Volume 7 Number 1 (February 2015) 31-37

Comparison of antifungal activities of various essential oils on the

ORIGINAL ARTICLE
Phytophthora drechsleri, the causal agent of fruit decay

Ali Mohammadi1, Maryam Hashemi2*, Seyed Masoud Hosseini**

1
Department of Microbiology, Faculty of Biological Sciences, Shahid Beheshti University, Tehran, Iran.
2
Microbial Biotechnology and Biosafety Department, Agricultural Biotechnology
Research Institute of Iran (ABRII), Karaj, Iran.

Received: October 2014, Accepted: January 2015

ABSTRACT

Background and Objectives: The efficacy of Mentha piperita L, Zataria multiflora Boiss and Thymus vulgaris L essential
oils (EOs) was evaluated for controlling the growth of Phytophthora drechsleri, the causative agent of damage to many crops
that is consumed directly by humans.
Materials and Methods: The EOs used in this study was purchased from Magnolia Co, Iran. The pour plate method in
petri dishes containing Potato Dextrose Agar (PDA) was used to evaluate the antifungal properties of EOs. The minimal
inhibitory concentrations (MIC), minimum fungicidal concentration (MFC) as well as mycelial growth inhibition (MGI)
were measured. The IC50 value (the concentration inhibited 50% of the mycelium growth) was calculated by probit analysis.
Results and Conclusion: The fungal growth was significantly reduced by increasing concentrations of tested EOs. The
complete reduction was obtained with Shirazi thyme at all concentrations, whereas the complete reduction for peppermint
and thyme was observed at 0.4% and 0.8% (v/v) concentrations, respectively. Meanwhile, the minimum inhibition was
observed when 0.1% peppermint (MGI values of 9.37%) was used. The IC50, MIC and MFC values of Shirazi thyme was
0.053, 0.1% and 0.2%, respectively. Similarly, MIC and MFC values of peppermint and thyme were recorded 0.4% and
0.8%, respectively. The results obtained from this study may contribute to the development of new antifungal agents to
protect the crops from this pathogenic fungus and many agricultural plant pathogens causing drastic crop losses.

Keywords: Mentha piperita, Zataria multiflora, Thymus vulgaris; Essential oil, Antifungal, Phytophthora drechsleri

INTRODUCTION

*
Corresponding author: Seyed Masoud Hosseini ph.D Fungal infections are very important in the
Address: Department of Microbial Biotechnology & agricultural economy due to the potential of causing
Biosafety, Agricultural Biotechnology Research Institute extensive damage to agricultural crops during
of Iran (ABRII), Karaj, Iran. storage, transport and cause significant economic
Tel: +98 21 32703536 losses in the commercialization phase (1, 2). The pre-
fax: +98 26 32704539. and postharvest losses in world crops due to fungal
E-mail: [email protected] disease may amount to more than 12% in developing
countries (3). Among post-harvest fungal pathogens,
**
Corresponding author: Maryam Hashemi Phytophthora is one of the common plant-damaging
Address: Department of Microbiology, Faculty of Biological agent (water molds), whose species have caused great
Sciences, Shahid Beheshti University, Tehran, Iran. economic losses to crops, natural vegetation and
Tel: +98 21 29902721 forestry worldwide (4).
Fax: +98 21 22736044 Multiple species of Phytophthora are known
E-mail: [email protected] to cause problems in agricultural production, that

