Annual Review of Phytopathology Volume 51 Issue 1 2013 (Doi 10.1146/annurev-Phyto-082712-102239) Venturi, Vittorio Fuqua, Clay - Chemical Signaling Between Plants and Plant-Pathogenic Bacteria

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Chemical Signaling Between

Plants and Plant-Pathogenic
Bacteria
Vittorio Venturi1, and Clay Fuqua2
1
International Center for Genetic Engineering and Biotechnology, 34149 Trieste, Italy;
email: vittorio.venturi@icgeb.org
2
Department of Biology, Indiana University, Bloomington, Indiana 47405-1847;
email: cfuqua@indiana.edu
Annu. Rev. Phytopathol. 2013. 51:1737
Keywords
The Annual Review of Phytopathology is online at

phyto.annualreviews.org
plant-bacteria interactions, interkingdom signaling, plant phenolic

compounds, quorum sensing, agrobacterium plant signaling,
acylhomoserine lactones, diketopiperazines
This articles doi:

10.1146/annurev-phyto-082712-102239
c 2013 by Annual Reviews.
Copyright
All rights reserved
Corresponding author
Abstract
Studies of chemical signaling between plants and bacteria in the past
have been largely conned to two models: the rhizobial-legume symbiotic association and pathogenesis between agrobacteria and their host
plants. Recent studies are beginning to provide evidence that many
plant-associated bacteria undergo chemical signaling with the plant host
via low-molecular-weight compounds. Plant-produced compounds interact with bacterial regulatory proteins that then affect gene expression.
Similarly, bacterial quorum-sensing signals result in a range of functional responses in plants. This review attempts to highlight current
knowledge in chemical signaling that takes place between pathogenic
bacteria and plants. This chemical communication between plant and
bacteria, also referred to as interkingdom signaling, will likely become
a major research eld in the future, as it allows the design of specic
strategies to create plants that are resistant to plant pathogens.
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INTRODUCTION

It is estimated that land plants evolved more

than 700 mya and that their emergence was
assisted by fungal associations, indicating that
they coevolved with microorganisms (47). In
addition, it is believed that molecular interactions with epiphytic, benecial rhizospheric,
symbiotic, and pathogenic bacteria also played
and continue to play an important role in their
evolution. During the course of these interactions, plants constantly monitor changes in
specic bacterial activities, whereas bacteria respond to variations in plant physiology, with
both organisms continuously making adjustments. This close association for millions of
years has therefore allowed bacteria and plants
to develop mechanisms of production and response for many signaling molecules released
by the host plant and its bacterial community.
Plants release large amounts of chemical
compounds (especially through their roots)
at a signicant cost; in some cases, these
combat pathogenic microorganisms and attract
benecial ones (4). Studies involving several
plant-pathogenic bacterial species have also
shown that they have evolved systems to sense
and respond to low-molecular-weight plant
compounds in order to regulate virulenceassociated traits (8). In fact, bacteria-to-plant
chemical signaling is increasingly recognized
as an important aspect of both benecial and
pathogenic interactions, although the details of
this communication are currently poorly understood. Chemical communication between
plant and bacteria (also called interkingdom
signaling) is an emerging research area that
is likely to continue expanding and represents
a major challenge for the future, with the
underlying reason for this being the large
number of different associations taking place
between plants and bacteria. Understanding
this signaling is pivotal to devising new ways
to improve disease resistance.
Plant compounds potentially involved in
chemical signaling with bacteria are thought
to include sugars, amino acids, and phenolics;
however, current knowledge of secondary plant
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metabolites that can serve as chemical signals

and trigger a bacterial response is very limited.
In addition, many plant compounds are likely
to be produced in trace amounts that are below
the current level of detection. Recent research
has provided evidence that bacteria produce
several compounds that are involved in cell-cell
communication within a bacterial population.
This process is known as quorum sensing (QS)
and is critical for the infection and invasion
processes of many phytopathogens (119). Are
these chemical signals perceived by plants or
do plants produce mimic signals that interfere
with this important bacterial communication
system? Researchers are asking these questions,
and results are beginning to reveal that bacterial
QS signals can behave as interkingdom chemical signals and furthermore that plants produce
compounds that interfere with bacterial QS.
This review focuses on interkingdom
chemical signaling that takes place between
pathogenic bacteria and plants and more specifically on the role of (a) low-molecular-weight
plant compounds in inuencing gene expression via bacterial signal transduction pathways
and of (b) bacterial signaling molecules in inuencing plant responses and gene expression.
We do not attempt to comprehensively review
local or contact-dependent responses by the
plant during pathogen attack (16) or the induction of bacterial gene expression in response
to physical contact with plant tissues or in response to the local nutritional and physical environment (e.g., nitrogen source, carbon source,
and pH temperature), as these have been extensively covered elsewhere (8).
Interkingdom signaling via chemical signals
has been extensively studied in the rhizobialegume symbiosis and between agrobacterial
pathogens and their host (8). Of these two systems only the chemical signaling between plants
and pathogenic Agrobacterium is discussed below, as this review focuses on plant pathogens.
In addition, recent studies have shown (a) the
role of plant phenolic compounds in the regulation of gene expression of virulence-associated
genes in pathogenic bacteria, (b) the role of
bacterial QS signals in regulating plant gene
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expression, and (c) the role of low-molecularweight plant compounds in the interference of
bacterial QS.

A BACTERIAL SUBFAMILY OF
LUXR PROTEINS THAT BIND
AND RESPOND TO PLANT
CHEMICAL SIGNALS
QS via N-acylhomoserine lactones (AHLs) is
used by many proteobacteria to regulate the expression of virulence-associated factors that orchestrate their temporal and spatial production
in the plant (12, 20, 41, 81, 119). QS via AHLs
is thus far the most common system found in
gram-negative bacteria, specically those in the
proteobacteria group. A typical system is composed of a LuxI-family synthase responsible
for synthesizing the AHL signal, which then
interacts at quorum concentrations with the
cognate LuxR-family transcription factors and
affects gene expression (33). AHLs vary in their
structure; they have different acyl chain lengths
(from 4 to 18 carbons) and show variation in the
oxidation state of the C3 position on this acyl
chain (which can be a methylene or a ketone,
or can be hydroxylated). Extensive studies on
AHL-QS have also revealed the presence of
proteins closely related to AHL-QS LuxRs
that specically interact with and respond to
plant signals. This unidirectional interkingdom
signaling circuit has evolved from canonical
AHL-QS systems in which the LuxR protein
no longer responds to endogenously produced
AHLs but rather to plant signals.
Features of Quorum Sensing LuxR

Family Proteins
Members of the family of QS LuxR-type
proteins are transcriptional regulators that
respond to AHLs; most commonly, they are approximately 250 amino acids long and have two
domains separated by a short linker region. The
autoinducer-binding domain is located within
the N-terminal region of the protein (99, 103),
and a DNA-binding helix-turn-helix (HTH)
domain is positioned within the C-terminal
region (17, 18). LuxR-type proteins bind to

