection incorporation into infect ion, growth and reproduction,
process one more time. To understand this, the the strain identification vary by geographical and host
spread of infectious material from one site to sources due to substrate properties (Sangeetha and
another is a control issue on crop losses, hence, Rawal, 2008).
elucidate its mechanism of dissemination is a complex
of mixed genes involved, and their identification
and characterization still generates challenges. On 3 Antagonistic microorganisms
this topic, some of these identified genes and
their function are listed below: i) Shpx2, Shpx5, on pathogens
Shpx6, Shpx12 and PepCYP (host defense); ii) Cap
20 and CgDN3 (host pathogenesis); iii) Chip 6
(pathogenesis, conidial germination and appressorium 3.1 Inhibition mechanisms
formation); iv) Pnl-1 and Pnl-2 (pathogenesis), v) Pel-
B (degrade plant cell-wall); vi) CgDN24 and Pel- Several research groups have studied the possible
1,Pel-2 (pathogenesis and hyphal development); vii) mechanisms of antagonist inhibition in pathogens,
CgCTR2 (putative copper transporter); viii) CgRac1 which can be: antibiosis, competition, parasitism,
(morphogenesis, nuclear division and pathogenesis); enzymatic cell-wall degradation, induction of systemic
ix) GDH2, GS1, GLT and MEP (induce ammonia resistance, and biofilm formation (Cook and Baker,
accumulation and pathogenesis); and x) PacC (create 1983; Fravel, 1988; Handelsman and Parke, 1989;
alkaline environment and regulate activity of several Adams, 1990; Bautista-Rosales et al., 2013; González-
genes) (Sharma and Kulshrestha, 2015). Polymerase Estrada et al., 2017a). In Figure 3 the aforementioned
chain reaction (PCR) still predominates on fungal mechanisms are briefly described.

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placed by submerging the fruit in a suspension with

a defined concentration of them (Figure 5). After
incubation at specific conditions for the pathogen,
diameters of inhibition and disease severity are
measured (Rahman et al., 2009).

3.3 Antagonistic activity of microorganisms

against Colletotrichum gloeosporioides
in papaya (Carica papaya L.)
Fig. 4. In vitro assays, challenge of antagonists against Gamagae et al. (2003) evaluated the inhibitory
Colletotrichum gloeosporioides, a) High inhibition of activity of yeast Candida oleophila, individually
pathogen b) Poor inhibition of pathogen.
Fig. 4. In vitro assays, challenge of antagonists against Colletotrichum glo
and in combination with a suspension of sodium
bicarbonate (2%), against C. gloeosporioides in
High inhibition of pathogen b) Poor inhibition of pathogen papaya (Carica papaya L.) at storage conditions
(13.5°C, 95% R.H., 10 days). They observed that
the combination of both treatments reduced the
population of the pathogen and anthracnose severity
in papaya inoculated and naturally infected with
C. gloeosporioides. Treatments by themselves were
effective suppressing the infection, but combination
of both proved to be better. Gamagae et al. (2004)
evaluated the same treatments inside a wax coating,
and results showed that the coating increased the
inhibitory activity of yeast and sodium bicarbonate
compared to the previous study. Wax coating created
a modified atmosphere, where C. oleophila was able
to adapt and survive while inhibiting the pathogen.
This suggests that coating methods enhance microbial
Fig. 5. In vivo assays, fruits are coated with a survival (Luján-Hidalgo et al., 2019) and could be
suspension of antagonists by immersion or aspersion. used as an important strategy to extend viability
Fig. 5. In vivo assays, fruits are coated with a suspension
of of antagonists
biological by to
agents immersion or
control postharvest diseases
aspersion (González-Estrada et al., 2017b).
3.1.1 In vitro assays of fungal inhibition
Three strains of Bacillus firmus and four of
In vitro assays can be conducted as described by Pseudomonas fluorescens were evaluated by Baños-
Hernández-Montiel et al. (2013), where a disc from a Guevara et al. (2004) against anthracnose disease in
previously grown inoculum of around 5 mm diameter Maradol red papaya (Carica papaya L). They found
is placed in the center of a Petri dish with PDA that in the in vitro assay, two strains of B. firmus
by substitution. BCA are inoculated at a defined (B10 and B3) reduced growth of C. gloeosporioides
concentration on sterile filter paper and placed at in 75.32 and 69.17% in 96 hours, respectively, while
equal distance from the center of the Petri dish. After P. fluorescens strains, did not present antagonism
incubation at specific conditions for the pathogen, against the pathogen. B. firmus strains were able to
diameters of inhibition are measured. Procedure is inhibit C. gloeosporioides in postharvest, this can
shown in Figure 4. Furthermore, spore germination be due to nutrient competition and space, or due to
test is needed to complete in vitro assays on the the production of antibiotics and other antimicrobial
antagonistic activity (Rahman et al., 2007). substances.
Epiphytic microorganisms from papaya leaves and
3.2 In vivo assays for antagonist-pathogen fruit were isolated by de Capdeville et al. (2007a),
164 distinct microorganisms were found, from which
interaction
67 yeasts were identified. 30 strains were able to
For in vivo assays, wounds are performed in papaya inhibit C. gloeosporioides growth in vitro, and 10
and C. gloeosporioides is inoculated. Antagonists are of these were evaluated in vivo. Ribosomal RNA

