Journal of Plant Pathology (2014), 96 (2), 295-301
295
DUAL BEHAVIOUR OF PLANTS AGAINST BACTERIAL QUORUM SENSING:
INHIBITION OR EXCITATION
E. Mahmoudi1, S. Tarzaban2 and P. Khodaygan2
1Department of Plant Protection, Faculty of Agriculture, Khorasgan (Isfahan) Branch, Islamic Azad University, Isfahan, Iran
2Department of Plant Pathology, College of Agriculture, Vali-e-Asr University, Rafsanjan, Iran
SUMMARY
Bacteria use an unique and sophisticated system for
regulating diverse physiological processes in function of
their population size. This regulatory procedure, called
“quorum sensing” (QS), depends on the synthesis and per-
ception between bacteria of small signal molecules such
as acyl-homoserine lactones (AHLs). It is now evident
that plants can listen to bacterial signals and respond in
sophisticated ways to the information. The anti-QS activ-
ity of the methanolic extract of 44 plant species was de-
tected through the inhibition of the QS-related violacein
pigmentation in Chromobacterium violaceum CV026 in
the presence of 5 mgl−1 of C6-homoserin lactone. In addi-
tion, the ability of test plants to produce AHL-mimicking
compounds that excite QS-related response in CV026 was
investigated. The results revealed that the QS inhibition
activity was observed in the leaves and stem extracts of
tarragon (Artemisia dracunculus), radish (Raphanus sativus)
and hollyhock (Althea officinalis), which repress violacein
production in CV026. We have also shown that Trifolium
repens contains AHL-mimicking molecules that can acti-
vate QS function in biosensor bacterium and induce viola-
cein production in CV026. Methanolic extracts were also
able to inhibit QS-regulated virulence in Pectobacterium
carotovorum subsp. carotovorum on potato tubers. The re-
sults suggest that plants have quorum sensing-mimicking
signals that could potentially be used for disrupting quo-
rum sensing of associated bacteria thus controlling their
infections.
Key words: Anti-QS activity, quorum sensing excitation,
Pectobacterium, plant extract
INTRODUCTION
Quorum sensing (QS) is a well-known phenomenon
of microbial communication and regulation of gene ex-
pression, which has extensively been studied in both
Corresponding author: E. Mahmoudi
Fax: +98.03115354016
E-mail: e.mahmoudi@khuisf.ac.ir
Edizioni ETS Pisa, 2014 Mahmoudi et al.
Gram-positive and Gram-negative bacteria. QS is medi-
ated by small signal molecules diffusible in microbial pop-
ulations, which accumulate during microbial growth and
act as “autoinducers”, thereby activating a number of cell
density-related processes when a specific concentration is
reached (Fuqua et al., 2001; Greenberg, 2000). In bacterial
infections, QS regulates a variety of biological processes
including bioluminescence, adequacy development, bio-
film formation, sporulation, virulence determinant induc-
tion, antibiotic synthesis, motility and other physiological
events (Greenberg, 2000; Mahmoudi et al., 2011).
Several signaling molecules mediate the QS system
(Dong and Zhang, 2005), the best-characterized being the
acyl-homoserine lactones (AHLs) in Gram-negative bacte-
ria (Fuqua et al., 2001). AHLs are highly conserved, having
the same homoserine lactone moiety, but differ in the acyl
side chains and substitution (carbonyl or hydroxyl) at the
C3 carbon (Greenberg, 2000).
Resistance to antibiotics and other antibacterial chemi-
cal compounds has recently developed in many types of
bacterial populations. Biofilm formation allows bacteria to
evade host defenses, so that the infections they induce re-
spond poorly to conventional antimicrobial chemotherapy
(Stewart and Costerton, 2001). One alternative approach
for controlling bacterial infections that may find applica-
tion in many different fields, such as medicine, agriculture,
and food technology, is to interfere with their QS mecha-
nisms (Williams, 2007). This approach is highly attractive
because it does not impose harsh selective pressure for
development of resistance, as it happens with antibiotics,
because QS is not directly involved in processes essential
for bacterial growth (Rasmussen and Givskov, 2006). Fur-
thermore, QS-inhibitory agents are not expected to elimi-
nate beneficial bacteria present in the host.
Recent studies have shown that the QS-inhibiting
organisms protect themselves from invasion by other
microbes (Hogan et al., 2004). Inhibitors disrupt QS in
various way, e.g. by acting as enzymes (AHL-lactonase
or AHL-acylase) which destroy signal molecules, or as
enzymes that degrade LuxR protein, or as AHL mimic
compounds that block signal molecules (Zhang and Dong,
2004). Many eukaryotes, fungi and plants in particular, but
also bacteria secrete compounds that can interfere with the
QS-regulated gene expression in the invading organism
(Mahmoudi et al., 2011; Persson et al., 2005).
296 Excitation and inhibition of bacterial quorum sensing
Plants can produce a multitude of diverse antimicro-
bial compounds such as phenolics, catechins, quinones,
flavanones, alkaloids, and terpenoids (Williams, 2007)
targeted at killing pathogens and working via a non spe-
cies-specific mechanism such as disruption of microbial
cell membranes. Furthermore, plants have another way of
dealing with microbes targeting a cell communication sys-
tem (Bauer and Tepletski, 2001), i.e production of anti-QS
agents that interfere with this mechanism. A number of
compounds, such as the halogenated furanone compounds
