In vitro Antifungal Activities of Extracts of Fruits and other
Morphological Parts of Xanthium strumarium Against the
Plant Pathogen, Rhizoctoniasolani
Nour A. Osmana, Samia E. Alsiddeegb, Nafeesa E. Ahmedc and Salah A.A.Elhusseind
a, University College at Alwajh, University of Tabuk, Saudi Arabia
b,National Oilseed Processing Research Institute (NOPRI) , University of Gezira . Wad
Medani ,Sudan
c, Plant Pathology Department , Agriculture Research & Technology
Corporation, Wad Medani, Sudan
d, Faculty of Industrial Sciences and Technology, Universiti Malaysia Pahang, Kuantan,
Malaysia; Correspondence Author;e-mail: elhusseinsalah@hotmail.com;Permanent
Address: NOPRI, University of Gezira, Wad Medani, Sudan
ABSTRACT
This study is concerned with the evaluation of in vitro antifungal activity of preparations
made from different plant parts of Xanthium strumarium (Compositae) against
Rhizoctoniasolani , the causal agent of damping off disease in several crops. A major
objective of the study was to seek safe natural alternatives to the harmful synthetic fungicides
in current use. The most active plant parts of Xanthium strumarium were seeds, extracted
with n-hexane, and the leaves, extracted with absolute ethanol. The two treatments resulted in
growth inhibition diameters of 45mm and 47mm, respectively .The value of MIC lied
between 350.0 and 175.0 μg of Xanthium oil / ml Attention was drawn to proper selection of
extraction solvent and extraction method when dealing with different morphological parts of
plants. Gas liquid chromatography of the seed oil of Xanthium strumariumrevealed the
presence of the usual fatty acids, palmitoleic (7.6%), oleic(21.6%) and linoleic(70.4%). The
oil was separated into two fractions namely: the free fatty acids fraction and the
unsaponifiable matter fraction. Oil antifungal activity wholly resided in the unsaponifiable
matter fraction. On TLC separation of the latter fraction, two compounds out of six separated,
were active against Rhizoctoniasolani. The infra-red spectra (FTIR) of these two purified
compounds pointed to a long chain hydrocarbon back-bone for both .One of them may
possess, in addition, an alcoholic moiety.
KEYWORDS: Xanthium strumarium, antifungal, Rhizoctoniasolani, seed- oil ,unsaponifiable
matter fraction, TLC , PDA
1
INTRODUCTION
Antifungal natural products of plant origin
Rhizoctoniasolani is a serious soil- and
were reviewed by Arifet al (2009). Our
seed- borne pathogen that causes damping
preliminary observations pointed to the
off disease resulting in severe losses, all
potential of Xanthium strumarium L. in the
around the world, to various crop plants
control of Rhizoctoniasolani. Xanthium
including important food crops (Anderson,
strumarium,
1982; Kataria and Verma, 1992) as well as
Cocklebur or Bur weed, belongs to the
forest
familyAsteraceae
trees
(Camporota
and
Perrin,
commonly
and
known
is
an
as
annual
1998).The fungus was first reported on
gregarious weed widely distributed in most
wheat in Sudan (Elnur and Chester, 1967).
parts of the world (Favieret al, 2005).
In Sudan yield losses incurred by R.
Cocklebur enjoys a reputation in the folk
solaniin cotton, wheat, sorghum, tomato
medicine of several nations of the world as
and anion crops were estimated at 20- 60%
a remedy for a number of ailments
(N.E. Ahmed, Personal Communication).
including malaria, rheumatism, leprosy,
etc., (Kamboj and Saluja, 2010). In
R. solani is very persistent in soil and
addition to being toxic to man and
only very few chemical fungicides were
animals,
Cocklebur
was
reported
to
found effective against it (Errampaliand
possess
Johnson,
interesting
biological
or
2001). Other, non-chemical,
pharmacological activities including anti-
methods were attempted for control of the
trypanosomal
(Talakalet
al,
1995),
fungus, most notably biological control
anticancer (Ramirez-Erasaet al, 2007),
agents (Fiddaman and Rossall, 1995).
anti-inflammatory (Han et al, 2007) and
Natural
chemicals
of
plant
origin
other
represent a diversified, renewable and a
safe
source
of
potential
activities
;Akarteetal, 2009).
pesticides.
