Received for publication: 15 July, 2015. Accepted for publication: 17 November, 2015. Doi: 10.15446/agron.colomb.v33n3.51900 1 Program of Environmental and Health Engineering, Faculty of Engineering, Universidad del Magdalena. Santa Marta (Colombia). sonia.aguirre.forero@gmail.com 2 Program of Agricultural Engineering, Faculty of Engineering, Universidad del Magdalena. Santa Marta (Colombia). 3 Program of Biology, Faculty of Basic Sciences, Universidad del Magdalena. Santa Marta (Colombia). Agronomía Colombiana 33(2), 348-355, 2015 Relationship between the nutritional status of banana plants and black sigatoka severity in the Magdalena region of Colombia Relación entre estado nutricional de plantas de banano y la severidad de sigatoka negra en el Magdalena - Colombia Sonia Esperanza Aguirre1, Nelson Virgilio Piraneque2, and Javier Rodríguez3 ABSTRACT RESUMEN The association between the severity (average percentage of infection-API) by Mycosphaerella fijiensis Morelet and the plant nutrient content in the banana growing zone of the department of Magdalena (Colombia) was established. Between 2011 and 2012, the foliar contents of N, P, K, Ca, Mg, Na, S, Cu, Fe, B, Zn, and Mn were determined in sectors with high, medium, and low incidences in order to establish their relationships with the API. Severity was determined with the Stover and Dickson methodology, modified by Gauhl for bananas, in order to obtain sanitary information for the zone. With the obtained data, a correlation analysis was completed and the ordination technique was utilized to establish the relationships between farms and variables using an Euclidean distance. The differ- ences between the farms and years were estimated with a two way analysis of variance with permutations and a canonical discrimination analysis in order to differentiate the farms using the measured foliar variables. The results highlighted the importance of the appropriate and balanced management of site-specific nutritional plans for the management of black sigatoka. En la zona bananera del departamento del Magdalena (Co- lombia), se determinó la asociación entre parámetros nutri- cionales y la severidad (porcentaje promedio de infección-PPI) producido por Mycosphaerella fijiensis Morelet. Entre 2011 y 2012 en sectores de alta, media y baja incidencia del patógeno, se determinó contenidos foliares de N, P, K, Ca, Mg, Na, S, Cu, Fe, B, Zn y Mn para establecer su relación con el PPI. La severidad se determinó con la metodología de Stover y Dickson, modificado por Gauhl para banano, obteniéndose información sanitaria de la zona. Con los datos se realizó análisis de cor- relación, se empleó la técnica de ordenación para establecer las relaciones entre fincas y variables mediante la distancia euclidiana. Las diferencias entre fincas y años se estimaron mediante análisis de varianza a dos vías con permutaciones y análisis discriminante canónico para determinar las dife- rencias entre fincas a partir de las variables foliares medidas. Los resultados obtenidos ponen de manifiesto la importancia del manejo sitio-específico de planes nutricionales adecuados y balanceados para reducir la severidad de la sigatoka negra. Key words: Mycosphaerella f ijiensis Morelet, Mu sa sp., integrated disease management, leaf tissue analysis. Palabras clave: Mycosphaerella fijiensis Morelet, Musa sp., manejo integrado de enfermedades, análisis de tejido foliar. Mycosphaerella fijiensis Morelet is the causal agent of black sigatoka (black leaf streak) in the majority of the cultivars of edible banana (Blomme et al., 2011; Churchill, 2011; Niño et al., 2011; Cordoba and Jansen, 2014); in favorable conditions, it is destructive and reduces yield by between 35-50% in susceptible cultivars. Annually, a typical planta- tion is submitted to 24-50 sprayings of fungicides, which is equivalent to approximately 30% of the production costs (Hall et al., 2006; Churchill, 2011). Over time, this pathogen has increased its resistance to chemicals and its distribution in productive areas (Ganry et al., 2012; Guzmán, 2012). Management strategies that Introduction The banana (Musa AAA Simmonds) is cultivated in tropi- cal and subtropical regions (Marín et al., 2003; Blomme et al., 2011; Churchill, 2011). It is a staple food in many countries, a source of income for farmers, and an important export product that generates foreign exchange income in developing countries (Cordoba and Jansen, 2014). In Colombia, 48,325 ha of banana are cultivated (36,325 ha in the Uraba zone and 12,000 ha in the Magdalena zone), with an average production of 95 million exported boxes per year, with a value of US$736 million per year, making it the third-largest exporter in the world (DANE, 2013). http://dx.doi.org/10.15446/agron.colomb.v33n3.51900 349Aguirre, Piraneque, and Rodríguez: Relationship between the nutritional status of banana plants and black sigatoka severity in the Magdalena region of Colombia allow for the aggressiveness of the pathogen to be con- fronted and for the chemical load to be reduced are neces- sary (Orozco-Santos et al., 2013). Pseudomonas, Bacillus, and Serratia sp. have been used as biological alternatives for