secreted by the macro-alga Delisea pulchra (Manefield et
al., 2002), or enzymes secreted by other bacteria (e.g. Ba-
cillus species), have been observed to inhibit QS through
AHLs (Reimmann et al., 2002; Mahmoudi et al., 2013).
Halogenated furanones bind to the transcriptional activa-
tor protein and enhance its degradation, whilst the bac-
terial enzymes act by degrading the signal molecules. In
addition to D. pulchra, various higher plants including pea
seedlings (Teplitski et al., 2000), Medicago truncatula seed-
lings (Gao et al., 2003), garlic, clove (Vattem et al., 2007),
Tremella fuciformis, water lily (Nymphaea sp.), pepper (Tan
et al., 2013), and extracts of various South Florida plants
(Adonizio et al., 2008) were also shown to secrete AHL
signal-mimicking substances and were found to possess
anti-QS activity (Persson et al., 2005). This discovery raises
the possibility that QS interference using AHL-mimicking
compounds might be of medical and agricultural interest
for bacterial infection control.
This research was aimed at investigating QS inhibition/
induction activity of 44 plant species from various families.
MATERIALS AND METHODS
Bacterial strains and culture media. Pectobacterium
carotovorum subsp. carotovorum strain EMPCC (Labo-
ratory of Plant Pathology, IAU- Isfahan Branch, Isfahan,
Iran) was used as a natural source of AHL molecules. C.
violaceum CV026 (McClean et al., 1997), provided by Dr.
V. Venturi, ICGEB, Italy, was used as AHL bio-indicator
strain and inducer of QS as it produces a purple pigmenta-
tion around the plant extracts. P. carotovorum subsp. caro-
tovorum and C. violaceum CV026 were routinely grown
on Luria-Bertani (LB) agar at 28°C. AHLs standards used
in this study were purchased from Sigma-Aldrich (USA).
Plant materials and extraction. Leaves and stems of
the 44 species classified as weeds, vegetables, crops, and
medicinal plants (Table 1) were used in this study. These
plants were raised from commercial seeds that were iden-
tified by the Department of Botany, IAU-Isfahan Branch,
Iran. Seeds were sterilized in a sodium hypochlorite solu-
tion (1%) for 30 min, washed twice with sterilized water
then planted in a sterilized peat substrate under green-
house conditions (28°C, with 50-70% relative humidity)
with a 16:8 light-dark photoperiod. Plants were harvested
Journal of Plant Pathology (2014), 96 (2), 295-301
for extraction after 5-7 weeks (depending on their growth
rate), their roots were cut, the aerial parts were washed in
running water and air-dried. Fresh plant material (25 g)
was exhaustively extracted with methanol, filtered through
Whatman filter paper and the filtrate was concentrated
under vacuum to obtain the methanolic extract. Resultant
residues were stored at -20°C until use.
Anti QS assay of plant extracts. The hole-diffusion
assay was used to detect anti-QS activity of the plant ex-
tracts by means of double-layer culture plates. An over-
night culture of C. violaceum CV026 in LB broth (OD600
of 0.4) was prepared. For the anti-QS assay, LB agar plates
supplemented by 5 mg l−1 C6-HSL were flooded with 1 ml
of C. violaceum CV026 culture to prepare a lawn. Four
5-mm diameter holes were bored in each agar plate using
a flame-sterilized cork borer and 25 ml of plant extracts
were placed into each hole. Distilled water and 30 mg ml−1
tetracycline were used as negative and growth inhibition
controls, respectively. Plates were then incubated at 30°C
for 24 h. In this assay, bacterial growth inhibition would
result in a clear halo around the hole and a positive result
of QS inhibition would consist in the production of a tur-
bid halo harboring pigmentless C. violaceum CV026 cells
(McClean et al., 1997).
Induction of violacein production in C. violaceum
CV026. Fresh leaves and stems were surface-disinfected
in 1% sodium hypochlorite solution for 10 min and thor-
oughly crushed in a sterilized mortar. Plant residues (1 g)
were placed on LB medium plates that had been flooded
with 1 ml of C. violaceum CV026 (106 CFU). Plates were
incubated overnight at 30°C and QS induction was de-
tected as purple growth of the bioreporter strain (CV026)
around the residues. Purified C6-HSL (5 mg l−1) was add-
ed to LB medium as positive control of exogenous QS
signal in the bioreporter strain, and ethyl acetate (20 ml) as
a negative control. The ethyl acetate was allowed to evapo-
rate before testing, to eliminate toxicity.
For chromatographic analysis, 25 g of fresh plant
material were frozen in liquid nitrogen and ground in a
mortar to a fine powder which was suspended in 25 ml
ethyl acetate after acidifying with 0.1% glacial acetic acid,
and gently mixed for 1 min. Plant residues were removed
filtering through Whatman paper and the extracts were
evaporated under vacuum at room temperature. Ethyl ac-
etate crude extracts of QS-inducing plants were separated
by tin layer chromatography on C18-reversed phase plate
(Sigma Aldrich, USA). To this aim, 25 ml of each extract
was spotted on the plate, and 5 ml of C6-HSL (5 mg l−1)
as well as 25 ml of acidified ethyl acetate were used as
positive and negative control, respectively. The plate was
developed with a solvent system of methanol-water (60:40,
v/v), then the solvent was evaporated, and the dried plates
were overlaid with a culture of the biosensor bacterium as
described by McClean et al. (1997). Appearance of violet
Journal of Plant Pathology (2014), 96 (2), 295-301 Mahmoudi et al. 297

