Fungal Ecology 33 (2018) 115e121

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Fungal Ecology
journal homepage: www.elsevier.com/locate/funeco

Short Communication

Shared weapons in fungus-fungus and fungus-plant interactions?

Volatile organic compounds of plant or fungal origin exert direct
antifungal activity in vitro
Elizabeth Quintana-Rodriguez a, 3, L.Enrique Rivera-Macias a, 4,
Rosa M. Adame-Alvarez a, 2, Jorge Molina Torres b, 5, Martin Heil a, *, 1, 6
a
Departamento de Ingeniería Gen

etica, CINVESTAV-Irapuato, Irapuato, Guanajuato, Mexico
b
Departamento de Biotecnología y Bioquímica, CINVESTAV-Irapuato, Irapuato, Guanajuato, Mexico

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

Article history: Fungi emit a diverse blend of volatile organic compounds (VOCs) that mediate multiple fungus-fungus
Received 14 May 2017 interactions. Plants emit VOCs as well, which can serve as resistance-inducing signals but might also
Received in revised form act as direct resistance agents. We screened 22 VOCs that are emitted from infected plants for putative
20 January 2018
inhibitory effects on three fungal phytopathogens: Colletotrichum lindemuthianum, Fusarium oxysporum
Accepted 28 February 2018
and Botrytis cinerea. The growth of all three fungi was significantly inhibited when the mycelia were
exposed to an atmosphere containing nonanal, (þ)-carvone, citral, trans-2-decenal, L-linalool, or ner-
Corresponding Editor: John Dighton olidol. Eugenol completely inhibited the growth of all three fungi, and 1-octen-3-ol, nonanal, 2,6-
dimethyl-2,4,6-octatriene, citral, a-terpineol and trans-2-decanal inhibited at least one fungus
Keywords: completely. Most of these VOCs are also emitted from fungi. We conclude that antagonistic fungus-
Antifungal effects fungus and plant-fungus interactions might share common mechanisms and that plant VOCs can
Plant-fungus interaction function as resistance agents that fungal pathogens must overcome for successful infection.
Plant resistance © 2018 Elsevier Ltd and British Mycological Society. All rights reserved.
VOCs
Volatiles
Phytopathogen

Fungi emit a diverse array of volatile organic compounds
(VOCs): low-weight, lipophilic molecules that play multiple roles in
fungus-fungus or fungus-plant interactions (Bennett and Inamdar,
2015; El Ariebi et al., 2016). On the one hand, fungal VOCs serve
as 'chemical weapons' in antagonistic fungus-fungus interactions
(Bennett and Inamdar, 2015). On the other hand, multiple fungi
colonize plants (Partida-Martinez and Heil, 2011), and VOC-
mediated growth promotion effects have been reported for
various fungal species, particularly in the genus Trichoderma (Hung
et al., 2013; Lee et al., 2016; Li et al., 2016). However, plants emit
* Corresponding author. Departamento de Ingeniería Gene
tica, Km 9.6 Libra-
miento Norte, Irapuato, Guanajuato 35821, Mexico.
E-mail address: mheil@ira.cinvestav.mx (M. Heil).
1
www.ira.cinvestav.mx/Dr.MartinHeil.aspx
2
www.facebook.com/plantecology/
3
www.researchgate.net/profile/Elizabeth_Quintana-Rodriguez2
4
www.researchgate.net/profile/Luis_Rivera_Macias
5
www.researchgate.net/profile/Jorge_Molina-Torres
6
www.researchgate.net/profile/MartinHeil_2
VOCs as well, for example in response to infection, and several of
these compounds act as signals and trigger the expression of plant
resistance genes (Scala et al., 2013; Heil, 2014). For example,
nonanal and methyl salicylate primed pathogenesis-related (PR)
genes in common bean (Phaseolus vulgaris) and lima bean
(Phaseolus lunatus) (Yi et al., 2009; Quintana-Rodriguez et al., 2015),
and the exposure to (S)-() limonene, L-linalool, nonanal, methyl
salicylate, or methyl jasmonate, induced resistance in P. vulgaris to
the fungal pathogen, Colletotrichum lindemuthianum. Interestingly,
the same compounds inhibited the growth of the fungus in vitro
(Quintana-Rodriguez et al., 2015), thereby supporting theoretical
predictions that a direct defensive function of a compound should
precede its signalling function in evolutionary trajectories (Maag
et al., 2015; Veyrat et al., 2016).
However, the effects of plant-derived VOCs on fungi range from
inhibition to promotion. Trans-2-hexenal inhibited the conidial
germination of Monilinia laxa (Neri et al., 2007) and citral inhibited
the growth of Botrytis cinerea, Trichoderma viride and Penicillium
digitatum (Simas et al., 2017). By contrast, Uromyces fabae stimu-
lated volatile emissions from its host plant and among the emitted