this purpose, but investigations on their effectiveness are in the preliminary phases and are not yet viable for commercial use (Hall et al., 2007; Blomme et al., 2011; Gutiérrez-Román et al., 2015). Another strategy is to increase the resistance of the host, but high sterility levels and large generation times (from seed to seed) are obstacles for breeding programs (Irish et al., 2013). Until recently, plant nutrition was considered to be an exogenous factor, with production as the main objective; but, today, it is considered to be a complementary strategy in disease management used to obtain products that are beneficial, since nutriments participate in the growth and survival of pests, predispose or increase plant resistance to pathogens, alter plant systems of defense, and increase the formation of mechanical barriers (lignification) and the synthesis of phytoalexins (Moreira et al., 2008). As such, the effect a nutrient element can have on diseased plants depends on the species, phenological stage, pathogen, environment, agricultural management, and nutriment availability (Jones and Huber, 2007; Marschner, 2012; Aguirre et al., 2012). Although resistance is genetically controlled, it is mediated by complexes and physiological processes that are affected by the nutritional state of the plant (Datnoff et al., 2007). Although biotic diseases cannot be completely eliminated due to the presence of a specific nutrient, their severity or incidence may be reduced. In this study, the relationship between the nutrient content in banana plants and the percentage of infection (API) produced by black sigatoka (M. fijiensis) was evaluated, as part of a macroproject that determined the associations between climate, soil properties and foliar content with black sigatoka (Aguirre, 2014). Materials and methods Study area. This study took place in the Magdalena Depart- ment, geographical coordinates: 10º46’00” N and 74º8’00” W, in an area composed of 11,000 ha situated at 20 m a.s.l., with an annual mean temperature of 27ºC; relative humid- ity of 82%, evaporation of 1,500 mm year-1, and precipita- tion of 1,371.7 mm year-1 (IGAC, 2009). The study area is classified as Tropical Dry Forest and Tropical Very Dry Forest in accordance with the Holdridge life zones (Chica et al., 2004). The region is recognized for its export banana production: 60% of the territory of the Banana Growing Zone has optimal soils for agriculture, with the inf luence of the Tucurinca, Sevilla, and Frio rivers providing water for most of the year. In the low zone, the water table is near the surface and close to the Cienaga Grande (large swamp) and, in the rainy season, there are f loods caused by the overf low of water ways (IGAC, 2009). The areas in which the study was conducted belong to eight farms: La Vega, Eva and Manuel in the low incidence zone (Aguja), Olga and Eufemia in the middle incidence zone (Orihueca); and Don Faud, Fortuna, and Ovidio in the high incidence zone (Sevilla). The Spatial location of transects and the Edaphic and climatic characteristics of the region were described by Aguirre et al. (2012). Soils in the zone correspond to Dystric Haplustepts, Typic Dystrustepts, and Typic Endoaquepts and are mineralogi- cally dominated by kaolinite (50%), quartz (5-15%), feldspar (5-15%), interbedded (trace), micas (5-30%), montmoril- lonite (30-50%) and vermiculite (5-30%) (IGAC 2009; Aguirre et al., 2012). Measurement of average percent of infection (API). The cultivars most representative of the Cavendish (Large, dwarf and Valery) banana were used in the study due to their production and adaptability. Ten plants per farm were used to determine the API weekly during 2011 and 2012, with the Stover methodology as modified by Gauhl (1989) (Fouré, 1985). The sanitary information for the youngest leaves (1, 2 and 3), growing normally, as measured by visual estimation as a function of six degrees of disease develop- ment in plants close to f lowering, was registered using the Biological Prewarning System (Marín et al., 2003). The foliar emission (number of leaves) of the plants; state of the leaf primordium; level of leaf infection (II, III, and IV); and state of development of black sigatoka were evaluated, with the objective of the estimating the weighted percentage of infection (API). Measurement of foliar variables. For the foliar analysis, samples of healthy fresh leaves and leaves in different states of disease were collected. These were processed and analyzed in the CIAT (Valle del Cauca) and Western Hemi- sphere Analytical Laboratory - Honduras laboratories, where the foliar element content was determined (Tab. 1). Information analysis. With the records from the pro- duction units, a database matrix of the health and foliar 350 Agron. Colomb. 