Plant Mol Biol

DOI 10.1007/s11103-016-0457-8

Beneficial effects of bacteria-plant communication based

on quorum sensing molecules of the N-acyl homoserine
lactone group
Adam Schikora1 • Sebastian T. Schenk2 • Anton Hartmann3

Received: 19 August 2015 / Accepted: 18 February 2016

Ó Springer Science+Business Media Dordrecht 2016

Abstract Bacterial quorum sensing (QS) mechanisms understanding of bacteria-plant interaction for the future
play a crucial role in the proper performance and ecolog- agricultural applications.
ical fitness of bacterial populations. Many key physiolog-
ical processes are regulated in a QS-dependent manner by Keywords Quorum sensing
N-acyl homoserine lactone
auto-inducers, like the N-acyl homoserine lactones (AHLs) (AHL)
AHL-priming
Inter-kingdom communication

in numerous Gram-negative bacteria. In addition, also the Quorum quenching
interaction between bacteria and eukaryotic hosts can be
regulated by AHLs. Those mechanisms gained much
attention, because of the positive effects of different AHL Bacterial communication systems
molecules on plants. This positive impact ranges from
growth promotion to induced resistance and is quite con- Bacteria living in communities, like biofilms on abiotic or
trasting to the rather negative effects observed in the biotic surfaces, or free-living, planktonic bacteria, produce
interactions between bacterial AHL molecules and animals. small molecules (chemical signals) in order to arrange
Only very recently, we began to understand the molecular commune activities. This process is called auto-induction
mechanisms underpinning plant responses to AHL mole- (AI). The signal molecules (autoinducers) are constitu-
cules. In this review, we gathered the latest information in tively synthesized at a very low rate and released from the
this research field. The first part gives an overview of the cell into the medium. When the concentration of these
bacterial aspects of quorum sensing. Later we focus on the signal molecules, due to an increased cell density or habitat
impact of AHLs on plant growth and AHL-priming, as one conditions reaches a defined threshold level (quorum), a
of the most understood phenomena in respect to the inter- receptor protein/transcription factor (R-protein) senses the
kingdom interactions based on AHL-quorum sensing concentration and the R-protein-AI complex induces the
molecules. Finally, we discuss the potential benefits of the transcription of quorum sensing-regulated genes but also
key AI biosynthesis genes (I-gene) accelerating the
response (Fuqua and Winans 1994). This auto-induction
& Adam Schikora
[email protected]
process is able to integrate additional environmental and
physiological signals and to optimize the expression of a
1
Julius Kühn–Institut, Federal Research Centre for Cultivated series of target genes. In this manner, the expression of the
Plants (JKI), Institute for Epidemiology and Pathogen genetic diversity and capacity of bacteria can be organized
Diagnostics, Messeweg 11/12, 38104 Brunswick, Germany
very efficiently. Auto-inducers are the basis of ‘‘quorum
2
Institute of Plant Sciences - Paris-Saclay, INRA/CNRS, 630 sensing’’ (signaling a critical cell density). Sometimes,
rue de Noetzlin, Plateau du Moulon, 91405 Orsay, France
because of the more general aspect integrating the opti-
3
Research Unit Microbe-Plant Interactions, Department for mized gene expression, the term ‘‘efficiency sensing’’ was
Environmental Sciences, German Research Center for
used (Hense et al. 2007). Since this behavior has excep-
Environmental Health (GmbH), Helmholtz Zentrum
München, Ingolstaedter Landstr. 1, 85764 Neuherberg, tional evolutionary importance, auto-inducing systems are
Germany abundant in nature. AI-systems guarantee homeostatic