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sequences for the yeast strain with better inhibitory to singled or commercial treatments (NaOCl).
activity resulted in Cryptococcus magnus MZKI Production of iturin A, fengycin and surfactin
K-479. in vivo tests were carried out in papaya were shown on fruit individually treated with B.
infected with C. gloeosporioides and inoculation amyloliquefaciens or in combination with 1-MCP,
of C. magnus on different cell concentration at suggesting that this bacterium can be used as a
three different times (0, 24 and 48 hours) prior to protectant of fruit when previously treated with 1-
pathogen inoculation. The results showed that high MCP.
cell concentration of C. magnus (107 and 108 cell/mL) Endophytic bacterial strain Pseudomonas putida
was effective, independently of the inoculation time. MGY2, was isolated from papaya fruit by Shi et al.
Later, electronic microscopy imaging of antagonist (2011). Papaya treated with P. putida MGY2, was
effect was observed. Fungal cells were able to colonize challenged against C. gloeosporioides in postharvest,
superficial lesions faster than the pathogen, competing and the possible inhibition mechanisms were studied.
for the space and probably the nutrients. This fungus They observed that fruit with treatment showed
produces a flocculent matrix that affects the integrity reduction in disease index, disease incidence and
of hypha. Summarizing, this yeast can inhibit C. lesion diameter. Decrease in reduction of firmness,
gloeosporioides growth by competition of space and and production of ethylene delay in papaya harvest
nutrients, and also, by modifying integrity of hypha and storage at 25°C was also observed. Reduction
(de Capdeville et al., 2007b). of disease severity was up to 35% compared to
Burkholderia cepacia and Pseudomonas the untreated control. Phenylalanine (PAL), catalase
aeruginosa were studied by Rahman et al. (2007). (CAT) and peroxidase (POD) activities were increased
Mycelial growth and spore germination of C. in the presence of P. putida and phenolic content rose.
gloeosporioides in presence of B. cepacia were They suggested that papaya inoculated with P. putida
completely inhibited, while P. aeruginosa only had MGY2, may activate defensive enzymes and genes
inhibitory activity over mycelial growth, but not that can induce resistance against pathogens disease.
on spore germination. The possible mechanism of Our group (Magallón-Andalón et al., 2012),
inhibition is due to bacterial production of antibiotics. observed parasitism mechanism of Rodothorula
Antifungal substances produced by B. cepacia, mucilaginosa 2 and Candida famata on C.
strain B23, were extracted by Kadir et al. (2008), gloeosporioides in papaya (Figure 6).
and evaluated against C. gloeosporioides. Cultured in
nutrient broth (NB), B. cepacia was able to produce
higher amounts of antifungal substances. Dilutions
of antifungal substances (1:8) in the supernatant
of B. cepacia B23, inhibited mycelial growth and
spore germination (41 and 100%, respectively) of C.
gloeosporioides. Substances produced in NB medium
inhibited mycelial growth in 82.67% at concentrations
of 1:1, where pyrrolnitrin was detected among other
compounds.
Rahman et al. (2009) combined B. cepacia B23
with chitosan and calcium chloride (0.75 and 3%,
respectively), and found that anthracnose infection
was effectively controlled in fruits inoculated with the
pathogen during storage at 14°C and 95% R.H. for
18 days. This combination reduced disease severity in
99% by the 14th day and at 6 days of ripening at 28 ±
2°C.
Osman et al. (2010) evaluated the efficiency Fig. 6. Candida famata (above) and Rhodotorula
of Bacillus amyloliquefaciens PPCB004 in Solo mucilaginosa 2 (below) adhesion to the
papaya, previously treated with 1-methylcyclopropene Colletotrichum gloeosporioides mycelium observed
(1-MCP) during storage, against anthracnose and
rottenness. The combined treatment of 1-MCP and B. Fig. 6. Candida famata (above) and Rh
by optical microscopy (100x) after a) 12h, b) 24h and
c) 48h (Magallón-Andalón et al., 2012).
amyloliquefaciens reduced disease severity compared
Colletotrichum gloeosporioides myceli
12h, b) 24h and c) 48h (Magallón-And
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Both yeasts were capable to attach to the pathogen, produces antibiotics and low molecular weigth
producing hydrolytic enzymes responsible for fungi siderophores; this bacteria was tested against various
cell wall degradation. The enzyme production in both fungi responsible for rotting in fruits. In vitro assays
