Performance of banana genotypes with resistance to black leaf streak disease in Northeastern Brazil

The objective of this work was to evaluate the growth and the production of banana plants with resistance to black leaf streak disease (BLSD), in comparison with the performance of traditional cultivars susceptible to the disease. Twenty cultivars were planted at the Jaguaribe-Apodi plateau, in Northeastern Brazil: 15 with resistance to BLSD, namely Pacovan Ken, PV42-68, BRS Vitória, BRS Japira, BRS Preciosa, BRS Garantida, Thap Maeo, BRS Tropical, BRS Platina, BRS Maravilha, FHIA 02, FHIA 18, Galil 18, Caipira, and Buccaneer; and five susceptible to the disease, namely Williams, Grande Naine, Pacovan, Prata Anã, and Maçã. Banana growth and production of bunches were evaluated during three successive cycles. 'BRS Tropical' and 'Caipira' can replace 'Maçã', which is very susceptible to Fusarium wilt. The BRS Maravilha, BRS Platina, FHIA 02, FHIA 18, and Galil 18 cultivars show adequate height and high yield potential, being alternatives to the traditional Prata subgroup. The Buccaneer cultivar is an alternative to the susceptible cultivars of the Cavendish subgroup and can be explored in an irrigated agrosystem.


Introduction
Banana (Musa spp.) plants are widely cultivated in tropical regions, and developing countries account for over a third of global banana production (FAO, 2016), generating opportunities and income for producers and other agents in the fresh fruit value chain.In Brazil, the banana crop is spread throughout all regions, with an annual harvest of 7 million tons.The Northeast of the country represents nearly 40% of the planted area and 35% of the national production (IBGE, 2015).However, despite the high production levels in this particular region, fruit yield is still low (<13 Mg ha -1 ), which is associated with the productivity potential of traditional cultivars, such as Prata (Donato et al., 2009), compared with other types of banana.
The banana cultivars traditionally planted in Brazil are susceptible to Panama disease and Sigatoka leaf spot disease (Silva et al., 2015).In addition, inadequate cultivation practices are often adopted, in particular Pesq.agropec.bras., Brasília, v.52, n.3, p.161-169, mar.2017 DOI: 10.1590/S0100-204X2017000300003 planting under rainfed conditions in semiarid regions.In irrigated areas, for example, the Prata cultivar can produce fruit yields of up to 40 Mg ha -1 (Donato et al., 2009), which can easily be exceeded by the cultivars of the Cavendish subgroup, mainly destined for the export market, such as Grande Naine.This cultivar produced 70 to 75 Mg ha -1 per year under irrigation and a dense spacing of 2,000 to 4,000 plants per hectare (Flori et al., 2004).It should be noted, however, that consumers in Northeastern Brazil show a preference for 'Prata', 'Maçã' (Matsuura et al., 2004), and 'Pacovan' (Garruti et al., 2012) bananas.
Several different diseases infect banana plants, but, of all fungal infections, black leaf streak disease (BLSD), also known as black Sigatoka, is considered to be the worst, due to its widespread occurrence in many countries, its severe negative impact on banana production (Robert et al., 2012), and its effects on cultivars belonging to different genomic groups (Churchill, 2011).In Brazil, BLSD causes significant losses in the humid areas of the Amazon (Gasparotto et al., 2006), affecting bananas of the 'Prata' and 'Cavendish' subgroups (Silva et al., 2014).The disease spreads through the spores of the fungus Mycosphaerella fijiensis (Silva et al., 2014), which could happen during the transport of banana plant material that could contain the pathogen propagules, causing concern in the banana agribusiness.As a result, strategies for the genetic improvement and the development of cultivars resistant to BLSD are being sought in Brazil (Silva et al., 2013).
No occurrences of BLSD have been reported in Northeastern Brazil to date.However, this can be a matter of time, since, during certain times of the year, the climatic conditions of some banana-producing areas are favorable to the development of the disease, with air temperatures of approximately 27ºC and high relative humidity of around 80% (Ghini et al., 2007;Jesus Júnior et al., 2008).Because of this, some researches on genotypes resistant to BLSD (Silva et al., 2015) and on cultivars tested in semiarid conditions (Lédo et al., 2008;Azevedo et al., 2010) are already being carried out.However, the plant size and the productive capacity of cultivars resistant to BLSD may not be suitable for growing in open coastal areas.
