Vol. 10(19), pp. 2041-2047, 7 May, 2015
DOI: 10.5897/AJAR2014.9246
Article Number: AC3FD7052814
ISSN 1991-637X
Copyright ©2015
Author(s) retain the copyright of this article
http://www.academicjournals.org/AJAR
African Journal of Agricultural
Research
Full Length Research Paper
Sensitivity of Colletotrichum lindemuthianum from
green beans to fungicides and race determination of
isolates from State of São Paulo, Brazil
Ronaldo Caravieri de Souza Filho1, Tadeu Antônio Fernandes da Silva Júnior1*, José
Marcelo Soman1, Ricardo Marcelo Gonçalves1, Alisson Fernando Chiorato2, Margarida
Fumiko Ito2 and Antonio Carlos Maringoni1
1
Plant Protection Department, School of Agronomic Sciences (FCA)/UNESP, Zip Code 18.610-307 Botucatu,
SP, Brazil.
2
Agronomic Institute of Campinas (IAC), Zip Code 13.012-970 Campinas, SP, Brazil.
Received 15 October, 2014; Accepted 15 April, 2015
This study determined the physiological races of Colletotrichum lindemuthianum isolates, causal agent
of anthracnose, collected in green bean producing regions, and assessed the in vitro and in vivo
sensitivity of isolates to fungicides. Physiological races of isolates were determined by inoculation of
bean differential cultivars under controlled conditions. In vitro sensitivity of colony growth and conidial
germination were evaluated for carbendazim, chlorothalonil, copper oxide, mancozeb, pyraclostrobin,
thiophanate-methyl and for the mixtures of mancozeb + copper oxychloride, metiram + pyraclostrobin
and thiophanate-methyl + chlorothalonil at concentrations of 1, 10, 100 and 1000 μg/mL on PDA
medium. In vivo sensitivity was determined in detached primary leaves of green beans previously
treated with the same fungicides (commercial doses) recommended for the crop, and then inoculated
with conidial suspensions of C. lindemuthianum. C. lindemuthianum isolates were identified as
belonging to races 65 and 81. Treatments with pyraclostrobin and the mixture metiram + pyraclostrobin
were the most effective in inhibiting the colony growth and conidial germination in vitro, a result also
observed for the in vivo experiments, where these chemicals were the most effective in controlling the
green bean anthracnose.
Key words: Chemical control, Phaseolus vulgaris, anthracnose, physiological race, snap bean.
INTRODUCTION
Anthracnose, caused by Colletrotrichum lindemuthianum,
is one of the major diseases of green bean, occurring in
almost all producing countries, including Brazil. The
disease affects leaves and pods of the plants, reducing
productivity and the product quality for commercialization,
being the cultivation of susceptible cultivars in regions
with mild temperatures and high humidity one of the main
factors for this wide distribution (Dalla Pria et al., 2003).
*Corresponding author. E-mail: tadeusilvajr@gmail.com. Tel: +55(14) 3880-7167.
Author(s) agree that this article remain permanently open access under the terms of the Creative Commons Attribution
License 4.0 International License
2042
Afr. J. Agric. Res.
Use of resistant cultivars and chemical control are
essential for the efficient control of anthracnose (Ghini
and Kimati, 2000). The knowledge of the physiological
races of C. lindemuthianum that occurs on green beans
and the sensitivity of isolates to fungicides are
fundamental for the adoption of effective control
measures, whether by the use of resistant cultivars to
prevalent races of the pathogen in a region or for the
chemical control in susceptible cultivars with appropriate
fungicides.
Early studies in Brazil about the races of C.
lindemuthianum were made during the 60's and 70's, but
due to high pathogenic variability of the pathogen and the
small number of differential cultivars used, the results
were not reliable, as well as the use of different systems
for naming the races caused difficulties to measure the
variability in the fungus pathogenicity (Paradela Filho et
al., 1991; Rodriguez-Guerra et al., 2003). After the work
of Pastor-Corrales (1991), using 12 differential bean
cultivars to study the pathogenic variability of C.
lindemuthianum isolates, there was the standardization
and creation of a binary scale for symptoms assessment,
according to anthracnose severity, which provided the
description of new races and breeding of new sources of
resistance. Several studies have identified the
occurrence of races of C. lindemuthianum in different
regions of Brazil (Somavilla and Prestes, 1999;
Thomazella et al., 2002; Bonett et al., 2008), but without
specifying the origin of the isolates according to host
(common beans or green beans).