31
Hosseini ET AL .

among them, P. drechsleri is very important because used in this study were purchased from Magnolia Co,
a wide host range of herbal and woody plants from IRAN. EOs quality parameters such as odor, color,
non-specific to highly specific (5). This oomycete appearance, purity, solubility and also chemical
pathogen causing damping off, gummosis and root rot properties including pH, acidity and brix were
in pistachio orchards and many vegetable crops in the described in an accompanying technical report.
Cucurbitaceae and Solanaceae (6, 7). For example,
gummosis is the most important disease of pistachio Microbial strain and culture media. The fungal
trees in Iranian pistachio orchards that cause with P. strain used was P. drechsleri, IRAN 1156C that
drechsleri. This soil borne disease affects the crowns obtained from the Iranian Research Institute of
and roots of the trees, causing average tree mortality Plant Protection (IRIPP). The fungi cultures were
of 1012% or greater (8). Moreover, the crown and maintained and grown on PDA slants at 25 C for 5
root rot of cucumber is one of the most important days. Cultures were stored at 4 C and subcultured
diseases on greenhouse cucumber in Iran caused by once a month.
P. drechsleri (9). First report of crown and root rot of
cucumber occurred in 1937 that Approximately 2.3 Antifungal assays. Antifungal assays of Shirazi
hectares of cucumber fields in the United States were thyme, peppermint and thyme EOs were performed
destroyed 100% (10). with the pour plate method as described by Askarne et
Over the past years, a variety of different synthetic al., (2012) (16). In this method, the agar plates were
chemicals such as mefenoxam (7), phosphite (11), prepared using PDA (15 ml per Petri dish) amended
bordeaux mixture, phenylamides (acylanilides) with various concentrations of EOs 0.1- 0.8% (v/v).
group includes furalaxyl (fongarid), metalaxyl For enhancing the oil solubility, Tween-80, 0.5%
(ridomil) and benalaxyl (galben) (7, 12) have been (v/v) was added. After inoculating the mycelia of
used as antifungal agents to inhibit the growth of fungus onto the center of agar, the dishes were
this pathogenic fungus. However, continuous use of incubated at 25 2C until the growth of the control
fungicides has faced two major obstacles; increasing dishes (without the EOs) had reached the edge of the
public concern regarding contamination of fruits and plate. Then, the mycelial growth inhibition (MGI)
vegetables with fungicidal residues, and proliferation percentage was calculated as follows:
of resistance in the pathogen populations (13). In this MGI = (dc-dt)/dc 100
regard, the use of plant-based essential oils (EOs) Where dc is colony diameter of control sets and
and extracts, which may be less damaging for pest dt is colony diameter measured in treatment sets (17,
and disease control, could be a useful alternative to 18). The IC50 values (the concentration inhibited 50%
synthetic fungicides in the management of rot fungi of the mycelium growth) were calculated by probit
during postharvest handling of fruit and vegetables (2). analysis. Minimal inhibitory concentrations (MICs)
The antifungal activity of EOs and plant extracts and minimum fungicidal concentrations (MFCs)
against a number of plant pathogens such as soil- were also examined using the methods reported by
born fungi, food and grain storage fungi and foliar Yen and Chang (2008). When the mycelium of fungi
pathogens has been reported (14, 15). reached the edges of the control dishes, the lowest
Despite these natural products potentially great concentration with no sign of growth was defined as
importance, there are little research has focused MIC. After the MIC was determined, a small piece
specifically on the effects of Iranian medicinal of agar (2 2 2 mm3) was taken from the colony of
plants EOs on P. drechsleri. The objective of the the MIC plate, and was inoculated on a drug-free PDA
present study was to evaluate the in vitro activity of medium. After 5 days, MFCs were determined by the
Shirazi thyme (Zataria multiflora Boiss), peppermint lowest concentration of the test compounds in which
(Mentha piperita L) and thyme (Thymus vulgaris L.) no recovery of microorganism was observed (19).
essential oils against P. drechsleri.
Statistical analysis. Data on effects of the extracts
MATERIALS AND METHODS on the growth of pathogens was analyzed by one-
way analysis of variance and comparison of means
Essential oil. Essential oils (Mentha piperita L, using the Duncans Multiple Range Test at the level
Zataria multiflora Boiss and Thymus vulgaris L) P < 0.05. The statistical analysis was performed

32 IRAN. J. MICROBIOL. Volume 7 Number 1 (February 2015) 31-37 http://ijm.tums.ac.ir

 antifungal activities of essential oils on Phytophthora drechsleri

Table 1. The effects of different concentrations of peppermint, Shirazi thyme and thyme essential oils on mycelial growth
of P. drechsleri

Concentration Mycelial Growth Diameter (mm)

(%) (v/v) 24h 48h 72h 96h 120h 144h 168h

Peppermint

0.1 13.67 2.12a 20.33 1.41a 26.67 2.12a 32.67 2.83 a 38.33 2.12a 44.00 0.71 a 48.33 0.71 a

0.2 0.00 0.00b 0.00 0.00b 0.00 0.00b 11.33 2.12b 13.67 4.95b 17.33 4.25b 21.67 4.95b

0.4 0.00 0.00b 0.00 0.00b 0.00 0.00b 0.00 0.00c 0.00 0.00c 0.00 0.00c 0.00 0.00c

0.8 0.00 0.00b 0.00 0.00b 0.00 0.00b 0.00 0.00c 0.00 0.00c 0.00 0.00c 0.00 0.00c

Shirazi thyme

0.1 0.00 0.00b 0.00 0.00b 0.00 0.00b 0.00 0.00c 0.00 0.00c 0.00 0.00c 0.00 0.00c

0.2 0.00 0.00b 0.00 0.00b 0.00 0.00b 0.00 0.00c 0.00 0.00c 0.00 0.00c 0.00 0.00c

0.4 0.00 0.00b 0.00 0.00b 0.00 0.00b 0.00 0.00c 0.00 0.00c 0.00 0.00c 0.00 0.00c

0.8 0.00 0.00b 0.00 0.00b 0.00 0.00b 0.00 0.00c 0.00 0.00c 0.00 0.00c 0.00 0.00c

Thyme

0.1 12.33 0.71c 17.33 2.12c 22.37 3.54c 29.00 6.36d 32.00 7.07d 36.67 8.49d 41.00 9.90d

