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B I O D I V E R S IT A S
ISSN: 1412-033X
Volume 20, Number 1, January 2019 E-ISSN: 2085-4722
Pages: 144-151 DOI: 10.13057/biodiv/d200117
Folic acid content and fruit characteristics of five Indonesian dessert
banana cultivars
RITA NINGSIH1,2,♥, RITA MEGIA1
1Department of Biology, Faculty of Mathematics and Natural Sciences, Institut Pertanian Bogor. Jl. Raya Dramaga, Bogor 16680, West Java, Indonesia
2Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Halu Oleo. Jl. H.E. Mokodompit, Anduonohu, Kendari 93231,
Southeast Sulawesi, Indonesia. Tel.: +62-401-3191929, email: rita_unhalu@yahoo.com
Manuscript received: 24 September 2018. Revision accepted: 7 December 2018.
Abstract. Ningsih R, Megia R. 2019. Folic acid content and fruit characteristics of five Indonesian dessert banana cultivars.
Biodiversitas 20: 144-151. Folic acid plays an important role in the many metabolic functions of organism, especially pregnant women.
Whereas banana is a fruit that rich in nutrients, high productivity, high diversity, well known, and widely consumed in many countries
and by various communities from infants to elderly. The research aimed to analyze folic acid content and describe the morphology of
mature fruits at three different genomic groups of five Indonesian dessert banana cultivars namely Ambon Kuning (AAA), Ambon
Lumut (AAA), Raja Sereh (AAB), Raja Bulu (AAB), and Lampung (AA). The folic acid content of fruit was analyzed using HPLC
equipped with a UV-vis detector. Fruit characters were analyzed based on 21 descriptors then subjected to clustering analysis. The result
shows that folic acid content of mature stage was 22.26; 21.39; 22.59; 21.2; and 24.58 µg/100 g fresh weight for those five banana
cultivars respectively. Lampung cultivar showed the highest value. Analysis of variance followed by DMRT at 5% probability showed
that folic acid, bunch weight, fruit weight, and fruit length were significantly diverse among those five cultivars. Clustering analyses
revealed that two groups were formed. The first comprises of Ambon Kuning and Ambon Lumut while the second of Raja Sereh,
Lampung, and Raja Bulu. Lampung cultivar was closely related to Raja Sereh than the other cultivars. Adjusted Rand Index analyzed
concluded that the immature peel color, mature pulp color, and predominant taste were the best distinctive characters. This knowledge
can be used as a consideration for the plant breeding program especially in nutrition improvement.
Keywords: Banana cultivar, folic acid, fruit, morphology
INTRODUCTION
Folate (Folic acid) is one of the B groups of vitamins
that are essential for human health. Chemical compounds
with similar chemical properties and biological activity to
folic acid are recognized as folate (Verma et al. 2015).
Folates participate in several metabolic functions, such as
DNA methylation and the biosynthesis of amino acids
(methionine, glycine, and serine), nucleic acids, and S-
adenosylmethionine (SAM) (Hanson and Gregory III
2011). Folate deficiency can cause serious health issues
including neural tube defect (NTDs), impaired cognitive
function, and cardiovascular diseases (Geisel 2003; Ramos
et al. 2005; Kolb and Petrie 2013). It is also associated with
numerous neurodegenerative disorders, including
Alzheimer’s disease (Seshadri et al. 2002) and various
cancers (Choi and Friso 2005). The Recommended Dietary
Allowance (RDA) of folates is 400 µg for adults and 600
µg for pregnant women (Institute of Medicine Food and
Nutrition Board 1998).
The human cannot synthesize folates and thus depend
upon their diet from plant and animal sources (Scott et al.
2000; Basset et al. 2005). Pulses and other legumes, as well
as beef liver, spinach, asparagus, lettuce, and Brussels
sprouts, are rich in folates (USDA-ARS 2012). However,
to gain folate from these sources some processing steps
required whereas folate character is unstable to heat.
Boiling can destroy folate 30-95% from the green bean and
hashed spinach (Bureau et al. 2015). Therefore, it is
necessary that the alternative foodstuffs can be consumed
directly without processing to obtain optimal folate such as
fruit.
Banana is a fruit that is rich in nutrients, are well known
and widely consumed in many countries and by various
communities from infants to the elderly. Production of
bananas and plantains in the world predicted to be around
125 million tons per year, ranks first rank of world fruit
production (FAO 2010). National banana production in
2015 reached 7,299,275.00 tons, while consumption was
1.545.543 tons (Badan Pusat Statistik 2015; Rohmah
2016). In addition to productivity, genetic diversity of
banana germplasm is very high, therefore it has great
potential as a medium to address nutritional problems.
Commercial bananas (cultivated) are currently thought to
have come from wild banana Musa acuminata Colla (2x =
22, symbolized A) and or Musa balbisiana Colla (2x = 22,
symbolized B). Triploid cultivars dominate most of the
world's banana production in the form of dessert varieties
of bananas or cooking bananas included in the genome
group AAA, AAB, and ABB. ABB genotype is generally a
cooking banana, plantain, and AAA or AAB classified as
dessert banana (Karamura and Mgenzi 2004). The number
of banana cultivars in the world is hard to pin down. It used
to be estimated at 500 or so, but it has also been suggested
that it could be twice as many (Promusa 2018). Meanwhile
recorded approximately 306 accessions of banana found in
NINGSIH & MEGIA – Folic acid of Indonesian dessert bananas
145
the garden collection of International Centre for
Horticultural Research and Development (ICHORD) in
Solok West Sumatra Indonesia and about 250 accessions
are cultivated (MGIS 2018).
