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Annals of Plant and Soil Research 17 (Special Issue): 311-316 (2015)

PROFILING OF ANTIFUNGAL COMPOUNDS FROM n-HEXANE EXTRACTS OF


MANGO FRUITS AGAINST MAJOR POST HARVEST PATHOGENS
PARTHASARATHY, S*., MOHAMMAD FAISAL, P., PRABAKAR., K., THIRIBHUVANAMALA, G. AND
RAJALAKSHMI, J.
Department of Plant Pathology, Centre for Plant Protection Studies,
Tamil Nadu Agricultural University, Coimbatore-641 003, India.
Corresponding author*: spsarathyagri@gmail.com.

ABSTRACT
Mango (Mangifera indica L.) is one of the most important tropical fruit crop. Most studies on exploitation of mango have been dealing with mango leaves, juice and bark, however little attention given to mango peel and latex. Biologically active compounds from
vegetal origins are a possible source of natural antifungic effect. Especially, unripe mango contains constitutive defence metabolites
against pathogens and induces quiescent. An n-hexane extraction was used to obtain bioactive metabolites from Mangifera indica L.
cv. Neelum unripe fruit peel and latex. Antifungal effectiveness was determined by challenging the extracts from the best extraction
treatment against two post-harvest fungal pathogens viz., Colletotrichum gloeosporioides and Lasiodiplodia theobromae. The peel
and latex extract exhibited the broadest action spectrum against post-harvest pathogens. The n-hexane extract from Mangifera indica L. cv. Neelum unripe fruit peel and latex were subjected to TLC and GC/MS analysis for compound profiling. These compounds
were resolute as potential source of secondary metabolites with antifungal properties against invading fungal pathogens.

Keywords: Antifungal compounds, Mango, GC/MS, Post harvest diseases

INTRODUCTION
Mango (Mangifera indica L.) is considered one
of the most popular fruits among millions of people in the
tropical area and increasingly in the developed countries.
Because of its delicious taste and high caloric value, it is
ranked as one of the good fruits in the international market.
This fruit has become an essential fruit crop in Asia, Southern
and Central America as well as in many parts of Africa.
Because of diverse production conditions and the vast area
grown, mango suffers from a number of diseases, some of
them taking heavy toll on the crop and representing limiting
factors. These diseases include anthracnose and stem end rot,
all largely caused by different fungi, mainly Colletotrichum
gloeosporioides and Lasiodiplodia theobromae. Synthetic
fungicides are essential to effectively controlling fungus
attacks on fruit. However, some of these fungicides are toxic
in the environment and to mammals that come into contact
with them, and their efficiency can be reduced as fungi
develop resistance due to improper application (Spalding,
1982). This demand has generated increased interest in the
potential of biological control of pathogens using vegetal
extracts containing secondary metabolites. Use of vegetal
extracts with antifungal properties has been a common
practice for thousands of years, for example, powders or
extracts of acacia, garlic, eucalyptus and mint all function
as fungicides capable of controlling different diseases.This
recent focus on natural management of phytopathogenic
fungi has been reflected in extensive research on biological
fungicides. Extracts from different mango tissues have been
shown to be bioactive. Aqueous extracts of leaves and unripe
fruit peel are known to have antifungal activity against
Colletotrichum gloeosporioides. The present study objective
was to describe the in vitro antifungal activity of n-hexane
extracts of mango harvest by products (leaves, seeds from
ripe and unripe fruit) and determine the minimum inhibitory
concentration of these extracts and qualitatively identify
some of the bioactive groups of compounds present in them.

MATERIAL AND METHODS


Vegetal Material
Unripe mango fruits at harvesting maturity were
obtained from a mango orchard in Coimbatore. Fruits with
no visible blemishes were chosen, washed in running tap
water, spread out on clean tissues and allowed to dry under
ambient conditions. For extraction of antifungal compounds,
peels (12 mm thick) were cut using a clean, sharp blade,
weighed and either used immediately or stored at -20C until
further use.
Isolation and pathogenicity test of fungal cultures
Colletotrichum gloeosporioides and Lasiodiplodia
theobromae were isolated from an anthracnose and stem
end rot lesions on a ripe mango fruit separately, following
surface sterilization with 1% NaOCl and maintained on
potato dextrose agar (PDA) at 28 2C. The pathogenicity
was maintained by inoculation into mango fruit and reisolation at 2 month intervals.
Extraction of antifungal compounds from unripe
mango fruits