2
(Yoon
et
al,
2008
X. strumarium is an invasive widely
Samples
spreading weed in Sudan particularly in
strumariumplants were collected from the
the irrigated agricultural schemes in
Blue Nile river banks near the Gezira
central Sudan. The spiny fruits easily cling
University area at Wad Medani city,
to the hair of grazing animals, aiding seed
Sudan. The collected plants were dissected
dissemination as well as causing some
into morphological parts (leaves, roots,
animal health problems. The rainy season,
etc.) and allowed to dry at ambient
in addition, supports considerable growth
temperature in the shade before grinding
of the plant outside these schemes.
and subsequent solvent extraction.
Crude extracts of X. strumarium have
Solvents and chemicals:
been shown to possess antifungal activity,
All
albiet
laboratory materials used in these studies
against
fungi
other
than
Rhizoctoniasolani (eg, Park et al, 2005).
were
of
solvents,
of
wild-growing
chemicals
analytical
Xanthium
and
grade.
other
Standard
laboratory procedures and equipment were
The objectives of this work were to test
used in weighing, drying, centrifugation,
solvent extracts prepared from different
etc.
morphological parts of X. strumarium for
their activity against the plant disease
Preparation of solvent extracts from
causing fungus R. solani and to chemically
xanthium plant parts:
characterize
Air-dried,
the
active
antifungal
powdered
xanthium
plant
material (leaf or seed parts ) was extracted
ingredients.
using either of three methods. The first is a
cold method that involved maceration of
METERIALS AND METHODS
powdered tissue with ca.20 volumes of
Collection and preparation of plant
solvent such as ethanol ( 95%) or n-hexane
material:
using conical flasks maintained at room
3
temperature for 72 hours with mild
transferred to sterilized sample bottles,
magnetic
eluted with solvent and taken for further
stirring.
Twohot
extraction
methods were used, in addition, one
studies.
involvingSoxhlet extraction and the other
Transmethylation of Xanthium oil fatty
employed refluxing in an appropriate
acids
solvent.All extracts or their filtrates were
Fatty
concentrated in a Rotatory evaporator and
acid
methyl
esters
were
derivatized using 0.5 N sodium methoxide.
kept for further chemical analyses and/or
About 0.5 gram of the oil was weighed in
bioassay.
a stoppered flask and 0.5 N sodium
Preparative
Thin
methoxide was added (7-8 ml). The
Layer
contents were heated for 3-5 mins in a
Chromatographic separations
water-bath at 800C with shaking and then
A few milliliters ofunsaponifiable matter
transferred to a separatory funnel. A few
fraction was applied as a band on a TLC
drops of glacial acetic acid were added
plate ( 0.5 mm, thickness). The plates were
followed by 15 ml of distilled water and
developed in a tank containing the solvent
10 ml of n-hexane. After equilibration,the
mixture, n-hexane: acetone (4:1). Bands
were
detected
using
the
n-hexane layer was collected and kept dry
Antimony
over anhydrous sodium sulphate before
trichloride reagent. The developed TLC
GLC analysis.
plates were partially covered with silica
gel-free glass plates to allow detection of
Gas Liquid Chromatography
separated compounds only at the edges of
The fatty acid composition was determined
the plates and recovery of detection
by GLC ( Varian Instrument Group Series
reagent-free bands inside the plates. These
bands
were
scraped
00-997140-01) equipped with computing
individually,
integrator. Analysis of fatty acid methyl
4
esters was carried out isothermally at
inhibition
column oven temp. of 1700C , column inlet
millimeter.
& detector oven temp. of 1800C and the
For
carrier gas flow was 50ml / minute. The
zone
statistical
was
measured
analysis,
T-tests
in
and
correlation tests were applied according to
identification of fatty acidswas carried out
M-state C and statistical Package for
according to the retention time of esters of
Social Science (SPSS).
authentic samples of fatty acid methyl
RESULTS AND DISCUSSION
esters.