Morphological characterization of mature fruits at
different genomic groups is important to be conducted as it
is related to the fruit identity and consumer's preferences.
Hapsari and Lestari (2016) describe that each banana
cultivar had specific characteristics related to their genomic
group. Pisang Berlin has bright yellow peel and pulp,
sugary taste. Pisang Ambon Hijau has fine curved fruit
shape, sweet taste and aromatic. Pisang Raja Bandung has
medium thickness and yellow peel, firm flesh, sweet and
slightly acidic taste. Pisang Kepok has thick coarse and
yellow peel with dark brown blotches, mildly sweet taste.
Fruit characters of Pisang Berlin and Ambon Hijau are
closely related to their ancestral parents’ Musa acuminata
wild species, whereas Pisang Kepok and Pisang Raja
Bandung as hybrid cultivars have intermediate characters
between Musa acuminata and Musa balbisiana wild species.
So far there is no specific scientific report about the
content of folic acid (B-9 vitamin) in various genotypes of
bananas. In this research, we choose five cultivars of
popular Indonesian dessert bananas are Ambon Kuning
(AAA), Ambon Lumut (AAA), Raja Sereh (AAB), Raja
Bulu (AAB) and Lampung (AA). These five popular
cultivars due to the large consumed, easy to obtained and
available along the season. According to the data from
University of Florida (2013), folic acid content in bananas
is 20 µg/100 g fresh weight. In addition to folic acid, the
information about banana fruit characteristics at different
genomic groups is still lacking. The purpose of this research
was to analyze the folic acid content and fruit characteristics
of five popular Indonesian dessert banana cultivars.
MATERIALS AND METHODS
Materials
Five popular dessert banana cultivars of Indonesia
represent three genomic banana groups were obtained from
commercial plantations and small estates around Bogor
district on January until March 2018 (Table 1). Three bunches
from three plants per cultivar are harvested and then one or
two middle hands are taken, wrapped in cardboard and
labeled then allowed to mature naturally indoors at room
temperature (Ekesa et al. 2015) until mature stage 6.
According to Stover and Simmonds (1987), mature stage 6
is a condition where all the fruit is yellow skin color with
soft pulp texture (already ripe but not overripe).
Folic acid analysis
Folic Acid analyses of ripe banana pulp were conducted
at PT Saraswanti Indo Genetech Laboratory in Duplo
reactions for each sample and repeated three times. Three
fingers randomly selected from the middle hands, then
washed, peeled, cut into 0.5-0.7 cm thick longitudinal
wedges, flesh-frozen in liquid nitrogen, and kept at -80°C
for folic acid extraction (Garcia-Salinas et al. 2016). Folic
acid is extracted and purified refers to a method Rahimi
and Goodarzi (2011) that has been modified. Five grams of
sample into a 25 mL measuring flask, add 10 mL of
phosphate buffer and 5 mL of acetonitrile then crush it with
the phosphate buffer and homogenize. The mixture was
centrifuged for 15 minutes at 8500 rpm. The supernatant
was filtered through 0.45 µm millipore filter then 10 mL
filtrate was passed into the SPE. Prior to HPLC analysis, all
samples were filtered through a 0.45 µm millipore filter.
The sample is ready to be injected. Each of the 20 µL
sample and standard solutions injected into HPLC under
the following measurement conditions: Lichrospher RP 18
column; isocratic, mobile phase are 2% acetic acid pH 2.8
(A) and acetonitrile (B); and 1.0 mL/min flow rate. The
Folic acid was detected with UV-vis at λ 283 nm. The folic
acid content in the sample is calculated and determined
using a straight-line calibration curve: Y = bx + a (PT
Saraswanti Indo Genetech 2013)
Folic acid content (mg/kg) = (intercept area)/slope x final volume (mL) x df
Sample weight (g)
Fruit characterization
Samples are taken from mid-hand and youngest hand of
the bunch. Immature fruit characteristic recorded on the
youngest hand of the bunch before maturity, meanwhile,
mature fruit characteristic recorded at mature stage 6 (ripe
but not overripe or full yellow stage). Morphological
characterizations were conducted according to the
descriptor for Banana from IPGRI (1996). Morphological
descriptors about 21 characters are fruit position, number
of fruit, fruit length, fruit shape, transverse section of fruit,
fruit apex, remain of flower relicts at fruit apex, fruit
pedicle length, fruit pedicle width, pedicle surface, fusion
of pedicles before joining the crown, immature fruit peel
color, mature fruit peel color, fruit peel thickness,
adherence of the fruit peel, cracks in fruit peel, pulp color
before maturity, pulp color at maturity, fruit fall from
hands, flesh texture and predominant taste. The agronomic
characters of the fruit were also recorded: fresh fruit weight
(pulp, peel and total), bunch weight, number of
hand/bunch, number of fruit/hand, and fruit length.