https://doi.org/10.1016/j.funeco.2018.02.005
1754-5048/© 2018 Elsevier Ltd and British Mycological Society. All rights reserved.
Table 1

116
Volatile organic compounds of fungal or plant origin with inhibitory effects on fungi.

Compound CAS Nr. Structure Fungus inhibiteda Fungi and plants as source

Fungal source Reference Plant source Reference

Ethanol 64-17-5 F Trichoderma sp., Tuber sp., Hung et al. (2013); Ebert
common in yeasts et al. (2016) Lee et al.
(2016); Li et al. (2016)
trans-2-Hexen-1-al 6728-26-3 B Arabidopsis thaliana Matsui et al. (2012)
infected with Botrytis
cinerea
cis-2-Hexen-1-ol 928-94-9 F,B P. vulgaris infected with Croft et al. (1993)
Pseudomonas syringae

1-Octen-3-ol 3391-86-4 F,B “Possibly the most Müller et al. (2013); Li et al. P. vulgaris infected with Quintana-Rodriguez et al.
widespread fatty acid (2016); Dickschat (2017) C. lindemuthianum (2015)
derived fungal volatile”

a-Terpinene 99-86-5 F,B “Emitted from fungi” Schmidt et al. (2016) Tomato infected with Fereres et al. (2016)

E. Quintana-Rodriguez et al. / Fungal Ecology 33 (2018) 115e121

Tomato severe rugose virus

() b-Pinene 18172-67-3 F,B Trichoderma sp. Lee et al. (2016) P. vulgaris infected with Quintana-Rodriguez et al.
C. lindemuthianum (2015)

(S)-()-Limonene 5989-54-8 C 'Limonene': Trichoderma Hung et al. (2013); El Ariebi P. vulgaris infected with Quintana-Rodriguez et al.
sp., interacting fungi et al. (2016); Lee et al. C. lindemuthianum (2015)
(2016)

2,6 e Dimethyl e 2,4,6 673-84-7 B P. vulgaris infected with Quintana-Rodriguez

C. lindemuthianum (unpubl.)
e octatriene

cis-3-Hexenyl acetate 3681-71-8 F P. lunatus (md or colonized Navarro-Melendez and Heil

with EF) (2014)

Nonanal 124-19-6 C,F,B Trichoderma sp. Hung et al. (2013); Lee et al. P. vulgaris infected with Yi et al. (2009); Quintana-
(2016) C. lindemuthianum, P. Rodriguez et al. (2015)
lunatus treated with BTH
(þ)- Carvone 2244-16-8 C,F,B Brassica oleracea treated Bruinsma et al. (2009);
with jasmonic acid, Cucumis Kappers et al. (2010)
sativus infested with spider
mite
Methyl salicylate 119-36-8 F,B Trichoderma sp.; Lee et al. (2016); Azeem P. vulgaris infected with Quintana-Rodriguez et al.
Debaryomyces hansenii et al. (2015) C. lindemuthianum, P. (2015)
lunatus treated with BTH

()-trans- Pinocarveol 547-61-5 B P. vulgaris infected with Croft et al. (1993)

Pseudomonas syringae

Citral 5392-40-5 C,F,B P. vulgaris infected with Quintana-Rodriguez

(3,7-dimethyl-2,6- F. oxysporum (unpubl.)
octadienal; mixture
of E- and Z-
stereoisomer)
a-Terpineol 98-55-5 F Common in yeasts Ebert et al. (2016) P. vulgaris infected with Yi et al. (2009); Quintana-
C. lindemuthianum Rodriguez et al. (2015)

E. Quintana-Rodriguez et al. / Fungal Ecology 33 (2018) 115e121

trans-2-Decenal 3913-81-3 C,F,B P. vulgaris infected with Quintana-Rodriguez
C. lindemuthianum (unpubl.)

