Abstract
Bananas and plantains (Musa sp.) are major staple foods in many developing countries of the world. Although bananas are rich in carbohydrate, fiber, protein, fat, and vitamins A, C, and B6 they are largely deficient of iron (Fe), iodine, and zinc (Zn). A small increase in the micronutrient content of bananas could play a major role in combating disorders that are due to deficiency of mineral micronutrients such as Fe and Zn. The objective of this study was to determine the Fe and Zn content of 47 banana genotypes from a germplasm collection in Uganda using atomic absorption spectrophotometry. The Fe and Zn content showed wide variability and highly significant differences (P < 0.001) within and among the different banana categories selected for this study. The highest average Fe content (1.42 mg/100 g) was found in ‘Saba’ (ABB) while the least Fe content (0.06 mg/100 g) was found in ‘Kikundi’ (AAA). The highest average Zn content (1.21 mg/100 g) among the analyzed accessions was found in ‘Kivuvu’ (ABB) while Zn was not detectable in both ‘Kabucuragye’ (AAA) and ‘Grand Naine’ (AAA). Considering these figures, there is a greater than 20-fold variation in the Fe and Zn levels of the banana genotypes used this study suggesting that genetic improvement of genotypes for enhanced micronutrient levels may be achieved by breeding.
Micronutrient malnutrition, particularly deficiencies in Fe and Zn, affects over three billion people in the world (Salim-Ur-Rehman et al., 2010; Wang et al., 2011; Welch and Graham, 2004). Iron is an important component in human diets since it regulates enzyme activity and plays a role in the immune system (Lynch, 2003); it is an important component of human blood (Tuman and Doisy, 1978). Iron deficiency can lead to mental and psychomotor impairment in children and an increase in both morbidity and mortality of mother and child at childbirth (Frossard et al., 2000). Anemia, the disease that is due to the impaired absorption of Fe from the bloodstream affects over 80 million African children and over 60 million adults. Similarly, health problems due to Zn deficiency include anorexia, dwarfism, weak immune system (Solomons, 2003), skin legions, hypogonadism, and diarrhea (McClain et al., 1992). Zinc plays an important role in the immune system; it is necessary for T lymphocyte development (Ronaghy, 1987).
Although plant foods contain almost all the mineral nutrients required for the human body (Grusak and DellaPenna, 1999) these are often not present in sufficient amounts (Vasconcelos et al., 2003). Improving the micronutrient composition of plant foods may become a sustainable strategy to combat deficiencies in human populations, replacing or complementing other strategies such as food fortification or nutrient supplementation (Hess, 2013; Zimmermann and Hurrell, 2002). The Fe and Zn content of plants could be increased by biofortification, i.e., defined as a strategy to increase the nutrient content of staple foods through agricultural means, including breeding, genetic engineering, mutagenesis, and agronomic approaches (Hotz, 2013).
Bananas and plantains (Musa sp.) are major staple foods in many developing countries of the world where they contribute to over 25% of the carbohydrate requirement and 10% of the daily calorie intake of the people. A large proportion of the bananas produced in countries such as India, Uganda, Brazil, and China are consumed locally in many different forms with each country having its own traditional dish and method of processing (Frison and Sharrock, 1998). Banana consumption rates can be quite high averaging between 200 and 250 kg per capita annually in New Guinea and countries surrounding the Great Lakes region of east Africa (Pillay and Tripathi, 2007). Although bananas are rich in carbohydrate, fiber, protein, fat, and vitamins A, C, and B6 (Marriott and Lancaster, 1983; Robinson, 1996), they are largely deficient of Fe, iodine, and Zn. It was observed that when cooking, banana was served as the sole weaning food for children in banana growing regions of Uganda; many children were exposed to diseases associated with Fe, Zn, vitamin A, and iodine deficiency (Kikafunda et al., 1996). A small increase in the micronutrient content of bananas could play a highly significant role in combating disorders that are due to deficiency of mineral micronutrients such as Fe and Zn.
Conventional breeding of bananas with enhanced micronutrient content represents a sustainable way of increasing the bioavailability of Fe and Zn (Harvestplus, 2004). The starting point for any breeding program aimed at increasing the micronutrient content of a crop is the screening of the germplasm. The extent of variability in the chemical composition of bananas will be useful for plant breeders and nutritionists who may wish to select/breed for a combination of desirable characteristics, including high micronutrient content. The objective of this study was to determine the content of Fe and Zn in a sample of bananas from east and central Africa.