DNA at a conserved site called a lux box, which
often consists of an inverted repeat recognition
sequence of a 1820-bp palindrome that is usually located at 42.5 from the transcriptional
start site (25, 107). Many QS LuxR-type proteins are transcriptional activators, but some
can act as repressors (33). The position of the
DNA-binding site dictates whether association
with the protein blocks or stimulates transcription. Most LuxR-type proteins are inactive
in the absence of the AHL. However, there
is a growing list of LuxR-type proteins that
function in the apo-form and are inactivated by
AHL binding. For those LuxR-type proteins
that are AHL-dependent activators, AHL
binding results in a conformational change
that allows the HTH domain to bind DNA
upstream of the 35 site of its target promoters;
the LuxR-AHL complex then recruits RNA
polymerase to the promoter by interacting with
the carboxy-terminal domain (CTD) of its subunit (107), thereby activating transcription
(136). However, binding of the LuxR-AHL
complex within the target promoter can block
transcription. For many of the LuxR-type
repressors, the apo AHL-free form binds
within the target promoter, blocking access
to RNA polymerase, repressing transcription.
When AHL binds to the LuxR-type protein,
conformational changes cause it to release the
promoter and in turn relieve repression (76).
Structural analysis of TraR of Agrobacterium
tumefaciens (118, 136) and SdiA of Escherichia
coli (129) have shown that the AHL-binding
cavity is composed of a -sheet that comprises
ve antiparallel strands with three -helixes on
each side. Binding of the AHL can be crucial
for LuxR protein stability and correct folding;
when TraR is expressed in E. coli in the absence
of its cognate AHL (3-oxo-octanoyl-HSL),
it is quickly proteolized or forms inclusion
bodies (138). However, when 3-oxo-C8-HSL
is present, TraR dimerizes and is folded and
soluble. Similar biochemical properties have
been observed for SdiA and other LuxR
proteins (80, 129), although binding of the
acyl side chain can differ between LuxR-type
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proteins with different cognate AHL ligands

(67). QS LuxR-family proteins show surprisingly low homologies (18% to 25%); however,
95% of them share nine highly conserved
amino acid residues (124, 136). Six of these
are hydrophobic or aromatic and form the
cavity of the AHL-binding domain. With
respect to TraR these are tryptophan 57 (W57 ),
tyrosine 61 (Y61 ), asparagine 70 (D70 ), proline
71 (P71 ), tryptophan 85 (W85 ), and glycine
113 (G113 ). The remaining three highly conserved residues, glutamine 178 (E178 ), leucine
182 (L182 ), and glycine 188 (G188 ), are in the
HTH domain.

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LuxR Solos and Bacterial Response to

Plant Chemical Signals
Many of the genes for LuxR and LuxI regulators are located adjacent to each other, and
in almost all systems studied these genetically
linked regulators function together in QS.
However, many proteobacteria also possess
LuxR-type proteins that are unpaired to a
cognate LuxI synthase. In 2008, an analysis of
265 proteobacterial genomes showed that 68
had a canonical, paired LuxI/LuxR system, and
of these, 45 contained more LuxRs than LuxIs.
Another set of 45 genomes contained only QS
LuxRs (11). These QS LuxR proteins that lack
a genetically linked LuxI have been termed
orphans (31) and, more recently, solos (109).
QS LuxR solos also possess an AHL-binding
domain in the N terminus and a DNA-binding
HTH in the C terminus; they have been
reported to expand the regulatory targets
of the canonical QS systems by responding
to endogenous or exogenous AHLs. For
the latter, they can regulate target genes by
eavesdropping on externally provided AHL
signals produced by neighboring bacteria (1) or
via interkingdom signaling when responding
to eukaryotic signals (28, 42, 108, 134). Two
well-studied solos are QscR from Pseudomonas
aeruginosa, which responds to endogenously
produced AHLs (64), and SdiA from Salmonella
enterica and E. coli, which eavesdrops on AHLs
produced by neighboring bacteria (1, 50, 93).
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A subgroup of LuxR solos has been discovered that is found in plant-associated bacteria
that bind to plant-produced compounds rather
than to AHLs (43, 108, 109). These have differences in one or two of the conserved residues in
the AHL-binding domain, more precisely, W57
and Y61 (positions with respect to TraR), which
are substituted by methionine (M) and tryptophan (W), respectively. It is likely that the evolution of these changes corresponds with the
ability of these proteins to bind low-molecularweight compounds produced by plants rather
than AHLs (17, 28, 29, 134). Members of
this subfamily include XccR of Xanthomonas
campestris, OryR of Xanthomonas oryzae, PsoR
of Pseudomonas uorescens, XagR of Xanthomonas
axonopodis, and NesR in Sinorhizobium meliloti
(87). Interestingly, the luxR solo genes are always found adjacent to the virulence-associated
proline iminopeptidase ( pip) gene (15, 28, 134).
In addition, the promoter region of pip almost
always contains a lux-box-like sequence. Although the exact biological function of these
specic proline iminopeptidase homologs is not
entirely clear, in general these enzymes cleave
the proline from the N terminus of proteins (95)
and can also hydrolyze D-alanine but do so at a
lower level of efciency (3).
OryR of the Rice Pathogen

Xanthomonas oryzae
X. oryzae pv. oryzae (Xoo) is a -proteobacterium
that is a vascular pathogen that causes leaf blight
disease on rice plants (Oryza sativa). Xoo does
not produce AHLs (28) but possesses OryR,
which is part of the subfamily of QS-related
LuxR solo proteins that bind plant compounds.
OryR was indirectly shown to bind to plant
compound(s) since it was found to be insoluble
when overexpressed in the presence of a wide
range of AHLs, but it can be solubilized if rice
plant macerate is provided to the growth media.
In addition, OryR was shown to regulate the
genetically linked pip gene, which possesses a
lux-type box in its promoter region, in response
to plant signals (28). Interestingly, this pip activation increases if macerate from Xoo-infected

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rice is provided to the media, indicating that the

plant compound(s) is more abundant in infected
rice; plants are known to increase production of
many compounds upon pathogen attack (29).
Genome-wide gene expression studies have
shown that OryR is a global regulator, and it
regulates the expression of 8% of the open reading frames (ORFs) in Xoo (42). Strikingly, approximately 20% of the genes that are positively
regulated are implicated in motility or chemotaxis (42). OryR was shown to regulate expression of the gene encoding the agellar regulator
FlhF in response to plant signals via a lux-type
box element in its promoter region. The current working model is that OryR plays a role
in the early phases of infection, allowing Xoo to
sense its arrival on/in the plant; detection of the
signal then results in hypermotility that enables
Xoo to rapidly colonize the vascular system (42).
XccR of the Crucifer Pathogen

Xanthomonas campestris
X. campestris pv. campestris (Xcc) is an important
pathogen infecting a wide variety of brassicas
worldwide. Xcc also contains a gene coding for a
LuxR solo protein called XccR, which is orthologous to OryR of Xoo and also responds to an
as yet unidentied plant compound (134). Just
as in Xoo, pip encodes a proline iminopeptidase
that possesses a lux-type box 20-bp palindromic
sequence in its promoter region and is adjacent
to xccR. Both pip and xccR have been shown to be
important for pathogenicity because null mutants show reduced virulence. Importantly, it
has been observed that activation of pip by XccR
occurs in planta, suggesting that a plant compound(s) is important for this regulation (134).
Induction of pip transcription increases almost
eightfold in planta and has been shown to require the presence of the lux-type box.
XagR of the Soybean Pathogen

Xanthomonas axonopodis
X. axonopodis pv. glycines (Xag) causes bacterial
leaf pustule on soybean (Glycine max). Xag also
contains a LuxR solo called XagR that is orthologous to XccR and OryR and is linked to the
adjacent pip gene (15). Both xagR and pip have

been shown to be important for virulence, and
XagR activates pip transcription in planta. Temporal studies have indicated that pip transcription in planta gradually increases after infection, reaching greatest activity after 72 hours,
before slowly decreasing. This induction of
pip has been suggested to be due to a plant
compound(s) that accumulates in response to
pathogen infectioninducing/activating XagR.
Transcriptome analysis revealed that XagR
regulates 77 ORFs; one of these is yapH, which
is involved in adhesion. It has been postulated
that XagR plays a role in Xag invasion by negatively regulating adhesion via yapH in response
to a plant compound(s) that accumulates upon
infection. The current working model shows
that when no plant signal molecule is detected,
YapH is not repressed and bacterial cells are attached to the plant. As the infection progresses,
XagR accumulates, activating pip transcription
and biosurfactant-related genes and repressing
yapH; this results in a decrease in adhesion,
allowing the cells to spread within the apoplast
and thereby increasing the bacterial load (15).
The LuxR-Solo Family Responding to