The objective of this work was to evaluate the growth and the production of banana plants with resistance to BLSD, in comparison with the performance of traditional cultivars susceptible to the disease.
The preparation of the area consisted of soil plowing, harrowing, and furrowing (0.4-m depth and 2 or 4 m apart).Bovine manure (12 L per plant) was placed in the furrows, along with 300 g per plant of monoammonium phosphate, 200 kg ha -1 P 2 O 5 , and 100 kg ha -1 N.These fertilizer dosages are commonly used for planting banana seedlings in the irrigation district of Jaguaribe-Apodi.After the furrows were closed and the soil incubated for a month, hose pipes and Gyronet micro-sprinklers (Netafim Brasil, Ribeirão Preto, SP, Brazil) were installed, with a flow rate of 40 L per hour and a wetting diameter of 4 m.On sunny days, up to 53 L of water per plant per day were used throughout the experimental period.
Micropropagated seedlings were planted (Table 1), which were initially acclimatized in 1-L capacity plastic bags, containing a mixture of vermicompost, soil, and washed sand (in a 1:6:3 ratio by volume), under a black shade cloth to reduce luminosity from sunlight in 25%.The substrate, according to the analytical methods of Silva (2009), showed: pH (H 2 O) 7.3 (ratio of 1:2.5); 43.8 mg kg -1 P, 7.5 mmol c kg -1 K, Pesq.agropec.bras., Brasília, v.52, n.3, p.161-169, mar. 2017 DOI: 10.1590/S0100-204X2017000300003 2.1 mmol c kg -1 Na, 0.4 mmol c kg -1 Cu, 29.7 mg kg -1 Fe, 43.1 mg kg -1 Mn, and 2.1 mg kg -1 Zn extracted with Mehlich-1; and 49.6 mmol c kg -1 Ca and 18.9 mmol c kg -1 Mg extracted with 1 mol L -1 KCl.In April 2008, when planting was performed in the field, the seedlings with root clods had more than 30 cm of shoot height.For the distribution of the seedlings of the 20 evaluated cultivars, a randomized complete block design was used, with three replicates with 20 plants.The spacing between planting rows was 2 and 4 m, and between plants in the row was 2.5 m.Seedlings of the Prata Catarina cultivar were planted in the external borders.Thirty days after planting, ferti-irrigation of the banana plants began.Every three days, on average, low doses of urea (45% N), potassium sulphate (18% S and 50% K 2 O), and potassium chloride (60% K 2 O) were provided, totaling almost 270 kg ha -1 N, 21 kg ha -1 S, and 233 kg ha -1 K 2 O in the first year.The management of the fertilizers and of the cultivation practices was carried out in alignment with the recommendations of Borges et al. (2009).
When bunches first appeared, the height and diameter of the pseudostem were measured at about 30 cm from the base, and the number of green leaves on 12 central plants per plot were counted.Data collection was programmed according to the appearance of bunches.For this, bunches were cut, the hands and fingers were separated, and their fresh weight was determined in order to calculate the production of bunches without stalks.In addition, in order to calculate the production cycles, the period of time between the planting of seedlings in the field and the harvest of bunches was noted.
Banana growth and production data were analyzed in a randomized complete block design, in a split-plot arrangement.The plots were considered the banana

Results and Discussion
A vigorous aerial growth and a satisfactory production of bunches were observed for 19 of the evaluated cultivars (Tables 2 and 3).The exception was 'Maçã', for which only a few small bunches were obtained due to the incidence of Fusarium wilt caused by the fungus Fusarium oxysporum f. sp.cubense (Foc).This result was expected in the areas that had been occupied five years before by banana plants of the Maçã cultivar.Although the BRS Platina, BRS Tropical, BRS Garantida, and Grande Naine cultivars were planted in neighbor plots to Maçã, no symptoms of the disease were detected, confirming the resistance of those plants to Foc, possibly race one.The cultivars Grande Naine and Williams from the Cavendish subgroup are susceptible to Foc, race TR4 (Ploetz, 2015), for which there are no known reports in the area, still considered under risk.Among the genotypes tested, 'BRS Tropical', 'Thap Maeo', and 'Caipira', also resistant to Fusarium wilt, produce small fruits and can be considered as a type of 'Maçã' banana (Carvalho et al., 2011).