Table 1. Banana material examined in this study
Cultivar
Synonim*)
Genomic Group
Location**)
Ambon Kuning
Pisang Embun, Gros Michel
AAA
Babakan, Cikalong, Cibatok
Ambon Lumut
Ambon Masak Hijau, Lakatan
AAA
Babakan, Bojong Jengkol, Cikalong
Raja Sereh
Rastali, Silk, Manzana
AAB
Babakan, Cikalong, Cibatok,
Raja Bulu
-
AAB
Babakan, Cibatok, Cikalong
Lampung
Empat puluh hari
AA
Babakan, Carang Pulang, Cibatok
Note: *) Source from Valmayor et al. (2000); **) villages in Bogor district
B I O D I V E R S I T A S
20 (1): 144-151, January 2019
146
Data analysis
The data of folic acid content and fruit characters were
analyzed by one way of analysis variance (ANOVA) using
the software SPSS version 22. If there were significant
differences followed by Duncan Multi-Range Test at 5%
probability. Folic acid content was also analyzed by
comparing to RDA (Recommended Dietary Allowance)
value both for women pregnant and adult. The fruit
characters were analyzed comparative and descriptively
based on 21 descriptors. All of them are analyzed using the
Adjusted Rand Index (ARI) to know main characters which
distinguish the cultivars. Qualitative analysis of fruit
characters are first numerical quantified using the unweighted
scoring method; subsequently, it is subjected to clustering
analysis using software of MINITAB version 16 with
paired group algorithm and Euclidean distance measure.
RESULTS AND DISCUSSION
Folic acid content and agronomic characters
Fruits of various cultivars significantly different in their
folic acid content based on the analysis of variance with a
5% confidence level. The highest content of folic acid in
100 g of fresh fruit weight was found in Lampung cultivar
(24.58 μg) and significantly different from the other four
cultivars based on Duncan Multi-Range Test analysis
(Table 2). The lowest content of folic acid is owned by the
Raja Bulu (21.10 μg) and for three other cultivars from high to
low are Raja Sereh (22.59 μg), Ambon Kuning (22.26 μg),
and Ambon Lumut (21.39 μg). However, the difference of
folic acid content of the four cultivars is not significant.
The folic acid content of local dessert banana in this study
is generally higher than unknown banana cultivar from
Florida Folic Acid Coalition (2017) data (20 μg/100 g fresh
weight) and also higher than apple fruit (5.5 μg/100 g fresh
weight) (Mateljan 2018). As another comparison, total folate
content from eight Indian banana varieties ranges between
10-188 μg/100 g fresh weight (Akilanathan et al. 2010).
Compared with the reference value of dietary allowance
(RDA, 400 μg/100 g for adult and 600 μg/100 g for
pregnant women), the folic acid content in 100 g of fresh
fruit weight in the five dessert banana cultivars is ranging
from 5.3 to 6.1 %. Meanwhile, the content in one piece of
fruit ranged from 8.16 μg in Lampung to 32.01 μg in
Ambon Kuning. The banana cultivars of Lampung though
contain the highest folic acid 24.58 μg/100 g fresh weight,
but the content in the one piece fruit is lowest due to the
size of the fruit itself.
Dessert banana fruit is often consumed fresh, common
folate losses due to oxidation and leaching associated with
processing are not the concern (Delchier et al. 2013).
Another folate source, for example, rice, wheat, potatoes,
tomatoes, and the highest content of beans reaches more
than 100 μg/100 g fresh weight (Jha et al. 2015). However,
the disadvantage of the sources is the loss of folate due to
heating and processing. Heat can destroy folate 60-70%
and boiling 30-95% from plant food material (Indrawati et
al. 2004; Bureau et al. 2015). Therefore eating dessert
banana is the best thing to get folate as a whole.
Table 2. Folic acid content and percentage to RDA value of five
dessert banana cultivars
Cultivar
Folic acid
(µg/100 g
FW)
% Folic
acid to
adult RDA
value
% Folic acid
to women
pregnant
RDA value
Folic
acid/fruit
(
µg/100 g
FW)
Ambon kuning
22.26 a
5.6
3.7
32.01
Ambon lumut
21.39 a
5.3
3.6
15.82
Raja sereh
22.59 a
5.6
3.8
16.82
Raja bulu
21.10 a
5.3
3.5
16.59
Lampung
24.58 b
6.1
4.1
8.16
Note: RDA = Recommended Dietary Allowance for adult 400
µg/100 g FW and women pregnant 600 µg/100 g FW (Fresh
Weight). Means with a different letter in the same column
indicate statistically significant differences calculated by Duncan
Multi-Range Tested (P < 0.05). Values are means of three
independent determinations.
Besides folic acid content, Indonesian dessert bananas
have good nutrition value. Hapsari and Lestari (2016)
described that nutrient values of Indonesian dessert
bananas from genome AAA, and AA in 100 g of edible
portion contained high carbohydrates (16.72-35.24 g/100
g), total sugar (12.12-20.82 g/100 g), potassium (275-375
g/100 g), and vitamin C (16.45-30.27 g/100 g); moderate
protein (1.48-1.78 g/100 g), low fat (0.03-0.08 g/100 g) and
high calories (73.43-148.80 calories/100 g). Due to its high
nutrient values, bananas are nutritious food recommended
for people at all ages, especially for baby, also diet food for
adults. Other advantages of banana as a folic acid source
and nutritious food are widely consumed in many countries
and by various communities, affordable prices, available
along the season, high productivity and genetic diversity of
germplasm.
The content of folic acid in fruit can vary depending on
the variety, environmental factors and methods of analysis.
Presently, the most common techniques of folates analysis
in food are microbial assays, ligand binding analysis, and
high performance liquid chromatographic (HPLC) methods
(Verma et al. 2015). In this study, we use the HPLC
method with a UV-vis detector at λ 283 nm. However, the
results of folic acid measurements are not too different if
compared with varying values of method. According to
Yon and Hyun (2003), folate content in bananas is 16
µg/100 g using microbiological assay, whereas 20 µg/100 g
from the University of Florida (2013) using HPLC method.