33(2) 2015 analysis was constructed. With the objective of determin- ing the existing relationships between the foliar variables and API, a graphic and numerical interpretation of the API was made for the different variables tested on the eight farms during the periods 2011 and 2012. A multivariate analysis was used, as well as its spatial-temporal variation with a factorial design in which the factors were constituted of the eight farms and the years 2011 and 2012. The API was considered to be the biotic variable and values for the twelve foliar variables were established (Tab. 1). As the assumptions of normality and homogeneity were not met, non-parametric tests were run. For the characterization of the farms and sample periods, exploratory multivariate techniques were utilized, followed by multivariate analysis of variance PERMANOVA (McCune et al., 2002). -Spearman’s Correlation Analysis: statistical procedure applied to determine the level of association between the API and foliar variables. -Ordination of farms and variables: the multivariate ordi- nation technique was utilized, applying Euclidian distances and the R function scale in order to standardize the mag- nitudes and units of measure of the evaluated variables. -Analysis of hypothesis checking (PERMANOVA): due to a lack of compliance with the supposed parameters of Multivariate Normality and Homogeneity of Covariance required for a multivariate variance analysis (MANOVA), a two way analysis of multivariate variance with permuta- tions (PERMANOVA) was utilized to evaluate the differ- ences between farms and years (factors). -Canonical Discriminant Analysis (CDA): done with data obtained from a lineal multivariate model. Transformation of continuous variables was done in a canonical space con- trolling the terms of the model. The R statistical program, version 3.02, was utilized for the analyses (R Development Core Team 2015). Results Relationships between the foliar nutrient content and API were established. The data showed (Tab. 2) that the zone with the lowest API showed the lower values of foliar levels of Mg (2.56-2.98 mg kg-1) in comparison with 3.046 mg kg-1, the average shown by the zone with the highest API. On the other hand, the analyses showed that the zone with the lowest API showed higher foliar levels of N (27.97 mg kg-1), P (1.99 mg kg-1), K (39.44 mg kg-1), Ca (9.004 mg kg-1), Fe (583.67 mg kg-1), B (22.71 mg kg-1), and Zn (30.72 mg kg-1), values with direct relationships between these nutrients and the API (Tab. 3), suggesting that these nutrients play a fundamental part in the resistance and tolerance of the banana to black sigatoka. Ordination of farms and variables. The ordination done permitted the farms to be associated with variables that characterized them. The variance explained by the TABlE 1. Determined element contents and methods used in the foliar samples of banana plats in the Magdalena region of Colombia. Element Symbol Unit Method Nitrogen N mg kg-1 Acid digestion, automated spectrophotometry Phosphorous P mg kg-1 Potassium K mg kg-1 Atomic absorption spectrophotometry Calcium Ca mg kg-1 Magnesium Mg mg kg-1 Sodium Na mg kg-1 Sulfur S mg kg-1 Manual spectrophotometry Iron Fe mg kg-1 Atomic absorption spectrophotometry Manganese Mn mg kg-1 Zinc Zn mg kg-1 Copper Cu mg kg-1 Boron B mg kg-1 Manual spectrophotometry TABlE 2. Levels of the nutrients (mg kg-1) and average percent of infection (API) in the banana leaves with presence of black sigatoka in farms the Magdalena region of Colombia. Farms Donfuad Fortuna Ovidio Olga Eufemia Eva Manuel la Vega API 3.22±0.53 3.68±0.67 3.04±0.54 3.89±0.94 3.49±0.93 1.99±0.43 1.97±0.4 2.35±0.35 K 36.2±4.4 29.7±4.4 32.87±4.16 32.7±1.42 38.49±2.04 39.44±3.88 40.5±2.3 44.62±5.59 N 29.2±2.2 24.57±4.54 23.94±4.23 27.17±1.35 26.15±1.08 27.85±2.44 27.65±2.96 28.43±2.61 P 1.79±0.16 1.56±0.37 1.51±0.29 1.92±0.13 1.74±0.12 1.82±0.17 1.74±0.27 1.99±0.15 Ca 8.26±1.3 8.17±0.76 6.8±1.03 7.97±1.0 6.56±0.55 8.69±1.78 9.06±1.27 9.26±1.01 Mg 3.03±0.59 3.13±0.34 3.13±0.49 3.2±0.18 2.74±0.17 2.56±0.34 2.98±0.45 2.62±0.28 Fe 108.0±43.21 164.9±94 166.2±15.7 88.79±26.4 82.87±29.05 166.6±62.03 1364.2±136.5 220.2±23.7 Zn 24.53±7.17 34.5±15.5 28.15±10.16 16.06±1.1 16.65±2.8 32.91±14.54 31.36±11.54 27.9±10.33 B 18.83±6.9 18.9±5.46 18.49±5.64 12.47±2.12 14.02±2.06 17.5±1.96 29.95±13.38 20.69±3.96 Means±SD. 351Aguirre, Piraneque, and Rodríguez: Relationship between the nutritional status of banana plants and black sigatoka severity in the Magdalena region of Colombia Analysis of hypothesis testing (PERMANOVA). Signifi- cant differences were found in the studied foliar variables between the farms and years, as in the interactions of the following factors (farm:year). In summary, it was shown that there are nutritional variables that inf luence the API, but they must be identified, which is why the canonical discriminant analysis (CDA) was run. Canonical discriminant analysis (CDA). In the first discriminant function (Can1), or canonical axis, 73.9% of the variation was captured (Fig. 2). The Manuel, Eva, and Vega farms, which had the lowest API, were completely differentiated from the rest. The variables that most clearly differentiated these farms were the foliar contents of K, Fe, B, and Ca. The Don Fuad, Fortuna, Ovidio, Olga and Eufemia farms, with the higher APIs (3.22, 3.68, 3.04, 3.89 and 3.49%, respectively), were differentiated from the rest of the farms and were directly associated with the Mg content. FIgURE 1. Ordination of the farms and variables for the years 2011-2012 with presence of black sigatoka in banana plantation the Magdalena region of Colombia. The average percent of infection (API) was inversely correlated to the foliar contents of K, Ca, B, and Fe. The left side shows the level of relationship of the farms based on different samples in linear relations, while the right shows the vectorial projection of the measured variables and their relationships with the API. A B d=2 d=0.2 Don Fuad Eufemia Manuel Fortuna Vega Eva Olga Ovidio API Zn Mg Cu Fe Mn Ca B K N S P Farm Canonical score Structure Don Fuad Eufemia ManuelFortuna VegaEva Olga Ovidio 2 0 -2 -4 -6 4 C an 1 (7 3. 