International Biodeterioration & Biodegradation 106 (2016) 157e160

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International Biodeterioration & Biodegradation

journal homepage: www.elsevier.com/locate/ibiod

Short communication

Antifungal activity of monoterpenes against wood white-rot fungi

Zhilin Zhang a, Ting Yang a, b, Na Mi c, Yong Wang a, Guoyuan Li a, Lihua Wang a,
Yongjian Xie c, *
a
Hubei Key Laboratory of Quality Control of Characteristic Fruits and Vegetables, Hubei Engineering University, Xiaogan 432000, Hubei, PR China
b
College of Life Sciences, Hubei University, Wuhan 430062, PR China
c
The Key Laboratory for Quality Improvement of Agricultural Products of Zhejiang Province, School of Agricultural and Food Science, Zhejiang A&F
University, Linan 311300, Zhejiang, PR China

a r t i c l e i n f o a b s t r a c t

Article history: Biodegradation of wood by fungi is a chronic problem for wood utilization. Natural products from plants
Received 15 September 2015 have great potential as novel fungicide sources for controlling wood decay fungi as alternative to syn-
Received in revised form thetic pesticides. Many plant extracts and essential oils contain monoterpenes, sesquiterpenes and
26 October 2015
aliphatic compounds. In the present study, 41 pure monoterpenes were tested for the toxicity against
Accepted 27 October 2015
Available online 8 November 2015
wood white-rot fungi, Trametes hirsuta, Schizphylhls commune, and Pycnoporus sanguineus. Results from
antifungal tests revealed that b-citronellol, geraniol, carvacrol, thymol, eugenol and citral showed good
antifungal activities against the three tested fungi. In addition, the carvacrol was the most toxic
Keywords:
Antifungal
monoterpenes against the three tested fungi, the IC50 values against T. hirsuta, S. commune and
Monoterpenes P. sanguineus were 87.6, 53.6 and 71.7 mg ml
1, respectively. The present results indicated that carvacrol
Wood white-rot fungi have potential to be developed as natural fungicidal agents, suggesting that further study of wood
Trametes hirsuta preservation treatment be warranted.
Schizphylhls commune 2015 Elsevier Ltd. All rights reserved.
Pycnoporus sanguineus

1. Introduction
Biodegradation of wood by fungi is a serious problem in many
tropical and some temperate region of the world, resulting in a
signicant economic and resource losses (Andrew et al., 2001).
White-rot fungi are the only microorganisms that are known to
degrade efciently all the components of wood, including lignin
(Kirk and Farrell, 1987; Shary et al., 2007; Bakar et al., 2013).
Traditionally, preservative treatments to wood are used to be cre-
osote, pentachlorophenol and inorganic arsenicals for addressing
this durability problem (Cheng et al., 2008). However, these pre-
servatives are used in long-term resulting to produce a signicant
problem on human health and environmental pollution. Therefore,
the search for natural, safe and none polluting bioactive chemical
compounds from plants as alternative to synthetic preservative
becomes much essential (Loh et al., 2011; Hu et al., 2015).
Many plant materials are believed to have antifungal properties
and fungicidal properties, and numerous essential oils have been
extensively studied against various fungi species (Cheng et al.,
* Corresponding author. Tel./fax: 86 571 61082619.
E-mail address: yjxie@zafu.edu.cn (Y. Xie).
2006, 2012; Yang and Clausen, 2007; Zabka et al., 2009; Hassiotis
and Dina, 2011; Chen et al., 2013; Jing et al., 2014; Kedia et al.,
rez et al., 2015;
2014; Regnier et al., 2014; Vieira et al., 2014; Jua
Salem et al., 2016). Futhermore, it has been found that the natural
compounds possess the fungicidal activities against wood decay
fungi, among of these natural compounds, eugenol, a-cadinol, T-
muurolol, T-cadinol, g-cadinene, cryptomeridiol, chamaecynone,
cinnamaldehyde and ferruginol were found to be more toxic
(Rudman, 1965; Kondo and Imamura, 1986; Morita et al., 1997;
Chang et al., 1999, 2000; Wang et al., 2005a,b; Wu et al., 2005;
Cheng et al., 2004, 2008; Yen and Chang, 2008). Notoriously,
many plant extracts and essential oils may be as the alternative
sources of fungal control agents because of their rich sources of
bioactive chemicals, including monoterpenes, sesquiterpenes and
aliphatic compounds. Our previous study demonstrated that the 42
evaluated monoterpenes had excellent anti-termitic activity (Xie
et al., 2014). Now we are interesting to know whether these
monoterpenes possess the antifungal property against white-rot
fungi. Therefore, this paper describes a laboratory study to
examine the toxicity of 41 monoterpenes against the three white-
rot fungi, Trametes hirsuta, Schizphylhls commune, and Pycnoporus
sanguineus.