L-Linalool 126-91-0 C,F,B 'Linalool': Saccharomyces Müller et al. (2013); Ebert P. vulgaris infected with Navarro-Mele
ndez and Heil
spp. and various other fungi et al. (2016) C. lindemuthianum; P. (2014); Quintana-
(e.g., Trichoderma spp.) lunatus (md or colonized Rodriguez et al. (2015)
with EF)
Eugenol 97-53-0 C,F,B P. lunatus (md or colonized
ndez and Heil
Navarro-Mele
with EF) (2014)

(þ)-Aromandendrene 489-39-4 B Trichoderma sp.; common Macias-Rubalcava et al. P. vulgaris infected with Quintana-Rodriguez
in EF, e.g., Muscodor (2010); Hung et al. (2013); C. lindemuthianum (unpubl.)
yucatanensis Kanchiswamy et al. (2015)

b-Caryophyllene 87-44-5 B Common in fungi, emitted Morath et al. (2012); Müller P. vulgaris infected with Quintana-Rodriguez
by various EM fungi and et al. (2013); Kanchiswamy C. lindemuthianum (unpubl.)
Fusarium oxysporum et al. (2015); El Ariebi et al.
(2016)

Farnesene 502-61-4 B 'a-Farnesene': Trichoderma Hung et al. (2013); Müller P. vulgaris infected with Quintana-Rodriguez et al.
(mixture of isomers) sp., 'Farnesene': common in et al. (2013); Kanchiswamy C. lindemuthianum (2015)
fungi and emitted by et al. (2015); Lee et al.
Trichoderma sp., trans-b- (2016)
farnesene: various fungi
Nerolidol 7212-44-4 C,F,B Emitted from various fungi Müller et al. (2013) P. vulgaris infected with Quintana-Rodriguez
(mixture of cis- and F. oxysporum (unpubl.)
trans-stereoisomers)

(continued on next page)

117
 118 E. Quintana-Rodriguez et al. / Fungal Ecology 33 (2018) 115e121

VOCs, nonanal, decanal, and hexenyl acetate promoted the devel-

Inhibited fungal strains: B ¼ Botrytis cinerea; C ¼ Colletotrichum lindemuthianum; F ¼ Fusarium oxysporum. BTH ¼ benzothiadiazole; EF ¼ endophytic fungus; EM ¼ Ectomycorrhiza, md ¼ mechanical damage; P. ¼ Phaseolus.
opment of haustoria in vitro (Mendgen et al., 2006). Similarly,
menthol and methyl salicylate enhanced the germination of spores
and the formation of appressoria by Lipaphis erysimi (Lin et al.,
2017), and (þ) and () limonene and g-terpinene stimulated the
Yi et al. (2009)

growth of P. digitatum (Simas et al., 2017).

Reference

Considering the diverse effects of VOCs on fungi, larger

screening efforts are required if we aim at predicting which VOC
will exert which effect on a certain type of fungus. As a first step in
this direction, we selected three fungal pathogens of P. vulgaris:
P. lunatus treated with BTH

C. lindemuthianum strain 1088 (kindly donated by Dr. June Simpson,

CINVESTAV, Irapuato), B. cinerea and Fusarium oxysporum (kindly
donated by Dr. Alfredo Herrera, Unidad de Geno
mica Avanzada,
CINVESTAV, Irapuato). These fungi were exposed in vitro to an at-
mosphere that contained one of 22 VOCs, selected from compounds
Plant source

that were detected in the headspace of infected P. vulgaris and

P. lunatus plants (Yi et al., 2009; Quintana-Rodriguez et al., 2015) or
other plants in response to infections (Table 1). All VOCs were
purchased from Sigma-Aldrich and Fluka Chemie (now Merck,
purchased via Sigma-Aldrich, Toluca, Mexico). For the bioassay, a
mycelial disc (5 mm diameter) was transferred from the periphery
of an actively growing culture to a square of PDA agar of
2.5  2.5 cm, which was placed on glass slide that subsequently was
Lee et al. (2016)

positioned inside a Petri dish (volume 70 ml). A stock solution of

each VOC (10 mg ml1) was prepared and 1 ml of this solution
Reference

(equivalent to 10 ng of pure VOC) was pipetted onto a filter paper,

which was located on the glass slide but avoiding physical contact
between the agar and the filter paper. As controls, we used dry filter
paper and filter paper to which pure ethanol had been added. The
Fungi and plants as source