Materials and Methods
Plant material.
The 47 banana accessions for this study (Table 1) were obtained from the banana germplasm collections located at the International Institute of Tropical Agriculture, now known as Namulonge Agricultural and Animal Research Institute/National Agricultural Research Organization (NAARI/NARO), and from the Kawanda Agricultural Research Institute (KARI) in Uganda. NAARI is at 0°32”N of the equator and 32°37”E. It is 27 km north of Kampala at an elevation of 1150 m above sea level. It has a relatively dry climate with an annual mean rainfall of 950 mm and temperature ranging from 25 to 30 °C, with a relative humidity of 70% for most of the days (NARO, 2005). KARI/NARO is at 0°25”N of the equator and 32°32”E. It is 5 km north west of Kampala at an elevation of 1190 m above sea level, with a moist subhumid climate and a mean annual rainfall of 1250 mm, with temperatures of 25 to 30 °C (Masanza et al., 2005).
Category, accessions, genomes, and average iron (Fe) and zinc (Zn) content of mature green bananas.
The sample represented a range of different banana genotypes and included 9 East African Highland Banana (EAHB) varieties, 11 varieties from Papua New Guinea (PNG), 7 dessert (sweet) varieties, 4 juice producing types, 9 roasting varieties, 6 artificially produced hybrids, and 1 diploid species.
Identification of samples.
Physiologically raw unripe mature bananas with about full angular fingers were sampled and the bunch was considered mature, when at least one finger was ripe in vivo (Thompson and Burden, 1995).
Zinc and Fe levels were determined by following the procedures outlined in Okalebo et al. (2002) using the atomic absorption spectrophotometer (AAS). Each analysis was repeated three times, over a period of 5 months. All data obtained were subjected to analysis of variance and where significant differences were observed, means were separated using Fisher’s Protected least significant difference test at 5% probability level.
Sample preparation and laboratory analysis.
Six banana fingers were systematically picked from the harvested bunch per banana variety. Two fingers each were picked from the top cluster, two from middle cluster, and two from the bottom cluster. The fingers were packed in a cooler box and transported immediately to the laboratory for micronutrient analysis. In the laboratory, three fingers were randomly selected from the six fingers per variety for analysis and the rest were kept in a refrigerator. The fingers were washed under running tap water and then peeled with stainless steel knife. The peeled bananas were washed and rinsed with deionized water, wiped with adsorbent paper, and cut into cubes of ≈2.5 cm2. A multipurpose household food processor [Magic Line, Model MFP 000; Nu-World Ind. (Pty) Ltd, Johannesburg, South Africa] with stainless steel blades was used to grate and blend the cubes into a fine pulp. Each extracted edible pulp per banana variety was divided into two subsamples. For the first subsample, the extracted fresh pulp was immediately sealed in the clean polyethylene bags and conserved at −20 °C for vitamin and anti-nutrient analysis while the other subsample were submitted to moisture determination and conserved for minerals analysis. Before conservation, the extracted pulp was dried in a ventilated oven (40 °C, 5 days) (AOAC International, 2002), minced into powder, and sealed in polyethylene bags for further analysis. The collection and laboratory analysis for each accession was repeated three times. All the analysis was carried out at the Uganda Government Chemist and Analytical Laboratory in Kampala, Uganda.
Fe and Zn analysis.
Procedures outlined by Okalebo et al. (2002) were used to determine Fe and Znlevels in the banana samples using the AAS.
Preparation of standards.
Standards for Fe and Zn analysis were prepared as follows: 0.8635 g of NH4 Fe (SO4)2.12H2O and 0.4398 g of ZnSO4.7H2O were placed in separate 100 mL volumetric flasks. One milliliter of concentrated HNO3 was added to each flask and diluted with water to the 100 mL mark. This produced a 1000 ppm sample for each corresponding metal. From this concentration, the corresponding 1, 2, 3, and 4 ppm were prepared by pipetting 0.1, 0.2, 0.3, and 0.4 mL into a 1000-mL volumetric flask and topped with distilled water. The 1 to 4 ppm samples were used to obtain a standard curve in an AAS.