Effect of extraction method on recovery
Bioassay of antifungal activity
of antifungal activity from different
Isolated and identified Rhizoctoniasolani
morphological
fungus was grown on PDA medium .Micro
(Xanthium):Table
fiber glass discs ( 0.5 cm in diameter )
cocklebur
shows
fungal
Rhizoctoniasolani Kuhn, of crude extracts
solutions) were placed in the middle of the
prepared from different morphological
plate for 24 hours before culturing ( using
parts of cocklebur (Xanthium strumarium
Disc Diffusion Method ). Two discs
L.). Two solvents, absolute ethanol and n-
of the test fungus
hexane, were used employing the Soxhlet
culture, were prepared using a cork borer,
method. Aliquots from each extract added
placed from each side of the Petri –plates.
in the in vitro antifungal test were
Discs saturated with either ethanol or n-
calculated
hexane alone were used as control
treatments.
1
of
inhibitory effects, on the growth of
saturated with plant extracts (or control
(0.5cm in diameter)
parts
to
correspond
to
those
obtainable from equal weights of the
The growth diameter (three
respective plant-part powder material. The
replicas for each test) was periodically
most active ethanol extracts were those of
measured for up to three days and the
the roots and leaves of the plant, resulting
5
in fungal growth inhibition diameters of 40
antifungal activity, although the latter
and 37 mm, respectively. The ethanol
method yielded somewhat lower activity.
extract of the stems was less active while
Using the ‘cold maceration’ method,
that of the directly extracted seeds (un-
dichloromethane, as extraction solvent,
defatted) was completely inactive against
was as good as absolute ethanol in the
R. solani. However, pre-extraction of
cases of both leaf and root plant material.
theseeds with hexane (defatting) followed
However, aqueous 70% ethanol gave an
by subsequent extraction of the marc with
extract
absolute ethanol, resulted in a considerably
towards the growth of R. solani, especially
active ethanol extract (Table 2). On the
when used with the leaf material. Again, as
other hand, hexane extracts of the seeds
observed for seed material (Table 2), prior
(representing the seed oil) were very
defatting
active, resulting in a fungal growth
extraction of the marc with absolute
inhibition zone of 32.0 mm, while hexane
ethanol resulted in increased activity of
extracts of the leaves and roots were
absolute ethanol extracts of both leaves
completely inactive towards growth of R.
and roots (Table 3).
solani.
with
with
less
inhibitory
hexane
activity
followed
by
There are no literature reports on the
Further work (Table 3), carried out using
antifungal activity, on R. solani, of crude
the leaf and root morphological parts of
extracts of any of the species of Xanthium.
cocklebur,
of
Crude extracts of cocklebur (Xanthium
extraction solvent and extraction method
strumarium) have been reported to possess
on recovery of antifungal activity. Using
considerable antifungal activity against
absolute ethanol as extraction solvent, the
fungal species of Phytophthora (Kim et al,
soxhlet (Table 1), maceration and reflux
2002), Sclerotinia and Aspergillus (Park et
(Table 3) methods gave similar results of
al, 2005). On the other hand,Murillo-
compared
the
effects
6
Table 1. Inhibitory activity of crude
absolute ethanol and hexane extracts of
Xanthium plant parts on the growth of
R. solani.Extractswere prepared using the
soxhlet method. Figures refer to inhibition
of fungal growth zone, measured in mm.
n.d. = not determined.
Plant part
Extraction Solvent
Table 3.The efficacy of extracts of leaves and roots
of Xanthium, prepared by different extraction
Absolute nEthanol hexane
solvents and methods, on growth inhibition of R.
solani.Figures refer to inhibition of fungal growth
0.0
Control (solvent
only)
0.0
seed
0.0
32.0
stem
12.0
n.d.
leaf
37.0
0.0
root
40.0
0.0
zone, measured in mm.
Extraction
solvent/method
Fungal growth
inhibition, mm
leaf
root
Control (solvent)
0.0
0.0
Absolute ethanol,
maceration
39.0
38.0
Absolute ethanol,
reflux
34.0
35.0
Table 2.Antifungal activity of crude
absolute ethanol extracts (on R. solani)
prepared from de-fatted and nondefatted xanthium seed powder. Seed
powder was directly extracted with ethanol
or first defatted by soxhlet extraction with
n-hexane before ethanol extraction and
bioassaying. Figures refer to inhibition of
fungal growth zone, measured in mm.