9% ) AP I M g Fe C a B K FIgURE 2. Contribution of the variables to the discriminant capacity of the analysis between the presence of black sigatoka and the foliar nutrient con- tent in banana plantations of the Department of Magdalena. Canonical punctuation (left) represents their differences. Structure (right) corresponds with vectorial projections of foliar variables to identify their relationships with the farms. TABlE 3. Correlational analysis between the average percent of infection (API) and foliar nutrient contents in the banana leaves with presence of black sigatoka in farms the Magdalena region of Colombia. Var 1 Var 2 Spearman P-value API K -0.47 <0.0001 N -0.15 <0.0001 P -0.08 0.0402 Ca -0.28 <0.0001 Mg 0.26 <0.0001 Fe -0.41 <0.0001 Zn -0.16 <0.0001 B -0.38 <0.0001 Correlation is significant at the 0.01 level two first principal components (inertia) was 52.3%, and showed significant patterns of ordination (Fig. 1) in which the smallest API was established, which was found on the Eva, Manuel, and Vega farms whit 1.99, 1.97 and 2.35%, respectively, and was determined by greater foliar contents of K, Ca, Mg, and B. 352 Agron. Colomb. 33(2) 2015 Discussion The dynamics of growth and development of the banana are a product of the relationships that occur during its cycle with different biotic and abiotic conditions; thus, the yield is determined by interactions between the genotype and the environment (Hay and Porter, 2006; Turner et al., 2007) and it is precisely in this last aspect where nutrition is found, immersed as a productive factor (Marschner, 2012). As a result of the pathogenic infection, physiological dam- age that affects the absorption, assimilation, transport, and redistribution of nutrients may happen (Marschner, 2012, Wang et al., 2013). Adequate nutrition diminishes the de- velopment of diseases through changes in plant physiology or direct effects on the pathogen (Dordas, 2008; Spann and Schumann, 2013). In this study, it was shown that a high foliar content of K is associated with a low API in the field. Many crops, among them banana, are strong nutrient extractors, requiring the application of K in every fertilization program (Bernstein et al., 2011). It is the most abundant cation in higher plants and plays an important role in essential processes, such as enzymatic activation (Cakmak, 2005; Zafar and, 2013), protein synthesis, photosynthesis, transport of solutes by the phloem, osmoregulation (Moreira et al., 2008), and stomatic regulation (Blatt, 2000; Cochrane and Cochrane, 2009). Because the pathogen enters the plant through the stomata (Manzo et al., 2012; Li et al., 2010; Manzo et al., 2005), proper attention must be given to potassium fertilization. The authors found that the incidence of black sigatoka was low when the K: Mg ratio was high in the soil, whereas a low K: Mg ratio increased the disease (Aguirre, 2014). Furthermore, vermiculite clays, as reported by Aguirre et al. (2012), may be fix potassium and a high Mg content could be generating a K induced deficiency, a phenomenon explained by Marschner (2012) and Sharma et al. (2005) and expanded in the study area. Other authors have reported that this element helps to reduce the incidence of pests and diseases (Cakmak, 2005; Datnoff et al., 2007; Dordas, 2008; Sharma et al., 2006; Sharma and Duveiller, 2004; Sharma et al., 2005). Reports have been made on the existence of a complex relationship between potassic nutrition and specific metabolic functions that alter the compatibility of the host-parasite-environ- ment relationship, which thus reduces the susceptibility of at least 140 diseases caused by fungi, bacteria, viruses, and nematodes as long as K remains in the tissues and helps thicken cellular walls (Wang et al., 2013; Römheld and Kirkby, 2010). Furthermore, Perrenoud (1977) revised 2,450 references and concluded that the use of K decreases the incidence of fungal diseases in more than 70% of the cases. The low API value obtained in the Aguja zone (including: Manuel, Eva and Vega) and that which showed the highest content leaf K, may be associated to better control of the permeability of the cytoplasmic membrane, thus avoiding the output of sugars and amino acids (pathogens feeds) to the apoplast or intercellular space and formation of phenolic compounds with different fungistatic properties. Furthermore, it may be highlighted that, in photosynthesis, K regulates the opening and closing of stomata and thus the absorption of CO2, triggering the activation of enzymes and is essential for the production of adenosine