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control of costly cooperative behavior, like the secretion of pathogens. Many plant extracts, e.g. from garlic (Bjarn-
public goods or switch to pathogenic or mutualistic life sholt et al. 2005) or horseradish (Jakobsen et al. 2012),
styles. The production of AI-signals constitutes a pre- inhibit quorum sensing. Those extracts may have inhibitory
assessment strategy for costly behaviors. The core princi- activities against many bacteria, including pathogens like
ples of this mechanism were recently described in the Pseudomonas aeruginosa (Jakobsen et al. 2012). Iberin and
hybrid ‘‘push–pull’’ model (Hense and Schuster 2015). related isothiocyanate compounds found in the Brassi-
Shortly: the ‘‘push’’ factors, e.g. cell density, diffusion, or caceae family are known to specifically block the expres-
spatial clustering, determine when a behavior becomes sion of QS-regulated genes in P. aeruginosa. These are just
effective, whereas ‘‘pull’’ factors, often stress, reduce the a few examples of how plants regulate the AHL-signaling
activation threshold. of associated Gram-negative bacteria. Nonetheless, in
In many Gram-negative bacteria, N-acyl homoserine addition to these defense-oriented responses to pathogenic
lactones (AHLs) are frequently used as auto-inducers bacteria, in this review we discuss the beneficial responses
(Fig. 1). These molecules consist of a hydrophilic lactone to AHLs observed in different plants.
ring and a carbon chain with different length (C4 to C18),
changing the molecule from hydrophilic to strongly
hydrophobic. The C3-atom can be unsubstituted, substi- AHL-molecules modulate plant performance
tuted with a carbonyl group, or hydroxylated. In some in different ways
cases, even double bonds are formed in the lipid chain.
While the product of a luxI-type gene performs the The first study reporting an impact of bacterial AHLs on
biosynthesis, hydrolytic enzymes with lactonase activity plant physiology was published more than a decade ago
can degrade these signal molecules. This seems to guar- (Mathesius et al. 2003). The authors performed a differ-
antee that the important AI-signal truly functions as a ential proteome analysis and revealed that amongst
signal for specific physiological or environmental circum- defense- and stress-related proteins, also proteins associ-
stances, examples for this can be found in Agrobacterium ated with flavonoid metabolism, hormones and several
tumefaciens or Pseudomonas putida (Buddrus-Schiemann regulatory proteins (including protein degradation and
et al. 2014). Bacteria with only the lactonase activity were synthesis) were differentially accumulated upon AHL
also reported, apparently they use the released AHLs as treatment in plants. The authors provided also the first
carbon sources; such activities might be also part of a report on an activation of the auxin-responsible GH3 pro-
phenomenon called quorum quenching. Some other varia- moter after application of AHLs (Mathesius et al. 2003).
tions of the auto-induction system are present in bacteria During the following years, several detailed studies on the
with just the LuxR-gene, so-called ‘‘LuxR-solos’’ (Patel relation between the changed auxin level and the modifi-
et al. 2013). These bacteria are able to sense AI but are cation of plant growth upon AHL perception were pub-
unable to produce their own AI. Interestingly, some of the lished. It was very remarkable that in addition to an up-
LuxR-solos have evolved from the ability to bind AHLs regulation of auxin-related genes, genes related to cytoki-
and respond to other molecules/signals. nin were down-regulated (von Rad et al. 2008). The
The relevance of the signaling systems based on AHLs resulting change in the ratio between auxin and cytokinin
is reflected in the abundance of quorum quenching activi- could explain the root growth-promoting effect observed
ties in plants and animals, which obviously have the after the application of C4- and C6-AHLs. Using another
function to destroy the signaling activity of bacterial system, mung bean plants, the AHL-induced basipetal
auxin transport was postulated to play a crucial role in the
formation of adventitious roots (Bai et al. 2012). Impor-
tantly, this effect seems to depend on cyclic GMP signaling
and H2O2 and NO production (see also the chapter on AHL
perception ‘‘Comparison of perception of AHLs in plant
and animal cells’’).
Based on the observations from recent studies and our
own experiments, we proposed a dual function of the AHL
molecules in Arabidopsis thaliana (Hartmann and Schikora
2012; Schenk et al. 2012). AHLs with a short acyl chain,
like C4 or C6, were shown to increase the growth rate and
Fig. 1 General structure of N-acyl homoserine lactones (AHLs), the
primary root elongation (Bai et al. 2012; Liu et al. 2012;
AI-molecules in many Gram-negative bacteria. R-acyl chain can
range from 4 to 18 carbon atoms; there may be a hydroxyl-group or Schenk et al. 2012; von Rad et al. 2008). In contrast,
carbonyl-group at C3-atom and/or double bond in the acyl-chain molecules with longer acyl chains (e.g. C12 or C14)