In relation to yellow Sigatoka (YS), no control measures were adopted in the experimental area.Although the disease has been controlled in the surrounding banana plantations, this did not prevent the emergence of mild symptoms of YS on older leaves of the Pacovan, Prata Anã, William, and Grande Naine cultivars.The tested materials did not exhibit symptoms of BSLD, however.It should be pointed out that the local climatic conditions are favorable to the emergence of BLSD, according to Guini et al. (2007) and Jesus Júnior et al. (2008), with milder temperatures from 25 to 27°C during April and May (rainy season) and a high relative humidity of >75%.Besides, the Jaguaribe-Apodi plateau, where the experiment was carried out, is not very far (just over 1,000 km) from the productive areas of the Amazon region, where BLSD appears to be endemic.
Data on the growth and production of all studied cultivars, except Maçã, were subjected to Anova, and an interaction between cultivars and cycles was observed (p<0.05)(Tables 2 and 3).Cultivars with different genealogy (Table 1) are expected to show a different performance even when uniform-sized plantlets are planted in the field.The Pacovan Ken, PV42-68, BRS Victoria, BRS Japira, BRS Preciosa, and BRS Garantida cultivars grew to be tall, measuring 5.8 m from the base to the insertion of the bunch, especially in the third cycle, together with the traditional cultivar Pacovan (Table 2); therefore, they are not recommended for crops grown in plateaus without windbreak protection.The Thap Maeo cultivar was also considered unsuitable, showing average height ranging from 3.5 m, in first cycle, to 5.1 m, in the third cycle, besides a thin pseudostem in the early cycles of bunch production.This banana plant cultivar is also subject to pseudostem drop at the bunch insertion point.It should be highlighted that, during the experiment, winds reached 9.17 m s -1 in February 2009 and 9.26 m s -1 in January 2010.Winds rated as force 4 (5.5 to 7.9 m s -1 ) according to Beaufort's scale can already cause minor damage to leaves, but, in the Jaguaribe-Apodi plateau, winds reaching force 6 (10.8 to 13.8 m s -1 ) occasionally occur.
Regarding the size of the banana plant, the following cultivars were selected: BRS Tropical, derived from Yangambi 02; BRS Platina and BRS Maravilha, both derived from Prata Anã; the FHIA cultivars, i.e., FHIA 02, FHIA 18, Galil 18, or false FHIA 18; and Buccaneer and Caipira, whose pseudostems did not exceed 4.3 m in height (Table 2).A lower plant height was accompanied by a greater pseudostem diameter, except for the Caipira cultivar, during the second and third production cycles.The green leaves varied between banana cultivars and cycles, but overall they were satisfactory when bunches first appeared.In general, shorter cultivars have a wider pseudostem that better supports the bunches, which is desirable for banana plantations on irrigated plateau areas, together with a large number of leaves that enable a greater banana production (Nomura et al., 2013).