Absolute ethanol,
defatted plant
material (hexanepre-extracted),
maceration
70% ethanol,
maceration
47.0
45.0
2.5
30.0
Dichloromethane, 40.0
maceration
40.0
Seed powder
treatment
Hexane extracted
(de-fatted)
None (non-defatted)
S.E.
4.05
Inhibition zone,
mm
10.0
0.0
7
4.35
ONTROL
FFA
SEED OIL
UM
Fig. 1. Typical photos of inhibition of
the growth of R. solani by the seed oil
(hexane extract) of Xanthium.
Fig. 2. Inhibition of the growth of R.
solani by the free fatty acid (FFA) and
unsaponifiable matter (UM) fractions of
Xanthium seed oil.
8
Table 4. Stability of fungal inhibitory
activity (against R. solani) of Xanthium
seed, leaf and root extracts stored at
room temperature for different time
periods.
Storage time,
hours
0
24
48
72
96
S.E.
Table 6.
Fatty acid composition of
Xanthiumseed- oil as determined by
GLC.
Fatty acid
Palmitic acid
Palmitoleic acid
Stearic acid
Oleic acid
Linoleic acid
Plant part/ Fungal
inhibition zone,
mm
Seed Leaf Root
30.0
40
37
34.0
35
40
45.0
45
47
43.0
42
45
30.0
30
30
2.14
2.74 2.74
%
0.5
7.2
0.7
21.6
70.0
Table7. Activity of the oil fractions of X.
strumarium,( FFA & UM) on growth of
R. solani.
Oil fraction
Table 5.Inhibition of R.solani growth by
different concentrations of Xanthium
seed oil. Xanthium seed fixed oil (2.8 g),
prepared by the Soxhlet method, was redissolved in n-hexane (200 ml) to give a
concentration of 14 mg of oil per ml.
Further dilutions were made to give the oil
concentrations indicated in the Table. The
disc diffusion method was used to assay
antifungal activity against R. solaniwhere
discs were saturated with each oil
concentration for the bioassay.
Free fatty acids
Unsaponifiable
matter
Seed oil
concentration,
mg/ml
14.0
11.2
8.4
5.6
2.8
1.4
0.7
0.35
0.175
S.E.
I
II
III
IV
V
VI
Control (eluted
spot-free silica gel)
Fungal growth
inhibition, mm
0.0
28.0
Table 8.Antifungal activity of TLCseparated components of xanthium seed
oil unsaponifiable fraction.
TLC band number
Fungal growth
inhibition zone, mm
40.0
38.0
30.0
28.0
26.0
20.0
12.0
12.0
0.0
3.14
9
Fungal growth
inhibition zone, mm
0.0
30.0
0.0
20.0
0.0
0.0
0.0
-Alvarez et al (2001) reported a low activity
obtained by mechanical expression of Aloe
for ethanol extracts of X. Strumarium, tested
vera (Rodriguez et al, 2005).
among extracts of 24 other plants, against
Our results emphasize the importance
Candidaalbicans. Also, Gupta and Banerjee
of properly choosing the right extraction
(1972) tested crude extracts of 170 different
solvent for different morphological parts of
West Bengal plants against the two fungi
the plant. The fact that seed antifungal
Aspergillusniger and Trichophytonrubrum
activity of X. Strumarium was hexane
and reported no antifungal activity for
soluble and that of the leaf, stem and root
aqueous or ethanol extracts of leaf, stem,
was ethanol soluble (Tables 1, 2) suggest the
root or fruit of X. Strumarium. Extracts of
presence, in X. strumarium, of at least two
other species of Xanthium also showed
different types of compounds active against
antifungal
not
R. solani. The more polar ethanol soluble
including R. solani, e.g., X. Spinsum
antifungal compound(s) was extractable
(Ginesta-Periset
and
from the seed by ethanol solvent only after
X.Macrocarpum(Landreauet al, 2005).Thus,
defatting the seed powder with hexane
to our knowledge, this is the first report on
(Table 2 ). This together with the finding
growth inhibitory effects, against R. solani,
that prior defatting with hexane also
of a member of the genus Xanthium.
improved the recovery of antifungal activity
Thereare, however, reports of preparations
from leaf and roottissues suggests that the
made from plant species not belonging to the
compound(s) is/are present in the seed, leaf
genus
growth
and root of cocklebur associated with
inhibition of R.solani. These included the
hydrophobic cellular components. In this
volatile oil of Chenopodiumambrosioides
case the polar ingredient would possess a
(Dubeyet al, 1983) and a preparation
hydrophobicmoiety at the molecular level.
activity
Xanthium
against
al,
that
fungi
1994)
showed
10
This may assume significance in future
slightly decreased. After 96 hours (4 days) of
studies on the mode of action of the
storage of the discs at room temperature,
antifungal compounds.