Meanwhile, Garcia-Salinas et al. (2016) reported it
amounted to 33.5 µg/100 g fresh weight.
The importance of plant foods to human folate nutrition
has spurred successful efforts to increase plant folate
content (‘biofortification’) using metabolic engineering
(Beakert et al. 2008). Initial studies in tomato fruit and
Arabidopsis thaliana overexpressed the first enzyme of the
pteridine branch of the folate pathway GTP cyclohydrolase
I (Diaz de la Garza 2004). The efforts to increase the
content of folic acid in bananas is becoming important both
with conventional and modern approaches in
biotechnology. Besides, the exploration of folic acid
content in germplasm of other banana plants is also urgent,
to find cultivars/varieties that have high folic acid content.
NINGSIH & MEGIA – Folic acid of Indonesian dessert bananas
147
The superior cultivar can be adopted directly in the field or
as a metabolite profile database useful for breeding
programs.
The result of variance analysis showed significant
differences in pulp, peel and total weight. The Ambon
Kuning cultivar has the highest pulp, peel, and total
(103.95; 39.46; 143.78 g) and the lowest of Lampung
(28.79; 4.32; 33.19 g). As a comparison, Mas Kirana
cultivar (AA) has 71.36 g (Prahardini et al. 2010) and
Cavendish cultivar (AAA) has 180.56 g fresh weight of
fruit, 114.54 g weight of pulp, 66.02 g weight of peel,
63.38 pulp % and 36.6 % peel (Soltani et al. 2011). The
weight of Ambon Kuning and Lampung cultivars differed
significantly against all cultivars while the Ambon Lumut,
Raja Sereh and Raja Bulu did not differ significantly from
each other. Lampung cultivar has the highest proportion of
pulp (86.74%) compared to the peel of the fruit (13.01%)
followed by Ambon Kuning, Raja Sereh, Raja Bulu and
lowest of Ambon Lumut (Table 3). The highlight for
Lampung cultivar, it has the highest in folic acid content
and % pulp to total fresh weight of fruit. In addition, bunch
weight and fruit length have differed significantly among
cultivars (Table 4). Ambon Kuning has the highest value
while Lampung has the lowest based on bunch weight and
fruit length. Fruit length is significantly different according
to the three genomic group, e.g. Ambon group (AAA),
Raja group (AAB), and Lampung (AA). Meanwhile, the
number of hand/bunch and number of fruit/hand of all
cultivars are not significantly different. The data is very
necessary as a consideration in the breeding program to get
a banana fruit that has high folate content with good
agronomic character. Other than it is important for
consumer preferences and basic scientific information for
society.
Fruit characteristics
Fruit characterization revealed that each banana cultivar
had specific characteristics due to their genomic group as
shown in Table 5 and Figure 1. Ambon Kuning (AAA) has
the largest hand and individual fruits size of all cultivars.
Its fruit peel is 3 mm, cracked and easy fall from hand and
it easy to peel. It has the yellow color of peel and ivory of
pulp also sweet aromatic taste so that very popular to
consumers. Ambon Lumut (AAA) has a smaller individual
fruit size than Ambon Kuning. It has dark green with black
spot of peel at immature then turn to yellowish-green with
black spot at mature. Lampung cultivar (AA) has the
smallest individual fruit size of cultivars. Its fruit peel is
very thin and easy to fall from hand with light green color
at immature then turn bright yellow at mature. It has the
cream color of immature pulp and turns yellow, sugary
taste and the straight rounded transverse section of fruit.
These three cultivars are favorite dessert bananas in
Indonesia that have the similar ‘ancestral parents’ wild
seeded M. acuminata species (Table 5; Figure 1).
Raja Sereh and Raja Bulu from the genomic group
AAB show the differences characteristics in fruit position
and fruit apex with the both Ambon cultivars (AAA). The
Raja cultivars have the curved fruit position and
bottlenecked apex while Ambon cultivars have
perpendicular to the stalk and pointed apex. Other than the
individual fruit size of them are smaller than Ambon
cultivars. Raja Sereh has rounded of the transverse section
of fruit and partially fused of pedicles before joining
crown. It has thin and green with black spot color of
immature peel then turning bright yellow at mature. The
immature pulp color is white then turning cream at mature
with sweet and acidic taste. Raja Bulu has slightly ridge of
the transverse section of fruit, persistent and very partially
of pedicles before joining crown. It has medium thick and
dark green color of immature peel then turning yellow at
mature. Differ from Raja Sereh, it has the ivory color of
pulp before maturity then turning yellow with sugary taste
at mature. Both of them are also popular dessert banana in
Indonesia from ‘hybrid ancestral parents” (M. acuminata x
M. balbisiana).
The basic characteristic of banana of AA group is small
size with attractive golden-yellow thin peel, light orange
and soft pulp, predominant sweet taste (slightly sour) and
aromatic fragrance. Bananas AAA group are more vigorous
than the diploids and bear heavy, symmetrical bunches of
large fruit and markedly curved with creamy white to the
yellow pulp, soft and fine textured, sweet taste with
aromatic flavor. Fruit of AAB group bananas are
characterized by its large fruit with thick coarse peel,
orange; pulp creamy-orange, coarse texture and sweet
tastes (Daniells et al. 2001; Espino et al. 1992; Hapsari
2013; Hapsari and Masrum 2011; Simmonds 1959; Vargas
and Sandoval 2005).