The production of banana hands and fruits was affected by the interaction of cultivars and cycles (Table 2).'BRS Garantida', 'BRS Tropical', and 'Caipira' produced fewer hands during the first cycle, similarly to 'Prata Anã'.In turn, the Thap Maeo cultivar showed the greatest potential to produce hands and fruits in the bunch during the second and third cycles, 13 and 19 months after the seedlings were planted, respectively.The last period covers the three production cycles, for which the BRS Tropical, BRS Maravilha, FHIA 02, FHIA 18, Galil 18, Caipira, and Prata Anã cultivars showed similar results.Unlike the second and third cycles, which were in part affected by thinning and scheduled harvest, the first cycle has been used as an indicator of precocity for banana production.The harvest time of the first banana bunches was quite short (>9 months) for the BRS Maravilha, FHIA 02, FHIA 18, and Buccaneer cultivars (Table 3).However, this precocity was also a notable feature in 'BRS Preciosa' and 'BRS Garantida', both tall, and in 'Thap Maeo'.Longer production cycles have been reported for banana cultivars under irrigation in other Table 2. Plant height from the ground up to the point of emission of the bunch (BPH), diameter of the base of the pseudostem (PD), number of green leaves at the flowering stage (GLN), and number of hands (HN) and of fruits in the bunch (FN) of banana (Musa spp.) cultivars planted at the Frutacor farm, in the municipality of Limoeiro do Norte, in the state of Ceará, Brazil (1) .Values followed by equal letters, lowercase in the columns and uppercase in the lines for each parameter, do not differ significantly by the Scott-Knott test, at 5% probability.
The fresh weights of fruits, hands, and bunches were also affected by the interaction between cultivars and cycles (Table 3).For bananas, a smaller size and lower weight are desirable, which were observed for the Thap Maeo, BRS Tropical, and Caipira cultivars, especially in the first two cycles.The shape of the fruits of the resistant cultivars is similar to that of the Maçã and Prata Anã bananas, which are preferred in the domestic consumer market (Matsuura et al., 2004).During the first cycle, large and heavy bunches were obtained with the BRS Platina, BRS Maravilha, FHIA 02, FHIA 18, Galil 18, and Buccaneer cultivars, which also showed good yield potential in the other cycles, and with banana plants derived from Pacovan, which were not recommended because of their height.
The choice of the most adequate cultivar by farmers naturally depends on their production goals and targets.However, considering the planting density used of 1,333 plants per hectare, a high production of bananas may be expected, ranging from 39.3 Mg ha - 1 , for the BRS Maravilha cultivar (first crop cycle), to 50.2 Mg ha -1 , for FHIA 02 (second cycle).Regarding high productive potential, the Buccaneer cultivar should also be considered, since it produced up to 41 Mg ha -1 in the first cycle and 47.5 Mg ha -1 in the third one, being an alternative to the Williams and Grande Naine cultivars, which are sensitive to BLSD and produce bananas with a similar shape (Lédo et al., 2008).Despite this, in the regional consumer market, there is still uncertainty on the intention of buying 'Buccanero' banana (Garruti et al., 2013), showing that it could be tested in new products and markets.
The cluster analysis according to the AHC enabled the formation of four major clusters with the assessed bananas (Figure 1).The first cluster consisted of only one cultivar, Thap Maeo, from the Mysore subgroup.The second cluster was formed by the Caipira and BRS Tropical cultivars from the Ibota and Prata subgroups, respectively, and by Prata Anã.The third cluster was the largest, with the following cultivars: Williams and Grande Naine, both from the Cavendish Table 3. Period from planting to harvest, as well as fresh weight of hands (HW), of fruits (FW), and of bunches without stalks (BW) of the banana (Musa spp.) cultivars planted at the Frutacor farm, in the municipality of Limoeiro do Norte, in the state of Ceará, Brazil (1) .subgroup; Buccaneer, from the Gros Michel subgroup; FHIA 02, FHIA 18, and Galil 18; and BRS Maravilha and BRS Platina.The fourth cluster consisted of the Pacovan cultivar and of its hybrids BRS Preciosa, BRS Vitória, PV42-68, BRS Japira, Pacovan Ken, as well as of BRS Garantida, a hybrid derived from Prata São Tomé.The formation of clusters was not an exact match to the genomic groups of banana plants.The major groups were identified mainly with tetraploid materials, whereas the small groups were formed by triploid materials (Table 1).The latter genomic group possibly shows a greater divergence regarding plant growth and production of bunches that could be further explored in future works on breeding for new resistant hybrids with desirable traits for the banana crop.PCA was also performed using the same matrix of multivariate data (Figure 2), which consisted of the means of the three production cycles of each variable.The first two components explained 70.9% of the total variance observed among the data.In the graphical analysis, the variables are represented by vectors that show the increase in the variable's intensity, while the samples are placed in the region of the graph next to the variables that characterize them.The length of vector decomposition in each component emphasizes its importance in the component, which helps to explain the differences between the samples that were observed in the present study.In the first component (F1) the cultivars were distinguished from each other according to growth, whereas, in the second one (F2), they were differentiated in terms of the size of the banana plants.