Digestion of samples.
About 0.3 g of finely ground and dried sample was weighed and placed in a dry and clean digestion tube. The samples were heated in a block digester at 110 °C for 1 h, allowed to cool and three successive portions of 1 mL of hydrogen peroxide were added to the sample. The tube contents were mixed thoroughly after each addition of hydrogen peroxide. The tubes were returned to the block digester and the temperature adjusted to 330 °C. Digestion was considered complete when the digest color turned colorless or light yellow. The tubes were then removed from the digester and cooled to room temperature. The contents were transferred into 50-mL volumetric flask and made up to the mark with deionized water.
Mineral determination.
Results and Discussion
Wide variability and highly significant differences (P < 0.001) were observed for the Fe and Zn content within and among the different banana groups selected for this study (Table 1). The highest average Fe content (1.42 mg/100 g fresh weight) was found in ‘Saba’ (ABB) while the least Fe content (0.06 mg/100 g) was found in ‘Kikundi’ (AAA). The highest average Zn content (1.21 mg/100 g) among the analyzed accessions was found in ‘Kivuvu’ (ABB) while Zn was not detectable in both ‘Kabucuragye’ (AAA) and ‘Grand Naine’ (AAA) and was very low in the hybrid ‘TMB × 5610’ at 0.0404 mg/100 g. Post hoc comparisons using the Tukey’s honestly significant difference test showed that Fe and Zn content of Saba and Kivuvu, respectively, were significantly different (P < 0.05) from the rest of the cultivars used in this study. There is a greater than 20-fold variation in the Fe and Zn levels of the banana genotypes measured in this study suggesting that genetic improvement of genotypes for enhanced micronutrient levels may be achieved by breeding. The variation in the Fe and Zn content of the genotypes in this study may be due to the presence of Fe and Zn transporter genes and their differential expression. It is know that the ZIP gene family is responsible for transporting a variety of cations including Fe and Zn in plants (Guerinot, 2000). Iron and Zn transporter gene sequences have been identified in Musa acuminata (NCBI, accessed 2 Aug. 2015). There is no sequence data for the other genotypes used in this study. However, M. acuminata (AA genomes) is one of the ancestral species of banana that has contributed the A genome in most cultivated bananas. The presence of the A genome in the genotypes used in this study may have influenced the uptake and transport of Fe and Zn. Further research is necessary to prove this assumption.
Only one study (Wall, 2006) has provided similar data for banana on the basis of fresh weight. In that study, Fe content varied from 0.35 mg/100 g to 1.04 mg/100 g while Zn levels ranged from 0.17 mg/100 g to 1.04 mg/100 g. Other studies have reported findings for Fe and Zn on a dry weight basis (Davey et al., 2007, 2009; Emaga et al., 2007). It is not possible to make a comparison of our results with these studies since the banana fruit is considered to have a moisture content of least 75% (Nguyen and Price, 2007).
Significant differences between the mineral content of similar plants may be due to different analytical procedures. In banana, variability for Fe and Zn appears to vary widely within fruit, within hand, and within plants (Davey et al., 2007). It is also known that the nutritional composition of banana and other fruit at harvest can vary widely due to cultivar, maturity, climate, soil type, and fertility (Lee and Kader, 2000; Mozafar, 1994; Shewfelt, 1990). Variability among genotypes for Fe and Zn content is not uncommon among crop plants. For example, the Fe concentration in the rice grain ranged from 8 to 24 μg·g−1 with an average of 12 μg·g−1 while Zn ranged from 14 to 42 μg·g−1 with an average value of 25 μg·g−1 (Ruel and Bouis, 1998). In common beans (Phaseolus vulgaris) Fe and Zn concentrations ranged from ≈24 to 105 μg·g−1 and from 19 to 56 μg·g−1, respectively, in 90 genotypes (Tryphone and Nchimbi-Msoila, 2010). Variability for Fe and Zn content has also been reported for many other crops such as pearl millet (Velu et al., 2008), wheat (Chatzav et al., 2010; Morgounov et al., 2007), tomato (Saha et al., 2010), finger millet (Upadhyaya et al., 2011), and rice (Nagesh et al., 2012).