triphosphate (ATP), a source of energy for chemical processes in plant cells. It also plays an important role in water regulation in terms of absorption through the roots and loss through stomata, and may be measured by the K content in the plant (Aguilar et al., 2003). In this sense, and using as a premise that the pathogen enters the plant through the stomata (Manzo et al., 2012; Manzo et al., 2005), it is necessary to emphasize care in potassium fertilization. Likewise, for the synthesis of proteins and starches, plants require K. Deficiencies in this element bring about the ac- cumulation of amino acids (contributing to the degradation of phenols) and soluble sugars (nutrients for pathogens), and its deficiency slows down the scarring of wounds, favoring the entrance of pathogens (Römheld and Kirkby, 2010; Wang et al., 2013). Therefore, K addition is only ef- fective in disease control if it alleviates K deficiency (Huber and Jones, 2013). The results of this study showed that an increase in Mg at the foliar level increases the API. Little information exists about the role of Mg in plant diseases. However, its role is attributed to indirect effects (ex. the absorption of other nutrients such as K) and direct effects on physiological functions in which the element acts (Huber and Jones, 2013; Jones and Huber, 2007). Dordas (2008) explained its link to the metabolism of other nutrients, in that it diminishes the content of calcium in peanuts and thus predisposes the plant to Rhizoctonia and Pythium. In the same sense, Pers- son and Olsson (2000) affirmed that increases in Mg may inhibit the absorption of K, Ca, and Mn. In this respect, Piraneque et al. (2007) and Aguirre et al. (2012), reported that an increased Mg content in onion bulbs reduced K uptake and increased the damage caused by Sclerotium 353Aguirre, Piraneque, and Rodríguez: Relationship between the nutritional status of banana plants and black sigatoka severity in the Magdalena region of Colombia cepivorum. Thus, it is generally accepted that the optimal nutrient supply improves disease resistance in plants (Hu- ber and Jones, 2013, Marschner, 2012; Katan, 2009), a situ- ation that could also be ref lected in the case of M. fijiensis in the high API zone, where there are possible K induced deficiencies that should be investigated. Higher levels of foliar Ca were correlated with a reduction in the API for black sigatoka, which was shown in the or- dination of the farms and in the canonical discriminant analysis (Figures 1 and 2). This is a vital element with many functions and essential in the development of a firm structure due to its role in the construction of the cellular membrane (Marschner, 2012; Merhaut, 2006; Sugimoto et al., 2010; Sugimoto et al., 2008; Springer, 2009; Azofeifa, 2007). If there is not a sufficient concentration of the ele- ment in the plant tissues, it causes losses of cellular com- pounds and consequently the death of the plant. Calcium functions as a secondary messenger for the absorption of other nutrients and is linked with processes that allow the plant to escape environmental stress (Marschner, 2012), an example is the heat stress that leads to long stems and small leaves, a circumstances present in the study area where temperatures exceeded 28°C. Boron is the least understood essential micronutrient in the development and growth of plants, but at the same time, among the micronutrients, its deficiency is the most exten- sive throughout the world (Blevins and Lukaszewski, 1998; Brown et al., 2002). It has a direct function in the structure and stability of cell walls and cellular membranes, in the metabolism of phenols and lignin, and in diminishing the severity of diseases (Brown et al., 2002). Also, this element is essential for the optimal functioning of ATPase and the redox systems of the plasmatic membrane, in which the activity of polyphenol oxidase and peroxidase is increased. Rajaratnam and Lowry (1974), working with seedlings of oil palm, demonstrated that an increase in the content of foliar B reduced the infestation of red mites (Tetranichus- pioroei) and reported that there is a correlation between B and the production of cyanide, a toxic polyphenol that forms complexes with nitrogenated compounds that are indigestible for mites. These results correspond with Marschner (2012), who af- firmed that this micronutrient diminishes the severity of diseases caused by Plasmodiophora brassicae in crucifers, Fusarium solani in beans, Verticillium albo-atrum in to- mato and cotton, mosaic virus in tobacco and beans, yellow stripe virus in tomato, and Blumeria graminis in wheat; and by Rolshausen and Gubler (2005), who affirmed that applications of B are an alternative to the use of Benlate. Little is known about the role of Fe in resistance to plant pathogens. Certain pathogens, such as Fusarium, have high requirements for this element, but there is still no certainty on the extent of iron contribution to the resistance (Dordas, 2008). However, Expert et al. (2012), and Kieu et al. (2012) made clear that new regulation cascades and virulence mechanisms inf luenced by iron levels have been discovered and