Plant Signals is Common Among
Plant-Associated Bacteria
Proteins highly homologous to OryR/XccR/
XagR are also present in the major genera of plant-associated bacteria, including
Xanthomonas, Pseudomonas, Dickeya, Rhodospirillum, Citreicella, Rhizobium, Sinorhizobium,
and Agrobacterium (43). Interestingly, such
LuxR solos are only found in plant-associated
bacteria, reinforcing the model that they are
involved in interkingdom signaling between
plants and bacteria. In addition, all of the genes
have an adjacent pip gene, and the proteins have
similar substitutions in their AHL-binding domains when compared with AHL-binding QS
LuxR-family proteins. Two of these proteins
have been studied in plant-benecial bacteria,
namely PsoR of P. uorescens and NesR of S.
meliloti (86, 108). PsoR of P. uorescens has been
shown to respond to rice and wheat (Triticum
aestivum) but not to cucumber (Cucumis
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sativus), indicating some level of specicity.

PsoR plays a role in biocontrol in rhizospheric
P. uorescens by controlling transcriptional
regulation in response to plant compound(s)
of various antimicrobial-related genes (108).
NesR of S. meliloti has not yet been studied for
its ability to respond to plant compounds but
has been associated with survival under stress
and utilization of various carbon sources (86).

BACTERIAL
N-ACYLHOMOSERINE
LACTONES AS PLANT
CHEMICAL SIGNALS
The long-term close association of AHLproducing bacteria with plants provides an
explanation as to why AHLs have been found
to inuence plant gene expression. AHLs have
thus evolved into interkingdom signals. In
parallel, plants have also evolved the ability to
inuence bacterial AHL-QS systems by producing low-molecular-weight compounds that
interfere by acting as agonists or antagonists
of canonical AHLs in bacteria. The role of
AHLs in plant gene expression, resistance, and
development as well as plant interference, via
AHL mimic compounds, to bacterial AHL-QS
is recently being intensively investigated and
current results and direction are discussed.
N-Acylhomoserine Lactones as Signals

for Plant Gene Expression
Many phytopathogenic bacteria employ
AHL-QS in order to spatially and temporally
express virulence-associated factors in the
plant (119). An outstanding question related
to AHL bacterial signals that has been and is
currently being investigated is whether plants
can also recognize and respond to AHLs. This
phenomenon was rst investigated in depth
in 2003 by Mathesius et al. (74) through a
global proteomic study of the model legume
Medicago truncatula in response to AHLs.
M. truncatula is a close relative of alfalfa
that forms a symbiotic relationship with the
nitrogen-xing symbiont S. meliloti. Axenically
grown M. truncatula roots were exposed to low
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AHL concentrations (10 nM2000 nM), and

root parts were then analyzed for their global
protein content. Such a concentration window
reects production of 3-oxo-C12-HSL (an
AHL produced by several plant pathogens,
including P. aeruginosa) and 3-oxo-C16:1 -HSL
(produced by S. meliloti ) in vitro. Exposure to
these AHLs signicantly changed the levels of
154 proteins variably at 48 h when compared
with a 24-h exposure. The global proteomic
response to AHLs represents approximately
6% of the total identiable proteins; of these,
23% had functions possibly related to plant
defenses and stress response, 14% to protein
degradation or processing, 5% to avonoid
biosynthesis, 5% to plant hormone responses
or synthesis, 10% to regulatory functions, 6%
to cytoskeletal elements, and 37% to primary
metabolism.
A similar global response to AHL exposure
has also been observed using Arabidopsis
thaliana (120). In this case, roots were exposed
to 10 M of C6-HSL, and gene expression via
microarrays was then assayed in leaf and root
tissue at different time points (4 h; 1 and 4 d).
In total, the expression of 721 and 1,095 genes
changed in leaf and root tissue, respectively.
Importantly, 6% of differentially regulated
genes in leaf tissue and 3% in root tissue are
involved in plant hormone response, especially
genes implicated in auxin and cytokinin, which
play critical roles in the control of plant growth
and several developmental responses. In agreement, measurement of auxin and cytokinin
levels after exposure to C6-HSL revealed that
concentration of cytokinin declined, whereas
that of auxin increased compared with the
untreated control plants. Other differentially
transcribed genes were grouped in several
functional categories, including energy and
metabolism (approximately 20%), transcription/translation (approximately 11%), and
lipid/protein/nucleic acidrelated (approximately 8%), as well as category for the remaining genes for which no clear annotated function
could yet be assigned. Surprisingly, exposure
to C6-HSL did not result in the differential
expression of typical/known defense-related
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genes. An earlier study reported that foliar

exposure of A. thaliana to 3-oxo-C8-HSL did
not result in signicant changes in gene expression (130). It therefore appears that plants
display specicity toward AHLs and respond
differently to structurally distinct AHLs.

N-Acylhomoserine Lactones and

Induction of Plant Systemic Resistance
Many AHL-producing bacteria colonize the
rhizosphere of plant roots (26). Most of these
bacteria are benecial [also known as plant
growthpromoting rhizobacteria (PGPR)] to
the plant, resulting in plant growth promotion
and/or protection from microbial pathogens
(71). Mechanisms of disease suppression of
microbial pathogens by PGPR strains include
niche exclusion by competition for nutrients,
production of antimicrobial compounds, and
induction of systemic resistance (ISR), in
which the inducing PGPR and pathogen do
not undergo any type of direct interaction.
ISR is different from pathogen-induced and
salicylate-mediated systemic acquired resistance (SAR) (117, 133). ISR that follows
colonization of PGPR strains leads to enhanced
expression of various signaling pathways, including jasmonate and ethylene. Using a
PGPR Serratia liquefaciens strain that produces
AHLs (C4- and C6-HSL), it was determined
that when gnotobiotically grown tomato plants
were inoculated with the wild-type strain,
the appearance of necrotic cell death and
the presence of fungal DNA after infection
with the fungal leaf pathogen Alternaria
alternata were reduced by more than 70% (98).
However, inoculation with the AHL-negative
mutant also reduced the development of
A. alternatainduced cell death, suggesting
that AHL signaling was in part responsible for
the observed ISR. Importantly, the colonization of the rhizosphere of tomato by both the
wild-type and AHL-negative mutants was comparable. Similar experiments were performed
in tomato and the pathogen A. alternata using a
Pseudomonas putida PGPR strain that produces
at least four different 3-oxo-HSLs with acyl
chains ranging in size from 6 to 12 carbons.