Table 3. Fruit fresh weight of five dessert banana cultivars
Cultivar
Pulp (g)
Peel (g)
Total
(g)
%
Pulp/
total
% Peel/
total
Ambon kuning
103.95 a
39.46 a
143.78 a
72.30
27.44
Ambon lumut
50.13 b
23.83 b
73.95 b
67.79
32.22
Raja sereh
56.62 b
17.25 b
74.45 b
76.05
23.17
Raja bulu
54.54 b
24.06 b
78.63 b
69.36
30.60
Lampung
28.79 c
4.32 c
33.19 c
86.74
13.01
Note: Means with the different letter in the same column indicate
statistically significant differences calculated by Duncan Multi-
Range Tested (P < 0.05). Values are means of three independent
determinations.
Table 4. Fruit agronomic characteristics of five dessert banana
cultivars
Cultivar
Bunch
weight
(kg)
Number
of hand/
bunch
Number
of
fruit/hand
Fruit
length
(cm)
Ambon kuning
24.63 a
9.00 a
15.67 a
16.43 a
Ambon lumut
13.30 b
7.00 a
12.67 a
13.03 a
Raja sereh
5.35 bc
6.00 a
12.67 a
10.63 b
Raja bulu
12.77 b
9.00 a
14.00 a
11.30 b
Lampung
3.35 c
8.00 a
15.33 a
8.37 c
Note: Means with the different letter in the same column indicate
statistically significant differences calculated by Duncan Multi-
Range Tested (P < 0.05). Values are means of three independent
determinations
B I O D I V E R S I T A S
20 (1): 144-151, January 2019
148
Table 5. Fruit morphological characteristics of five dessert banana cultivars
Code
Character
Ambon Kuning
(AAA)
Ambon Lumut
(AAA)
Raja Sereh
(AAB)
Raja Bulu
(AAB)
Lampung (AA)
C1
Fruit position
Perpendicular to
the stalk
Perpendicular to
the stalk
Curved upward
(obliquely at a 45°
angle upward)
Curved toward
stalk
Parallel or
curved towards
stalk
C2
Number of fruit per hand
13-16
13-16
13-16 or ≤ 12
13-16 or ≤ 12
13-16 or ≥ 17
C3
Fruit length (cm)
16-20
≤15 or 16-20
≤ 15
≤ 15
≤ 15
C4
Fruit shape
Curved
Curved
Curved
Curved
Straight
C5
Transverse section of fruit
Slightly ridged
Slightly ridged
Rounded
Slightly ridged
Rounded
C6
Fruit apex
Pointed
Pointed
Bottle-necked
Bottle-necked
Bottle-necked
C7
Remain of flower relicts
at fruit apex
Base of the style
prominent
Base of the style
prominent
Base of the style
prominent
Base of the style
prominent
Base of the style
prominent
C8
Fruit pedicel length (mm)
< 10
11-20
11-20
11-20
< 10
C9
Fruit pedicel width (mm)
5-10
5-10 or >10
5-10
5-10 or >10
5-10
C10
Pedicel surface
Hairless
Hairless
Hairless
Hairless
Hairless
C11
Fusion of pedicels before
joining the crown
very partially
very partially
Partially fused
very partially
Very partially
C12
Immature fruit peel color
Green
Dark green with
black spot
Green with black
spot
Dark green
Light green
C13
Mature fruit peel color
yellow
Yellowish green
with black spot
Bright yellow
with black spot
Yellow
Bright yellow
C14
Fruit peel thickness (mm)
3
3
2
3
2
C15
Adherence of the fruit
peel
Fruit peels
easily
Fruit peels
easily
Fruit peels easily
Fruit peels
easily
Fruit peels
easily
C16
Cracks in fruit peel
Cracked
Without cracks
Cracked
Without cracks
Cracked
C17
Pulp color before maturity
cream
cream
White
Ivory
Cream
C18
Pulp color at maturity
Ivory
Ivory
Cream
yellow
Yellow
C19
Fruit fall from hands
Deciduous
Deciduous
Deciduous
Persistent
Deciduous
C20
Flesh texture
Soft
Soft
Soft
Soft
Soft
C21
Predominant taste
Sugary,
aromatic
Sugary,
aromatic
Sweet and acidic
Sugary
Sugary
Table 6. Adjusted Rand Index (ARI) of 21 fruit morphological
characters from five dessert banana cultivars
Code
Description
Adjusted
Rand Index
(ARI)
C13
Mature fruit peel color
0.857
C18
Pulp color at maturity
0.857
C21
Predominant taste
0.857
C01
Fruit position
0.800
C06
Fruit apex
0.800
C08
Fruit pedicel length (mm)
0.800
C12
Immature fruit peel color
0.800
C03
Fruit length (cm)
0.724
C14
Fruit peel thickness (mm)
0.724
C05
Transverse section of fruit
0.714
C17
Pulp color before maturity
0.714
C19
Fruits fall from hands
0.714
C04
Fruit shape
0.524
C11
Fusion of pedicels
0.524
C16
Cracks in fruit peel
0.524
C02
Number of fruits
0.486
C09
Fruit pedicel width (mm)
0.486
C07
Remain of flower relicts at fruit apex
NA
C10
Pedicel surface
NA
C15
Adherence of the fruit peel
NA
C20
Flesh texture
NA
Note: NA: Not Available
During the fruit ripening process, a series of changes
occur physiologically, biochemically and morphologically.