The most important variables in F1, with a significant coefficient of correlation, were number of hands, number of fingers in the hand, fresh weight of the bunch, height or length of the pseudostem, number of green leaves, and cycle or period from planting in the field until harvest of the first bunch.In F2, the most important variables with high positive correlation were fresh fruit and hand weight (Table 4).In this way, it was possible to visualize four distinct groups, very similar to those obtained by the cluster analysis.The Pacovan, Pacovan Ken, PV42-68, BRS Vitória, BRS Japira, and BRS Preciosa cultivars were grouped on the negative side of F1, predominantly in the upper quadrant (Figure 2), and were characterized as being tall, having a larger pseudostem diameter, and presenting a low production potential compared with the other cultivars.The BRS Garantida cultivar showed  ) plant height from the ground up to the point of emission of the bunch (BPH); diameter of the base of the pseudostem (PD); fresh weight of fruits (FW), of hands (HW), and of bunches without stalks (BW); number of hands (HN) and of fruits in the bunch (FN); number of days from planting to harvest of the first bunch (Cycle); and number of green leaves in the flowering phase (GLN).F1, first component; and F2, second component.Values underlined represent significant correlations by the least significant difference t-test, at 5% probability.PD, pseudostem diameter; BPH, banana plant height; GLN, number of green leaves at the flowering stage; HN, number of hands in the bunch; FN, number of fruits in the bunch; BW, fresh weight of bunches; FW, fresh weight of fruits; HW, fresh weight of hands; and Cycle, number of days from planting to harvest.

Figure 1 .
Figure 1.Dendrogram constructed by the cluster analysis (UPGMA) of banana (Musa spp.) cultivars planted at the Frutacor farm, in the municipality of Limoeiro do Norte, in the state of Ceará, Brazil.Dissimilarity generated with the average values of the agronomic variables evaluated during the three production cycles.

Figure 2 .
Figure2.Principal component analysis with average values from the three production cycles for: banana (Musa spp.) plant height from the ground up to the point of emission of the bunch (BPH); diameter of the base of the pseudostem (PD); fresh weight of fruits (FW), of hands (HW), and of bunches without stalks (BW); number of hands (HN) and of fruits in the bunch (FN); number of days from planting to harvest of the first bunch (Cycle); and number of green leaves in the flowering phase (GLN).F1, first component; and F2, second component.

Table 1 .
(Sneath & Sokal, 1973)Musa spp.) cultivars planted at the Frutacor farm, in the municipality of Limoeiro do Norte, in the state of Ceará, Brazil., and the subplots, the production cycle.Data were subjected to the analysis of variance (Anova) using the Sisvar software, version 5.6 (Universidade Federal de Lavras, Lavras, MG, Brazil), and the means of treatments were grouped by the Scott-Knott test, at 5% probability.The means of the variables for all three cycles were subjected to ascending hierarchical classification (AHC), using the Euclidean distance matrix as a measure of dissimilarity and the unweighted pair-group method with arithmetic mean (UPGMA) for the formation of clusters(Sneath & Sokal, 1973).The variable "cycle" was considered as the number of days between planting and harvest of the first bunch, assuming that the later cycles would be affected by the thinning of banana plants.Moreover, to help define and select genotypes with the desired agronomic traits, the same data matrix was subjected to Pearson's multivariate principal component analysis (PCA) and to a correlation biplot with the automatic coefficients.
Values followed by equal letters, lowercase in the columns and uppercase in the lines for each parameter, do not differ significantly by the Scott-Knott test, at 5% probability.

Table 4 .
Correlation matrix among the studied variables of banana (Musa spp.) cultivars planted at the Frutacor farm, in the municipality of Limoeiro do Norte, in the state of Ceará, Brazil(1).