Results showed that P. putida AHLs are also
involved in systemic resistance but to a lesser
extent (98). It was further established that physiological concentrations of C4- and C6-HSLs,
which are produced by S. liquefaciens, resulted
in elevated levels of salicylic acid and increased
expression of several defense loci, including
salicylic acid and ethylene-dependent genes as
well as antioxidant-related loci. ISR by AHLs
was also recently reported in A. thaliana and
barley (Hordeum vulgare) (97). Root exposure
to 3-oxo-C14-HSL led to higher resistance
toward the fungal pathogen Bumeria graminins
in barley and in A. thaliana to the fungus Golovinomyces orontii and the bacterial pathogen Pseudomonas syringae. Further studies on the possible
mechanism revealed that exposure to certain
long-chain-3-substituted AHLs prolongs the
activities of several mitogen-activated protein
kinases (MAPKs) and related cascades involved
in pathogen perception (97). AHLs therefore
need to be further investigated and should be
considered as potential candidates for elicitors
of plant defense as they induce expression of
typical defense-related proteins resulting in
increased resistance against pathogens.
N-Acylhomoserine Lactones Affect

Plant Growth and Development
As described above, AHLs affect gene expression, altering the levels of many proteins,
including those involved in hormonal and
defense functions. Consequently, AHLs have
also been reported to affect plant growth
and development. The growth responses of
A. thaliana to many different bacterial AHLs
suggested that C10-HSL was particularly
active in modifying root system architecture
by affecting primary root growth, lateral root
formation, and root hair development. It was
further established that C10-HSL modulates
primary root growth by inuencing cell division
in the meristem (84). A recent study compared
the effects of exposure to several different AHLs
on the growth of roots and shoots in A. thaliana
(96). Exposure of seedlings to 6-M C6-HSL
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resulted in a signicant increase in root and

shoot biomass after 11 days. This effect on the
shoot biomass decreased as AHLs with longer
acyl side chains were utilized. Root biomass
was only signicantly altered in response to
C6-HSL. In contrast, root length decreased
in response to AHLs with longer acyl side
chains. These experiments also raise the issue
of internalization and transport of AHLs into
the plant. Although transport of short-chain
C4- and C6-HSL from the root to the shoot in
barley and A. thaliana has been demonstrated,
this was not the case for either C10-HSL or
3-oxo-C14-HSL (44, 97, 120). Understanding
the uptake and transport of AHLs needs to
be claried and will be an important aspect of
this interkingdom chemical signaling between
plants and plant-associated bacteria.

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Transgenic Plants Producing

N-Acylhomoserine Lactones and
Bacterial Pathogenesis
As many phytopathogenic bacteria employ
AHL-QS to temporally express virulenceassociated factors in the plant following
successful colonization, several studies have
examined whether providing high exogenous concentrations of AHLs affect bacterial
pathogenicity. Experiments have been performed with transgenic plants that produce
AHLs by expressing a bacterial luxI-type
gene and studying plant susceptibility after challenge with a bacterial pathogen(s).
AHL-producing plants interfere with the QSregulated phenotypes of pathogenic bacteria,
thereby affecting the course of the disease. For
example, transgenic potato and tobacco plants
were engineered to harbor and express the yenI
gene of Yersina enterocolitica, resulting in the
production of C6-HSL and 3-oxo-C6-HSL
(30, 72, 113); both of these AHLs are naturally
produced by the pathogen Erwinia carotovora.
This soft-rot pathogen uses AHL-QS to
regulate the expression of a cocktail of plant
cell walldegrading enzymes (PCWDE) involved in virulence. Upon infection of potato
stems with E. carotovora, differences in disease
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development between the wild-type and transgenic plant were observed, including disease
severity and time of onset: The transgenic
plant displayed a level of disease signicantly
higher than the control. This difference in
pathogenicity was, however, seen only when
the inoculum was below a certain level: No
observable differences were present when the
bacterial inoculum exceeded 106 cells per inoculation site (113). Several experiments have
conrmed that more disease development is
seen in transgenic potatoes than in the control
plants as the level of bacterial inoculum in the
plants is reduced. These data have suggested an
important role for the correct timing of expression of PCWDE via QS either via triggering
host defenses or by another mechanism.
Interestingly, provision of exogenous AHLs
in another plant-pathogen model resulted in
the transgenic plant that produced the AHLs
that were resistant to the bacterial pathogen at
different inoculum levels. These data were obtained using the tobacco pathogen P. syringae
pv. tabaci (Pst), transgenic tobacco that also contained the yenI bacterial gene that directs production of 3-oxo-C6-HSL, and an AHL recognized by Pst (100). Several experiments showed
that providing exogenous AHLs in transgenic
tobacco conferred a decreased susceptibility to
Pst, particularly in the early stages of infection when using a low inoculum concentration (102 cfu leaf disc1 ) (92). It has been proposed that AHL production by the transgenic
plant could induce the expression of virulenceassociated traits even at low population densities, enabling the recognition of the pathogen
by the plant, which consequently initiates a successful defense reaction. The scenario changes
when large numbers of cells are inoculated into
plants, as they are present in sufcient numbers
to better overcome plant defenses and switch
on virulence gene expression.
Plant Interference of Bacterial

Quorum Sensing via
N-Acylhomoserine Lactone Mimics
Several studies have demonstrated that plants
are able to synthesize compounds that mimic

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AHL compounds and interfere with bacterial

QS. This has been observed using plants and
plant extracts (for example, from pea, Medicago
truncatula, and rice) that appear to stimulate
or inhibit AHL-mediated gene expression as
judged using bacterial sensors that do not produce AHLs (5, 23, 37, 54, 106, 112). Most of
the experiments using extracts from plants stimulated rather than inhibited QS-gene expression; however, none of these plant compounds
have yet been chemically identied. Many of
these compounds have been detected in root
exudates, and their chemical properties suggest
that they are distinct from AHLs. Plant mimics acting as agonists of AHL-QS might lead to
pathogen confusion and decreased pathogenicity because they can stimulate premature expression of virulence genes, as indicated by the
work using transgenic plants expressing AHLs
(see above). More progress with respect to AHL
mimics has been achieved using algae, especially
for compounds that inhibit AHL-QS systems
(40, 48, 60, 73, 94, 111). Some of these inhibiting compounds have been identied as halogenated furanones produced by algae (48, 73)
and lumichrome (a derivative of the vitamin riboavin) produced by the alga Chlamydomonas.
A compound inhibiting AHL-QS has also been
identied from leguminous plants and has been
identied as L-canavanine (an arginine analog)
(56). All of these inhibiting compounds have
been implicated in enhancing the proteolytic
degradation of QS LuxR receptors, thus affecting the QS response (60, 94). Research is continuing to focus on identifying QS inhibitors,
as it is believed these will have considerable applications in medicine and agriculture for controlling bacterial populations (7).
CHEMICAL SIGNALING
BETWEEN AGROBACTERIUM
SPECIES AND HOST PLANTS
A. tumefaciens and Agrobacterium rhizogenes are
closely related terrestrial bacteria within the
family Rhizobiaceae of the -proteobacterial
group. The Agrobacterium genus is in fact
polyphyletic with rhizobial genera (including
species of Sinorhizobium, Mesorhizobium, and

Rhizobium), which are symbionts of leguminous plants that supply organic nitrogen to
their hosts (131). However, A. tumefaciens and
A. rhizogenes are pathogenic to plants, often
to those from a wide range of dicotyledonous
species, and cause the diseases known as crown
gall and hairy root. Crown gall is a site of uncontrolled, tumorous tissue growth, typically
at the plant crown (the subterranean-to-aerial
transition zone), whereas hairy root is a large
entangled mass of roots (2, 45). Development
of both diseases on plants requires large virulence plasmids, the tumor-inducing (Ti) plasmid for crown gall and the root-inducing (Ri)
plasmid for hairy root (55, 110). These plasmids encode many of the virulence functions
required for disease, and Agrobacterium derivatives cured of these plasmids (historically described as Agrobacterium radiobacter) are completely avirulent.
The mechanism by which agrobacteria
cause disease is remarkable and relies on
cross-kingdom horizontal gene transfer. The
genes required to drive this process are clustered on each plasmid and are known as vir
(virulence) genes. These vir genes encode as
many as 30 proteins and are organized in up
to 10 operons (137). During pathogenesis,
a specic segment or multiple segments of
the Ti or Ri plasmid are copied from the
so-called T-region (transferred region) of the
plasmid via a conjugation-type mechanism to
generate a single-stranded intermediate called
the T-DNA. The T-DNA and associated
Vir proteins are transferred through a type
IV secretion system from the bacteria into
plant cells at the site of infection (19) and
are ushered into the plant nucleus, where the
T-DNA is stably integrated into the plant
chromosomal DNA (115). T-DNA-specied
gene products drive hormonal imbalances
within the infected tissues, which causes the
visible manifestation of the diseases crown gall
and hairy root. Other T-DNA genes cause the
synthesis and release of unusual metabolites
that are collectively known as opines, which are
consumed by agrobacteria in and around the
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infection site as sources of carbon, nitrogen,