Chemical control of anthracnose with fungicides have
shown satisfactory results, resulting in high grain yield in
common bean (Conner et al., 2004; Garcia et al., 2007;
Gillard et al., 2012). In Brazil, there are more than 100
chemicals registered for the control of anthracnose in
common bean, however, for green beans, only seven
fungicides, from four different active ingredients (copper
oxide, mancozeb, mancozeb + copper oxycloride and
thiophanate-methil) are registered for use (Agrofit, 2015).
Some chemicals used to control the anthracnose of
common beans cannot be used on green bean, due to
problems of residues. C. lindemuthianum isolates from
common beans have shown a variation in the sensitivity
of mycelial growth for benzimidazole fungicides
(benomyl,
carbendazim
and
thiophanate-methyl)
(Maringoni and Barros, 2002; Sartorato, 2007; Sartori
and Maringoni, 2007), but there is no information about
the sensitivity of isolates from green beans.
The knowledge of physiological races and the
sensitivity of C. lindemuthianum isolates to fungicides are
essential for the efficient management of the anthracnose
of green bean. On this study, the physiological races of
12 monosporic isolates of C. lindemuthianum from green
bean producing regions of State of São Paulo, Brazil,
were identified, as well the in vitro and in vivo sensitivity
of isolates to fungicides recommended for the crop were
determined.
MATERIALS AND METHODS
Cultures and growth conditions
Pods of green beans naturally infected by C. lindemuthianum were
collected from producing regions of State of São Paulo, Brazil.
Small portions of conidia present in the lesions were transferred to
potato dextrose agar medium (PDA) (Acumedia, Baltimore, USA),
followed by incubation in the dark (25°C/10 days). Isolates 3149,
3151, 3152, 3153 and 3158 (collected in Botucatu), 3148
(Campinas), 3154 (Itatiba), 3147 (Jaú), 3150 (Morungaba), 3156
(São Manuel), 3155 (São Paulo) and 3157 (Vinhedo) were purified
and monosporic cultures obtained and preserved according to
Castellani's modified method (Dhingra and Sinclair, 1995). All
isolates had typical cultural and morphological characteristics of C.
lindemuthianum according to Schwartz (1991). For all experiments,
inoculum was produced on PDA in the dark (25°C/10 days). For the
in vitro sensitivity of conidial germination experiment, inoculum was
produced on oatmeal agar medium (60 g oat meal, 12 g agar and
1.000 mL distilled water) at same conditions, but for 15 days.
In vitro sensitivity of C. lindemuthianum isolates to fungicides
Colony growth sensitivity of all isolates were assessed to
commercial fungicides carbendazim, chlorothalonil, copper oxide,
mancozeb, pyraclostrobin, tiophanate-methyl and to the mixtures
mancozeb + copper oxychloride (57% + 43%), metiram +
pyraclostrobin (92% + 8%) and chlorothalonil + thiophanate-methyl
(71% + 29%) at 1, 10, 100 and 1000 µg/mL in 90 × 16 mm Petri
dishes with PDA medium. PDA medium without fungicides was
used as control. Mycelial discs (7 mm) were transferred to the Petri
dishes with the treatments and plates were incubated in the dark
(25°C/10 days). The average diameter of the colonies (mm) was
assessed and the percentage of inhibition calculated based in the
control treatment growth. Experimental design was completely
randomized with four replications for each fungicide concentration
and for each isolate. The effective dose causing 50% inhibition of
mycelial growth (ED50) was determined according to Sartori and
Maringoni (2007), and numerical index for each range of ED50 were
assigned: index 1 (ED50 < 1 µg/mL), index 2 (ED50 from 1 to 10
µg/mL), index 3 (ED50 from 10 to 100 µg/mL), index 4 (ED50 from
100 to 1000 µg/mL) and index 5 (ED50 > 1000 µg/mL).