http://dx.doi.org/10.1016/j.ibiod.2015.10.018
0964-8305/ 2015 Elsevier Ltd. All rights reserved.
158 Z. Zhang et al. / International Biodeterioration & Biodegradation 106 (2016) 157e160
2. Materials and methods
2.1. Chemicals
Forty-one monoterpenes, (
)-a-pinene (1), (
)-b-pinene (2), r-
cymene (3), 3-carene (4), g-terpinene (9), terpinolene (10), b-cit-
ronellene (11), eugenol (23), (
)-verbenone (29), ()-citronellal
(34) were purchased from SigmaeAldrich chemical Co. (Shanghai,
China). ()-camphene (5), ()-limonene (6), myrcene (7), a-terpi-
nene (8), a-terpineol (12), ()-terpinen-4-ol (13), ()-menthol (14),
isopulegol (15), (
)-borneol (16), nerol (17), linalool (18), dihy-
drolinalool (19), b-citronellol (20), geraniol (21), 3,7-dimethyl-1-
octanol (22), thymol (24), carvacrol (25), isoeugenol (26),
()-camphor (27), (
)-fenchone (28), ()-pulegone (30), (
)-car-
vone (31), (
)-menthone (32), citral (33), cuminaldehyde (35),
bornyl acetate (36), linalyl acetate (37), terpinyl acetate (38), neryl
acetate (39), citronellyl acetate (40), geranyl acetate (41) were
purchased from Tokyo chemical Industry Co., Ltd. (Shanghai,
China).
2.2. Fungi
Three white-rot fungi (T. hirsuta, S. commune, and P. sanguineus)
were obtained from the college of life science, Hubei Engineering
University and used in antifungal experiments.
2.3. Antifungal assays
The method of Chang et al. (1999) was employed for antifungal
evaluation of 41 monoterpenes. Briey, 400, 200, 100 and
50 mg ml
1 of compounds were added to sterilize potato dextrose
agar (PDA) in 9 cm Petri dishes. Fungicide stock solutions were
prepared at a standard concentration of 100 mg ml
1 in analytical-
grade acetone. For liquid monoterpenes compounds, directly took a
certain amount for experimental study. Antifungal assays were
performed three times. After fungal mycelia reached the edges of
control plates (without adding compounds) by incubating at
26 1  C for ca. 7 d, the antifungal index was calculated as follows:
Antifungal index (%) (1
Da/Db)  100 where, Da the diameter
of growth zone in the experimental plate (cm), Db the diameter of
growth zone in the control plate (cm).
2.4. Statistical analyses
All results were obtained from three independent experiments
and expressed as mean SD (n 3). Signicant differences
(P < 0.05) were determined by using the Scheffe's test.
3. Results and discussion
Fig. 1 presents the results of antifungal activity of these com-
pounds against white-rot fungus T. hirsuta, S. commune, and
P. sanguineus at the concentration of 400 mg ml
1. Results from
antifungal tests revealed that compounds 17, 20e21, 23e25 and 33
were the most active against T. hirsuta amongst the 41 tested
compounds, with antifungal indices higher than 81.8%; while other
compounds were the lower active, with antifungal indices lower
than 53.7%. Similarly, compounds 17, 20e21, 23e26 and 33 also
exhibited strong antifungal action with antifungal indices higher
than 66.3% against S. commune at the concentration of 400 mg ml
1,
while other compounds did not express antifungal activities at the
same concentration, with antifungal indices lower than 44.8%. In
addition, compounds 17, 20, 22, 23e26 and 33 exhibited strong
antifungal action with antifungal indices higher than 63.5% against
P. sanguineus at the concentration of 400 mg ml
1, while other
compounds did not express antifungal activities at the same con-
centration, with antifungal indices lower than 53.3%. It was noticed
that compounds 23e25 and 33 exhibited the strongest activity
against T. hirsuta, S. commune, and P. sanguineus.
The IC50 values of the 9 compounds were determined in Table 1.
In terms of the IC50 values, the antifungal activity of compounds 17,
20e21, 23e25 and 33 against T. hirsuta is ranked as eugenol (23)