and, in some cases, phosphorus (24). Multiple opine types can be specied by a single
T-DNA, and virulent agrobacteria have
historically been subclassied by the specic
opines that they cause plants to produce upon
infection (131). Genes for opine catabolism are
also encoded on the virulence plasmids. Opine
production from infected tissues provides a
selective benet to the bacteria harboring the
corresponding virulence plasmid, improving
their competitive advantage (91).
The complex processes that lead to agrobacterial disease are tightly regulated, as is the
control circuitry that mediates the transition of
the bacteria to colonizing the opine-producing,
transformed plant tissue (8). The overall process may be viewed as a series of signal
exchanges between the plant and the infecting
agrobacteria. The initial stages of infection,
culminating in T-DNA transfer, are activated
primarily by phenolic compounds, considered
to be lignin precursors, released from wounded
plant tissue, that can be augmented by certain
sugars, low phosphorus levels, and acidic
pH at the site of infection (104). Following
successful transformation of the plant cells,
release of opines is perceived by bacteria in
or around the infected tissue, stimulating
catabolism of the opine(s) and also inducing a
QS process that ultimately results in increased
copy number and conjugation of the virulence
plasmid (58, 123). The intricate, multistage
interplay between pathogenic agrobacteria and
plants is among the best-studied examples of
host-microbe interactions.
A. tumefaciens and A. rhizogenes cause plant
disease via a similar horizontal gene transfer
mechanism. However, the plant-microbe
signaling mechanisms are best studied for A.
tumefaciens. Therefore, the sections that follow
are based primarily on experimental ndings
from A. tumefaciens, but much of it can be
broadly generalized to both species.

PY51CH02-Venturi
Activation of Virulence Functions

The primary regulators of Ti plasmid virulence
gene expression make up a two-component reg26
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ulatory system, with VirA functioning as a histidine sensor kinase and VirG as a DNA-binding
response regulator (105, 126). Phosphorylated
VirG activates expression of most vir genes
with the exception of virA. At least four signals
produced by plant tissues are thought to inuence virulence activation through VirA-VirG.
Phenolic compounds are the primary signal
but are augmented by certain sugars, acidic
conditions, and low levels of phosphorus (125).
A. tumefaciens can respond to a broad
range of phenolic compounds produced
by plants. The optimal phenolic signals
can vary depending on the A. tumefaciens
isolate, but acetosyringone (4 -hydroxy-3 ,5 dimethoxyacetophenone) was one of the rst
characterized vir inducers and is used as a
model phenolic inducer (104). These phenolics
generally share a benzene ring with a hydroxyl
group at position 4 and a methoxy group at
position 3 on the ring (75). Inducing activity
is enhanced by a second methoxy group at ring
position 5. There is signicant variation tolerated at position 1 among active compounds.
Some of the plant-released phenolics can also
be inhibitory to the growth of A. tumefaciens,
and consequently virH2 encodes a cytochrome
P450 that can decrease the toxicity of these
compounds by O-demethylation, in some cases
allowing metabolism of the products (53).
The response to phenolics requires the
VirA-VirG system. VirA is a sensor kinase that
has two transmembrane segments that ank a
large periplasmic domain. On the cytoplasmic
side of the second transmembrane segment is
a so-called linker domain, initially thought to
play a passive connecting function in the protein but now considered to comprise a small
ligand-binding GAF (cGMP-specic phosphodiesterases, adenylyl cyclases and FhlA)-type
motif implicated in the perception of phenolics (39). Associated with the C-terminal portion of the linker domain is the canonical kinase
domain, including the conserved histidine (H)
residue at which autophosphorylation occurs.
Finally, there is a carboxy-terminal receiver domain that is homologous to the aminoterminal
phosphoreceiver domain in response regulators

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and contains a conserved aspartate (D) residue.

Surprisingly, the phenolic inducers were found
to be perceived through interactions with the
cytoplasmic linker domain rather than the
periplasmic domain (14). Although some disagreement remains whether VirA directly binds
to the phenolics (62), it is clear that the VirA
linker region is required for the phenolic response, and the simplest interpretation is that
this is through direct binding to the presumptive GAF domain. Consistent with this model,
several lines of genetic evidence suggest that
VirA imparts specicity to phenolics (63, 68).
The presence of certain monosaccharide
sugars can have a profound impact on VirAVirG-dependent activation of virulence genes,
potentiating the vir response at lower levels
of phenolics. Sugar perception is mediated
through the VirA periplasmic domain and
its interaction with a specic binding protein
known as chvE (chromosomal virulence) that
is similar to other periplasmic, sugar-binding
proteins (10, 101). Inducing sugars bind ChvE
in the periplasm and transduce this information
to an alphahelical region of VirA thought to
resemble sensory domains of methyl chemotaxis proteins (79). There is specicity in the
sugar inducers, and it is thought that the most
active compounds are similar to plant cell wall
components.
Acidic pH also contributes to vir gene
activation in multiple ways. VirA is responsive
to acidic pH, via its periplasmic domain,
through its interaction with ChvE and sugars
(38). In addition, expression of the virG gene
is activated under low pH via one of its two
promoters (125), presumably by the ChvGChvI two-component system, which is known
to mediate a transcriptional response to low
pH (132). VirG levels are limiting for vir gene
induction, so increases in VirG levels would
boost the strength of the response to phenolics.
Expression of virG is also activated by limiting
phosphate availability through the activity of its
other promoter (125). This is presumed to be
through the PhoR-PhoB, which is a phosphateresponsive two-component system. Activation
of virG requires so called pho box promoter
sequences, but PhoR-PhoB-dependent regulation has never been established, probably

because of the essentiality of phoR and phoB in
A. tumefaciens (21).
Response to Opines
Successful A. tumefaciens transformation of
plants with the natural T-DNA is a very
energetically expensive process, but the payoff
for the pathogen is access to opines, which
are a source of custom nutrients (90, 91). For
wild-type A. tumefaciens, catabolic functions for
opines are largely encoded on the Ti plasmid.
The presence of opines produced by crown
gall tissue can be viewed as an indicator of
successful transformation. Opines are generally
taken up via active transport, and once in the
cytoplasm, can interact with opine-responsive
transcriptional regulators that control the
plasmid-encoded catabolic functions (46, 116).
These systems are regulated much like other
catabolic systems in bacteria, in which the
genes specifying uptake and degradation are
only strongly expressed in the presence of the
catabolite. Several opine-responsive repressors
and activators have been identied, representing completely different protein families
(6, 121). Opines derived from amino acids,
such as octopine and nopaline, are recognized
by LysR-type transcription regulators. For
example, in the presence of octopine, the OccR
protein activates a promoter upstream of a
large 15-kb operon that encodes the octopine
uptake system and catabolic functions (35, 46).
For other opines derived from sugars, such as
the agrocinopines and mannopine, LacI-type
repressors (AccR and MocR, respectively)
function to limit catabolic gene function in the
absence of the catabolite, and these genes are
derepressed when the inducing opine binds
and inactivates the repressor (6). In either case,
catabolic capacity for the opine is strongly
elevated in the tumor environment.
Opine Signals Activate