100%, 86% and 75% of the original
antifungal activities of extracts of the seed,
Stability of antifungal activity of crude
root and leaf, respectively, still remained.
cocklebur extracts:
Thus, the three extracts, particularly those of
strumarium
Three extracts of X.
prepared
from
the
seeds
the seed, were quite stable under the
(hexane/Soxhlet method) or the leaves and
conditions of the test.
roots (absolute ethanol/maceration method)
Minimum inhibitory concentration (MIC)
were applied to 2cm- diameter disks in
of the seed oil of cocklebur towards R.
amounts corresponding to equivalent plant
solani:
powder weight of each plant part. The discs
against R. solani of different concentrations
were then placed onto the growth media
of X. strumarium seed oil obtained by
(PDA) and allowed to stand at room
Soxhlet extraction with n-hexane. The
temperature for the time periods indicated in
inhibition zone of fungal growth decreased
Table 4, before cultures of Rhizoctoniasolani
with
were introduced for the antifungal bioassay.
concentration used to saturate the assay
With the three extracts, fungal growth
discs. The value of MIC lied between 350.0
inhibitory
and 175.0 μg of Xanthium oil / ml.
activity
somewhat
increased
Table 5 shows antifungal activity
decreasing
Xanthium
seed
oil
initially and was maximal in extract-loaded
Partial characterization of the active
discs stored for 48 hours before running the
antifungal ingredients of cocklebur seed
bioassay. This increase could be due to
oil:
increased
antifungal
studies since it was quite active against R.
components of the extracts with incubation
solaniand represented a somewhat more
time. Thereafter, antifungal activity only
homogenous
diffusion
of
the
11
The seed oil was chosen for further
(lipid)
fraction.
Given the fact that many so called
components. These were numbered (I)
‘unusual’ fatty acids such as short chain,
through to (VI), according to increasing Rf
cyclopropanoid and acetylenic fatty acids
value in the TLC solvent system n-hexane:
have
by
acetone (4:1). Bands representing each of
Carballeira, 2008), one might suspect these
these components were scraped, eluted in a
compounds as responsible for the observed
solvent and bioassayed for growth inhibition
antifungal activity of cocklebur seed oil.
of R. solani. Two of the six, designated as
However, GLC analysis (Table 6) revealed
spots II and IV, were active against the
that the oil contained no unusual fatty acids.
growth of R. solani(Table 8 ). The two
Linoleic and oleic acids constituted
over
compounds were subjected to infra-red
90% of cocklebur seed oil fatty acids.
spectroscopic analysis.Thus far we could
Palmitoleic acid, a usual fatty acid, was
only infer that compound II is a long chain
present
alcohol (absorption at 3453 cm-1 due to O-H;
antifungal
in
activity
(review
a relatively large amount,
at 1165 cm-1 due to C-O; relatively intense
however.
Cocklebur seed oil was next separated into
absorption at 2960- 2850 cm-1 and long
two fractions, the free fatty acid (FFA) and
chain methyl rocking at 725 cm-1 ). The
the unsaponifiable matter (UM) fractions, as
presence of a hydrophobic moiety (the long
described under Materials and Methods.
hydrocarbon chain) is consistent with the
Both fractions were bioassayed for their
results observed for increased recovery of
inhibition of the growth of R. solani. Indeed,
antifungal activity from seed, leaf and root
no antifungal activity was detected for the
tissues of xanthium on defatting. Further
FFA fraction and it was associated solely
chemical characterization work is underway.
with the UM fraction (Table 7, Fig. 2).
Subsequently the UM fraction was subjected
to
TLC
analysis
yielding
six
major
12
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