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induced resistance in a phenomenon named AHL-priming measured (Götz-Rösch et al. 2015). This difference might
(Schenk et al. 2014; Schenk and Schikora 2015; Schikora be due to lack of AHL-transport to the shoot in yam bean
et al. 2011). The impact of AHLs on plant growth in other probably caused by a lactonase-driven degradation. Yet
plant species seems more complex (Hartmann et al. 2014), another interesting example is the modification of plant cell
however, very specific as demonstrated in mung bean and walls in AHL-primed plants (see below). In this primed
Medicago truncatula plants. For example, the long-chain stage, plants upregulate the transcription of several genes
3-oxo-C14-HSL produced by Sinorhizobium meliloti related to secondary metabolism (e.g. phenols). In conse-
enhanced the nodulation in roots of Medicago truncatula quence, upon a challenge with pathogens, those plants
(Veliz-Vallejos et al. 2014). Very striking was the fact that accumulate callose and phenolic compounds (Schenk and
the increased number of nodules was observed only after a Schikora 2015). The first report on an interaction between
treatment with 3-oxo-C14-HSL, the predominant AHL of AHLs and the plant reproduction was a study on two algae,
S. meliloti, treatment with other AHLs showed no effect. In the green macroalga Ulva and the red macroalga
mung bean plants only the 3-oxo-C10-HSL, but not the Gracilaria. In this study, the short-chained C4- and C6-
unsubstituted C10-HSL or C12-HSL, was able to induce HSLs produced by bacteria in biofilms were shown to
adventitious roots (Bai et al. 2012). Although several stimulate the release of carpospores (Singh et al. 2015).
reports linked the growth-modulating effect of AHLs to Interestingly, both the cystocarps and the cystocarp-bearing
auxin, some postulated that the impact of 3-oxo-C10-HSL plantlets treated with AHLs had protein patterns different
on Arabidopsis (an increased formation of lateral roots) is from the pattern in control algae.
independent of auxin concentration (Ortiz-Castro et al.
2008). Palmer and coworkers proposed yet another mech-
anism, based on the change in transpiration rate (Palmer AHLs prime for induced resistance
et al. 2014). The authors postulate that AHLs could be
metabolized to L-homoserine, which increases stomata In preparation for an upcoming biotic or abiotic stress,
opening and consequently fosters the water and mineral plants can strengthen their defense mechanisms with a
flow through the plant. sensibilization mechanism, called priming. Diverse low-
molecular weight metabolites and natural compounds can
induce this state. In the last decades, several priming
Uptake and physiological influence of AHL phenomena were described which generally result in a
stronger and faster response to a stress agent. Priming has
The strong impact of AHLs on plants raised the question of been shown, e.g. for b-aminobutyric acid (BABA), which
whether those molecules act via a systemic signal (or sig- improves the plant’s ability to resist biotic and abiotic
nals) which would be initiated after the perception of AHLs stresses (Ton et al. 2005). The mobile metabolite azelaic
on the root surface, or whether they are taken up into the acid primes the plant for higher salicylic acid-related
plants’ tissues and act locally. Only few reports addressed defense response (Jung et al. 2009). Also, pipecolic acid
this question in a systemic manner. Using radioactively can sensitize plants for systemically acquired resistance
labeled C8- and C10-HSL, Sieper et al. (2013) reported an (Navarova et al. 2012). Other priming inducers comprise
ATP-dependent transport of AHLs within barley roots. The biocontrol bacteria, which can prepare the plant for an
majority of the molecules were transported within the upcoming pathogen attack (Ryu et al. 2003). In the last
central cylinder. The transport rate of the AHL-molecules years, many molecular aspects of priming were discovered,
within the root and shoot tissues correlated negatively with including an involvement of MAP-kinases, modifications
the length of the acyl chain (Sieper et al. 2013). Similarly, of histones in promoter regions of defense-associated
in Arabidopsis the short-chain AHL, C6-HSL, was relo- transcription factors, and other epigenetic mechanisms
cated into leaves after application to roots. However, the conveying a trans-generational memory effect (Beckers
long-chain AHL, oxo-C14-HSL, was not transported et al. 2009; Jaskiewicz et al. 2011; Luna et al. 2012;
(Schikora et al. 2011). Both studies confirm an earlier Fig. 2).
report on barley (Hordeum vulgare) and yam beans Several reports documented that also AHLs are able to
(Pachyrhizus erosus) (Götz et al. 2007). A more recent function as priming agents. AHLs induce resistance against
study on the same plants revealed that C6-, C8- and C10- a broad spectrum of plant pathogens in different plant
HSLs influence the activity of specific detoxification species. Short- and medium-length carbon chain AHLs
enzymes, namely glutathione S-transferase and dehy- produced by Serratia liquefaciens strain MG1 and Pseu-
droascorbate reductase in barley with the largest influence domonas putida strain IsoF were responsible for the
on the leaf-located enzyme even when C6-HSL was Induced Systemic Resistance (ISR) against the fungal leaf
applied to the roots; in yam bean no influence was pathogen Alternaria alternata in tomato plants (Hartmann

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Fig. 2 The AHL-induced resistance (ALI) is a priming for enhanced of phenolic compounds, or stomatal closure. In root-associated
defense observed in several plant species. ALI is based on the yet bacteria, the bacterial cells produce QS auto-inducer molecules
unknown perception of AHL molecules by plant cells, which triggers (AHLs) in LuxI-dependent manner (AHL-synthase). At a threshold
a signaling cascade based on MAP kinases and an enhanced level of AHL-concentration, the AHL-production is largely induced;
expression of the WRKY-type transcription factors, if primed plants the molecules are perceived by LuxR-type receptors in the bacteria,
are challenged with a pathogen. In systemic tissues, primed plants which in combination with the ligand act as transcriptional activators
accumulate higher amount of oxylipins and SA, which governs for QS-regulated genes. The AHL-molecules can also be perceived by
subsequent defense reactions like: callose depositions, accumulation root cells (see above) and provoke plant responses

