Article
DOI: http://dx.doi.org 10.1590/0100-29452018202
Sources of resistance to
Fusarium oxysporum f. sp. cubense
in banana germplasm
Lindinéia Rios Ribeiro1, Sebastião de Oliveira e Silva2,
Saulo Alves Santos de Oliveira3, Edson Perito Amorim4,
Janay Almeida Santos Serejo5, Fernando Haddad6
Abstract – Fusarium wilt (syn= Panama disease), caused by Fusarium oxysporum f. sp. cubense
(FOC), is one of the most destructive diseases of banana, being genetic resistance the main
management strategy for this disease. Since the pathogen is constantly evolving to supplant
the genetic resistance, new sources of resistance must be investigated by genetic improvement
programs aiming to developing new varieties. The objective of the present study was to identify
sources of resistance from the different accessions maintained in the banana active germplasm
bank (BAGB) at Embrapa Mandioca e Fruticultura. Forty-one BAGB accessions were evaluated,
including 17 diploids, 21 triploids, and two tetraploids. The area under the disease progress curve,
disease index, and incubation period were also evaluated. In relation to FOC resistance, there is
genetic variability available among the BAGB accessions. The genotype M53 is notable for the
complete resistance it expressed, and the accessions Birmanie, PA Songkla, Pirua, Imperial, Poyo,
Ambei, Walebo, and Kongo FRF 1286 expressed quantitative resistance.
Index terms: Musa spp., Panama disease, varieties, genetic resistance.
Fontes de resistência a
Fusarium oxysporum f. sp. in banana germosplasma
Resumo – O murcha de Fusarium, causado por Fusarium oxysporum f. sp. cubense (FOC), é uma
Corresponding author:
E-mail: alexandreserquiz@gmail.com
Received: October 07, 2016.
Accepted: April 24, 2017.
Copyright: All the contents of this
journal, except where otherwise
noted, is licensed under a Creative
Commons Attribution License.
das principais doenças da cultura da bananeira. A principal estratégia de controle da doença faz-se
com o uso de variedades resistentes, sendo que, para a sua obtenção, faz-se necessário identificar
genótipos para utilização nos programas de melhoramento genético da cultura. O objetivo do
presente estudo foi identificar fontes de resistência em acessos do Banco Ativo de Germoplasma
(BAG) de Bananeira da Embrapa Mandioca e Fruticultura. Foram avaliados 41 acessos do BAG,
sendo 17 diploides, 21 triploides e dois tetraploides. Também foram avaliados a área abaixo da
curva do progresso da doença, o índice interno da doença e o período de incubação. Há variabilidade
genética disponível entre os acessos do Banco de Germoplasma de Bananeira para resistência ao
FOC, com destaque à imunidade expressada pelo genótipo M53. Os acessos Birmanie, PA Songkla,
Pirua, Imperial, Poyo, Ambei, Walebo e Kongo FRF 1286 expressaram resistência.
Termos para indexação: Musa spp., mal do Panamá, variedades, resistência genética.
1
Agronomist, M.Sc., D.Sc. student in Plant Production, Universidade Federal do Recôncavo da Bahia, Cruz das Almas – BA, E-mail: neiarios@hotmail.com
Agronomist, D.Sc. Professor of Universidade Federal do Recôncavo da Bahia, Cruz das Almas - BA. E-mail: ssilva3000@gmail.com
3
Agronomist, D.Sc., Researcher at Embrapa Mandioca e Fruticultura, Cruz das Almas –BA. E-mail: saulo.oliveira@embrapa.br
4
Agronomist, D.Sc., CNPq Research Productivity Scholarship, Researcher at Embrapa Mandioca e Fruticultura, Cruz das Almas – BA. E-mail: edson.amorim@
embrapa.br
5
Agronomist, D.Sc., Researcher at Embrapa Mandioca e Fruticultura, Cruz das Almas – BA. E-mail: janay.almeida@embrapa.br
6
Agronomist, D.Sc., Researcher at Embrapa Mandioca e Fruticultura, Cruz das Almas –BA.E-mail: fernando.haddad@embrapa.br
2
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L. R. Ribeiro et al.
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Introduction
Banana farming has high potential for generating
jobs and income, and Brazil is one of the five largest
producers of bananas in the world (FAOSTAT, 2016).
However, the most commonly grown varieties in Brazil are
affected by Fusarium wilt, but fortunately this disease can
be efficiently controlled using resistant varieties (SILVA
et al., 2016; PLOETZ, 2015).