Morphological characters of peel color, and fruit flesh on
the five varieties of bananas change during maturation. In
general, fruit peel changes color from green to yellow
except the variety of Ambon Lumut. Its banana skin color
turns from dark green with black spot to yellowish green
with black spot. The pulp color before maturity is quite
varied, ranging from white, cream to ivory, while when
maturity turns into cream, ivory to yellow. In addition to
the ripening process, variations in some morphological
characters are also influenced by the types of varieties as
shown in Table 5 and Figures 1.
Differences in fruit characters among the five cultivars
can be seen easily by farmers, researcher or any public
interest with bananas. But not so for the common people,
often appear confusion in determining the type of a banana
when shopping. In addition, fruit morphological
information is needed by agribusiness entrepreneurs, food
industry managers, researchers who are involved in the
field of plant breeding, agronomy, post-harvest processing,
and biotechnology. Adjusted Rand Index (ARI) analyzed to
21 descriptors was carried out to find out the distinguishing
characters among those five cultivars (Table 6).
NINGSIH & MEGIA – Folic acid of Indonesian dessert bananas
149
AMBON KUNING (AAA)
AMBON LUMUT (AAA)
RAJA SEREH (AAB)
RAJA BULU (AAB)
LAMPUNG (AA)
Figure 1. Mature fruit morphological characteristics of five Indonesian dessert banana cultivars: A. A hand of fruit, B. Fruit longitudinal
section, C. Fruit cross section. Bar = 2 cm
Raja Bulu (AAB)
Lampung (AA)
Raja Sereh (AAB)
Ambon Lumut (AAA)
Ambon Kuning (AAA)
16.76
11.18
5.59
0.00
Distance
Figure 2. Dendrogram clustering analysis based on fruit
morphological characters
The results show that there are three best characters as
differentiator, e.g., mature fruit peel color (C13), pulp color
at maturity (C18), and predominant taste (C21). ARI value
of the three characters is close to one (0.857), which means
that all show considerable similarity to the reference
cluster. In addition, the fruit position (C1), fruit apex (C6),
fruit pedicel length (C8), and immature fruit peel color
(C12) are quite good as distinguishing characteristics
(Table 6). It can be seen in Table 5 and Figure 1 that C13
(mature fruit peel color) character is varied. Similarly, C18
(pulp color at maturity) and C21 (predominant taste) are
quite different. The C07, C10, C15, and C20 are not
different from each other on the five cultivars so they can’t
be used as distinguishing characters.
Clustering analysis
The fruit characters of Ambon Kuning (AAA) and
Ambon Lumut (AAA) were closely related to their
‘ancestral parent’ wild seeded M. acuminata species.
Phenotypic variation of fruit character is a qualitative trait
that very much affected by genetic factor inherited from the
parental. There are some other banana cultivars in which
included as AAA genomic group, e.g., Ambon Badak,
Ambon Putih, Ambon Hijau, Ambon Hong, Udang,
Angleng, Ampyang, Nona, Santen, Williams, Byok, Kayu,
Kreas, etc. (Valmayor et al. 2000; Hapsari 2013).
Raja Sereh (AAB) and Raja Bulu (AAB) as hybrid
cultivars have intermediate characters between two
ancestral parents’ wild seeded species M. acuminata and
M. balbisiana. They are much closely related to M.
acuminata than M. balbisiana since it contained two ‘A’
genomes. Other banana cultivars that have AAB genomic
group, e.g. Keling, Longong, Seribu, Tanduk, Nangka,
Agung (Valmayor et al. 2000). Not all AAB genomic
group has functioned as dessert banana but some other as
cooking banana (plantain), i.e. Raja Nangka, Raja Kasman,
Raja Marto, Raja Puser, Rojomolo, Tanduk, Tanduk Hijau,
Austroli, etc (Retnoningsih et al. 2010).
Cluster analysis revealed that its fruit characters
clustered according to its genome constitution. It was
clustered into two groups. Ambon Kuning (AAA) was
clustered together with Ambon Lumut (AAA) as group 1
with taxonomic distance 10.2 whereas Raja Sereh (AAB)
was clustered together with Raja Bulu (AAB) as group 2
with taxonomic distance 14.5. Interestingly, Lampung
(AA) was clustered with Raja Sereh (AAB) with taxonomic
distance 12.08 exactly between Raja Sereh and Raja Bulu.
Both groups were separated with taxonomic distance about
16.76 (Figure 2). Lampung cultivar (AA) was separated
C
B
A
B
C
A
B
C
A
B
C
A
C
A
B
B I O D I V E R S I T A S
20 (1): 144-151, January 2019
150
from AAA genomic group and much closer to Raja Sereh
(AAB) according to four characters e.g fruit length, fruit
apex, mature fruit peel color, and fruit peel thickness.
Opposite to result of Hapsari and Lestari (2016) Berlin
cultivar (AA) and Ambon Hijau (AAA) were together in
the same group when compared with cultivars from ABB
genomic group. It can be explained that Hapsari and Lestari
analyze AA, AAA and ABB genomic groups, while in this
research investigate AA, AAA, and AAB genomic groups.
Therefore some of the fruit morphological characters
analyzed are very different.