Table 1. The list of plants tested for quorum sensing inhibition activity in this research

Common name Scientific name Violacein Common name Scientific name Violacein
inhibition inhibition
Geranium Pelargonium hortorum − Wheat Triticum aestivum −
Tomato Lycopersicum esculentum − Barely Hordeum vulgare −
Cucumber Cucumis sativus − Rice Oryza sativa −
Garlic Allium sativum − Corn Zea mays −
Coriander Coriandrum sativum − Bell pepper Capsicum annuum −
Mint Mentha sp. − Sainfoin Onobrychis sativa −
Leek Allium porrum − Fennel Foeniculum vulgare −
Olive Olea europaea − Sage Salvia officinalis −
Parsley Petroselinum crispum − White kidney bean Phaseolus vulgare −
Lentil Lentis sativa − Chickpea Cicer arietinum −
Basil Ocimum basilicum − Pea Pisum sativum −
Radish Raphanus sativus + Mung bean Vicia radiata −
Garlic chives Allium ampeloprasum − Pinto bean Phaseolus vulgare −
Dill Anethum graveolens − Sugar beet Beta vulgare −
Okra Abelmoschus esculentus − Fennel Foeniculum vulgare −
Eggplant Solanum melongena − Alfalfa Medicago sativa −
Pepper Capsicum annuum − Amaranth Amaranthus blitum −
Shiraz Oregano Zataria multiflora − Tarragon Artemisia dracunculus +
Celery Apium graveolens − White Clover Trifolium repens −
Savory Satureja hortensis − Hollyhock Althea officinalis +
Cantaloupe Cucumis melo − Thyme Thymus sp. −
Potato Solanum tuberosum −