Trichoderma sp. (in vitro)

Petri dishes were sealed with Parafilm (Pechiney Plastic Packaging

dihydrojasmonate':

Company, West Chester, PA, USA). After 48 h of exposure, the

diameter of the mycelium was measured to the nearest millimetre
Fungal source

to calculate mycelia extension. The entire experiment was per-

formed twice, each time with n ¼ 10 for each fungus-VOC
'Methyl-

combination.
Under these conditions, both the fungal species and the identity
of the VOC significantly affected mycelial growth (result of an
Fungus inhibiteda

ANOVA for the first experiment: F ¼ 1305.31 for 'VOC0 , F ¼ 105.57

for 'fungal species' and F ¼ 30.88 for the 'VOC x fungus' interaction,
P < 0.0001 for all three sources of variance. Second experiment:
F ¼ 1716.68 for 'VOC0 , F ¼ 145.82 for 'fungal species' and F ¼ 39.31
for the 'VOC x fungus' interaction, P < 0.0001 for all three sources of
F,B

variance). A significant inhibition was observed in 49 out of the 66

VOC-fungus combinations tested (P < 0.05 according to LSD post
hoc tests). In 12 combinations, fungal growth was inhibited
completely (zero growth, see Fig. 1). Five compounds significantly
inhibited the growth of C. lindemuthianum partly, and five addi-
tional compounds caused a complete inhibition (Fig. 1A). F. oxy-
sporum was partly inhibited by 15 compounds and completely
inhibited by three compounds (Fig. 1B), and B. cinerea was partly
Structure

inhibited by 16 compounds and completely inhibited by four

compounds (Fig. 1C). For example, nonanal, (þ)-carvone, citral,
trans-2-decenal, L-linalool, or nerolidol reduced the growth of all
39924-52-2

three fungi, whereas at least one of the fungi showed zero growth
after exposure to 1-octen-3-ol, nonanal, 2,6-dimethyl-2,4,6-
CAS Nr.

octatriene, citral, a-terpineol, or trans-2-decanal. However,

eugenol was the only compound that completely inhibited the
growth of all three fungi (Fig. 1).
Can we predict which VOC will inhibit a specific fungus? Un-
Methyl jasmonate
Table 1 (continued )

fortunately, as of now, the answer is no. First, the wide range of

concentrations and modes of application used in the literature does
Compound

not allow direct comparisons among the different published

studies and second, the multiple ecological functions of fungal and
plant-derived VOCs in combination with their enormous structural
a

diversity (Morath et al., 2012; El Ariebi et al., 2016; Dickschat, 2017)