In conclusion, the folic acid content of five Indonesia
popular dessert banana cultivars is ranging from 22.26-
24.58 µg/100 g fresh weight. Lampung cultivar shows the
highest of folic acid content. Its content averages about
6.15 % of the RDA value for adults and 4.10 % for women
pregnant. Fruit characters Ambon Kuning (AAA) and
Ambon Lumut (AAA) were closely related to their
ancestral parents’ M. acuminata wild Species, whereas
Raja Sereh (AAB) and Raja Bulu (AAB) have intermediate
characters between M. acuminata and M. balbisiana wild
species. Lampung (AA) was closely related to hybrid
genome (AAB) cultivar. There are three morphological
characters are good enough to distinguish them: mature
fruit peel color, pulp color at maturity and predominant
taste. Those Five cultivars of Indonesian dessert bananas
have a good nutrition value as a source of folic acid. They
have great potential as a medium to address nutritional
problems especially folic acid deficiency. Further study of
folic analysis to more samples of other Indonesian banana
cultivars followed by selection will support the banana
breeding program to find cultivars that have higher folic
acid content.
REFERENCES
Akilanathan L, Vishnumohan S, Arcot J, Uthila L, Ramachandran S.
2010. Total folate: diversity between fruit varieties commonly
consumed in India. Intl J Food Sci Nutr 61 (5): 463-472.
Badan Pusat Statistik. 2015. Statistik Tanaman Buah-buahan dan Sayuran
Tahunan Indonesia. Badan Pusat Statistik Indonesia, Jakarta.
[Indonesian]
Basset GJC, Quinlivan EP, Gregory III JF, Hanson AD. 2005. Folate
synthesis and metabolism in plants and prospects for biofortification.
Crop Sci 45: 449-453.
Beakert S, Storozhenko S, Mehrshahi P, Bennett MJ, Lambert W, Gregory
JF III, Schubert K, Hugenholtz J, van der Straeten D, Hanson AD.
2008. Folate biofortification in food plants. Trends Plant Sci 13: 28-
35.
Bureau S, Mouhoubi S, Touloumet L, Garcia C, Moreau F, Bedouet V,
Renard CMGC.2015. Are folates, carotenoids, and vitamin affected
by cooking? Four domestic procedures are compared on a large
diversity of frozen vegetables. LWT-Food Sci Technol 64: 735-741.
Choi SW, Friso S. 2005. Interaction between folate and aging for
carcinogenesis. Clin Chem Lab Med 43: 1151-1157.
Daniells J, Jenny C, Karamura D, Tomekpe K. 2001. Musalogue: A
catalogue of Musa germplasm. Diversity in the genus Musa.
International Network for the Improvement of Banana and Plantain.
Montpellier, France.
Delchier N, Ringling C, Le Grandois J, Aoude-werner D, Galland R,
George S, Rychlik M, Renard CMGC. 2013. Effects of industrial
processing on folate content in green vegetables. Food Chem 139 (1-
4): 815-824.
Diaz de la Garza R, Quinlivan EP, Klaus SMJ, Basset GJC, Gregory III
JF, Hanson AD. 2004. Folate biofortification in tomatoes by
engineering the pteridine branch of folate synthesis. Proc Natl Acad
Sci USA 101: 13720-13725.
Ekesa B, Nabuuma D, Blomme G, Bergh IV. 2015. Provitamin A
carotenoid content of unripe and ripe banana cultivars for potential
adoption in eastern Africa. J Food Compos Anal. 43: 1-6. DOI:
10/1016/j.jfca.2015.04.003.
Espino RRC, Jamaludin SH, Silayoi B, Nasution RE. 1992. Musa L.
(edible cultivars). In: Verheij EWM, Coronel RE (eds.). Plant
Resources of South-East Asia. No. 2, Edible Fruits and Nuts. Pudoc,
Wageningen, Netherlands.
Florida Folic Acid Coalition. 2017. Food Chart. Available on: http:
//www.folicacidnow.net/folic_acid/food_chart.shtml. [21 September
2018].
Food and Agricultural Organization of the United Nations (FAO). 2010.
Available on: www.faostat.fao.org/site/340/default.aspx
Garcia-Salinas C, Ramos-Parra PA, Diaz De La Garza RI. 2016. Ethylene
treatment induces changes in folate profiles in climacteric fruit during
postharvest ripening. Postharvest Biol Technol 118: 43-50.
Geisel J. 2003. Folic acid and neural tube defects in pregnancy - a review.
J Perinat Neonat Nurs 17: 268-279.
Hanson AD, Gregory JF. 2011. Folate biosynthesis, turnover, and
transport in plants. Ann Rev Plant Biol 62: 105-125.
Hapsari L, Lestari DA. 2016. Fruit characteristics and nutrient values of
four Indonesian Banana Cultivars (Musa spp.) at different Genomic
Groups. Agrivita J Agr Sci 38 (3): 303-311.
Hapsari L. 2011. Keragaman dan karakteristik pisang (Musa acuminata)
kultivar grup diploid AA koleksi Kebun Raya Purwodadi. In:
Widyatmoko D, Puspitaningtyas DM, Hendrian R, Irawati,
Fijridiyanto IA, Witono JR, Risna RA, Ariati SR, Rahayu S,
Praptosuwiryo TNg. (eds.). Konservasi Tumbuhan Tropika: Kondisi
Terkini dan Tantangan ke Depan. Proceedings of Seminar Cibodas
Botanic Garden 159th Anniversary, Cibodas. Indonesian Institute of
Sciences, Cibodas. [Indonesian]
Hapsari L. 2013. Performance of seven accessions banana cultivars
triploid Musa acuminate group (AAA) collection of Purwodadi
Botanic Garden. In Scheer H, Pradhan B, Brotosudarmo THP,
Sadtono E, Ane BK. (Eds.). Paper presented at Proceedings of
Humboldt Kolleg: Synergy, Networking and the Role of Fundamental
Research Development in ASEAN, in conduction with: The
International Conference on Natural Science (ICONS). 2011, Batu,
Jawa Timur.