Quorum Sensing
In addition to the regulation of opine
catabolism, interbacterial conjugation of the Ti
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plasmid from Ti-harboring strains to recipient

agrobacteria lacking the Ti plasmid is activated
by a subset of the opines, known as conjugal
opines, produced from infected tissues (27,
58). Extensive studies have determined in the
best-studied A. tumefaciens strains that although
opines are absolutely required for conjugation,
they do not directly activate conjugal transfer
(tra) genes. Rather, conjugal opines induce the
expression of the QS LuxR-type transcriptional
activator called TraR (36, 88, 135). TraR was
one of the rst LuxR-type proteins, in addition
to LuxR itself, found to respond to AHLs and
to drive the QS process. TraR responds to
3-oxo-octanoyl-L-homoserine lactone (3-oxoC8-HSL), the synthesis of which is directed by
the TraI AHL synthase, also encoded on the
Ti plasmid (36, 52, 78). TraR-AHL complexes
activate expression of the tra operons, driving
conjugation in response to the population
density of Ti plasmidharboring bacteria (34).
The traI gene is also activated by TraR, creating a positive feedback loop. The Ti plasmid
replication genes are also under TraR control,
and thus the plasmid copy number is increased
as a function of QS (65, 85). An antiactivator
protein called TraM is required to keep TraR
in the inactive conguration through formation
of a heterocomplex, and traM itself is under
TraR control, creating a negative feedback
loop (32, 51). Remarkably, the strict opinedependent regulation of traR expression has
been maintained between different A. tumefaciens strains, even though the regulators, operon
organization, and regulatory mechanism can
be quite different. For example, the LysR-type
regulator OccR activates traR expression, and
hence conjugation and increased copy number
in response to octopine, the conjugal opine
for octopine-type plasmids (35). In contrast,
the LacI-type repressor AccR represses traR
expression, but is inactivated by agrocinopine,
the conjugal opine for nopaline-type Ti plasmids (89). There is clearly a strong selection for
the TraR-dependent QS control to be under
the strict regulation of plant-released opines.
A further twist on opine control is found in the
octopine-type A. tumefaciens strains, in which

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the mannityl opines that are also specied by

the T-DNA of this strain activate expression of
a truncated TraR homolog, known as TrlR (or
TraS), and this serves as an additional inhibitor
of TraR-dependent activation (13, 82). In this
case, the mixture of opines produced by the
infected plant dictates the copy number of
the Ti plasmid and the degree to which it is
horizontally transferred. It is not clear what advantage, if any, this baroque opine-dependent
control of the Ti plasmid might provide.
PLANT PHENOLICS AS SIGNALS

FOR PHYTOPATHOGENIC
BACTERIAL GENE EXPRESSION
IN OTHER BACTERIAL SPECIES
Studies on the induction of toxigenesis in
the plant pathogen P. syringae pv. syringae
(a leaf pathogen of several crops) revealed
that virulence genes were induced by specic
plant signal molecules. More precisely, the
genes involved in the biosynthesis of the
two lipodepsipeptide phytotoxins (syringomcyin and syringopeptin) that are synthesized
nonribosomally are induced by plant signal
molecules (77, 122). The syr and syp gene
clusters encoding for syringomycin and syringopeptin biosynthesis, respectively, are
adjacent, consisting of a genomic region of
approximately 132 kb. These loci are under
the control of the SalA and SyrF regulators
(69, 70, 122). Another element involved in the
regulation of syr and syp expression is the global
two-component GacA/GacS signal transduction system, which regulates salA and syrF (57,
69). Importantly, induction of syr and syp genes,
which leads to the phytotoxin synthesis, occurs
in the plant environment via a response to the
plant signal molecules arbutin and D-fructose
(122). The current working model shows that
P. syringae senses the signal molecules in the
plant apoplast via the GacS transmembrane
sensor or some currently unidentied sensor.
GacS then leads to activation of salA transcription via the GacA response regulator; nally,
SalA activates expression of the syrF regulator,
which then directly transcriptionally activates

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syr and syp genes. This model has several points

of uncertainty, especially regarding which regulatory protein(s) senses the plant compounds
and whether more plant signals are involved.
Interestingly, the regulation of lipodepsipeptide by plant compounds via GacA/GacS has
also been reported for a benecial rhizosphere
PGPR Pseudomonas strain (61).
Plant phenolic compounds have also been
shown to regulate virulence genes in plantpathogenic Dickeya dadantii, the causative agent
of soft-rot, wilt, and blight diseases on several plant species. Studies have shown that
plant phenolics o-coumaric acid (OCA) and tcinnamic acid (TCA) affect expression of the
type III secretion system (T3SS) (66, 128). As
the main role of the T3SS of phytopathogens is
to neutralize the plant host defense system during bacterial invasion, it is important that it is
activated in planta. Three T3SS-related genes
(dspE, which encodes a T3SS effector; hrpA,
which encodes a structural protein of the T3SS
pilus; and hrpN, which encodes for a T3SS hairpin) are induced by TCA and OCA at concentrations that mimic physiological in planta conditions. Just as with P. syringae, this regulation
in response to plant phenolic compounds requires the GacA/GacS system. Evidence suggests that GacA/GacS regulates the levels of the
regulatory RNA rsmB, which then modulates
the activity of the RsmA posttranscriptional
regulator, affecting RNA levels of target genes
(66, 128). Interestingly, very recently plant phenolic compounds that induce T3SS genes via
GacA/GacS have also been reported to act in
the human opportunistic pathogen P. aeruginosa, which can also associate with plants (127).
BACTERIAL
DIKETOPIPERAZINES AS
PLANT SIGNALS
Diketopiperazines (DKPs) are cyclodipeptides
produced by several bacterial species. Their
current biological role in bacteria is not clear,
but they may represent a new class of bacterial
QS signals (59, 102). Furthermore, in gramnegative bacteria they have also been reported
to interfere with AHL-QS, further highlighting their possible role in cell-cell signaling (9,
22, 49). Recently, DKPs have been implicated
in interkingdom signaling between plants and
bacteria, whereby bacterially produced DKPs
have a role in plant signaling (83). Three
DKPs produced by P. aeruginosa, cyclo(L-ProL-Tyr), cyclo(L-Pro-L-Val), and cyclo(L-ProL-Phe), stimulate root and shoot biomass and
lateral root development in A. thaliana. Interestingly, production of these three compounds
in P. aeruginosa is negatively regulated by the
LasI/R AHL-QS system (83). Importantly, the
three DKPs produced by P. aeruginosa possess a heterocyclic system also found in auxin,
and all three show a weak auxin-like activity. Several lines of evidence, including computational molecular docking analysis with the
TIR1 auxin receptor, indicate that DKPs could
act as auxin signal mimics (83). Interestingly,
several plant growthpromoting Pseudomonas
spp. release several DKPs (22, 49), hence these
could be involved in plant growth promotion.
It is therefore possible that further studies on
DKPs will reveal that they represent a new class
of molecules involved in bacterial and interkingdom signaling.
SUMMARY POINTS
1. Interkingdom chemical signaling has been extensively studied between agrobacterial
pathogens and their host, and this has revealed complex and pervasive interkingdom
communication.
2. The recent nding of a widespread bacterial LuxR subfamily of proteins that binds plant
compounds and regulates plant-bacteria interactions is evidence that the same family of
proteins that are involved in bacterial communication can also serve in interkingdom
signaling.
29
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3. Plant phenolic compounds affect gene expression in several bacterial species that directly
or indirectly involve the GacA/GacS two-component system.
4. Bacterial QS signals can behave as plant cues linking QS to interkingdom signaling.
Plants have a range of functional responses to AHLs that might have important roles in
pathogenic outcomes.
5. Plants produce AHL-mimic compounds that may be involved in QS interference, suggesting an important role in pathogenic interactions.
6. Bacterial DKPs may represent a new class of signaling molecules involved in bacterial
and interkingdom signaling.
7. Current knowledge in interkingdom signaling is limited and will most probably become
a major research eld in the future.
8. Many compounds produced by plants inuence their interactions with bacteria.
9. The interaction of A. tumefaciens with plants represents a well-characterized series of
plant-microbe and microbe-microbe signaling processes.
10. Plant interkingdom signaling molecules can possibly result in temporal and spatial regulation directing complex changes in bacterial gene expression affecting plant-bacteria
interaction.
11. Understanding interkingdom signaling will allow the future design of specic strategies
to create plants with enhanced resistance to plant pathogens.
FUTURE ISSUES
1. Are many of the low-molecular-weight compounds synthesized de novo by plants upon
pathogen attack involved in interkingdom signaling?
2. Are plant interkingdom signals host-specic or conserved throughout the plant kingdom?
3. Do plant-benecial and pathogenic bacteria respond to the same plant interkingdom
signals?
4. Strigolactones have been recently shown to be important interkingdom signals between plant and mycorrhizal fungi. Are these molecules also involved in plant-bacteria
communication?
5. Are specic host-pathogen signals, as are found in Agrobacterium, common among plantassociated bacteria?
6. Are there other unrecognized subfamilies of regulatory proteins widely found in plantassociated bacteria that bind and respond to plant signals?
DISCLOSURE STATEMENT
The authors are not aware of any afliations, memberships, funding, or nancial holdings that
might be perceived as affecting the objectivity of this review.
30
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ACKNOWLEDGMENTS
The laboratory of V.V. is supported by Progetto AGER (grant number 20102369), by the Italian
Institute of Technology via the project Inese, and by ICGEB core funding. Research on Agrobacterium and quorum sensing in the laboratory of C.F. is supported by the U.S. National Institutes
of Health (GM092660, GM080546) and the U.S. National Science Foundation (MCB-0703467).