0.2 0.00 0.00b 0.00 0.00b 9.33 0.71d 9.33 3.67b 10.67 4.08b 10.67 4.9e 11.00 5.72e

0.4 0.00 0.00b 0.00 0.00b 0.00 0.00b 0.00 0.00c 0.00 0.00c 0.00 0.00c 0.00 0.00c

0.8 0.00 0.00b 0.00 0.00b 0.00 0.00b 0.00 0.00c 0.00 0.00c 0.00 0.00c 0.00 0.00c

Control 16.67 1.15d 23.33 2.08d 29.67 3.21e 36.00 4.00e 42.00 3.61a 46.67 3.51a 53.33 2.89f

The results are means standard errors of four replications. Means within a column indicated by the same letter were not
significantly different according to Duncans multiple range tests at the level P < 0.05.

using statistical package for the social sciences 15.0 the minimum activity was recorded for peppermint
software for Windows (SPSS Inc., Chicago, IL, USA) EOs. By increasing the oil concentration from 0.1%
to 0.8%, antifungal activity of peppermint and thyme
RESULTS were substantially increased (Fig. 1). Peppermint
and thyme at 0.4% and 0.8% concentration showed
The results of inhibitory effects of EOs on mycelial complete (100%) antifungal effect while other
growth of the fungus and MGI values are presented concentrations (0.2% and 0.1%) were only prevented
in Tables 1 and 2. The inhibitory eff e cts of EOs in percentage of growth by Phytophthora, with MGI
pour plate method showed that Shirazi thyme, thyme values of 9.37% and 59.38% for peppermint and
and peppermint were effective in prev e nting P. 23.13% and 79.38% for thyme, respectively (Figs.
drechsleri growth at different concen t rations (Figs. 3 & 4). The maximum and minimum fungal growth
1-3). By increasing concentration from 0.1 to 0.8% at concentration 0.1% was recorded by peppermint
(v/v), antifungal activity of these E O s increased (4.83 mm) and Shirazi thyme (0 mm), respectively.
substantially. The comparison between tested EOs was
According to the results reported in Table 2, the further confirmed by comparing their effective
Shirazi thyme was the most effective essential oil concentrations, MIC and MFC values that shown in
on the P. drechsleri because caused 100% growth Table 3. The values of IC50, MIC and MFC for Shirazi
inhibition at all concentrations tested (Fig. 2). Also thyme were 0.053%, 0.1% and 0.2%, respectively,

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 Hosseini ET AL .

which were significantly lower than those of thyme

and peppermint (p 0.05). The results, as seen in
a b Table 3, showed that the least effect was also observed
for peppermint with significantly higher values of
IC50 (0.186%), MIC (0.4%) and MFC (0.8%) than
that of Shirazi thyme. While, the mentioned values
b
a of peppermint were no different to values of thyme
(p 0.05).
d c