EAHBs (AAA genomes).
Among the EAHB, ‘Nakhaki’ had the highest levels of both Fe and Zn. The Fe and Zn content of ‘Nakhaki’ is comparable to 0.78 mg/100 g and 0.84 mg/100 g DW, respectively, reported by Davey et al. (2009). In our previous study, ‘Nakhaki’ had a relatively high concentration of vitamin A (462 μg/100 g) and ranked third among nine EAHBs that were studied (Fungo and Pillay, 2011). ‘Nakhaki’ belongs to Nfuuka, the most heterogeneous clone set of the Lujugira–Mutika subgroup. Members of this clone set mutate readily, producing genotypes which may be very similar but differ only in one or two characteristics. ‘Nakhaki’ resembles many other clones but has a yellow orange firm textured pulp (Karamura, 1999). The cultivars in the Nfuuka clone set also differ in the selection and absorption rate of minerals from the soil. ‘Nakhaki’ could have such a trait and is able to select specific nutrients from the soil (D.A. Karamura, personal communication). Nakhaki could perhaps qualify as a cultivar that should be targeted for genetic improvement of micronutrients by hybridization or promoted for consumption because of its levels of essential elements. However, the male and female fertility of ‘Nakhaki’ should be investigated before it can be used in breeding since nothing is known about the fecundity of this cultivar. The mineral content of two other cultivars Mbwazirume and Nakitembe used in this study were also assessed by Davey et al. (2009) on a dry weight basis. Our estimates for Fe and Zn (Table 1) are relatively low compared with the estimates of Davey et al. (2009). Generally, there are wide differences in soil properties in Uganda due to land-use history, eco-region, and management (Tenywa et al., 1999). The Fe levels of the soils from which the plant material were obtained ranged from 32.9 to 37.1 mg·kg−1 in the Ap horizon while that of Zn varied from 2.9 to 4.0 mg·kg−1. The pH of the soils ranged from 4.8 to 6.3 (Th. Karyotis et al., unpublished data). The optimum Fe and Zn requirements for banana production are not known. Since the sampled plants showed no deficiency systems for these micronutrients it can be assumed that the different concentrations of Fe and Zn in the sampled plants were due to genotype/cultivar differences. The uptake of trace elements by the root system of plants and the accumulation of trace elements is likely to be limited by the capacity of the plant to take up and transport these ions (Welch, 2002).
A highly significant correlation (P = <0.001) was found between vitamin A and Fe while the correlation between Zn and Fe was very highly significant (P = <0.0001). No correlation was found between Zn and vitamin A among the EAHBs (P = 0.068). These results suggest that increasing the vitamin A content by breeding may also increase the Fe content.
Bananas from PNG.
Dimaemamosi (AA) was the most interesting among the cultivars from PNG with the highest Fe content. The Zn level of the cultivar was comparatively high with 0.49 mg/100 g. This cultivar also had a very high β-carotene (2416.7 μg/100 g) content (Fungo and Pillay, 2011). The high levels of micronutrients of this diploid AA genotype makes it an ideal male or female parent for improving the β-carotene, Fe, and Zn content of bananas by conventional breeding.
Dessert bananas.
‘Dwarf Cavendish’ had the highest Fe and Zn content in this group. The data from this study are comparable to those reported in other studies of Cavendish bananas (Holland et al., 1991; Mohapatra et al., 2010; Wills et al., 1984).
Roasting bananas.
In the roasting bananas (ABB), Fe levels ranged from 0.13 mg/100 g in ‘Cachaco’ to 1.42 mg/100 g in ‘Saba’ while the Zn content varied from 0.12 mg/100 g in ‘Kivuvu’ to 0.59 mg/100 g in ‘Kidhozi’. The Fe content of ‘Saba’ grown in the Philippines was reported to be 0.9 mg/100 g (Abdon and del Rosario, 1980) and is lower than that found in this study. The plantain ‘Gonja Nakatasese’ (AAB) was included in this group since it is used primarily for roasting in eastern Africa while it is usually fried in west Africa. The Fe and Zn levels of ‘Gonja Nakatasese’ in our study were 0.26 mg/100 g and 0.23 mg/100 g, respectively, and was comparable to those reported for plantains by Davey et al. (2009) although the latter study was conducted on a dry weight basis.