LITERATURE CITED
1. Ahmer BM. 2004. Cell-to-cell signalling in Escherichia coli and Salmonella enterica. Mol. Microbiol. 52:933
45
2. Aloni R, Ullrich CI. 2008. Biology of crown gall tumors. See Ref. 114, pp. 56591
3. Alonso J, Garcia JL. 1996. Proline iminopeptidase gene from Xanthomonas campestris pv. citri. Microbiology
142(10):295157
4. Badri DV, Weir TL, van der Lelie D, Vivanco JM. 2009. Rhizosphere chemical dialogues: plant-microbe
interactions. Curr. Opin. Biotechnol. 20:64250
5. Bauer WD, Mathesius U. 2004. Plant responses to bacterial quorum sensing signals. Curr. Opin. Plant
Biol. 7:42933
6. Beck von Bodman S, Majerczak DR, Coplin DL. 1998. A negative regulator mediates quorum-sensing
control of exopolysaccharide production in Pantoea stewartii subsp. stewartii. Proc. Natl. Acad. Sci. USA
95:768792
7. Bjarnsholt T, Givskov M. 2007. Quorum-sensing blockade as a strategy for enhancing host defences
against bacterial pathogens. Philos. Trans. R. Soc. Lond. B 362:121322
8. Brencic A, Winans SC. 2005. Detection of and response to signals involved in host-microbe interactions
by plant-associated bacteria. Microbiol. Mol. Biol. Rev. 69:15594
9. Campbell J, Lin Q, Geske GD, Blackwell HE. 2009. New and unexpected insights into the modulation
of LuxR-type quorum sensing by cyclic dipeptides. ACS Chem. Biol. 4:105159
10. Cangelosi GA, Ankenbauer RG, Nester EW. 1990. Sugars induce the Agrobacterium virulence genes
through a periplasmic binding protein and a transmembrane signal protein. Proc. Natl. Acad. Sci. USA
87:670812
11. Case RJ, Labbate M, Kjelleberg S. 2008. AHL-driven quorum-sensing circuits: their frequency and
function among the Proteobacteria. ISME J. 2:34549
12. Cha C, Gao P, Chen YC, Shaw PD, Farrand SK. 1998. Production of acyl-homoserine lactone quorumsensing signals by gram-negative plant-associated bacteria. Mol. Plant-Microbe Interact. 11:111929
13. Chai Y, Zhu J, Winans SC. 2001. TrlR, a defective TraR-like protein of Agrobacterium tumefaciens, blocks
TraR function in vitro by forming inactive TrlR:TraR dimers. Mol. Microbiol. 40:41421
14. Chang C-H, Winans SC. 1992. Functional roles assigned to the periplasmic, linker, and receiver domains
of the Agrobacterium tumefaciens VirA protein. J. Bacteriol. 174:703339
15. Chatnaparat T, Prathuangwong S, Ionescu M, Lindow SE. 2012. XagR, a LuxR homolog, contributes to
the virulence of Xanthomonas axonopodis pv. glycines to soybean. Mol. Plant-Microbe Interact. 25:110417
16. Chisholm ST, Coaker G, Day B, Staskawicz BJ. 2006. Host-microbe interactions: shaping the evolution
of the plant immune response. Cell 124:80314
17. Choi SH, Greenberg EP. 1991. The C-terminal region of the Vibrio scheri LuxR protein contains an
inducer-independent lux gene activating domain. Proc. Natl. Acad. Sci. USA 88:1111519
18. Choi SH, Greenberg EP. 1992. Genetic dissection of DNA binding and luminescence gene activation
by the Vibrio scheri LuxR protein. J. Bacteriol. 174:406469
19. Christie PJ, Atmakuri K, Krishnamoorthy V, Jakubowski S, Cascales E. 2005. Biogenesis, architecture,
and function of bacterial type IV secretion systems. Annu. Rev. Microbiol. 59:45185
20. Danhorn T, Fuqua C. 2007. Biolm formation by plant-associated bacteria. Annu. Rev. Microbiol. 61:401
22
21. Danhorn T, Hentzer M, Givskov M, Parsek M, Fuqua C. 2004. Phosphorous limitation enhances biolm
formation of the plant pathogen Agrobacterium tumefaciens through the PhoR-PhoB regulatory system.
J. Bacteriol. 186:4492501
31
ARI
1 July 2013
18:30
22. Degrassi G, Aguilar C, Bosco M, Zahariev S, Pongor S, Venturi V. 2002. Plant growthpromoting
Pseudomonas putida WCS358 produces and secretes four cyclic dipeptides: cross-talk with quorum sensing
bacterial sensors. Curr. Microbiol. 45:25054
23. Degrassi G, Devescovi G, Solis R, Steindler L, Venturi V. 2007. Oryza sativa rice plants contain molecules
which activate different quorum sensing N-acyl homoserine lactone biosensors and are sensitive to the
specic AiiA lactonase. FEMS Microbiol. Lett. 269:21320
24. Dessaux Y, Petit A, Farrand SK, Murphy PJ. 1998. Opines and opine-like molecules involved in plantRhizobiaceae interactions. In The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria, ed. HP
Spaink, A Kondorosi, PJJ Hooykaas, pp. 17397. Boston: Kluwer Acad.
25. Devine JH, Shadel GS, Baldwin TO. 1989. Identication of the operator of the lux regulon from the
Vibrio scheri strain ATCC7744. Proc. Natl. Acad. Sci. USA 86:568892
26. Elasri M, Delorme S, Lemanceau P, Stewart G, Laue B, et al. 2001. Acyl-homoserine lactone production
is more common among plant-associated Pseudomonas spp. than among soilborne Pseudomonas spp. Appl.
Environ. Microbiol. 67:1198209
27. Ellis JG, Kerr A, Petit A, Tempe J. 1982. Conjugal transfer of nopaline and agropine Ti-plasmids: the
role of agrocinopines. Mol. Gen. Genet. 186:26973
28. Ferluga S, Bigirimana J, Hofte M, Venturi V. 2007. A LuxR homologue of Xanthomonas oryzae pv. oryzae
is required for optimal rice virulence. Mol. Plant Pathol. 8:52938
29. Ferluga S, Venturi V. 2009. OryR is a LuxR-family protein involved in interkingdom signaling between
pathogenic Xanthomonas oryzae pv. oryzae and rice. J. Bacteriol. 191:89097
30. Fray RG. 2002. Altering plant-microbe interaction through articially manipulating bacterial quorum
sensing. Ann. Bot. 89:24553
31. Fuqua C. 2006. The QscR quorum-sensing regulon of Pseudomonas aeruginosa: an orphan claims its
identity. J. Bacteriol. 188:316971
32. Fuqua C, Burbea M, Winans SC. 1995. Activity of the Agrobacterium Ti plasmid conjugal transfer
regulator TraR is inhibited by the product of the traM gene. J. Bacteriol. 177:136773
33. Fuqua C, Parsek MR, Greenberg EP. 2001. Regulation of gene expression by cell-to-cell communication:
acyl-homoserine lactone quorum sensing. Annu. Rev. Genet. 35:43968
34. Fuqua C, Winans SC. 1996. Conserved cis-acting promoter elements are required for density-dependent
transcription of Agrobacterium tumefaciens conjugal transfer genes. J. Bacteriol. 178:43540
35. Fuqua C, Winans SC. 1996. Localization of the OccR-activated and TraR-activated promoters that
express two ABC-type permeases and the traR gene of the Ti plasmid pTiR10. Mol. Microbiol. 20:1199
210
36. Fuqua WC, Winans SC. 1994. A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid
conjugal transfer in the presence of a plant tumor metabolite. J. Bacteriol. 176:2796806
37. Gao M, Teplitski M, Robinson JB, Bauer WD. 2003. Production of substances by Medicago truncatula
that affect bacterial quorum sensing. Mol. Plant-Microbe Interact. 16:82734
38. Gao R, Lynn DG. 2005. Environmental pH sensing: resolving the VirA/VirG two-component system
inputs for Agrobacterium pathogenesis. J. Bacteriol. 187:218289
39. Gao R, Lynn DG. 2007. Integration of rotation and piston motions in coiled-coil signal transduction.
J. Bacteriol. 189:604856
40. Givskov M, de Nys R, Maneeld M, Gram L, Maximilien R, et al. 1996. Eukaryotic interference with
homoserine lactone-mediated prokaryotic signalling. J. Bacteriol. 178:661822
41. Gonzalez JE, Marketon MM. 2003. Quorum sensing in nitrogen-xing rhizobia. Microbiol. Mol. Biol.
Rev. 67:57492
42. Gonzalez JF, Myers MP, Venturi V. 2013. The inter-kingdom solo OryR regulator of Xanthomonas
oryzae is important for motility. Mol. Plant Pathol. 14:21121
43. Gonzalez JF, Venturi V. 2013. A novel widespread interkingdom signaling circuit. Trends Plant Sci.
18:16774
44. Gotz C, Fekete A, Gebefuegi I, Forczek ST, Fuksova K, et al. 2007. Uptake, degradation and chiral discrimination of N-acyl-D/L-homoserine lactones by barley (Hordeum vulgare) and yam bean (Pachyrhizus
erosus) plants. Anal. Bioanal. Chem. 389:144757