A, PEEL

Antifungal compounds were extracted by vacuum


infiltration (Adikaram and Bandara 1998) of mango fruit
peel. Ten grams of peel tissue (1 mm thick) cut from unripe
mangoes (cv. Neelum), 60 ml of n-hexane: methanol
(1: 1, v v) and a magnet were placed in each of the four
conical flasks (250 ml) with side arms. They were placed on
magnetic stirrers, and the side arms of the four flasks were
serially connected via tubes. The mouth of the fourth flask
was sealed with a stopper, while the first flask was connected
to a vacuum pump. Solvent infiltration was carried out with
continuous stirring for 30 minutes and the extracts were

311

pooled and filtered through Whatman No.1 filter paper. Fresh


solvent was added to the residue and similarly extracted
thrice. Extracts were pooled and concentrated in vacuo at
40C to 1 10th of the original volume and then partitioned.
The viscous phase was freeze-dried. The residues were resuspended in n-hexane solvents. The n-hexane extract was
further used for TLC and GC-MS analysis.

B, Latex
Mango fruits (cv. Neelum) at maturity were picked
with 5 cm long peduncle. The fruit surface and pedicel
were disinfected with 70% ethanol, and the fruit pedicel
was broken at the peduncle pedicel abscission point. Fruit
were inverted and the exuding latex was collected into a
glass vial. A drop of toluene was added to prevent microbial
growth. The latex was allowed to separate into an upper oily
and lower aqueous phase. The antifungal compounds in the
aqueous phase was extracted by n-hexane solvent infiltration
and concentrated in vacuo and used for further analysis.

Antifungal efficacy of n-hexane extracts by


mycelial inhibition assay
Two
post-harvest
pathogens
Colletotrichum
gloeosporioides and Lasiodiplodia theobromae were used
for assay of antifungal efficacy of mango peel and latex
extract. Pathogens were kept in potato dextrose agar (PDA),
and the cultures stored at room temperature for 47 days
before use in the antifungal activity tests. Inhibition of
mycelial growth was determined by cutting approximately 5
mm diameter discs from the edge of a young fungus culture
colony, and placing the disc in the center of a Petri dish
on PDA containing different dilutions (0.10%, 0.05% and
0.01%) of previously extracts from mango peel and latex
separately with control. The dishes were left to incubate at
room temperature and the experiment terminated when the
control culture (PDA without extract) completely colonized
the agar surface. Radial growth was measured and based
on three replicates per experiment. Results were expressed
as the percentage of radial growth inhibition in the extract
containing media versus the control medium.

Detection of antifungal compound through


chromatography
A, Thin Layer Chromatography (TLC)
Aliquots (10 l), equivalent to 0.5 g of tissue (FW),
of the n-hexane phase of peel extract and latex, were loaded
on to TLC plates (0.5 mm thick, (Merck, Silica gel 60
F254, Germany). The plates were developed in chloroform:
methanol: ethyl acetate, (90 : 5 : 5, v v v) and air-dried
overnight (Karunayake et al. 2011). The experiment was
performed thrice. Then the band was observed under UV light.

rate of 10C/min without hold was followed by increasing


up to 200C and kept at the same temperature for 8 minutes
hold; the electron impact energy was 70eV, Julet line
temperature was set at 2000C and the source temperature
was set at 200C. Electron impact (EI) mass scan (m/z) was
recorded in the 45-450 aMU range. The total chromatogram
was obtained for each sample of mango peel and latex. The
base peak of each spectrum was compared with the base
peak of the chemical components in the NIST Ver.2005 MS
data library through on-line and comparing the spectrum
obtained through GC/MS. The compounds present in the
n-hexane extracts were identified. The relative percentage
of the extract constituents was expressed as percentage with
peak area normalization.

RESULT AND DISCUSSION


Pathogenicity test
Pathogenicity test was conducted in vitro on fully
matured ripe mango fruits by following pin prick plus
spore suspension method. Typical symptoms developed on
all the mango fruits inoculated with the spore suspension
of Colletotrichum gloeosporioides and Lasiodiplodia
theobromae seven days after inoculation. The uninoculated
control fruits did not show any symptoms. Inoculations were
repeated twice and similar results were obtained.