Conidial germination sensitivity was evaluated for isolates 3147,
3150, 3155 and 3158 that showed sensitivity in the colony growth
experiment to mancozeb and to the chlorothalonil + tiophanatemethyl mixture. PDA preparation, fungicides and concentrations
were the same used for the assessment of colony growth
sensitivity. Suspensions were standardized to 5×105 conidia/mL
(Maringoni and Barros, 2002) and 100 µL of each suspension were
distributed on the surface of the media with fungicides followed by
incubation in the dark (25°C/24 h). Mycelial discs (1.5 cm) were
transferred to microscope slides and stained with lactophenol
cotton blue to paralyze the fungal growth. For each isolate and
fungicide concentration the germination of 100 conidia were
assessed per disc. Experimental design was completely
randomized with four replications and each plot represented by a
mycelial disc. With the results the effective dose causing 50%
inhibition of conidial germination (ED50) was determinated according
to the numerical index previously described.
In vivo sensitivity of C. lindemuthianum isolates to fungicides
Green beans plants cv. Itatiba II were cultivated in 2 L pots with
substrate (mixture of soil, weathered cattle manure and sand
(1:1:1), plus 0.6 kg of ammonium sulfate, 17 kg of superphosphate,
0.6 kg of potassium chloride and 0.8 kg of lime for every m3 of the
Filho et al.
2043
Table 1. Effective dose causing 50% inhibition of mycelial growth (ED50) for Colletotrichum lindemuthianum isolates from green beans to
fungicides.
Fungicides
Carbendazim
Chlorothalonil
Chlorothalonil + thiop.-methyl
Copper oxide
Mancozeb
Mancozeb + copper oxychloride
Metiram + pyraclostrobin
Pyraclostrobin
Thiophanate-methyl
3147
5
4
4
5
5
5
3
2
5
3148
5
5
5
5
5
5
4
2
5
3149
5
4
4
5
5
5
4
2
5
3150
5
3
4
5
5
5
3
2
5
3151
5
4
4
5
5
5
4
2
5
Isolate
3152 3153
5
5
4
3
4
3
5
5
5
4
5
5
4
4
2
2
5
5
3154
5
3
4
5
5
5
4
2
5
3155
5
3
4
5
4
5
4
2
5
3156
4
3
4
5
5
5
4
2
5
3157
5
4
5
5
5
5
4
2
5
3158
5
4
4
5
5
5
4
2
5
Numerical index from 1 to 5 correspond to different ranges of ED50: index 1 - ED50 < 1 µg/mL; index 2 - ED50 from 1 to 10 µg/mL; index 3 - ED50 from
10 to 100 µg/mL; index 4 - ED50 from 100 to 1000 µg/mL and index 5 - ED50 > 1000 µg/mL.
mixture) under greenhouse conditions (20-28°C/70-90% RU) till the
phenological growth stage V2. The primary leaves were collected,
immersed in a solution of 10% Tween 80 (10 s), and then
immersed, separately, in suspensions of commercial fungicides
carbendazim (1 mL/L), chlorothalonil (1.5 g/L), copper oxide (1.72
g/L), mancozeb (3.20 g/L), mancozeb + copper oxychloride (0.88 +
0.66 g/L), metiram + pyraclostrobin (1,65 + 0.15 g/L), pyraclostrobin
(0.15 mL/L), thiophanate-methyl (1.40 g/L) and chlorothalonil +
thiophanate-methyl (1.75 + 0.70 g/L) for 5 s. The leaves were
transferred in Petri dishes (150 × 15 mm) containing two paper
filters wetted with distilled water and sprayed with conidial
suspensions (106 conidia/mL) of each isolate, after 24 h of the
fungicide treatment (Gulart, 2009). Petri dishes containing two
primary leaves each were kept in the dark for 24 h and incubated in
BOD (20°C/7 days) under a 12 h photoperiod (2400 Lux). Control
treatment consisted of leaves immersed in water and inoculated
with conidial suspensions. Absolute control consisted of leaves
immersed in water without inoculation. Disease severity on leaves
was determined seven days after inoculation according to the
diagrammatic scale proposed by Dalla Pria et al. (2003).
Experimental design was completely randomized, with three
replicates for each isolate and fungicide. Data were subjected to
variance analysis and means were compared by Scott-Knott's test
at 5% probability.
Determination of physiological races of C. lindemuthianum
isolates
Seedlings of bean differential cultivars AB 136, Cornell 49-242, G
2333, Kaboon, Mexico 222, Michelite, Michigan Dark Red Kidney,
Perry Marrow, Pi 207262, TO, TU and Widusa were obtained under
greenhouse conditions in plastic trays of 84 cells containing sterile
vermiculite. The aerial part of five seedlings of each cultivar were
inoculated by spraying with a suspension (106 conidia/mL) of each
isolate, 10 days after emergence, according to Pastor-Corrales
(1991) and Carbonell et al. (1999). One plant of Pérola cultivar,
susceptible to most races of C. lindemuthianum, was used as a
negative control for each differential series. Seedlings were kept in
a climatic room (23°C/90% RU) under a 12 h photoperiod (2400
Lux).