strains was increased when yeast was in presence of demonstrated that C. gloeosporioides growth was
sterile mycelium of C. gloeosporioides, confirming the inhibited in about 30 mm, also they correlated the
usage of mycelium as a nutrient. When cultured in production of antibiotics with the biomass formation;
a medium enriched with nutrients, C. famata had a by the third day, production of antibiotics reached
better inhibition of C. gloeosporioides, probably due its maximum values, as well as the inhibition zone.
to faster intake of nutrients. Extraction of antifungal compounds was carried out
Colletotrichum gloeosporioides is considered with five organic solvents, with n-butanol being the
the most significant of fungal species that cause best at percentage of extraction and antifungal activity.
anthracnose in papaya in Brazil. To suppress it, Further analysis demonstrated that this antifungal
two killer yeasts, Wickerhamomyces anomalus and compounds are of polyene nature (Choudhary et al.,
Meyerozyma guilliermondii, were tested against C. 2015).
gloeosporioides, and the influence of inoculation Landero-Valenzuela et al. (2016) compiled
time was examined along with the occurrence of information with different methods for controlling
mycoparasitism. Assays of hydrolytic enzyme β- C. gloeosporioides in different fruits. The most
1-3-glucanase and chitinase were carried out. In commonly used is the addition of chemical fungicides,
papaya that was treated with W. anomalus 24 h although they represent a threat to consumers due to
before the inoculation of C. gloeosporioides, fruits residues remaining in the fruits. Another alternative
showed lesions 31.35% smaller than those without for controlling C. gloeosporioides, is the application
the treatment, while on those inoculated 24 h after, of biorationals produced by different antagonist
lesions were 4% smaller. M. guilliermondii had a microorganisms, like essential oils, chitosan (Sotelo-
similar response, 24 h before inoculation of C. Boyás et al., 2015), or glucosinolates. Molecular
gloeosporioides, a lesion 41.17% smaller than control manipulations have been carried out to repress the
was observed, while 24 h after inoculation lesion expression of genes involved in ripening (production
was 10% smaller (Lima et al., 2013). W. anomalus of ethylene). Although this is a promising technique,
reduced the lesion induced by C. gloeosporioides in it requires major investments and results take longer
24.62%, and M. guilliermondii in 20.68% after 6 days than other methods.
of inoculation. Table 1 summarizes the studied microorganisms
Colonization of killer yeast achieved maximum for C. gloeosporioides inhibition. Percentage of
growth between the third and fourth day after inhibition for both in vivo and in vitro tests, and
inoculation, with a posterior stabilization of similar antagonist mechanism are also shown.
levels to the initial inoculum. The speed of
colonization of the yeast was faster than the growth of 3.4 Perspectives and challenges
the pathogen, providing protection to the fruits. This is
related to the competition for nutrients and space used Papaya is a valuable fruit due to its nutritional
as a mechanism for biocontrol. contribution and bioactive compounds (Vallejo-
Killer yeast mycoparasitism was observed on Castillo et al. 2020), but its shelf life in postharvest
C. gloeosporioides, causing physical damage, like storage is short, with consequent economic
turgidity loss, occurrence of concave areas and, losses. Anthracnose caused by Colletotrichum
in some cases, complete hypha rupture with yeast gloeosporioides is the main disease responsible for
penetration into the pathogen hyphae, possibly due to these losses. In order to control the disease, traditional
production of hydrolytic enzymes. Activity of β(1-3)- chemical fungicides are still in use since alternative
glucanase was of 1.18 and 0.78 nkat/mg protein for W. treatments, like antagonist microorganism studied in
anomalus and M. guilliermondii, respectively. 1 nkat this review, have not proved to be sustainable and/or
is equivalent to 1.0 nmol glucose released/mL/s. This attractive for commercialization yet, due to various
enzyme hydrolyzes glucans, an abundant component factors such as temperature and humidity conditions
of the fungal cell wall, giving support to the use of for pathogen growth. Biocontrol agents are a capable
this yeast against the anthracnose disease induced by technique, despite that, control efficiency could vary
C. gloeosporioides (Lima et al., 2013). from in vitro to in vivo conditions significantly;
perhaps biocontrol efficacy is influenced by the
Another bacteria, Streptomyces violascens