Fusarium wilt is caused by Fusarium oxysporum
f. sp. cubense (FOC), which is a fungus that inhabits the
soil. The pathogen has high evolutionary potential, with
23 known vegetative compatibility groups (VCGs), three
physiological races (races 1, 2 and 4) that infect banana
species, and a fourth race that only infects Heliconia plants
(FOURIE et al., 2011; PLOETZ, 2015).
Race 1 affects the cultivars Gros Michel, Musa
textilis (abacá), ‘Gros Michel’ (AAB), ‘Silk’ or ‘Maçã’
(AAB), ‘Pomme’ or ‘Prata’ (AAB), ‘Pisang Awak’ (ABB),
and ‘IC2’ (improved AAAA hybrid).Race 2 affects
‘Bluggoe’ (ABB) and improved AAAA hybrids, and has
already been found in seedlings of Musa balbisiana (BB)
and ‘Gros Michel’ (AAB). Race 4 affects various cultivars,
including all of subgroup Cavendish (FOURIE et al, 2011;
PLOETZ, 2015). The strains of this race are divided into
Tropical (TR4) and Subtropical (ST4) (PLOETZ, 2006;
BUTLER, 2013). FOC races 1 and 2 are distributed
throughout almost all of Brazil, but TR4 is still not present
in the country. However, if it was accidently introduced
it could affect all the cultivars resistant to races 1 and 2
(DITA et al., 2013).
The banana active germplasm bank (BAGB) from
Embrapa comprises 323 accessions with a wide variety
of characteristics of agronomic importance, and includes
valuable sources of resistance to the main banana diseases.
For this germplasm to meet the demands of banana genetic
improvement programs, collection, characterization, and
maintenance activities are indispensable to preserve and
increase the existing genetic variability.
The first step to develop new improved varieties
is through is the identification of sources of resistance
(SILVA et al., 2016). Testing the resistance of genotypes
can be done in an experimental field previously infested
with FOC isolates. In this case, the evaluation process
is long, lasting, on average, two years. However, tests
conducted in a greenhouse reduce the evaluation time
up to three months (RIBEIRO et al., 2015) and allow
the use of different isolates. The objective of the present
work was to identify banana accessions with resistance
to Fusarium oxysporum f. sp. cubense race 1 to use to
genetically improve the crop.
Rev. Bras. Frutic., Jaboticabal, 2018, v. 40, n. 1: (e-202)
Material and Methods
Two experiments were performed in a greenhouse
conditions at Embrapa Mandioca e Fruticultura in Cruz das
Almas, Bahia, with 41 banana accessions including wild
genotypes, improved diploids, triploids, and commercial
tetraploids (Table 1). The plants were micropropagated
using the in vitro culture technique followed by
acclimatization for 90 days in a greenhouse.
The pathogenicity tests were conducted for the
FOC isolate ‘CPMF0801’ (race 1), and the inoculum
produced in a sand:cornmeal (SC) mixture (5:1), with
an additional 150 mL of distilled sterilized water. The
mixture was placed in plastic bags and autoclaved at
120 °C for two hours, two times, with an interval of 24
hours between each sterilization procedures. Disc of PDA
(potato dextrose agar) containing the FOC growth were
transferred to the SC substrate, after cooled, and the plastic
bags were maintained in a growth chamber at 25 ± 3 °C
for 15 days. To quantify the concentration of inoculum,
serial dilutions were used, with an adjustment to 106
colony-forming units of FOC.g-1 of substrate.
For the first trial the following genotypes were
evaluated: S.A; Mambee Thu; Pisang Rojo Uter; Pisang
Pipit; Poyo; Birmanie; Pirua; Imperial; PA Songkla;
Walebo; Pisang Nangkla; Pisang Jaran; Pisang Berlin;
2803-01; Tjau Lagada; Mangana; Ambei and Gros Michel.
In the second trial the genotypes evaluated were:
Grande Naine; P. Formoso; Malaccensis; Pisang Tongat;
Figo Cinza; M61; Nanicão Magário; FRP 1292; Tuugia;
Buitenzorg; Platina; Nanica; M53; Kongo; FRF 1286;
PV03-76; Pacovan; Pisang Ustrali; Fako Fako; Figue Rose
Naine; Prata-Anã 2; Robusta; Musa Ornata x Velutina;
Prata Maceió; Prata-Anã and Markatooa.