(85.1 mg ml
1) > carvacrol (25) (87.6 mg ml
1) > thymol (24)
(139.0 mg ml
1) > nerol (17) (166.3 mg ml
1) > citral (33)
(184.5 mg ml
1) > geraniol (21) (189.3 mg ml
1) > b-citronellol (20)
(266.4 mg ml
1). On the other hand, the order of IC50 values against
S. commune are carvacrol (25) (53.6 mg ml
1) > thymol (24)
(67.1 mg ml
1) > eugenol (23) (122.2 mg ml
1) > isoeugenol (26)
(132.0 mg ml
1) > citral (33) (207.5 mg ml
1) > b-citronellol (20)
(219.5 mg ml
1) > geraniol (21) (224.4 mg ml
1) > nerol (17)
(337.6 mg ml
1). In addition, the IC50 values against P. sanguineus are
carvacrol (25) (71.7 mg ml
1) > thymol (24) (116.8 mg ml
1) > eugenol
(23) (137.7 mg ml
1) > citral (33) (178.5 mg ml
1) > b-citronellol (20)
(190.2 mg ml
1) > 3,7-dimethyl-1-octanol (22) (221.5 mg ml
1) >
nerol (17) (242.7 mg ml
1) > isoeugenol (26) (247.1 mg ml
1) > ge-
raniol (21) (367.6 mg ml
1).
In this study, we found carvacrol was the most toxic mono-
terpenes against the three tested fungi, the IC50 values of carvacrol
against T. hirsuta, S. commune and P. sanguineus were 87.6, 53.6 and
71.7 mg ml
1, respectively. As for IC50, the similar results were found
in earlier literature, such as that the IC50 values of T-muurolol
against Laetiporus sulphureus, Lenzites betulina, Trametes versicolor
and Pcynoporus coccineus were 93.3, 74.1, 81.0 and 57.3 mg ml
1,
respectively (Cheng et al., 2004). Cheng et al. (2008) had proven
that cinnamaldehyde was a strong antifungal agent against
L. betulina and L. sulphureus with the IC50 values of 58.9 and
35.3 mg ml
1, respectively, and these observations were in accor-
dance with the results reported previously (Wang et al., 2005a; Hsu
et al., 2007; Yen and Chang, 2008). On the other hand, Cheng et al.
(2004) reported that the IC50 values of a-cadinol against
L. sulphureus, L. betulina, and T. versicolor were 9.9, 28.6, and
30.4 mg ml
1, respectively. These results show that carvacrol is a
potential compound for the development of fungicides in the near
future.
In our study, eugenol exhibited good antifungal activities
against the three tested fungi, the IC50 values of eugenol against
T. hirsuta, S. commune and P. sanguineus were 85.1, 122.2 and
137.7 mg ml
1, respectively. Comparing our results with those re-
ported earlier in the literature, Cheng et al. (2008) stated that the
IC50 values of eugenol against L. betulina and L. sulphureus were
36.9 mg ml
1 and 62.9 mg ml
1, respectively. Similar results were
also obtained by Wang et al. (2005a) and Yen and Chang (2008).
These results suggested that the susceptibility of the same com-
pounds to different fungi species varies considerably.
In the present study, we found that the antifungal activity of
oxygenated monoterpenes was higher than that of monoterpene
hydrocarbons against white-rot fungi. Relatively lower toxicity of
monoterpene hydrocarbons can be attributed to their higher
evaporation rate as compared with oxygenated monoterpenes. A
similar observation was also noted in previous studies on the
insecticidal property (Regnault-Roger and Hamraoui, 1995;
Abdelgaleil, 2010; Xie et al., 2014). At the same time, a different
nding was also observed in the other bioactivity assays. Kordali
et al. (2006) showed that oxygenated monoterpenes were less
toxic than monoterpene hydrocarbons against the larvae of Lep-
tinotarsa decemlineata. In addition, phenolic compounds showed
strongest antifungal activities against white-rot fungi, i.e. carvacrol,
thymol and eugenol possesses much stronger antifungal activity,
and carvacrol was more effective than thymol. Similarly, it has been
found that carvacrol as fumigants were more effective than thymol
 Z. Zhang et al. / International Biodeterioration & Biodegradation 106 (2016) 157e160 159