Antifungal bioassay of n-hexane extract from


mango peel and latex
Antifungal efficacy of the mango peel extract against
the Colletotrichum gloeosporioides and Lasiodiplodia
theobromae, three different dilutions were evaluated by using
poisoned food technique. Among the three concentrations,
growth was well inhibited in two concentrations. The mango
peel extract concentration, 0.1 and 0.05 per cent showed
complete inhibition of mycelial growth of C. gloeosporioides
(100 per cent inhibition) and 0.10 per cent showed maximum
inhibition of mycelial growth of L. theobromae was observed,
when compared to control [Table 1]. Similarly, mango latex
aqueous extracts concentration, 0.10 and 0.05 per cent showed
complete inhibition of mycelial growth of C. gloeosporioides
(100 per cent inhibition) and 0.10 per cent showed maximum
inhibition of mycelial growth of L. theobromae (87.44 per
cent inhibition), when compared to control [Table 1].

B, Gas Chromatography/Mass Spectrometer (GC/


MS)
The n-hexane extract from mango peel and latex was
analyzed through GC/MS (Thermo scientific Trace GC Ultra
DSQ II) equipped with column (30mm 0.25mm 0.25m)
under the following conditions: carrier gas as helium with
flow rate at 1ml per minute and 1l sample injection with
pre injection of solvent by AI/AS 3000 Method; split-less
mode injection with 30 second of sampling time; the column
temperature maintained initially at 110C at the increasing
312

Table. 1 In vitro testing of n-hexane extract against C. gloeosporioides and L. theobromae by poisoned food technique
Peel extract
C. gloeosporioides
L. theobromae
S.
(7 DAI)*
(5 DAI)*
Conc. (%)
No
Mycelial
Per cent
Mycelial
Per cent
growth inhibition over growth
inhibition
(cm)
control
(cm)
over control
0.40d
c
1
0.10
0.00
100.00
95.56
(3.67)
3.10c
2
0.05
0.00c
100.00
65.56
(10.15)
b
b
5.67
6.13
3
0.01
37.00
31.89
(13.77)
(14.33)
9.00a
9.00a
4
Control
(17.46)
(17.46)

Latex extract
C. gloeosporioides
L. theobromae
(7 DAI)*
(5 DAI)*
Mycelial
Per cent
Mycelial
Per cent
growth
inhibition
growth
inhibition
(cm)
over control
(cm)
over control
1.13d
c
0.00
100.00
87.44
(6.10)
1.89c
0.00c
100.00
79.00
(7.90)
b
b
4.78
2.36
46.89
73.78
(12.62)
(8.83)
9.00a
9.00a
(17.46)
(17.46)

*DAI- Days after inoculation; *Mean of five replications


In a column, means followed by a common letter is not
significantly different at the 5% level by DMRT; Values in
parentheses are arcsine transformed values.
Quiescence of Alternaria alternata (Droby et al. 1986)
and C. gloeosporioides (Hassan et al. 2007) in the immature
mango fruit has been attributed to antifungal resorcinols in
fruit peel and latex. Although the presence of gallotannins
in the mango peel was known (Berardini et al. 2004),
they have not been classified as antifungal. Gallotannins
appear to display antimicrobial activity (Berardini et al.
2004; Engels et al. 2010). The oily fraction of mango latex
contains antifungal compounds, and coating fruits with 1000
ppm of oily fraction retarded anthracnose development
(Kumpoun et al. 2007). However, the oily fraction may not
be commercially acceptable because of possible allergic
reactions and risk of skin damage. Mango latex is a rich
source of resorcinol (Oka et al. 2004; Hassan et al. 2007) as
the non aqueous phase of fruit latex contains several times
greater resorcinols than the fruit peel (Hassan et al. 2007).

Detection of antifungal compounds of n-hexane


extracts from mango by TLC
The antifungal compounds extracted from the mango
peel and latex was detected under UV light, through thin layer
chromatography at the Rf value of 0.84 and 0.91 respectively,
when compared to untreated control [Plate 1]. Same kind of
result was earlier obtained by Karunayake et al. (2011)
detected the antifungal compounds of mango latex by

overlapping TLC bioassays with peel extracts, a distinct


antifungal zone was observed at Rf value 0.89, showing
their invariable presence in the mango fruit peel and strong
antifungal activity against post-harvest pathogens of mango.