The plants were inoculated by adding ten grams of
the SC substrate containing the inoculum in four holes in
the soil around the seedlings. As control (mock), the same
accessions listed previously wereplanted in pots with noninfested soil. Eight repetitions per genotype were used, in
a completely randomized design.
The incubation period (IP) was considered as the
amount of time between inoculation and the appearance of
symptoms in at least 50% of the plants. The severity of the
disease was evaluated through the external appearance of
symptoms, assessed every three days up to 85 days after
inoculation, and was based on the following rate scale
(MOHAMMED, 1999):
0: no symptoms;
1: initial yellowing of old leaves;
2: yellowing of old leaves and initial discoloration
of young leaves:
3: intense yellowing of all leaves;
4: dead plant.
Sources of resistance to Fusarium oxysporum f. sp. cubense...
3
Table 1- Description of the banana genotypes used in the genetic resistance test to Fusarium oxysporum f. sp. cubense
race 1 in a greenhouse. Embrapa, 2017.
Genotype
Genome
Classification
2803-01
AA
Resistant
Ambei
AA
Resistant
Birmanie
AA
Resistant
Buitenzorg
AA
Resistant
Fako Fako
AA
Susceptible
Figo Cinza
ABB
Resistant
Figue Rose Naine
AAB
Resistant
Grande Naine P. Formoso
AAA
Resistant
Gros Michel
AAA
Susceptible
Imperial
AAA
Resistant
Kongo FRF 1286
AAA
Resistant
M53
AA
Resistant
M-61
AAA
Resistant
Malaccensis
AA
Resistant
Mambee Thu
AA
Resistant
Mangana
AA
Resistant
Markatooa
AAA
Resistant
ES
Susceptible
Musa ornata x Musa velutina
Nanica
AAA
Resistant
Nanicão Magario FRF 1292
AAA
Resistant
PA Songkla
AA
Resistant
Pacovan
AAB
Resistant
Pirua
AAA
Resistant
Pisang Berlin
AA
Resistant
Pisang Jaran
AA
Resistant
Pisang Nangka
AAB
Resistant
Pisang Pipit
AAA
Resistant
Pisang Rojo Uter
AA
Resistant
Pisang Tongat
AA
Resistant
Pisang Ustrali
AAB
Resistant
Platina
AAAB
Resistant
Poyo
AAA
Resistant
Prata-Anã
AAB
Susceptible
Prata-Anã 2
AAB
Susceptible
Prata Maceió
AAB
Susceptible
PV03-79
AAAB
Resistant
Robusta
AAA
Resistant
S.A
AA
Susceptible
Tjau Lagada
AA
Resistant
Tuugia
AA
Resistant
Walebo
AAA
Resistant
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L. R. Ribeiro et al.
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Eighty-five days after inoculation, the plants were
removed from the substrate and the discoloration of the
rhizome was evaluated based on the rate scale described
by Cordeiro et. al. (1993):
0: no symptoms
1: isolated areas of infection;
2: discoloration in up to 1/3 of the ring formed by
the origin region of the roots;
3: discoloration in 1/3 to 2/3 of the ring;
4: discoloration in over 2/3 of the ring;
5: discoloration throughout rhizome.
Based on these notes disease indices (DI) were
calculated for external (EDI) and internal (IDI) symptoms
using the formula proposed by McKinney (1923): ID (%)
= 100.∑[(f.v)/(n.x)]; where DI is the disease index; f is
the number of plants with the same note; v is the observed
note; n is the number of plants evaluated; and x is the
maximum note from the scale.
In addition, the area under the disease progress
curve (AUDPC) was calculated, as proposed by Madden
et al. (2007):
where:
yi is the severity of the disease (based on the DI)
in the observed i;
yi+1 is the severity of the disease at the time of the
subsequent evaluation i + 1;
ti is the time (days) at the time of observation i;
ti+1 is time (days) at the time of the subsequent
evaluation i + 1;
n is total number of evaluations.
All statistical analyses were conducted using the
software R (RCORE TEAM R, 2014). The k-means
and PCA analyses wereused to group the treatments and
the Pearson correlation test was used to measure the
correlation between the variables.
Results and Discussion
The BAGB accessions evaluated in the two
experiments, were grouped in two categories regarding
the genetic resistance: susceptible (S)and resistant(R). For
the first trial five genotypes were classified as susceptible
(S) and 17 as resistant to the Fusarium wilt (Figure 1). For
the second trial a total do 15 genotypes were considered
as ‘R’ and only three as ‘S’ (Figure 2).