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Table 1. C. gloeosporioides inhibition with biocontrol agents. DSR: Disease Severity Reduction, MG: Mycelial
Growth, SG: Spore Germination, NR†: Not Reported. 1-MCP: 1-methyl-cyclopropene.
In vivo inhibition
Treatment In vitro inhibition (%) Antagonist mechanism Reference
(%) DSR

C. oleophila + NaHCO3 NR† NR† NR† Gamagae et al. (2003)

C. oleophila+ NaHCO3 + wax NR† NR† NR† Gamagae et al. (2004)

coating

B. firmus B10 75.32 MG NR† Competition Baños- Guevara et al. (2004)

B. firmus B3 69.17 MG NR† Competition Baños-Guevara et al. (2004)

C. magnus NR† NR† Competition de Capdeville et al. (2007)

B. cepacia 100 MG, 100 SG NR† Antibiosis Rahman et al. (2007)

P. aeruginosa 100 MG, 3.7 SG NR† Antibiosis Rahman et al. (2007)

B. cepacia 41 MG, 100 SG NR† Antibiosis Kadir et al. (2008)

B. cepacia + chitosan + CaCl2 NR† 98.2 Antibiosis Rahman et al. (2009)

P. putida NR† 35 Induction of systemic resistance Shi et al. (2010)

B. amyloliquefaciens + 1-MCP NR† NR† Antibiosis Osman et al. (2010)

W. anomalus NR† 24.62 Competition, parasitism, cell-wall degrading enzymes Lima et al. (2013)

M. guilliermondii NR† 20.68 Competition, parasitism, cell-wall degrading enzymes Lima et al. (2013)

amount of pathogen present (Roberts, 1994; Siddiqui (Salman et al., 2010). In addition, some authors
and Ali, 2014). have bet on combining the antagonists with different
Although several antagonist have proved to vehicles to improve disease management (Gamagae
be efficient in suppressing ancthranose caused by et al., 2004). Clearly, there is still much research
C. gloeoesporioides, several reports do not have needed in order to use antagonists. Future studies
tests simulating in situ conditions (Bautista-Baños could contemplate nanotechnology with greener
et al., 2013), which makes this technique not methods for encapsulation and for strengthening
sustainable yet. Antagonist mechanism of action the antagonist capacity. These studies could also
requires more elucidation. Furthermore, several include the use of biofilms with antagonists in a
preharvest studies are needed because papaya can be bioactive matrix (González-Estrada et al., 2017b) and
infected with conidia from isolates of Colletotrichum perhaps a new generation of hybrids that allows these
gloeosporioides, regardless of the original host plant. microorganisms to be sustainable and attractive to
For example, Colletotrichum isolates from papaya producers and consumers.
can cause infection in mango fruits (Freeman and
Shabi, 1996). On this regard, genetic and geographical
data provided, suggest that C. gloeosporioides was Conclusions
disseminated as an endophyte around the world
(Akem, 2006). Thus, understanding the origins and
diversity of C. gloeosporioides in papaya would have In order to explore full potential of microbial
importance to future research on control techniques, antagonists, preliminary research goals should
according to specific locations (Siddiqui and Ali, be focused on its inhibition mechanism and
2014). Even to improve the preharvest studies, the molecular analysis, microbial viability, market
existing pathogen could be identified, using infrared storage conditions, among others. Certainly, the
spectroscopy as a spectral marker, and in this way, above reviewed studies demonstrate that antagnostic
it could provide quicker information in comparison microorganisms are able to suppress the disease.
with PCR; therefore, an early action could be Hence, further studies should be conducted to escalate
established for the control of postharvest diseases their activity at industrial levels as eco-friendly

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technology. Protection 49, 8-20. https://doi.org/10.

1016/j.cropro.2013.02.011
Acknowledgements Bautista-Rosales, P.U., Calderón-Santoyo, M.,
Jorge M. Silva-Jara thanks CONACyT for the Servín-Villegas, R., Ochoa-Álvarez, N.A.
postdoctoral grant MOD.ORD./50/2017 and Rafael and Ragazzo-Sánchez, J.A. (2013). Action
López-Cruz for the doctoral grant 305354. mechanisms of the yeast Meyerozyma
caribbica for the control of the phytopathogen
Colletotrichum gloeosporioides in mangoes.
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