Plate. 1. Thin layer chromatography of n-hexane


extracts
GC/MS analysis of n-hexane extracts of mango
peel and latex
Antifungal metabolite of unripe healthy mango
peel and latex were extracted and profiled. Antifungal
metabolite profile of healthy unripe mango fruits peel was
determined by GC-MS analysis of its n-hexane solvent
extraction method and the result presented in Table 2.
From the result, twenty six metabolites were determined.
Predominated among them were 5-(1,1-Dimethylethyl)
2,2,2,2,
2-pentamethoxy[1,1:3
,1:
3,1:3.1-quinquephenyl]
3,3-dimethanol,
(18.83%), 2(3H)-Furanone, dihydro-4-hydroxy- (18.61%),
2,7,12,17-tetrabrom-(all-s) cyclotetrathiophen(2,7,12,17tetrabromcycloocta[1,2-b:4,3-b:5,6-b:8,7-b]
tetrathiophen (18.54%), and the least was 2-(tert-Butyl)-5phenyl dihydroisoxazolepentacarbonylchromium (0.51%)
peak area. Ejap 13 is antifungal terpenoid molecule in
Euonymus japanicus (Connolly and Hill 1991). 2(3H)Furanone, dihydro-4-hydroxy- is an active principle for pest
repellent in tobacco (Pino et al. 2005) [Table. 2].

Table. 2 GC/MS chromatogram of n-hexane extracts from Mango peel


S.
No.

RT

Name of the compound

Peak
Area
(%)

S. No.

RT

Name of the compound

Peak
Area
(%)

2.48

2,7,12,17-tetrabrom-(all-s)
cyclotetrathiophen(2,7,12,17tetrabromcycloocta[1,2-b:4,3-b':5,6b":8,7-b"']tetrathiophen

18.54

14

18.22

2-(Ethylenedioxy)
ethylamine,N-methyl-N-[4-(1pyrrolidinyl)-2-butynyl]

1.42

3.12

5"-(1,1-Dimethylethyl) 2,2',2",2"',
2""-pentamethoxy[1,1':3 ',1":
3",1''':3"'.1""-quinquephenyl]
3,3""-dimethanol

18.83

15

19.47

Dodecachloro-3,4benzophenanthrene

0.53

313

S.
No.

RT

Name of the compound

Peak
Area
(%)

S. No.

RT

Name of the compound

Peak
Area
(%)

6.55

2(3H)-Furanone, dihydro-4-hydroxy-

18.61

16

20.17

15-Bromo-4,4',12-tris(tbutyl)naphtho[1,2-f]
phenanthro[2,1-d]

0.53

8.31

15,31-Bis(dicyanomethylene)
-5,8,21,24-pentaoxa 2,11,18,
27tetrathiatricyclo[19(12,17)]

14.37

17

20.76

2-(tert-Butyl) -5-phenyl
dihydroisoxazolepentacarbonylchromium

0.51

9.56

N-Methoxy-N-ethylpropionamide

7.33

18

22.32

Nona-2,3-dienoic acid, ethyl


ester

1.68

9.98

Methanol, triethylsilyl

7.33

19

24.54

2H-1-Benzopyran-4-ol,
3,4-dihydro-2-phenyl-

1.56

10.23

3,5-Diphenyl-2-(3',4'dimethoxyphenyl)-pyrrole

1.93

20

26.67

Spiro[N-Benzylpyrrolidin
-2-one-3,9'-xanthene]

1.56

12.43

Supinine

1.93

21

28.58

(Z)-[(Phenylthio)methyl]

1.56

13.26

Styrene-7,8-oxide

1.93

22

29.36

1,2-Bis(t-tributylsilyl)-1,2diphenylcyclotrisilan

0.94

10

13.87

Ethyl 2-{[(6'ethylimidazo [2,1-b]


(1,3)-thiazol-5'yl) carbonyl]a mino}
acetate

0.68

23

31.28

Ejap-13

0.94

11

15.34

4-Phenyl-1-buten-3-yne

3.15

24

33.83

Lipo-3-episapelin A

0.94

12

16.78

10-Methyldodecan-5-olide

1.42

25

37.01

5,10-Dibutyltetra
benzoporphyrin

1.00

13

17.21

5-Cyclotetradecyn-2-one, 8-hydroxy14-penyl-1-oxa

1.42

26

41.19

3,4,5,6-Tetrahydro-7acetoxy-2-(1,3-dithian-2-yl)
2,6-methano-2H-1-benzoxocin

1.31

The results of GC-MS analysis of the n-hexane extract of


mango latex were presented in Table 3. From the result, twenty eight metabolites were determined predominated peak
area by Quinic acid (8.50%) followed by Desulphosinigrin
(8.15%), 2(3H)-Furanone, 5-ethoxydihydro- (3.14%) and
9-Oxabicyclo[3.3.1]nonane-2,6-diol was the least (1.06%)
. The present findings that benzaldehyde (2H-1-Benzopyran-4-ol, 3,4-dihydro-2-phenyl- and Spiro[N-Benzylpyrrolidin-2-one-3,9-xanthene]) was strong growth inhibitors
confirm previous reports of their strong inhibition of mycelial growth of other microorganisms such as C. gloeospori-