et al. 2004; Schuhegger et al. 2006). The AHL-induced Pseudomonas syringae pathovar tomato (Pst) in Ara-
resistance was proposed to depend on salicylic acid (SA)- bidopsis (Schenk et al. 2014; Schikora et al. 2011). Along
and ethylene-related defense reactions. Pang et al. (2009) with those observations, the resistance against Pst in Ara-
demonstrated resistance induction by AHLs produced by bidopsis was enhanced by the oxo-C14-HSL-producing
the strain Serratia plymuthica HRO-C48, which protected Sinorhizobium meliloti strain expR?, which in contrast to
cucumber plants against the damping-off disease-causing its parental isolate Rm2011, produces significantly more
Pythium apahnidermatum (Pang et al. 2009). Furthermore, AHL due to a correct version of the expR gene (Zarkani
the authors described an AHL-dependent stimulation of et al. 2013). The potential significance of AHL-priming for
systemic resistance to Botrytis cinerea in beans and agriculture became more obvious with a study on the
tomatoes (Pang et al. 2009). Similarly to AHL molecules resistance against Blumeria graminis, Puccinia graminis,
produced by bacteria, commercially available pure AHL- and Phytophthora infestans, induced by the same AHL-
molecules also induce priming. The long-chain AHL, oxo- producing S. meliloti strain expR?, in barley, wheat and
C14-HSL, activates resistance towards different obligate tomato plants (Hernández-Reyes et al. 2014). The AHL-
biotrophic pathogens such as Golovinomyces orontii and effects triggered by S. meliloti expR? seems to be based on
Blumeria graminis in Arabidopsis and barley, respectively, an enhanced production of reactive oxygen species (ROS).
as well as against the hemibiotrophic pathogen The induced accumulation of ROS in AHL-primed plants

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was namely observed in barley plants, which showed an immune mediators. However, in contrast to plant cells, the
elevated level of hypersensitive response (HR) after biological activity requires more than 10 C-atoms in the
infection with Blumeria graminis. This high level of HR acyl chain. Recently, these findings were reviewed by
correlated with an increased number of vesicle formation at Holm and Vikström (2014). Similar to animal cells, where
the site of infection and an increased transcription of the the MAP kinases p38 and p44/42 are involved in the
Peroxidase7 (HvPRX7) gene (Hernández-Reyes et al. response to AHLs, the AHL-priming was abolished in
2014). Very recently, the molecular mechanism of the plants lacking MPK6 (Schikora et al. 2011). Likewise, the
AHL-induced priming was deciphered in Arabidopsis Ca-signaling plays an important role in perception of AHL
(Schenk and Schikora 2015), we postulated an SA and in animals and plants. For example in animals, the 3O-C12-
oxylipin-dependent pathway, which could activate cell wall HSL can increase the intracellular calcium concentrations
and stomata-based defense responses (Schenk et al. 2014). through influx from surrounding and release from thapsi-
Schuhegger and colleagues also suggested the involvement gargin-sensitive stores (Vikström et al. 2010). In plants,
of SA in AHL-systemic effects on tomato plants treatment with C4-HSL induced a transient and immediate
(Schuhegger et al. 2006). Those first findings were later increase in cytosolic Ca2? levels. Since a pretreatment with
supported by mutant analysis in Arabidopsis. Mutants La3?, verapamil or ethylene glycol tetraacetic acid (EGTA)
impaired in SA-signaling, such as npr1-1 or tga2/5/6, as inhibited this increase, though a pretreatment with Li?
well as the mutant in oxylipin synthesis, lox2, failed to failed to do so, the contributing Ca2? was thought to be
induce AHL-priming. In addition, an enhanced accumula- mobilized, similarly to animals, from the extracellular
tion of SA and the defense-related hormone OPDA was medium via the plasma membrane Ca2? channels (Song
detected in AHL-primed plants (Schenk et al. 2014). The et al. 2011). Moreover, a recent study on 3-oxo-C6-HSL
strong upregulation of oxylipin-dependent GST6, GSTU19, revealed that in Arabidopsis mutants in calmodulin (CaM)
HSP70, HSP17 and of cytochrome P450 (CYP81D11), all genes do not show the growth-promoting effect of C6-
of them usually regulated by OPDA treatment (Mueller HSL, otherwise observed after treatment with C6-HSL in
et al. 2008), after oxo-C14-HSL pretreatment and the fol- wild-type plants (von Rad et al. 2008; Zhao et al. 2015).
lowing inoculation with Pst was also in line with the SA- Another open question in the perception of short-chain
and oxylipins-dependency (Schenk et al. 2014). Altogether, AHLs in Arabidopsis is the role of G-proteins. Whereas in
several lines of evidence indicate the importance of animal cells, the IQ-motif-containing GTPase-Activating
oxylipins (and SA) in AHL-priming (Table 1). Protein1 (IQGAP1) interacts directly with 3-oxo-C12-HSL
In addition to the changed transcriptome and hormonal (Karlsson et al. 2012), such interaction for plant proteins
balance, modification of the cell wall could account for the remains uncharacterized. Analysis of mutants in the
defense mechanisms induced upon AHL-priming. Higher G-protein Coupled Receptor1 (GCR1) and two others,
numbers of papilla formed at the site of fungal infection namely cand2 and cand7, as well as in the canonical sub-
(Schikora et al. 2011), enhanced accumulation of callose unit G-alpha GPA1 revealed that those proteins are
and cell wall-bound phenolic compounds, as well as higher required for the stimulatory effect of C6- and C8-HSLs on
accumulation of lignins (Schenk et al. 2014), suggest that Arabidopsis growth (Jin et al. 2012; von Rad et al. 2008;
cell wall undergoes substantial changes during AHL- Zhao et al. 2015). Nevertheless, besides those very
priming. Another AHL-resistance phenotype could be the promising results, bona fide AHL-interactor proteins in
increased amount of closed stomata in response to Pst plants remain still undiscovered. Hydrophobic AHLs, with
challenge in oxo-C14-HSL-pretreated plants (Schenk et al. carbon chain lengths of 12C or more, may form micelle
2014). This AHL-induced stomata defense response seems structures and interact with components and structures of
similar to the flg22-induced stomata closure described as the plant cell membrane system triggering in this way
RES-oxylipin and SA-dependent by Montillet et al. (2013). cellular responses, similarly to antimicrobial lipopeptides
or the antibiotic fengycin of Bacillus (Lin and Grossfield
Comparison of perception of AHLs in plant 2015).
and animal cells
Potential use of quorum sensing mechanisms
In mammalian cells, AHLs can trigger multiple signaling
pathways including calcium mobilization, activation of The increasing demand for food and the concerns regarding
Rho GTPases, MAPK, and NFjB. Those pathways control food quality are the todaýs driving forces leading to new
diverse functions and behaviors modified upon AHL per- strategies in agriculture. Efficient (crop) plant protection
ception, such as cytoskeleton remodeling, chemotaxis, methods hold a great potential to ensure a sufficient and
migration, phagocytosis, epithelial barrier function, dif- high-quality food supply. Amongst them, the use of bio-
ferentiation, proliferation, apoptosis, and production of logicals or biocontrol agents, even though widely spread,