b
DISCUSSION
a

129 d c In recent years, increased interest has been generated

Fig.1. Radial growth of P. drechsleri mycelium treated with in the development of healthy and natural antifungal
Shirazi thyme EOs at 0.1% to 0.8% (v/v) concentrations.(a)
agents such as plant-based essential oils and extracts
0.1% (b) 0.2% (c) 0.4% (d) 0.8% (v/v) after 7 days at 25 C.
129 to control phytopathogens in agriculture (20). In
ad c
this study, we investigated the antifungal effects of
b
three essential oils including peppermint, thyme and
Shirazi thyme on the major agricultural pathogen (P.
129 drechsleri) and determined their mycelial growth
a
b inhibition rate, minimum inhibitory concentration
and minimum fungicidal concentration. Our results
c showed that the essential oils from Shirazi thyme and
d
a
b
thyme have more acceptable antifungal properties on
P. drechsleri than peppermint in vitro. The efficacy
of these EOs was positively correlated with the
130 d
c
concentration and by increasing concentrations from
0.1% to 0.8% in EOs, antifungal activity increased
substantially (Tables 1 and 2).
130 d
c Antifungal activities of Shirazi thyme and thyme
Fig.a 2. Radial growth of P. drechsleri mycelium treated found in this study are consistent with several reports
b
with thyme at 0.1% to 0.8% (v/v) concentrations.(a) 0.1% of these oils against various plant pathogenic fungi
(b) 0.2% (c) 0.4% (d) 0.8% (v/v) after 7 days at 25 C. (21, 22). These activities can be attributed to the
130
presence of various constituents such as thymol and
a
b carvacrol. It has been accepted that the anti-microbial
activity of Shirazi thyme and thyme is related to
d c
high percentage of thymol and carvacrol which are
a
b well-known antifungal agents (23-25). Furthermore,
both EOs contained -terpinene and p-cymene with
131 antimicrobial activities, which are biochemical
d c precursors of thymol and carvacrol in the phenols
biosynthetic pathway (24, 26). Specific studies
have linked these compounds to antifungal activities
131 d 7 c against Phytophthora. Camele et al. (2012) reported
that the essential oil of three Mediterranean aromatic
plants (Verbena officinalis, Thymus vulgaris and
131 Origanum vulgare) consists mainly of carvacrol and
7
Fig. 3. Radial growth of P. drechsleri mycelium treated thymol as main constituents, and exhibited a complete
with peppermint at 0.1% to 0.8% (v/v) concentrations.(a)
mycelial inhibition effect on the Phytophthora
0.1% (b) 0.2% (c) 0.4% (d) 0.8% (v/v) after 7 days at 25 C.
citrophthora (27). Kim et al. (2008) reported that
7
the essential oil of thyme (Thymus vulgaris) consists

34 IRAN. J. MICROBIOL. Volume 7 Number 1 (February 2015) 31-37 http://ijm.tums.ac.ir

 antifungal activities of essential oils on Phytophthora drechsleri

Table 2. Antifungal activity of various concentrations of EOs against P. drechsleri.

Essential oils Concentration (%) (v/v) Mycelial Growth Diameter (cm) MGI%

0.1 4.83 0.07 a 9.37 a

0.2 2.17 0.49 b 59.38 b

Peppermint
0.4 0.00 0.00 c 100.00 c

0.8 0.00 0.00 c 100.00 c

0.1 0.00 0.00 c 100.00 c

0.2 0.00 0.00 c 100.00 c

Shirazi thyme
0.4 0.00 0.00 c 100.00 c

0.8 0.00 0.00 c 100.00 c

0.1 4.10 0.99 d 23.13 d

0.2 1.10 0.57 e 79.38 e

Thyme
0.4 0.00 0.00 c 100.00 c

0.8 0.00 0.00 c 100.00 c

The results are means standard errors of four replications. Means within a column indicated by the same letter were not
significantly different according to Duncans multiple range tests at the level P < 0.05.

mainly of carvacrol and thymol as major components, et al. (1996) hypothesized that the antifungal activity
and exhibited a complete mycelial inhibition effect of Shirazi thyme and thyme oils might be due to
on the growth of P. cactorum (21).In another studies, the fact that carvacrol and thymol disintegrated
thymol and carvacrol were again reported to show the fungal hyphae which appeared emptied of their
complete inhibition of P. capsici (28, 29). Moreover, cytoplasmic content (33). Moreover, several studies
recently, Sokovi et al (2009) reported a relationship have demonstrated that terpenes (i.e. thymol and
between the high activity of some Thymus oils and carvacrol) which are the major components of EOs,
the presence of phenol components, such as thymol alter cell permeability by penetrating between the fatty
and carvacrol (30). acyl chains making up the membrane lipid bilayers,
Studies suggested that the antifungal activity disrupting lipid packing and changing membrane
resulted from a direct effect of essential oil on fungal fluidity (34, 35). Braga and Dal Sasso (2005) showed
mycelium and postulated that the lipophilic nature that these phenomena led to major surface alterations
of EOs was as possible for them being absorbed by and morphological modifications, also reducing the
fungal mycelia (31, 32). In this regard, Zambonelli adherence capacity of plant pathogenic fungi (34). In

Table 3. MIC, MFC and IC50 values of test compounds against P. drechsleri.

Compounds IC50 (%) MIC (%) MFC (%)

Peppermint 0.186 a 0.4 a 0.8 a

Shirazi thyme 0.053 b 0.1 b 0.2 b

Thyme 0.147 c 0.4 a 0.8 a

MIC, minimum inhibitory concentration; MFC, minimum fungicidal concentration; IC50, median inhibition concentration
Within the column, mean values followed by the same letter are not significantly different according to Duncans multiple
range test at the level P < 0.05.

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Hosseini ET AL .

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