pointed out the importance of the strict control of iron levels in the plant-pathogen subsystem, as this element is related to metabolic activities during infection. Graham (1983) and Graham and Webb (1991) reported a diminished severity of diseases such as rust, wheat rot, Sphaeropsis malarum in apples and pears, Olpium brassicae in cabbage, and Colletotrichum musae in banana after an increased absorption of Fe. Kieu et al. (2012) and Expert et al. (2012) posited that Fe promotes antimycosis without interfering in the synthesis of lignin although it is a fun- damental part of peroxidase and stimulates other enzymes involved in the biosynthetic pathway that is responsible for generating compounds charged with the defense of the plant, such as polyphenols. Conclusion High levels of foliar potassium, calcium, boron, and iron are associated with a low disease severity, whereas high levels of magnesium correlate with a high disease severity. Also, the evaluated farms were differentiated, where the higher APIs and higher Mg contents characterized the Don Fuad, Fortuna, Eufemia, Olga and Ovidio farms, while the lower APIs and higher contents of K, Ca, Fe and B characterized the Manuel, Vega and Eva farms. These results highlight the importance of an appropriate and balanced management and site-specific nutritional plans to manage black sigatoka. Acknowledgements The authors would like to thank the engineers Yesid Chávez and Fabián Fonseca from the C.I Técnicas Baltime de Co- lombia S.A company. literature cited Aguilar, E.A., D.W. Turner, D.J. Gibbs, W. Armstrong, and K. Siv- asithamparam. 2003. Oxygen distribution and movement, respiration and nutrient loading in banana roots (Musa spp. L.) subjected to aerated and oxygen-depleted environments. Plant Soil 253, 91-102. Doi: 10.1023/A:1024598319404. Aguirre, S. 2014. Relación entre parámetros edáficos y nutricionales con la severidad de daño producida por Micosphaerella fijiensis en la zona bananera departamento del Magdalena. PhD thesis. Faculty of Agricultural Sciences, Universidad Nacional de Colombia, Palmira, Colombia. http://doi.org/10.1023/A:1024598319404 354 Agron. Colomb. 33(2) 2015 Aguirre F., S.E., N.V. Piraneque G., and J.C. Menjivar F. 2012. Rela- ción entre las propiedades edafoclimáticas y la incidencia de Sigatoka negra (Mycosphaerella fijiensis Morelet) en la zona bananera del Magdalena-Colombia. Rev. Investig. Agrar. Ambient. 3, 13-25. Azofeifa A., D. 2007. Efecto de la fertilización foliar con Ca, Mg, Zn y B en la severidad de la sigatoka negra (Mycosphaerella fijiensis Morelet), en el crecimiento y la producción del banano (Musa AAA, cv. Grande Naine). Undergraduate thesis. School of Agronomy, Instituto Tecnológico de Costa Rica, Santa Clara de San Carlos, Costa Rica. Bernstein, N., M. Ioffe, G. Luria, M. Bruner, Y. Nishri, S. Philosoph- Hadas, S. Salim, I. Dori, and E. Matan. 2011. Effects of K and N nutrition on function and production of Ranunculus asiaticus. Pedosphere 21, 288-301. Doi: 10.1016/S1002-0160(11)60129-X Blatt, M.R. 2000. Cellular signaling and volume control in stomatal movements in plants. Annu. Rev. Cell Dev. Biol. 16, 221-241. Doi: 10.1146/annurev.cellbio.16.1.221 Blevins, D.G. and K.M. Lukaszewski. 1998. Boron in plant structure and function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 481-500. Doi: 10.1146/annurev.arplant.49.1.481 Blomme, G., S. Eden-Green, M. Mustaffa, B. Nwauzoma, and R. Thangavelu. 2011. Major diseases of banana. pp. 85-119. In: Pillay, M. and A. Tenkouano (eds.). Banana breeding: prog- ress and Challenges. Vol. 1. CRC Press, Boca Raton, FL. Doi: 10.1201/b10514-7 Brown, P.H., N. Bellaloui, M.A. Wimmer, E.S. Bassil, J. Ruiz, H. Hu, H. Pfeffer, F. Dannel, and V. Römheld. 2002. Boron in plant biology. Plant Biol. 4, 205-223. Doi: 10.1055/s-2002-25740 Cakmak, I. 2005. The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J. Plant Nutr. Soil Sci. 168, 521-530. Doi: 10.1002/jpln.200420485 Chica, R., M. Herrera, I. Jiménez, S. Lizcano, J.A. Montoya, L.F. Patiño, P.A. Rodríguez, and L.H. Ruiz. 2004. Impacto y manejo de la sigatoka negra en el cultivo de banano de exportación en Colombia. pp. 53-62. In: Memorias 16th Reunión Internacional Acorbat. Oaxaca, Mexico. Churchill, A.C.L. 2011. Mycosphaerella fijiensis, the black leaf streak pathogen of banana: progress towards understanding pathogen biology and detection, disease development, and the challenges of control. Mol. Plant Pathol. 12, 307-328. Doi: 10.1111/j.1364-3703.2010.00672.x Cochrane, T.T. and T.A. Cochrane. 2009. The vital role of potassium in the osmotic mechanism of stomata aperture modulation and its link with potassium deficiency. Plant Signal Behav. 4, 240-243. Cordoba, D. and K. Jansen. 2014. Same disease-different research strategies: bananas and black sigatoka in Brazil and Colombia. Singap. J. Trop. Geogr. 35, 345-361. Doi: 10.1111/sjtg.12072 DANE, Departamento Nacional de Estadísticas. 2013. Encuesta Nacional Agropecuaria - ENA (Estadísticas). Bogota. Datnoff, L.E., W.H. Elmer, and D.M. Huber. 