Indrawati, Arroqui C, Messagie I, Nguyen MT, Van Loey A, Hendrickx
M. 2004. Comparative study on pressure and temperature stability of
5-methyl tetrahydrofolic acid in model systems and in food products.
J Agric Food Chem 52: 485-492.
Institute of Medicine, Food, and Nutrition Board. 1998. Dietary Reference
Intakes: Thiamin, Riboflavin, Niacin, Vitamin B6, Folate, Vitamin
B12, Pantothenic Acid, Biotin, and Choline External Link Icon.
National Academy Press, Washington DC.
IPGRI. 1996. Descriptors for banana (Musa spp.). International Plant
Genetic Resources Institute (IPGRI), FAO< Rome.
Jha AB, Kaliyaperumal A, Diapari M, Ambrose SJ, Zhang H, Tar’an B,
Bet KE, Vandenberg A, Warkentin TD, Purves RW. 2015. Genetic
diversity of folate profiles in seeds of common bean, lentil, chickpea,
and pea. J Food Compos Anal 42: 134-140.
Karamura, Mgenzi B. 2004. On-farm conservation of Musa diversity in
the Great Lakes region of East Africa. Afr Crop Sci J 12 (1): 75-83.
Kolb AF, Petrie L. 2013. Folate deficiency enhances the inflammatory
response of macrophages. Mol Immunol 54: 164-172.
Mateljan G. 2018. Apple in-depth nutrient profile. Available on: http:
//www.whfoods.com/genpage.php?tname=nutrientprofile&dbid=94.
MGIS. 2018. Accessions Collection of International Centre for
Horticultural Research and Development (ICHORD).
https://www.crop-diversity.org/mgis/collection/01IDN150
Prahardini PER, Yuniarti, Krismawati A. 2010. Karakterisasi pisang
unggul Mas Kirana dan Agung Semeru di Kabupaten Lumajang.
Buletin Plasma Nutfah 16 (2): 126-133. [Indonesian]
Promusa. 2018. Diversity of banana cultivars. Available on: http:
//www.promusa.org/Diversity+of+banana+cultivars+portal
PT Saraswanti Indo Genetech. 2013. Diagram alir metode pengujian asam
folat metode HPLC dan UPLC. Instruksi Kerja No. Instruksi 18-5-
38/MU/SMM-SIG. PT Saraswanti Indo Genetech, Bogor.
[Indonesian]
Rahimi R, Goodarzi N. 2011. Determination of folic acid in mint
vegetable by High-Performance Liquid Chromatography. Org Chem J
1: 31-35
NINGSIH & MEGIA – Folic acid of Indonesian dessert bananas
151
Ramos MI, Allen LH, Mungas DM, Jagust WJ, Haan MN, Green R,
Miller JW. 2005. Low folate status is associated with impaired
cognitive function and dementia in the Sacramento Area Latino Study
on Aging. Am J Clin Nutr 82: 1346-1352.
Retnoningsih A, Megia R, Hartana A. 2010. Molecular verification and
diversity analysis of Indonesian BB, AAB and ABB banana cultivars.
Tree For Sci Biotechnol 4 (1): 69-76.
Rohmah Y. 2016. Outlook Komoditas Pisang. Pusat Data dan Sistem
Informasi Pertanian. Kementerian Pertanian. Jakarta. [Indonesian]
Scott J, Ŕebeilĺe F, Fletcher J. 2000. Folic acid and folate: the feasibility
for nutritional enhancement in plant foods. J Sci Food Agric 80: 795-
824.
Seshadri S, Beiser A, Selhub J, Jacques PF, Rosenberg LH, D’Agostino
RB, Wilson PWF, Wolf PA. 2002. Plasma homocysteine as a risk
factor for dementia and Alzheimer’s disease. N Engl J Med 346: 476-
483.
Simmonds NW. 1959. Bananas. Longmans Green and Co., London.
Soltani M, Alimardani R, Omid M. 2011. Some physical properties of
full-ripe banana fruit (Cavendish variety). Intl J Agr Sci Res Technol
1 (1): 1-5.
Stover NW, Simmonds RH. 1987. Bananas. Longman Inc., England.
USDA ARS 2012. USDA National Nutrient Database for Standard
Reference, Release 25, Nutrient Data Laboratory. United State
Department of Agriculture, Agricultural Research Service,
Washington, DC. Available on:
http://www.ars.usda.gov/ba/nhnrc/ndl.
Valmayor RV, Jamaluddin SH, Silayoi B, Kusumo S, Danh LD, Pascua
OC, Espino RRC. 2000. Banana cultivar names and synonyms in
Southeast Asia. International Network for the improvement of Banana
and Plantain-Asia and the Pacific office, Los Banos.
Vargas A. Sandoval J A. 2005. Agronomic evaluation of production and
quality of ‘Yangambi km 5’ (AAA) and ‘Dátil’ (AA). Info Musa. 14
(1): 6-10.
Verma AK, Pandey AK, Dubey NK. 2015. Physico-chemical
characteristics, analytics, and metabolism of folate in plants. J Food
Process Technol 7 (1): 1-7.
Yon M, Hyun TH. 2003. Folate content of foods commonly consumed in
Korea measured after tri-enzyme extraction. Nutr Res 23: 735-746.