Juice bananas.
In this group of bananas, ‘Yangambi Km 5’ is also consumed as a dessert banana in some countries in Africa had the highest Fe and Zn levels.
Diploids, tetraploids, and hybrids.
The Fe and Zn content of the wild diploid (AA) banana genotype M. acuminata ssp. malaccensis was quite low in comparison with the other AA genotypes used in this study. Musa acuminata sp. malaccensis is not an edible banana but has been used widely in breeding programs since it harbors a number of useful genes (Pillay et al., 2002). Musa acuminata is also an ancestral species in the origin of cultivated bananas. This may suggest two scenarios: that the A genomes of banana are very different from each other or that other factors such as the environment are influencing the micronutrient content of the banana genotypes.
The possibility of increasing the micronutrient content of banana by breeding is highly likely as exemplified by the Fe and Zn content of the hybrid ‘TMB × 5610’. This hybrid resulted from the cross ‘Kabucuragye’ × ‘TMB2 × 7197-2’ while ‘TMB2 × 446S-1’ was derived from ‘Sukali ndizi’ × M. acuminata subsp. malaccensis. The Fe and Zn levels of both the parents of ‘TMB2 × 446S-1’ are shown in Table 1. This hybrid showed a 2-fold increase in both Fe and Zn content compared with its female and male parent. Similarly, the hybrid ‘TMB × 5610’ showed a higher level of Fe and Zn than its female parent. Although preliminary, these results suggest that breeding with selected parents may increase the micronutrient levels of plants. Greater gains in micronutrient content may be achieved if the heritability of these traits in banana can be researched.
The Recommended Dietary Allowance (RDA) of Fe for all age groups of men and postmenopausal women is 8 mg/d; the RDA for premenopausal women is 18 mg/d. The median dietary intake of Fe is ≈16 to 18 mg/d for men and 12 mg/d for women (Food and Nutrition Board, Institute of Medicine, 2001). The Zn RDA for adults is 8 mg/d for women and 11 mg/d for men (Food and Nutrition Board, Institute of Medicine, 2001). In this study, the highest Fe concentrations was found in ‘Saba’ followed by ‘Nakhaki’, ‘Kivuvu’, and ‘Dimaemamosi’ with values ranging from 0.50 to 1.42 mg/100 g. The highest Zn values were found in ‘Kivuvu’, followed by ‘FHIA 25’ and ‘FHIA 23’. Similar to the conclusion reached by Davey et al. (2009), if Fe and Zn were fully bioavailable, we concur that considerable quantities of banana would have to be eaten to meet the RDA values of these micronutrients. The bioavailability for Fe is estimated to ≈10% of the ingested values while that of Zn is in the range of 40% (Davey et al., 2009). Bioavailability of Fe and Zn is also restricted by phytate or phytic acid in foods (Afify et al., 2011) and phytate has been reported in banana although in low concentrations (Adeniji et al., 2007). The bioavailability of Fe is also inhibited by Zn and depends on the total amount of both minerals found in the intestinal lumen (Olivares et al., 2007). While some banana accessions could play a role in enhancing the daily intake of Fe and Zn, they would not make a significant contribution to the RDA for these elements.
Conclusion
A literature survey indicates that there are no attempts to breed bananas for enhanced micronutrients. However, transformation studies to enhance the Fe content of banana with the soybean ferritin gene showed that there was 4.58-fold increase in the Fe levels in the leaves of transgenic plants (Kumar and Srinivas, 2011). Whether such expression levels could be achieved in the fruits remains to be seen. The Queensland University of Technology and the National Agricultural Research Organisation of Uganda are developing transgenic bananas for Fe (Saltzman et al., 2013). Exploitation of the existing variability for micronutrients among germplasm accessions is the first step for developing micronutrient-dense banana cultivars. The variability for Fe and Zn content of the banana genotypes in this study suggests scope for selection of nutrient-rich genotypes for use in breeding programs. Some of the cultivars that have been identified as being relatively rich in Fe and Zn in this study and vitamin A (Fungo and Pillay, 2011) could be introduced immediately to afflicted regions for multiplication and direct distribution to the population.
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