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Table 1 Different effects were observed on plants after application of pure AHL molecules or inoculation with AHL-producing bacteria
AHL Effect Plant References

C4-HSL Intracellular Ca2? elevation Arabidopsis Song et al. (2011)

C4-HSL, C6-HSL, Primary root growth Arabidopsis Liu et al. (2012), von Rad
C8-HSL et al. (2008)
Serratia liquefaciens Resistance against necrotrophic pathogens, SA-levels, Tomato Schuhegger et al. (2006)
(C4-HSL, C6-HSL) defense-gene regulation
Serratia phymuthica Resistance against necrotophic pathogens Tomato, Beans, Pang et al. (2009)
(AHL?) Cucumber
C6-HSL Alteration in auxin/cytokini level Arabidopsis von Rad et al. (2008)
Oxo-C6-HSL Primary root growth, calmodulin signaling Arabidopsis Zhao et al. (2015)
C6-HSL Herbivore susceptibility N. attenuata Heidel et al. (2010)
C6-HSL, C8-HSL Root growth, plant biomass increase Arabidopsis Schenk et al. (2012)
Oxo-C8-HSL Changes in protein pattern Arabidopsis Miao et al. (2012)
Oxo-C8-HSL Primary root growth promotion, ethylene-level Arabidopsis Palmer et al. (2014)
C6-HSL, oxo-C10-HSL, Specific response to different AHL molecules Arabidopsis Schenk et al. (2014)
Oxo-C14-HSL
Oxo-C10-HSL Axin-induced adventitious root formation Mung beans Bai et al. (2012)
Oxo-C10-HSL Root development, root hair formation Arabidopsis Ortiz-Castro et al. (2008)
C10-HSL, C12-HSL Inhibition of primary root growth Arabidopsis Zhao et al. (2015)
Oxo-C12-HSL, Auxin-response M. truncatula, White Mathesius et al. (2003)
oxo-C16-HSL Clover
Sinorhizobium meliloti Enhanced nodulation in roots M. truncatula Veliz-Vallejos et al.
(oxo-C14-HSL) (2014)
Oxo-C14-HSL Resistance to biotrophic pathogens, activation of MAP- Arabidopsis, Barley Schikora et al. (2011)
Kinases, defense- gene regulation
Oxo-C14-HSL SA/oxylipine-related defense against biotrophic pathogenes Arabidopsis Schenk et al. (2014)
Sinorhizobium meliloti Resistance against biotrophic pathogens Tomato, Barley, Wheat, Hernández-Reyes et al.
(oxo-C14-HSL) Arabidopsis (2014)
The findings are arranged according to the increasing length of the AHL acyl chain