pigment in C. violaceum CV026 colonies revealed the pres-
ence of AHL-like compounds in plant extracts.
Interfering of soft rot-related QS on potato tubers.
In this assay, the effects of QS- interfering plants on the
virulence of P. carotovorum subsp. carotovorum (Pcc) were
evaluated. Potato tubers of cv. Agria were surface-steril-
ized with 10% sodium hypochlorite for 2 min, rinsed with
tap water, air-dried under sterile conditions, then sprayed
with 70% ethanol. Potatoes were co-inoculated with 50 ml
of a Pcc suspension (1×106 CFU) and 50 ml of each QS-
interfering plant extracts. Control potatoes were injected
with a 50 ml Pcc suspension (1×106 cfu) alone and 50 ml of
each extracts. Four potato tubers were used for each com-
bination of treatments and the experiments were repeated
twice. Potato tubers were incubated at 30°C in a moist
chamber (80% relative humidity). After 3-day incubation,
the tubers were cut in the middle and the results were as-
sessed by determining the percentage of tissue maceration.
QS-interfering activity was expressed as mean ± S.D. and
the SPSS statistical package (SPSS, Version 11.5 for Win-
dows) was used for calculations.
RESULTS AND DISCUSSION
The presence of QS inhibitors in the extract of 44
plants was assessed through inhibition of violacein pig-
mentation in C. violaceum CV026 growing on LB agar
plates. The results shown that the extracts of three plant
species (Table 1) exhibited detectable inhibition of vio-
lacein pigmentation in CV026, as opposed to complete
clearing of bacterial growth around the well in the antibi-
otic control (30 mg ml−1 tetracycline). With some plant ex-
tracts, like radish (Raphanus sativus), a growth-clear zone
was observed very close to the wells containing the ex-
tracts. Beyond this zone, where the extract concentration
decreases, the bacterial growth had a markedly reduced
pigmentation. While this could mean that the extract
causes a partial growth inhibition, it is clear that the cells
growing in this region had reduced or no pigmentation.
This implies that the extract is growth-inhibitory at high
concentrations but is QS-inhibitory at lower concentra-
tions. A clear zone of inhibition, indicating bactericidal
activity, was produced by the antibiotic that was effective
against CV026. Interestingly, plant extracts produced inhi-
bition zones smaller than those of the commercial antibi-
otic. This growth-clear zone was not observed for tarragon
(Artemisia dracunculus) and hollyhock (Althea officinalis)
(Fig. 1A). On the other hand, colorless CV026 colonies
were observed around the wells, whereas beyond this zone
violacein pigmentation was obvious (Fig. 1B).
Many eukaryotic organisms are able to produce and se-
crete compounds that mimick QS signals, thus affecting
the behavior of associated bacteria (Keshavan et al., 2005).
The halogenated furanones of the marine alga Delisea pul-
chra, share structural similarity with bacterial AHLs and
strongly inhibit QS-regulated behaviors in a variety of bac-
terial species (Manefield et al., 2002). As afore mentioned,
although the chemical structure of AHL-mimicking com-
pounds has not yet been identified most of them have QS
inhibitory activity. By contrast, Trifolium repens extracts
showed QS incitation activity and stimulated violacein
production in CV026 (Fig. 1D).
298 Excitation and inhibition of bacterial quorum sensing Journal of Plant Pathology (2014), 96 (2), 295-301