 E. Quintana-Rodriguez et al. / Fungal Ecology 33 (2018) 115e121 119

Fig. 1. Inhibitory effects of VOCs on growth of fungal pathogens. Diameters of mycelia were measured 48 h after exposure to the different VOCs at 10 ng ml1 in the atmosphere
of (A) C. lindemuthianum, (B) F. oxysporum and (C) B. cinerea. Bars display means ± SE, and asterisks mark significant differences to the control (p < 0.05 according to LSD post hoc
tests, n ¼ 10). Ctrl: Control (without volatile), Et: ethanol, Hal: trans-2-hexen-1-al, Hol: cis-2-hexen-1-ol, Oct: 1-octen-3-ol, Ter: a-terpinene, Pin: () b-pinene, Lim: (S)-
()-limonene, DO: 2,6 e dimethyl e 2,4,6 e octatriene, Cha: cis-3-hexenyl acetate, Non: nonanal, Cve: (þ)-carvone, MS: methyl salicylate, Pcv: ()-trans-pinocarveol, Cit: citral, Tol:
a-terpineol, T2D: trans-2-decenal, Lin: L-linalool, Eug: eugenol, Aro: (þ)-aromandendrene, Car: b-caryophyllene, Far: farnesene, Ner: nerolidol, MJ: methyl jasmonate.
120 E. Quintana-Rodriguez et al. / Fungal Ecology 33 (2018) 115e121
make it difficult to identify structural motifs or ecological contexts
that would allow prediction of the effect of a certain VOC.
Assuming complete evaporation of the solvent with the dis-
solved VOC in our experiments, the fungi were exposed to an at-
mosphere with 0.14 mg l1 of VOC over 48 h and had no direct
contact with the VOC solution. Under these conditions, eugenol
completely inhibited the growth of all three fungi. Eugenol can
denature proteins and change the permeability of membranes, and
eugenol and several synthetic derivatives caused 50% inhibition of
the growth of various Candida strains at a concentration of
0.035e0.125 mg l1 (Mastelari-Martins et al., 2016) or inhibited
Rhizoctonia solani and F. oxysporum at a concentration of 0.1 mg l1
(Xie et al., 2017). However, in both studies, the compounds were
added directly to the growing medium. The common fungal VOC, 1-
octen-3-ol, inhibited B. cinerea and F. oxysporum in our study and
the growth of Fusarium verticillioides in another (Herrera et al.,
2015). However, the use of concentrations of more than
0.53 mM l1 of 1-octen-3-ol in the gas phase (which is equivalent to
67 000 mg l1) in the second study make its ecological relevance
questionable. This compound has toxic effects on animals because
it leads to the degeneration of dopamine-dependent neurons
(Inamdar et al., 2013), but we are not aware of a mechanistic
explanation of the effect of 1-octen-3-ol on fungi.
Two recent studies investigated the relationships of structural
motifs of different eugenol derivatives with their antifungal activity
and concluded that the substitution of the hydroxyl group of
eugenol with an aryl group (Mastelari-Martins et al., 2016) or the
presence of conjugated double bonds and the length of the CH
chain outside the ring (Xie et al., 2017), had the strongest influence
on the anti-fungal properties of different compounds. Again, the
structural diversity of the VOCs tested by us shows clearly that their
inhibitory effects cannot be explained exclusively by these rather
simple motifs.
Concerning their biological origin, all of the VOCs used in our
study are emitted from plants and a quick, non-exhaustive litera-
ture search revealed that at least 14 of them are also produced by
fungi. This difference makes it tempting to speculate that fungi
might respond differently to compounds that are, or are not, pro-
duced by themselves or by other fungi. Indeed, we found no reports
on a putative fungal origin for (þ)-carvone, citral and eugenol, all
being compounds that inhibited all three fungi. However, nonanal
and linalool inhibited all three fungi as well and for these com-
pounds, a fungal origin has been reported (Hung et al., 2013; Müller
et al., 2013; Ebert et al., 2016; Lee et al., 2016). In addition, at least
(þ)-carvone can be metabolised by several fungi (Aquino et al.,
2012; Nunes et al., 2013), although we found no report that this
compound is produced by fungi. Perhaps, the capacity of a fungus to
metabolize a certain compound might be more relevant for a pu-
tative inhibitory effect than its capacity to synthesize this
compound.
In summary, generalisations concerning an inhibitory effect of
VOCs on fungi seem not to be possible so far and likely will require
larger data sets and large-scale in silico methods, such as the
computational structure-activity screens that were used to identify
novel mosquito repellents (Kain et al., 2013; Tauxe et al., 2013).
However, most of the VOCs that inhibited the fungi in our study can
be emitted from both, plants and fungi. We conclude that antago-
nistic fungus-fungus and plant-fungus interactions are partly
mediated by the same compounds and that plant VOCs can function
as resistance agents that fungal pathogens must overcome for
successful infection.
Authorship statement
EQR and MH designed the experiments and EQR and LERM
performed them. LERM and RMAA cultured the fungi and RMAA
confirmed their identity using microscopic and molecular tech-
niques. JMT helped with the identification of VOCs using GC-MS,
EQR and MH wrote a first draft of the manuscript and all authors
contributed to writing the final version of the paper.
Acknowledgements
We thank Dr. Jorge Acosta (INIFAP, Celaya) for kindly donating
the bean lines, Dr. June Simpson and Dr. Alfredo Herrera Estrella for
donating the fungal strains and two anonymous referees for helpful
comments on an earlier version of this manuscript. Financial sup-
port from CONACyT (grant to 22234 EQR and 212715 to MH) is
gratefully acknowledged.
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