still did not achieve its full abilities. Today several prod- between bacterial and animal or human cells, inducing
ucts based on bacterial inoculum, mainly consisting of several immune responses. Therefore, the possibility to
Bacillus, Pseudomonas or Serratia spp., reached the mar- interfere with bacterial QS mechanism, via mimicry or
ket. Our research, however, shows that the use of N2-fixing enzymatic degradation of QS molecules approaches could
Rhizobia (e.g. Sinorhizobium meliloti) with enhanced pro- be a good strategy to lower the impact of AI molecules on
duction of specific AHLs, could enhance the beneficial eukaryotic targets. Such approaches would also lower the
effects of bacteria and enlarge the impact to plant species virulence of pathogenic bacteria and could be in the center
usually not associated with the particular strain (Hernán- of new cure strategies against infectious diseases (Jakobsen
dez-Reyes et al. 2014; Zarkani et al. 2013). Such strategy et al. 2013; LaSarre and Federle 2013; Kusari et al. 2015).
could be a great addition or alternative to those currently
used. Such approach, based on AHL-producing bacteria as Acknowledgments The authors would like to apologize to all col-
leagues whose work was not cited due to the space limitation. AS is
a possible soil amendment, is currently tested in our lab- supported by the grant 13HS026 ‘‘plantinfect’’ from the Federal
oratory. In a different field, a better understanding of the Office for Agriculture and Food (BLE), Germany. This publication
interaction between bacterial quorum sensing molecules has been written with the support of the AgreenSkills? fellowship
and eukaryotic host cells could open new possibilities in program which has received funding from the EU’s Seventh Frame-
work Program under grant agreement N° FP7-609398 (AgreenSkills?
medicine, or more precisely in the prevention of infectious contract) to STS. AH acknowledges the additional funding of the
diseases. During the infection process, QS molecules interdisciplinary research topic ‘‘Molecular Interactions in the Rhi-
govern the bacterial ability to form biofilms, express vir- zosphere’’ by Helmholtz Zentrum München (HMGU) and greatly
ulence factors, and other density-regulated features. Those appreciates fruitful discussions with Dr. Burkhard Hense (Institute of
Biological Computing, HMGU).
molecules play also a crucial role in the interaction