A Tarragon Hollyhock B C G

Methanol

D E F

C6HSL Wc.ex ET
Fig 1. A, B, C. Interference with quorum sensing (QS) in Chromobacterium violaceum strain CV026 by plant extracts. Anti-QS
activity was tested using 25 μl of methanolic extracts from Hollyhok (Althea officinalis) and Tarragon (Artemisia dracunculus).
A. The creamy halo of bacteria surrounding the well containing the extract indicates the anti-QS effect. B. Magnification of the
areas surrounding the well containing the methanolic extract of A. officinalis, showing white colonies of CV026 which have lost
the ability to produce violacein. C. Effect of tetracycline (30 μg ml−1) used as growth inhibitor control. D, E, F. Stimulation of QS
in C. violaceum CV026 by placing crushed material of white clover (Trifolium repens) on the surface of LB medium inoculated
with CV026. D. QS induction shown by the growth of encircled purple colonies of CV026 around plant residues. E. Violacein-
producing bacterial colonies in the vicinity of white clover extracts. F. Lack of QS stimulation in CV026 by lentil (Lens esculenta)
residues. G. Thin layer chromatogram for purification of AHL-like components from white clover extracts. Bioluminescence (vio-
let spots) resulting from the presence of molecules capable of inducing the AHL biosensor. C6-AHL; white clover extract (WC.
ex); ethyl acetate (ET). Bars: A, C, D, F = 5 mm; B, E = 10 μm; G = 10 mm.

Several plant species secrete AHL-mimicking sub-
stances that can either stimulate or inhibit bacterial AHL
QS systems (Teplitski et al., 2011; Chenia, 2013), but their
structure and biological significance of are currently un-
known. Extracts from vegetating rice (Oryza sativa) con-
tain molecules that are sensitive to aiiA lactonase and stim-
ulate QS-related functions in bioreporter strains (Degrassi
et al., 2007). These compounds are thought to inhibit the
synthesis of some virulence factors (e.g. protease, lipase,
and polygalacturonase) without reducing bacterial growth,
thus supporting the notion that they may act as QS inhibi-
tors rather than as antibacterial substances (Krishnan et
al., 2012).
In the attempt to learn whether higher plants secrete
substances that mimick AHL signal molecules that regu-
late population density-dependent behaviours, we have
used C. violaceum CV026, a well-known reporter strain
that detects exogenous AHLs (McClean et al., 1997).
When residue aliquots (1 g) from 44 different plants were
added to growth media, pigment production in CV026 was
stimulated only by the white clover (Trifolium repens) ex-
tract (Fig. 1D). Although, the amount of pigment produc-
tion was low and only some of the colonies near the plant
residues became purple, the intensity of pigment produc-
tion increased when plant tissues were carefully crushed
and placed directly on the medium (Fig. 1E).
Inhibition of bacterial growth was not observed around
the crushed plant extracts. The induction of violacein syn-
thesis in areas adjacent to the plant material was similar to
that caused by the addition of C6-HSL on CV026-hosting
medium. No QS inhibition activity of white clover was
shown in the presence of C6-HSL in CV026 colonies as it
could only stimulate signal behavior in the QS system of
the bioreporter strain. Thin layer chromatography sepa-
ration of AHL-like compounds in white clover extracts
showed that CV026 induced a reaction in the clover ex-
tract which was small and pale as compared with that of
standard C6-HSL (Fig. 1G).
It is known that plant extracts have QS inhibitory activ-
ity in C. violaceum and the possibility that they may also
be able to inhibit QS-mediated phenotypes in other Gram-
negative bacteria was investigated (Taganna et al., 2011).
Pcc was chosen for this purpose because of the known
QS system that controls a number of genes involved in
biofilm formation and production of virulence factors such
as pectinolytic enzymes (Barnard and Salmond, 2007; Burr
et al., 2006). QS mutants of Pcc were shown to be low pro-
ducers of pectinolytic enzymes contrary to the wild type
strains, which induce a severe soft rot (Cirou et al., 2009;
Mahmoudi et al., 2013).
The ability of plant methanolic extracts to attenu-
ate the pathogenicity of Pcc was evaluated by injecting
Journal of Plant Pathology (2014), 96 (2), 295-301 Mahmoudi et al. 299