Although classified as resistant, the internal disease
index (IDI) values of the resistant accessions varied from
0.0 for the genotype M53 to 56.7%. The diploid 280301 had an IDI value of, the highest among the resistant
accessions, and a long incubation period (64 days).
Positive correlations were observed between
variables (Figure 3) in different experiments. For the
first trial, positive correlations were noticed between
the AUDPC and number of dead plants (0.86, P<0.001);
Rev. Bras. Frutic., Jaboticabal, 2018, v. 40, n. 1: (e-202)
AUDPC and IDI (0.84, P<0.01); and also between IDI
and number of dead plants (0.88, P<0.001). No significant
correlation was found between the other variables (Figure
3A).
In the second experiment, there were positive
correlations for the same variables described for the
first trial, with positive correlation between AUDPC and
number of dead plants (0.77, P<0.01); between IDI and
number of dead plants (0.56, P<0.05), and positive but no
significant correlation between AUDPC and IDI (0.43, ns).
No significant correlation was found between the other
variables (Figure 3B).
Although the intensity of Fusarium wilt is diagnosed
visually by analyzing external and internal symptoms,
often these values are not directly proportional. A plant
can exhibit external characteristics, such as yellowing
caused by nutritional deficiency and excess water, but
internally not exhibit discoloration in the rhizome. Thus,
the most precise evaluation of the disease depends on the
internal symptoms. The disease symptoms are expressed
primarily in the roots; however, this depends on the genetic
background of the plant.
Although in the same group, the resistant accessions
(Group 2) had well differentiated AUDPC and IDI values.
Most were wild diploids, evaluated as individuals with
good agronomic characteristics (e.g., productivity, plant
size, bunch size, flavor and appearance of the fruit,
tolerance to certain pests and diseases, and adaptability
to certain climate conditions), which is important to
genetic improvement programs (CORDEIRO et al., 1993;
AMORIM et al., 2008; SILVA et al., 2013).
The accessions ‘Birmanie’, ‘Pirua’, ‘Poyo’,
‘Walebo’, ‘Imperial’, ‘PA Songla’ and ‘Pisang Nangka’
had low internal disease indices and could be used as
parents in crosses. A study conducted by Rebouças et al.
(2015), which used microsatellite markers and evaluated
the severity of the disease under greenhouse and field
conditions, also observed that the accessions Birmanie
and Pisang Jaran are resistant to the disease. The accession
‘Tjau Lagada’, classified in the resistant group, was also
found to be resistant in fieldwork conducted by Cordeiro
et al. (1993). Thus, the methodology of early detection
of Fusarium wilt developed by Ribeiro et al. (2011) is
efficient at evaluating FOC.
The genotypes ‘Gros Michel’ (AA), ‘Mambee Thu’
(AAA) and ‘S.A’ (AA) exhibited the highest severity of
the disease due to their high susceptibility to FOC. These
accessions had high internal disease indices (96.7, 86.7
and 83.3%, respectively) and short incubation periods
(23 days for the first accession and 21 for the second and
third). In addition, they had a high number of dead plants,
with values of 62.5% for ‘Gros Michel’ and 50% for ‘S.A’
and ‘Mambee Thu’. Although these accessions have only
the AA genome, it was not possible to observe a relation
between the genome and susceptibility to FOC.
In the second experiment, accessions were also
classified as susceptible (‘Prata Maceió’, ‘Fako Fako’,
Sources of resistance to Fusarium oxysporum f. sp. cubense...
5
‘Prata-Anã 2’, ‘Musa ornata x velutina’ and ‘Prata-Anã’)
and resistant (‘Grande Naine P. Formoso’, ‘Malaccensis’,
‘Pisang Tongat’, ‘Figo Cinza’, ‘M61’, Nanicão Magário
FRF 1292’, ‘Buitenzorg’, ‘Tuugia’, ‘Platina’, ‘Nanica’,
‘PV03-76’, ‘Pacovan’, ‘Pisang Ustrali’, ‘M53’, ‘Kongo
FRF 1286’, ‘Markatooa’ and ‘Robusta’) (Figure 2).