The disease severity was evaluated 10 days after inoculation
based on disease scale from 1 to 9, with grades from 1 to 3
representing resistant genotypes, and grades above 3, susceptible
genotypes (Pastor-Corrales, 1991; Gonçalves-Vidgal et al., 2007).
RESULTS
In vitro sensitivity of C. lindemuthianum isolates to
fungicides
Results of colony growth and conidial germination in vitro
sensitivity of C. lindemuthianum isolates to fungicides
are described in Tables 1 and 2, respectively. All isolates
showed low sensitivity on colony growth and conidial
germination (ED50 > 1000 μg/mL) to thiophanate-methyl.
For
chlorothalonil
and
thiophanate-methyl
+
chlorothalonil, 50% and 75% of isolates had ED50
between 100 and 1000 μg/mL for colony growth,
respectively. For conidial germination, 100% of the
isolates showed ED50 between 10 and 100 μg/mL to
chlorothalonil + thiophanate-methyl, while chlorothalonil
was the most effective fungicide for inhibition of conidial
germination of isolates (100% of isolates with ED50 < 1
μg/mL). It was also observed a low sensitivity to
carbendazim (ED50 > 1000 μg/mL) to 100% (conidial
germination) and 91.7% (colony growth) of the isolates.
Regarding to mancozeb and mancozeb + copper
oxychloride, 83.4% and 100% of isolates had an ED50
higher than 1000 μg/mL for colony growth, respectively,
while 100% of the isolates showed ED50 between 10 and
100 μg/mL for conidial germination for these chemicals.
All isolates evaluated were sensitive to pyraclostrobin
and metiram + pyraclostrobin (ED50 from 1 to 10 μg/mL)
for conidial germination. For colony growth, the sensitivity
was reduced in the mixture metiram + pyraclostrobin
(83.4% of isolates with ED50 from 100 to 1000 μg/mL) in
relation to pyraclostrobin (100% of isolates with ED50
from 1 to 10 μg/mL). The isolates did not show sensitivity
to copper oxide with an ED50 higher than 1000 μg/mL for
colony growth and conidial germination.
2044
Afr. J. Agric. Res.
Table 2. Effective dose causing 50% inhibition of conidial germination (ED50) for C. lindemuthianum
isolates from green beans to fungicides.
Isolate
Fungicides
Carbendazim
Chlorothalonil
Chlorothalonil + thiop.-methyl
Copper oxide
Mancozeb
Mancozeb + copper oxychloride
Metiram + pyraclostrobin
Pyraclostrobin
Thiophanate-methyl
3147
5
1
3
5
3
3
2
2
5
3150
5
1
3
5
3
3
2
2
5
3155
5
1
3
5
3
3
2
2
5
3158
5
1
3
5
3
3
2
2
5
Numerical index from 1 to 5 correspond to different ranges of ED50: index 1 - ED50 < 1 µg/mL; index 2 - ED50
from 1 to 10 µg/mL; index 3 - ED50 from 10 to 100 µg/mL; index 4 - ED50 from 100 to 1000 µg/mL and index 5 ED50 > 1000 µg/mL.
Table 3. Anthracnose severity in detached primary leaves of green bean cv. Itatiba II treated with fungicides and inoculated with C.
lindemuthianum isolates.
Fungicide
Control (water)
Carbendazim
Chlorothalonil
Chlorothalonil + thiop.-methyl
Copper oxide
Mancozeb
Mancozeb + copper oxychloride
Metiram + pyraclostrobin
Pyraclostrobin
Thiophanate-methyl
V.C.%
Isolate
3147
71.7a*
66.7a
4.0c
8.7c
31.7b
c
1.7
4.0c
0f
0f
41.7b
17.6
3150
100.0a**
41.7b
1.7c
6.0c
40.0b
2.7c
2.7c
0f
0f
43.3b
17.0
3155
100.0 a
51.7 b
1.7 e
9.3 d
35.0 c
1.7 e
2.0 e
0f
0f
43.3b
10.7
3158
100.0a
46.7c
1.7e
8.0d
40.0c
3.0e
5.0d
0f
0f
55.0b
9.6
*
Data transformed in arcsen√x/100. **Means followed by same letter are not significantly different at P<0.05 probability using Scott-Knott's
test.