oides, Altenaria alternata, Botrytis cinerea, and Fusarium


sambucinum (Vaughn et al. 1993). The fungicidal properties
of benzaldehyde were already reported against Monillinia
fructicolla and B. cinerea (Wilson et al. 1987). The fatty acids 10-Methyldodecan-5-olide, Nona-2,3-dienoic acid, ethyl
ester have previously been reported to be present in mango
(Pino et al. 2005). The quinic acid derivatives (including
4-feruoyl quinic and 5-ferruoyl quinic acids) characterized
for first time in propolis samples HPLC analysis (Pereira et
al. 2003). Desulphosinigrin is active elicitor bio molecule in
Brassica napus (Brudenell et al. 1999) [Table. 3].

Table. 3 GC/MS chromatogram of n-hexane extracts from Mango latex


S.
No.

RT

3.22

Propane,2-(9 borabicyclo [3.3.1]


non-9-yloxy)-3-(9 borabicyclo
[3.3.1]non-9-ylthio)-1-phenoxy

6.98

Na-(3,5 dinitrobenzoyl) tyrosine


N' (1methyl hexylidene)hydrazide

Name of the compound

Peak
Area
(%)

S.
No.

RT

2.99

15

26.08

Methyl -dgalactopyranoside

1.26

26.79

3-Methoxymethoxy3,7,16,20-tetramethylheneicosa-1,7,1
1,15,19-pentaene

1.31

2.99

314

16

Name of the compound

Peak
Area
(%)

S.
No.

RT

Name of the compound

Peak
Area
(%)

S.
No.

RT

8.65

4H-Pyran-4-one, 2,3-dihydro-3,5dihydroxy-6-methyl

2.68

17

31.34

-Cedrol

1.31

9.12

2,3-Dihydro-3,5-dihydroxy-6methyl-4H-pyran-4-one

2.68

18

31.76

7-epi-cis-sesquisabinene
hydrate

1.31

11.50

alpha-(2-(1,3,2methyldioxazano))
-isobutyric acid methyl ester

2.68

19

32.17

-D-Glucopyranose,
4-O--Dgalactopyranosyl

3.14

12.02

N-(1-Methoxycarbonyl-1methylethyl)-4-methyl-2-aza-1,3dioxane

2.68

20

32.69

Diethylvinylsilane

3.12

13.87

l-Alanyl-l-alanine ethylamide

2.68

21

33.43

2(3H)-Furanone,
5-ethoxydihydro-

3.14

15.08

9-Oxabicyclo[3.3.1]nonane-2,6diol

1.08

22

33.89

Betaxolol

2.18

17.55

-Pyrrolidone,
5-[3hydroxybutyl]-

1.08

23

35.20

Quinic acid

8.50

10

19.90

Pyrrolidine,1,2-dedihydro-5-[3acetoxy-1-butyl]-2-methylthio-

1.08

24

35.24

Desulphosinigrin

8.15

11

20.34

Piperidine-4-carboxylic acid,1-[2(2-methyl-2,3-dihydroindol-1-yl)2-oxoethyl]-, amide

1.35

25

35.78

Phenol, 4-(3-hydroxy-1propenyl)-2-methoxy-

1.65

12

21.71

8-n-Hexyl-cis-7 thiabicyclo[4.3.0]
nonane

1.35

26

36.87

13

22.31

4-Azido-3-methylfuroxan

1.35

27

37.11

14

23.54

Phenol, 3-methyl-5-(1methylethyl)-, methylcarbamate

1.20

28

37.69


These results suggests that n-hexane extracts from
Mangifera indica L. cv. Neelum proved that the, antifungal
compounds in the peel and latex of mango is a potent
source for constitutive defence against Colletotrichum
gloeosporioides and Lasiodiplodia theobromae. Antifungal
compounds have previously been implicated for quiescence
on mango. This study revealed the presence of several
antifungal compounds in the unripe mango fruit peel and
latex. Antifungal activity was greater in immature fruits than
in a mature fruits.

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