Fig. 2. Effect of plant methanolic extracts on the maceration of potato tissue by Pectobacterium carotovorum subsp. carotovorum
(PCC). A. Soft rot of potato tuber caused by (PCC). Inhibition of QS-mediated rotting by the methanolic extract from Athelia of-
ficinalis (B) and Artemisia dracunculus (C). D. Negative control (distilled water-injected potato tuber). All bars = 10 mm. E. Potato
soft rot reduction in potato tubers co-inoculated with PCC and plant extracts. PCC, Pectobacterium carotovorum subsp. carotovo-
rum; AO, Athelia officinalis; RS, Raphanus sativus; AD, Artemisia dracunculus; DW, distilled water.

surface-disinfected potatoes with a bacterial suspension
together with the methanolic extract and measuring mac-
eration at 72 h post inoculation. Results showed that the
methanolic extracts from A. officinalis, A. dracunculus
and R. sativus significantly reduced soft rot in contrast
to inoculation of Pcc alone. However, the radish extracts
showed a growth inhibitory effect on CV026 in violacein
inhibition test, there was no obvious detectable difference
in percentage of the maceration between co-inoculating
Pcc with three test plants (Fig. 2 A-E). In the anti-QS assay,
these plants disrupted violacein production in CV026 and
it seems that reduction of potato tissue maceration resulted
as QS interfering in Pcc.
Microbiological research is now focused on the devel-
opment of molecules that are structurally related to autoin-
ducers. Such molecules have potential use as antimicrobial
drugs against QS bacteria to control virulence (Galloway
et al., 2012). Our results indicate that plant extract may act
as contrary signals for regulation of bacterial virulence.
Our finding supports previous works which suggested
that some plant tannin-rich fractions inhibited swarming
and virulence factor expression in Pseudomonas aeruginosa
(Taganna et al., 2011). A group of researchers have stud-
ied QS inhibition using the P. aeruginosa model proving
the inhibitory activity of furanone compounds (Manefield
et al., 2002), South Florida plant extract (Adonizio et al.,
2008), and Scutellaria extract in Pectobacterium carotovo-
rum (Song et al., 2012). This is a highly specific and ef-
fective approach for attenuating bacterial virulence and
controlling bacterial infections (Galloway et al., 2012).
In conclusion, the anti-QS potential of plants may be
as important as the antibacterial effect. The use of QS
inhibitors/exciters that mimic natural interference sys-
tems is a appealing approach to the development of novel
biocontrol strategies (Galloway et al., 2012). The goal of
such studies is to learn how organisms naturally disrupt
QS, then identify active compounds in natural sources for
manipulating them into better inhibitors through either
synthetic chemistry or genetic engineering. In this study,
we have shown three plant species to have anti-QS and one
plant extract having QS exciting activity. The QS interfer-
ing effect of the said plants could be useful and represent
a new approach in the control of bacterial infections in
medicine and agriculture (Taganna et al., 2011). Most re-
cent studies have investigated only the antibacterial effect
of plants or their anti-QS activity (Romero et al., 2005;
Song et al., 2012). We have shown that other mechanisms
of action, including QS exciting activity or QS signal stim-
ulation are present in plant compounds which should not
be overlooked. Since the QS inhibition potential of plants
could provide an alternative control method against phy-
topathogenic bacteria that use QS to regulate virulence
expression, investigating the nature of QS inhibitor/exciter
compounds and the mechanisms by which they interfere
with QS would be of paramount importance.
ACKNOWLEDGEMENTS
Work funded by the Research Council of the Isfa-
han (Khorasgan) Branch, Islamic Azad University, Iran.
The help provided by Dr. Payam Najafi, Research Vice
President of IAU-Isfahan Branch, Iran is gratefully ack-
owledged and thanks are due to Dr. Vittorio Venturi
(ICGEB, Trieste, Italy) for providing the AHL biosensor
strain.
300 Excitation and inhibition of bacterial quorum sensing
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Received July 14, 2013

Accepted December 3, 2013