In vivo sensitivity of C. lindemuthianum isolates to
fungicides
Results of in vivo sensitivity of C. lindemuthianum
isolates to fungicides are described in Table 3, and were
very similar to those obtained from the in vitro
experiments. Pyraclostrobin and metiram + pyraclostrobin
were the most effective fungicides for the control of
anthracnose on green beans leaves, independent of the
C. lindemuthianum isolate evaluated, showing complete
absence of symptoms in the inoculated leaves.
The treatments with chlorothalonil, mancozeb and the
mixtures
mancozeb+
copper
oxychloride
and
chlorothalonil + thiophanate-methyl were also effective in
the reduction of anthracnose severity on green beans
leaves. However, the fungicides from the group of
benzimidazole (carbendazim and thiophanate-methyl)
and copper oxide did not controlled the disease on the
leaves, similar results to those obtained from in vitro
studies.
Determination of physiological
lindemuthianum isolates
races
of
C.
Isolates 3149, 3151, 3152, 3158, 3147, 3148, 3150 and
3157 of C. lindemuthianum were identified as race 65,
while isolates 3153, 3154, 3155 and 3135 were identified
as race 81 (Table 4).
DISCUSSION
The variation in colony growth sensitivity of
lindemuthianum isolates from common bean
C.
to
Filho et al.
2045
Table 4. Reaction of bean differential cultivars inoculated with C. lindemuthianum isolates from green beans from various locations of São Paulo State.
Differential cultivar
Michelite
Michigan Dark Red Kidney
Perry Marrow
Cornell 49-242
Widusa
Kaboon
México 222
Pi 207262
TO
TU
AB 136
G 2333
Race
Binary
value
1
2
4
8
16
32
64
128
256
512
1024
2048
3147
S
R
R
R
R
R
S
R
R
R
R
R
65
benzemidazole fungicides (benomyl, carbendazim
and thiophanate-methyl) has been reported in
several studies in Brazil with ED50 ranging from 1
to 1000 μg/mL (Maringoni and Barros, 2002;
Sartorato, 2007; Sartori and Maringoni, 2007). On
this study we detected an low sensitivity of colony
growth of C. lindemuthianum isolates from green
beans to benzimidazoles fungicides (carbendazim
and thiophanate-methyl) (Table 1). The low
sensitivity of conidial germination from C.
lindemuthianum isolates evaluated on this study
to carbendazim and thiophanate-methyl agrees
with Maringoni and Barros (2002), where isolates
from common beans were also resistant to these
fungicides.
C. lindemuthianum isolates from common beans
also exhibit variation in colony growth sensitivity to
chlorothalonil with ED50 ranging from 10 to 800
μg/mL (Rava et al., 1998; Maringoni and Barros,
2002), results similar to the obtained in this study
3148
S
R
R
R
R
R
S
R
R
R
R
R
65
3149
S
R
R
R
R
R
S
R
R
R
R
R
65
3150
S
R
R
R
R
R
S
R
R
R
R
R
65
3151
S
R
R
R
R
R
S
R
R
R
R
R
65
Isolate
3152
3153
S
S
R
R
R
R
R
R
R
R
R
R
S
S
R
R
R
R
R
R
R
R
R
R
65
81
for green beans isolates. Most isolates here
evaluated showed an ED50 from 100 to 1000
μg/mL for colony growth to chlorothalonil +
thiophanate-methyl, results discrepant to those
obtained by Balardin and Rodrigues (1995) and
Sartori and Maringoni (2007), who reported
inhibition of C. lindemuthianum isolates from
common beans to concentrations ranging from 10
to 100 μg/mL. Regarding conidial germination,
chlorothalonil was the most effective fungicide
(ED50 < 1 μg/mL), while thiophanate-methyl did
not show a satisfactory result (ED50 > 1000
μg/mL). These results show that the best
performance of the mixture chlorothalonil +
thiophanate methyl (ED50 from 10 to 100 μg/mL)
in comparison with thiophanate-methyl alone is
due to the chlorothalonil activity, showing the
absence of a synergistic action between these
fungicides.