2007. Mineral nutri- tion and plant disease. American Phytopathological Society Press, St. Paul, MN. Dordas, C. 2008. Role of nutrients in controlling plant diseases in sustainable agriculture. A review. Agron. Sustain. Dev. 28, 33-46. Doi: 10.1051/agro:2007051 Expert, D., T. Franza, and A. Dellagi. 2012. Iron in plant-pathogen interactions. pp. 7-39. In: Expert, D. and M.R. O’Brian (eds.). Molecular aspects of iron metabolism in pathogenic and sym- biotic plant-microbe associations. SpringerBriefs in Molecular Science. Springer Netherlands, Dordrecht, The Netherlands. Doi: 10.1007/978-94-007-5267-2_2 Fouré, E. 1985. Black leaf streak disease of bananas and plantains (Mycosphaerella fijiensis Morelet), study of the symptoms and stages of the disease in Gabon. Irfa, Paris. Ganry, J., E. Foure, L.L. Bellaire, and T. Lescot. 2012. An integrated approach to control the black leaf streak disease (BLSD) of bananas, while reducing fungicide use and environmental impact. In: D. Dhanasekaran (ed.). Fungicides for plant and animal diseases. InTech, Rijeka, Croatia. Doi: 10.5772/29794 Gauhl, F. 1989. Untersuchungen zur Epidemiologie und Ökologie der Schwarzen Sigatoka-Krankheit (Mycosphaerella fijiensis Morelet) an Kochbananen (Musa sp.) in Costa Rica. PhD thesis. University of Göttingen, Göttingen, Germany. Graham, R.D. 1983. Effects of nutrient stress on susceptibility of plants to disease with particular reference to the trace elements. Adv. Bot. Res. 10, 221-276. Doi: 10.1016/S0065-2296(08)60261-X Graham, R.D. and R.M. Webb. 1991. Micronutrients and disease resistance and tolerance in plants. pp. 329-370. In: Micronu- trients in agriculture. 2nd ed. Soil Science Society of America, Madison, WI. Gutiérrez-Román, M.I., F. Holguín-Meléndez, M.F. Dunn, K. Guillén-Navarro, and G. Huerta-Palacios. 2015. Antifungal activity of Serratia marcescens CFFSUR-B2 purified chitino- lytic enzymes and prodigiosin against Mycosphaerella fijiensis, causal agent of black Sigatoka in banana (Musa spp.). BioCon- trol 60, 565-572. Doi: 10.1007/s10526-015-9655-6 Guzmán, M. 2012. Control biológico y cultural de la Sigatoka-negra. Trop. Plant Pathol. 37(suppl.), 1-4. Doi: 10.13140/2.1.2927.7442 Hall, R.J., S. Gubbins, and C.A. Gilligan. 2007. Evaluating the performance of chemical control in the presence of resis- tant pathogens. Bull. Math. Biol. 69, 525-537. Doi: 10.1007/ s11538-006-9139-z Hay, R.K.M. and J.R. Porter. 2006. The physiology of crop yield. 2nd ed. Wiley-Blackwell, Singapore. Huber, D.M. and J.B. Jones. 2013. The role of magnesium in plant disease. Plant Soil 368, 73-85. Doi: 10.1007/s11104-012-1476-0 IGAC, Instituto Geográfico Agustín Codazzi. 2009. Estudio general de suelos y zonificación de tierras departamento del Magda- lena. Bogota. Irish, B.M., R. Goenaga, C. Rios, J. Chavarria-Carvajal, and R. Ploetz. 2013. Evaluation of banana hybrids for tolerance to black leaf streak (Mycosphaerella fijiensis Morelet) in Puerto Rico. Crop Prot. 54, 229-238. Doi: 10.1016/j.cropro.2013.09.003 Jones, J.B. and D.M. Huber. 2007. Magnesium and plant disease. pp. 95-100. In: Datnoff, L.E., W.H. Elmer, and D.M. Huber (eds.). Mineral nutrition and plant disease. APS Press, St. Paul, MN. Katan, J. 2009. Mineral nutrient management and plant disease. IPI K Centre - Newsletter e-ifc 21, 6-8. http://doi.org/10.1016/S1002-0160(11)60129-X http://doi.org/10.1146/annurev.cellbio.16.1.221 http://doi.org/10.1146/annurev.arplant.49.1.481 http://dx.doi.org/10.1201/b10514-7 http://dx.doi.org/10.1055/s-2002-25740 http://doi.org/10.1002/jpln.200420485 http://doi.org/10.1111/j.1364-3703.2010.00672.x http://doi.org/10.1111/sjtg.12072 http://doi.org/10.1051/agro:2007051 http://dx.doi.org/10.1007/978-94-007-5267-2_2 http://dx.doi.org/10.5772/29794 http://dx.doi.org/10.1016/S0065-2296%2808%2960261-X http://doi.org/10.1007/s10526-015-9655-6 http://dx.doi.org/10.13140/2.1.2927.7442 http://doi.org/10.1007/s11538-006-9139-z http://doi.org/10.1007/s11538-006-9139-z http://dx.doi.org/10.1007/s11104-012-1476-0 http://doi.org/10.1016/j.cropro.2013.09.003 355Aguirre, Piraneque, and Rodríguez: Relationship between the nutritional status of banana plants and black sigatoka severity in the Magdalena region of Colombia Kieu, N.P., A. Aznar, D. Segond, M. Rigault, E. Simond-Côte, C. Kunz, M.-C. Soulie, D. Expert, and A. Dellagi. 2012. Iron de- ficiency affects plant defence responses and confers resistance to Dickeya dadantii and Botrytis cinerea. Mol. Plant Pathol. 13, 816-827. Doi: 10.1111/j.1364-3703.2012.00790.x Li, W., P. He, and J. Jin. 2010. Effect of potassium on ultrastructure of maize stalk pith and young root and their relation to stalk rot resistance. Agr. Sci. China 9, 1467-1474. Doi: 10.1016/ S1671-2927(09)60239-X Manzo S., G., S. Guzmán G., C.M. Rodríguez G., A. James, and M. Orozco. 2005. Biología de Mycosphaerella fijiensis Morelet y su interacción con Musa spp. Rev. Mex. Fitopatol. 23, 87-96. Manzo S., G., H. Carrillo M., S. Guzmán G., and M. Orozco S. 2012. Análisis de la sensibilidad in vitro de Mycosphaerella fijiensis, agente causal de la sigatoka negra del banano a los fungicidas benomyl, propiconazol y azoxistrobin. Rev. Mex. Fitopatol. 30, 81-85. Marín, D.H., R.A. Romero, M. Guzmán, and T.B. Sutton. 2003. Black sigatoka: an increasing threat to banana cultivation. Plant Dis. 87, 208-222. Doi: 10.1094/PDIS.2003.87.3.208 Marschner, P. (ed.). 