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Author contributions All authors contributed equally to this Holm A, Vikström E (2014) Quorum sensing communication between
manuscript. bacteria and human cells: signals, targets, and functions. Front
Plant Sci 5:309. doi:10.3389/fpls.2014.00309
Jakobsen TH et al (2012) Food as a source for quorum sensing
inhibitors: iberin from horseradish revealed as a quorum sensing
References inhibitor of Pseudomonas aeruginosa. Appl Environ Microbiol
78:2410–2421. doi:10.1128/AEM.05992-11
Bai X, Todd CD, Desikan R, Yang Y, Hu X (2012) N-3-oxo- Jakobsen TH, Bjarnsholt T, Jensen PO, Givskov M, Hoiby N (2013)
decanoyl-L-homoserine-lactone activates auxin-induced adventi- Targeting quorum sensing in Pseudomonas aeruginosa biofilms:
tious root formation via hydrogen peroxide- and nitric oxide- current and emerging inhibitors. Future Microbiol 8:901–921.
dependent cyclic gmp signaling in mung bean. Plant Physiol doi:10.2217/fmb.13.57
158:725–736. doi:10.1104/pp.111.185769 Jaskiewicz M, Conrath U, Peterhansel C (2011) Chromatin modifi-
Beckers GJ, Jaskiewicz M, Liu Y, Underwood WR, He SY, Zhang S, cation acts as a memory for systemic acquired resistance in the
Conrath U (2009) Mitogen-activated protein kinases 3 and 6 are plant stress response. EMBO Rep 12:50–55. doi:10.1038/embor.
required for full priming of stress responses in Arabidopsis 2010.186
thaliana. Plant Cell 21:944–953. doi:10.1105/tpc.108.062158 Jin G et al (2012) Two G-protein-coupled-receptor candidates, Cand2
Bjarnsholt T et al (2005) Garlic blocks quorum sensing and promotes and Cand7, are involved in Arabidopsis root growth mediated by
rapid clearing of pulmonary Pseudomonas aeruginosa infec- the bacterial quorum-sensing signals N-acyl-homoserine lac-
tions. Microbiology 151:3873–3880. doi:10.1099/mic.0.27955-0 tones. Biochem Biophys Res Commun 417:991–995. doi:10.
Buddrus-Schiemann K et al (2014) Analysis of N-acylhomoserine 1016/j.bbrc.2011.12.066
lactone dynamics in continuous cultures of Pseudomonas putida Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT
IsoF by use of ELISA and UHPLC/qTOF-MS-derived measure- (2009) Priming in systemic plant immunity. Science 324:89–91.
ments and mathematical models. Anal Bioanal Chem doi:10.1126/science.1170025
406:6373–6383. doi:10.1007/s00216-014-8063-6 Karlsson T, Turkina MV, Yakymenko O, Magnusson KE, Vikstrom E
Fuqua WC, Winans SC (1994) A LuxR-LuxI type regulatory system (2012) The Pseudomonas aeruginosa N-acylhomoserine lactone
activates Agrobacterium Ti plasmid conjugal transfer in the quorum sensing molecules target IQGAP1 and modulate
presence of a plant tumor metabolite. J Bacteriol 176:2796–2806 epithelial cell migration. PLoS Pathog 8:e1002953. doi:10.
Götz C et al (2007) Uptake, degradation and chiral discrimination of 1371/journal.ppat.1002953
N-acyl-D/L-homoserine lactones by barley (Hordeum vulgare) Kusari P, Kusari S, Spiteller M, Kayser O (2015) Implications of
and yam bean (Pachyrhizus erosus) plants. Anal Bioanal Chem endophyte-plant crosstalk in light of quorum responses for plant
389:1447–1457. doi:10.1007/s00216-007-1579-2 biotechnology. Appl Microbiol Biotechnol 99:5383–5390
Götz-Rösch C, Sieper T, Fekete A, Schmitt-Kopplin P, Hartmann A, LaSarre B, Federle MJ (2013) Exploiting quorum sensing to confuse
Schröder P (2015) Influence of bacterial N-acyl-homoserine bacterial pathogens. Microbiol Mol Biol Rev 77:73–111. doi:10.
lactones on growth parameters, pigments, antioxidative capac- 1128/MMBR.00046-12
ities and the xenobiotic phase II detoxification enzymes in barley Lin D, Grossfield A (2015) Thermodynamics of micelle formation
and yam bean. Front Plant Sci 6:205. doi:10.3389/fpls.2015. and membrane fusion modulate antimicrobial lipopeptide activ-
00205 ity. Biophys J 109:750–759. doi:10.1016/j.bpj.2015.07.011
Hartmann A, Schikora A (2012) Quorum sensing of bacteria and Liu F, Bian Z, Jia Z, Zhao Q, Song S (2012) The GCR1 and GPA1
trans-kingdom interactions of N-acyl homoserine lactones with participate in promotion of Arabidopsis primary root elongation
eukaryotes. J Chem Ecol 38:704–713. doi:10.1007/s10886-012- induced by N-acyl-homoserine lactones, the bacterial quorum-
0141-7 sensing signals. Mol Plant Microbe Interact 25:677–683. doi:10.
Hartmann A et al (2004) N-acyl homoserine lactones of rhizosphere 1094/MPMI-10-11-0274
bacteria trigger systemic resistance in tomato plants. In: Luna E, Bruce TJ, Roberts MR, Flors V, Ton J (2012) Next-
Lugtenberg B, Tikhonovich I, Provorov N (eds) 11th Interna- generation systemic acquired resistance. Plant Physiol
tional congress on molecular plant-microbe interactions, St. 158:844–853. doi:10.1104/pp.111.187468
Petersburg, Russia, 2004. Biology of plant–microbe interactions. Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anolles G,
APS Press, St. Paul, MI, pp 554–556 Rolfe BG, Bauer WD (2003) Extensive and specific responses of
Hartmann A, Rothballer M, Hense BA, Schröder P (2014) Bacterial a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad
quorum sensing compounds are important modulators of Sci USA 100:1444–1449. doi:10.1073/pnas.262672599
microbe–plant interactions. Front Plant Sci 5:131 Miao C, Liu F, Zhao Q, Jia Z, Song S (2012) A proteomic analysis of
Heidel A, Barazani O, Baldwin I (2010) Interaction between Arabidopsis thaliana seedling responses to 3-oxo-octanoyl-
herbivore defense and microbial signaling: bacterial quorum- homoserine lactone, a bacterial quorum-sensing signal. Biochem
sensing compounds weaken JA-mediated herbivore resistance in Biophys Res Commun 427:293–298. doi:10.1016/j.bbrc.2012.
Nicotiana attenuata. Chemoecology 20:149–154. doi:10.1007/ 09.044
s00049-009-0031-9 Montillet JL et al (2013) An abscisic acid-independent oxylipin
Hense BA, Schuster M (2015) Core principles of bacterial autoin- pathway controls stomatal closure and immune defense in
ducer systems. Microbiol Mol Biol Rev 79:153–169. doi:10. Arabidopsis. PLoS Biol. doi:10.1371/Journal.Pbio.513
1128/MMBR.00024-14 Mueller S, Hilbert B, Dueckershoff K, Roitsch T, Krischke M,
Hense BA, Kuttler C, Mueller J, Rothballer M, Hartmann A, Kreft JU Mueller MJ, Berger S (2008) General detoxification and stress
(2007) Opinion—Does efficiency sensing unify diffusion and responses are mediated by oxidized lipids through TGA
quorum sensing? Nat Rev Microbiol 5:230–239. doi:10.1038/ transcription factors in Arabidopsis. Plant Cell 20:768–785.
Nrmicro1600 doi:10.1105/Tpc.107.054809
Hernández-Reyes C, Schenk ST, Neumann C, Kogel KH, Schikora A Navarova H, Bernsdorff F, Doring AC, Zeier J (2012) Pipecolic acid,
(2014) N-acyl-homoserine lactones-producing bacteria protect an endogenous mediator of defense amplification and priming, is
plants against plant and human pathogens. Microb Biotechnol. a critical regulator of inducible plant immunity. Plant Cell
doi:10.1111/1751-7915.12177 24:5123–5141. doi:10.1105/tpc.112.103564