C. lindemuthianum isolates evaluated in this
3154
S
R
R
R
R
R
S
R
R
R
R
R
81
3155
S
R
R
R
R
R
S
R
R
R
R
R
81
3156
S
R
R
R
R
R
S
R
R
R
R
R
81
3157
S
R
R
R
R
R
S
R
R
R
R
R
65
3158
S
R
R
R
R
R
S
R
R
R
R
R
65
study showed an ED50 for mancozeb and the
mixture mancozeb + copper oxychloride higher to
those described by Rava et al. (1998) for isolates
from common beans, indicating a lower sensitivity
of these isolates to these chemicals. No
information about the sensitivity of C.
lindemuthianum isolates to copper oxide was
found, although Tsai et al. (2006) evaluated
isolates of C. gloesporioides and C. musae from
fruit species and found and ED50 ranging from 10
to 100 μg/mL for cupric fungicides, values lower to
those found on this study.
ED50 values for the colony growth to
pyraclostrobin found on this study were lower to
those reported by Sartorato (2007) for C.
lindemuthianum isolates from common beans
(ED50 of 187.5 μg/mL) and close to the results
obtained by Sartori and Maringoni (2007) to
trifloxystrobin, a strobilurin from the same group of
pyraclostrobin. However, colony growth sensitivity
2046
Afr. J. Agric. Res.
of C. lindemuthianum isolates from green beans was
reduced for the mixture metiram + pyraclostrobin, which
most of the isolates had and ED50 ranging from 100 to
1000 μg/mL, concentration higher than that reported by
Tsai et al. (2006) for C. gloesporioides and C. musae
(ED50 from 10 to 100 μg/mL). There is no information
about conidial germination sensitivity from C.
lindemuthianum isolates to pyraclostrobin and metiram +
pyraclostrobin, however, there is information about other
fungi, such as Cylindrocladium candelabrum on
eucalyptus (Ferreira et al., 2006) and Cercospora sojina
on soybean (Zhang et al., 2012), demonstrating the
sensitivity of conidial germination of these fungi to
strobilurins.
Pyraclostrobin was also the most effective fungicide for
the control of anthracnose on green bean leaves, a result
that agrees with Conner et al. (2004) and Gillard et al.
(2012) for white and common beans, respectively. The
high sensitivity of isolates here evaluated to metiram +
pyraclostrobin may have occurred due probably to the
sensitivity showed by them to the pyraclostrobin. There
are no reports of C. lindemuthianum sensibility to
metiram and copper oxide.
The disease severity reduction found on this study for
the mixture chlorothalonil + thiophanate-methyl,
compared to thiophanate-methyl alone, demonstrates the
sensitivity of C. lindemuthianum isolates to chlorothalonil
and the low sensitivity to benzimidazole fungicides,
results also observed by Garcia et al. (2007) in common
beans.
According to Bashir et al. (1985), benomyl and
chlorothalonil were effective for the control of
anthracnose on mung bean; results similar to those
obtained in this study to chlorothalonil, but differed for
thiophanate-methyl, fungicide with mode of action similar
to benomyl. Castro et al. (1991) also reported the
efficiency of chlorothalonil for the control of anthracnose
in common beans.
The efficiency of mancozeb and mancozeb + copper
oxychloride observed on this study in reducing the
severity of anthracnose on green bean leaves also
agrees with Castro et al. (1991), who reported a disease
severity reduction in common beans treated with these
chemicals. The authors also demonstrated the
effectiveness of carbendazim in controlling the
anthracnose in common beans, result not observed on
this study with green bean isolates.
Studies with C. lindemuthianum isolates from common
beans also identified the prevalence of races 65 and 81
in Brazil (Somavilla and Prestes, 1999; Carbonell et al.,
1999; Thomazella et al., 2002). Until now there was no
information about the races of C. lindemuthianum that
occur on green beans demonstrating that genotypes with
resistance to races 65 and 81 of C. lindemuthianum
should be used in genetic breeding programs of green
beans, aiming the incorporation of resistance genes to
anthracnose in susceptible cultivars.
Conflict of Interest
The authors have not declared any conflict of interest.
ACKNOWLEDGEMENTS
The authors thank the Coordination of Improvement of
Higher Education Personnel (CAPES, Brazil) for the
granting of the scholarship to the first author.
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