2012. Marschner's mineral nutrition of higher plants. 3rd ed. Elsevier, Amsterdam, The Netherlands. McCune, B., J. Grace, and D.L. Urban. 2002. Analysis of ecological communities.: MjM Software Design, Gleneden Beach, OR. Merhaut, D.J. 2006. Magnesium. pp. 146-181. In: Barker, A.V. and D.J. Pilbeam (eds.). Handbook of plant nutrition. CRC Press, Boca Raton, FL. Moreira, C.G.Á., K.R.F. Schwan-Estrada, S.M. Bona ldo, J.R. Stangarlin, and M.E.S. Cruz. 2008. Caracterização parcial de frações obtidas de extratos de Cymbopogon nardus com atividade elicitora de fitoalexinas em sorgo e soja e efeito sobre Colletotrichum lagenarium. Summa Phytopathol. 34, 332-337. Doi: 10.1590/S0100-54052008000400006 Niño, J., Y.M. Correa, and O.M. Mosquera. 2011. In vitro evaluation of Colombian plant extracts against black sigatoka (Myco- sphaerella fijiensis Morelet). Arch. Phytopathol. Plant Prot. 44, 791-803. Doi: 10.1080/03235401003672939 Orozco-Santos, M., K. García-Mariscal, G. Manzo-Sánchez, S. Guzmán-González, L. Martínez-Bolaños, M. Beltrán-García, E. Garrido-Ramírez, J.A. Torres-Amezcua, and B. Canto-Can- ché. 2013. La sigatoka negra y su manejo integrado en banano. Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación (SAGARPA); Instituto Nacional de Investiga- ciones Forestales, Agrícolas (Inifap); Centro de Investigación Regional Pacífico Centro (CIRPAC), Tecoman, Mexico. Perrenoud, S. 1977. Potassium and plant health. Neth. J. Plant Pathol. 85, 82. Doi: 10.1007/BF02349770 Persson, L. and S. Olsson. 2000. Abiotic characteristics of soils suppressive to Aphanomyces root rot. Soil Biol. Biochem. 32, 1141-1150. Doi: 10.1016/S0038-0717(00)00030-4 Piraneque, N., S. Aguirre, and J.C. Menjivar F. 2007. Evolución del contenido de elementos nutrientes en suelos cultivados con cebolla de bulbo. Acta Agron. 56, 37-42. Rajaratnam, J.A. and J.B. Lowry. 1974. The role of boron in the oil- palm (Elaeis guineensis). Ann. Bot. 38, 193-200. Rolshausen, P.E. and W.D. Gubler. 2005. Use of boron for the control of Eutypa dieback of grapevines. Plant Dis. 89, 734-738. Doi: 10.1094/PD-89-0734 Römheld, V. and E.A. Kirkby. 2010. Research on potassium in ag- riculture: needs and prospects. Plant Soil 335, 155-180. Doi: 10.1007/s11104-010-0520-1 Sharma, R.C. and E. Duveiller. 2004. Effect of helminthosporium leaf blight on performance of timely and late-seeded wheat under optimal and stressed levels of soil fertility and moisture. Field Crops Res. 89, 205-218. Sharma, S., E. Duveiller, R. Basnet, C.B. Karki, and R.C. Sharma. 2005. Effect of potash fertilization on Helminthosporium leaf blight severity in wheat, and associated increases in grain yield and kernel weight. Field Crops Res. 93, 142-150. Doi: 10.1016/j. fcr.2004.09.016 Sharma, P., E. Duveiller, and R.C. Sharma. 2006. Effect of mineral nutrients on spot blotch severity in wheat, and associated increases in grain yield. Field Crops Res. 95, 426-430. Doi: 10.1016/j.fcr.2005.04.015 Spann, T.M. and A.W. Schumann. 2013. Mineral nutrition contrib- utes to plant disease and pest resistance. Publication #HS1181. Cooperative Extension Service, Institute of Food and Agricul- tural Sciences, University of Florida, Gainesville, FL. Springer, Y.P. 2009. Edaphic quality and plant-pathogen interactions: effects of soil calcium on fungal infection of a serpentine f lax. Ecology 90, 1852-1862. Doi: 10.1890/08-0740.1 Sugimoto, T., K. Watanabe, S. Yoshida, M. Aino, K. Irie, and A.R. Biggs. 2008. Select calcium compounds reduce the severity of phytophthora stem rot of soybean. Plant Dis. 92, 1559-1565. Doi: 10.1094/PDIS-92-11-1559 Sugimoto, T., K. Watanabe, S. Yoshida, M. Aino, M. Furiki, M. Shiono, T. Matoh, and A.R. Biggs. 2010. Field application of calcium to reduce phytophthora stem rot of soybean, and calcium distribution in plants. Plant Dis. 94, 812-819. Doi: 10.1094/PDIS-94-7-0812 Turner, D.W., J.A. Fortescue, and D.S. Thomas. 2007. Environmental physiology of the bananas (Musa spp.). Braz. J. Plant Physiol. 19, 463-484. Doi: 10.1590/S1677-04202007000400013 Wang, M., Q. Zheng, Q. Shen, and S. Guo. 2013. The critical role of potassium in plant stress response. Int. J. Mol. Sci. 14, 7370- 7390. Doi: 10.3390/ijms14047370 Zafar, Z.U. and H.R. Athar. 2013. Reducing disease incidence of cot- ton Leaf curl virus (CLCuV) in cotton (Gossypium hirsutum L.) by potassium supplementation. Pak. J. Bot. 45, 1029-1038. http://doi.org/10.1111/j.1364-3703.2012.00790.x http://doi.org/10.1016/S1671-2927(09)60239-X http://doi.org/10.1016/S1671-2927(09)60239-X http://dx.doi.org/10.1094/PDIS.2003.87.3.208 http://doi.org/10.1590/S0100-54052008000400006 http://doi.org/10.1080/03235401003672939 http://dx.doi.org/10.1007/BF02349770 http://doi.org/10.1016/S0038-0717(00)00030-4 http://doi.org/10.1094/PD-89-0734 http://doi.org/10.1007/s11104-010-0520-1 http://doi.org/10.1016/j.fcr.2004.09.016 http://doi.org/10.1016/j.fcr.2004.09.016 http://doi.org/10.1016/j.fcr.2005.04.015 http://doi.org/10.1890/08-0740.1 http://doi.org/doi:10.1094/PDIS-92-11-1559 http://doi.org/10.1094/PDIS-94-7-0812 http://doi.org/10.1590/S1677-04202007000400013 http://doi.org/10.3390/ijms14047370