123
 Plant Mol Biol

Ortiz-Castro R, Martinez-Trujillo M, Lopez-Bucio J (2008) N-acyl-L- Sieper T, Forczek S, Matucha M, Kramer P, Hartmann A, Schröder P
homoserine lactones: a class of bacterial quorum-sensing signals (2013) N-acyl-homoserine lactone uptake and systemic transport
alter post-embryonic root development in Arabidopsis thaliana. in barley rest upon active parts of the plant. New Phytol
Plant, Cell Environ 31:1497–1509. doi:10.1111/j.1365-3040. 201:545–555. doi:10.1111/nph.12519
2008.01863.x Singh RP, Baghel RS, Reddy CR, Jha B (2015) Effect of quorum
Palmer AG, Senechal AC, Mukherjee A, Ane JM, Blackwell HE sensing signals produced by seaweed-associated bacteria on
(2014) Plant responses to bacterial N-acyl-L-homoserine lactones carpospore liberation from Gracilaria dura. Front Plant Sci
are dependent on enzymatic degradation to L-homoserine. ACS 6:117. doi:10.3389/fpls.2015.00117
Chem Biol 9:1834–1845. doi:10.1021/cb500191a Song S, Jia Z, Xu J, Zhang Z, Bian Z (2011) N-butyryl-homoserine
Pang YD, Liu XG, Ma YX, Chernin L, Berg G, Gao KX (2009) lactone, a bacterial quorum-sensing signaling molecule, induces
Induction of systemic resistance, root colonisation and biocon- intracellular calcium elevation in Arabidopsis root cells.
trol activities of the rhizospheric strain of Serratia plymuthica Biochem Biophys Res Commun 414:355–360. doi:10.1016/j.
are dependent on N-acyl homoserine lactones. Eur J Plant Pathol bbrc.2011.09.076
124:261–268. doi:10.1007/S10658-008-9411-1 Ton J et al (2005) Dissecting the beta-aminobutyric acid-induced
Patel HK, Suarez-Moreno ZR, Degrassi G, Subramoni S, Gonzalez priming phenomenon in Arabidopsis. Plant Cell 17:987–999.
JF, Venturi V (2013) Bacterial LuxR solos have evolved to doi:10.1105/tpc.104.029728
respond to different molecules including signals from plants. Veliz-Vallejos DF, van Noorden GE, Yuan M, Mathesius U (2014) A
Front Plant Sci 4:447. doi:10.3389/fpls.2013.00447 Sinorhizobium meliloti-specific N-acyl homoserine lactone quo-
Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, rum-sensing signal increases nodule numbers in Medicago
Kloepper JW (2003) Bacterial volatiles promote growth in truncatula independent of autoregulation. Front Plant Sci
Arabidopsis. Proc Natl Acad Sci USA 100:4927–4932. doi:10. 5:551. doi:10.3389/fpls.2014.00551
1073/pnas.0730845100 Vikström E, Bui L, Konradsson P, Magnusson KE (2010) Role of
Schenk ST, Schikora A (2015) AHL-priming functions via oxylipin calcium signalling and phosphorylations in disruption of the
and salicylic acid. Front Plant Sci 5:784. doi:10.3389/fpls.2014. epithelial junctions by Pseudomonas aeruginosa quorum sensing
00784 molecule. Eur J Cell Biol 89:584–597. doi:10.1016/j.ejcb.2010.
Schenk ST, Stein E, Kogel KH, Schikora A (2012) Arabidopsis 03.002
growth and defense are modulated by bacterial quorum sensing von Rad U et al (2008) Response of Arabidopsis thaliana to N-
molecules. Plant Signal Behav 7:178–181. doi:10.4161/psb. hexanoyl-DL-homoserine-lactone, a bacterial quorum sensing
18789 molecule produced in the rhizosphere. Planta 229:73–85. doi:10.
Schenk ST et al (2014) N-acyl-homoserine lactone primes plants for 1007/s00425-008-0811-4
cell wall reinforcement and induces resistance to bacterial Zarkani AA et al (2013) Homoserine lactones influence the reaction
pathogens via the salicylic acid/oxylipin pathway. Plant Cell of plants to rhizobia. Int J Mol Sci 14:17122–17146. doi:10.
26:2708–2723. doi:10.1105/tpc.114.126763 3390/ijms140817122
Schikora A, Schenk ST, Stein E, Molitor A, Zuccaro A, Kogel KH Zhao Q, Zhang C, Jia Z, Huang Y, Li H, Song S (2015) Involvement
(2011) N-acyl-homoserine lactone confers resistance towards of calmodulin in regulation of primary root elongation by N-3-
biotrophic and hemibiotrophic pathogens via altered activation oxo-hexanoyl homoserine lactone in Arabidopsis thaliana. Front
of AtMPK6. Plant Physiol 157:1407–1418. doi:10.1104/pp.111. Plant Sci 5:807. doi:10.3389/fpls.2014.00807
180604
Schuhegger R et al (2006) Induction of systemic resistance in tomato
by N-acyl-L-homoserine lactone-producing rhizosphere bacteria.
Plant, Cell Environ 29:909–918

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