The diploid M53 was notable for not exhibiting
symptoms of Fusarium wilt. This hybrid has been used as
a parent in crosses to generate some cultivars (e.g., BRS
Platina, BRS Princesa, BRS Preciosa and BRS Pacovan
Ken) that are widely used in the internal market because
they have good characteristics. This result corroborates
the work developed by Cordeiro et al. (1993), to analyze
BAGB banana diploids in the field.
The ‘Malaccensis’ accession is in the resistant
group and exhibited a long incubation period (62 days)
and no plant death. Subspecies Malaccencis belongs to the
species Musa acuminata, is highly resistant to races 1 and
2 and tropical and subtropical race 4, and demonstrates
quantitative or polygenic resistance (LI et al., 2015).
The cv. Malaccensis, Grande Naine P. Formoso and
Pisang Tongat had the same incubation period value (62
days) and exhibited no symptoms of the disease. It was
observed that shorter incubation periods were related to
the lowest AUDPC values.
The cv. BRS Platina was classified in the group
of individuals resistant of FOC race 1. This cultivar
is a tetraploid hybrid (AAAB) from a cross between
the triploid Prata-Anã, which is susceptible and has
an AAB genetic constitution, and the diploid M53,
which is resistant and has an AA genetic constitution.
This genotype was developed by Embrapa Mandioca e
Fruticultura (SILVA et al., 2016) and has good production
characteristics, such as good tillering and a medium size,
and sensory characteristics similar to the cultivar PrataAnã (SILVA et al., 2016).
Among the resistant triploids, the accessions
‘Nanicão Mangário FRF 1292’, ‘Grande Naine P.
Formoso’ and ‘Marakatooa’ had low IDI indices and long
incubation periods. This study demonstrated the existence
of genetic variability in relation to FOC race 1 resistance
in the BAG of banana plants at Embrapa Mandioca e
Fruticultura.
Figure 1. Principal component analysis of Experiment 1, based on the internal disease index (IDI), area under the
disease progress curve (AUDPC), number of dead plants (DP) and incubation period (IP). Embrapa, 2017.
Rev. Bras. Frutic., Jaboticabal, 2018, v. 40, n. 1: (e-202)
6
L. R. Ribeiro et al.
Figure 2. Principal component analysis of Experiment 2, based on the internal disease index (IDI), area under the
disease progress curve (AUDPC), number of dead plants (DP) and incubation period (IP). Embrapa, 2017.
Figure 3. Correlogram displays for the evaluated parameters: internal disease index (IDI), area under the disease
progress curve (AUDPC), number of dead plants (DP) and incubation period (IP). Above diagonal depicts pie chart
for the Pearson’s correlation coefficient.Shades of blue indicating positive correlations and shades of red indicating
negative correlations. Dark blue corresponds to significant values at P<0.01, medium blue corresponds to a significance
of P<0.05, light blue and pink corresponds to no significant positive and negative correlation, respectively. Embrapa,
2017.
Rev. Bras. Frutic., Jaboticabal, 2018, v. 40, n. 1: (e-202)
Sources of resistance to Fusarium oxysporum f. sp. cubense...
7
Conclusion
There is genetic variability available among the
BAGB accessions in relation to FOC CNPMF0801 race
1 resistance. Notable plants were the genotype M53 for
not exhibiting symptoms of Fusarium wilt, the accessions
‘Birmanie’, ‘PA Songkla’, ‘Pirua’, ‘Imperial’, ‘Poyo’,
‘Ambei’, ‘Walebo’ e ‘Kongo FRF 1286’ that were resistant
because they had low disease index values, and the
accessions Birmanie’, ‘Pisang Nangkla’, ‘Pisang Jaran’,
‘Pisang Berlin’, ‘Tjau Lagada’, ‘Mangana’, ‘Pisang Pipit’,
‘Pisang Rojo Uter’ and the selection 2803-1 that had low
values for all of the variables.
For the second experiment, the accessions ‘Grande
Naine P. Formoso’, ‘Malaccensis’, ‘Pisang Tongat’,
‘Figo Cinza’, ‘M61’, ‘Nanicão Magário FRF 1292’,
‘Buitenzorg’, ‘Tuugia’, ‘Platina’, ‘Nanica’, ‘PV0376’, ‘Pacovan’, ‘Pisang’Ustrali’, ‘Kongo FRF 1286’,
‘Markatooa’ and ‘Robusta’ were notable.
Acknowledgements
The authors would like to thank CAPES for the
Doctor´s fellowship awarded to the first author and CNPq
and Bill e Melinda Gates Foundation for the financial
support of the project.
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