Fig. 1. Antifungal activities of the 41 monoterpenes (A: Hydrocarbons; B: Alcohols; C: Phenols; D: Ketones; E: Aldehydes; F: Acetates) against white-rot fungus T. hirsuta, S. commune
and P. sanguineus at the concentration 400 mg ml
1. Bars with different letters are statistically different at p < 0.05 according to the Scheffe's test.

Table 1 insecticidal and fungicidal activities (Wen et al., 2003; Percival

IC50 values (mg ml
1) of 9 compounds against white-rot fungus T. hirsuta, S. commune et al., 1999; Prats et al., 2007; Maddox et al., 2010; Chen et al., 2013).
and P. sanguineus.

Compounds Fungi
4. Conclusions
T. hirsuta S. commune P. sanguineus

17 166.3 337.6 242.7 From the results of our present study, carvacrol, thymol, eugenol
20 266.4 219.5 190.2 and citral showed good antifungal activities against the three tested
21 189.3 224.4 367.6
22 >400 >400 221.5
fungi. Thus, carvacrol, thymol, eugenol and citral have potential to
23 85.1 122.2 137.7 be developed as natural fungicidal agents. In our previous study, we
24 139.0 67.1 116.8 also found that these compounds were the most toxic mono-
25 87.6 53.6 71.7 terpenes to R. chinensis (Xie et al., 2014). Therefore, carvacrol,
26 >400 132.0 247.1
thymol, eugenol and citral could be used for wood preservative as
33 184.5 207.5 178.5
alternative to synthetic preservative. However, further systematic
investigation on the antifungal activity of monoterpenes against
white-rot fungi on wood, and against brown-rot fungi are needed
to be done. Moreover, these results could be useful in the research
against Lycoriella ing enue (Park et al., 2008) and Reticulitermes
for selecting the plant essential oils, containing the high content of
chinensis (Xie et al., 2014). These results indicated that the position
these compounds can be used as new fungicide.
of the hydroxyl group plays an important role in the insecticidal
activity. Previously, eugenol has been reported to possess anti-
termitic and antifugal activity (Wang et al., 2005a; Cheng et al., Acknowledgments
2006; Pandey et al., 2012; Xie et al., 2014). Phenolic compounds
are widely distributed in plants and have been showed good The authors would like to thanks the Natural Science
160 Z. Zhang et al. / International Biodeterioration & Biodegradation 106 (2016) 157e160
Foundation of Hubei Province (No. 2014CFB571) and Zhejiang A&F
University research fund for nancial supports (No. 2013FK008,
2014FR009).
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