PY51CH02-Venturi
32
Venturi
Fuqua

PY51CH02-Venturi
ARI
1 July 2013
18:30
45. Guillon S, Tremouillaux-Guiller J, Pati PK, Rideau M, Gantet P. 2006. Hairy root research: recent
scenario and exciting prospects. Curr. Opin. Plant Biol. 9:34146
46. Habeeb LF, Wang L, Winans SC. 1991. Transcription of the octopine catabolism operon of the Agrobacterium tumorinducing plasmid pTiA6 is activated by a LysR homolog. Mol. Plant-Microbe Interact.
4:37985
47. Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB. 2001. Molecular evidence
for the early colonization of land by fungi and plants. Science 293:112933
48. Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, et al. 2002. Inhibition of quorum sensing
in Pseudomonas aeruginosa biolm bacteria by a halogenated furanone compound. Microbiology 148:87102
49. Holden MT, Ram Chhabra S, de Nys R, Stead P, Bainton NJ, et al. 1999. Quorum-sensing cross
talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other
gram-negative bacteria. Mol. Microbiol. 33:125466
50. Hughes DT, Terekhova DA, Liou L, Hovde CJ, Sahl JW, et al. 2010. Chemical sensing in mammalian
host-bacterial commensal associations. Proc. Natl. Acad. Sci. USA 107:983136
51. Hwang I, Cook DM, Farrand SK. 1995. A new regulatory element modulates homoserine lactonemediated autoinduction of Ti plasmid conjugal transfer. J. Bacteriol. 177:44958
52. Hwang I, Li P-L, Zhang L, Piper KR, Cook DM, et al. 1994. TraI, a LuxI homologue, is responsible
for production of conjugation factor, the Ti plasmid N-acylhomoserine lactone autoinducer. Proc. Natl.
Acad. Sci. USA 91:463943
53. Kalogeraki VS, Zhu J, Eberhard A, Madsen EL, Winans SC. 1999. The phenolic vir gene inducer ferulic
acid is O-demethylated by the VirH2 protein of an Agrobacterium tumefaciens Ti plasmid. Mol. Microbiol.
34:51222
54. Karamanoli K, Lindow SE. 2006. Disruption of N-acyl homoserine lactone-mediated cell signaling and
iron acquisition in epiphytic bacteria by leaf surface compounds. Appl. Environ. Microbiol. 72:767886
55. Kerr A. 1969. Transfer of virulence between isolates of Agrobacterium. Nature 223:117576
56. Keshavan ND, Chowdhary PK, Haines DC, Gonzalez JE. 2005. L-Canavanine made by Medicago sativa
interferes with quorum sensing in Sinorhizobium meliloti. J. Bacteriol. 187:842736
57. Kitten T, Kinscherf TG, McEvoy JL, Willis DK. 1998. A newly identied regulator is required for
virulence and toxin production in Pseudomonas syringae. Mol. Microbiol. 28:91729
58. Klapwijk PM, Scheulderman T, Schilperoort R. 1978. Coordinated regulation of octopine degradation
and conjugative transfer of Ti plasmids in Agrobacterium tumefaciens: evidence for a common regulatory
gene and separate operons. J. Bacteriol. 136:77585
59. Klose KE. 2006. Increased chatter: cyclic dipeptides as molecules of chemical communication in Vibrio
spp. J. Bacteriol. 188:202526
60. Koch B, Liljefors T, Persson T, Nielsen J, Kjelleberg S, Givskov M. 2005. The LuxR receptor: the sites
of interaction with quorum-sensing signals and inhibitors. Microbiology 151:3589602
61. Koch B, Nielsen TH, Sorensen D, Andersen JB, Christophersen C, et al. 2002. Lipopeptide production
in Pseudomonas sp. strain DSS73 is regulated by components of sugar beet seed exudate via the Gac
two-component regulatory system. Appl. Environ. Microbiol. 68:450916
62. Lee K, Dudley MW, Hess KM, Lynn DG, Joerger RD, Binns AN. 1992. Mechanism of activation
of Agrobacterium virulence genes: identication of phenol-binding proteins. Proc. Natl. Acad. Sci. USA
89:866670
63. Lee YW, Jin S, Sim WS, Nester EW. 1995. Genetic evidence for direct sensing of phenolic compounds
by the VirA protein of Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. USA 92:1224549
64. Lequette Y, Lee JH, Ledgham F, Lazdunski A, Greenberg EP. 2006. A distinct QscR regulon in the
Pseudomonas aeruginosa quorum-sensing circuit. J. Bacteriol. 188:336570
65. Li PL, Farrand SK. 2000. The replicator of the nopaline-type Ti plasmid pTiC58 is a member of the
repABC family and is inuenced by the TraR-dependent quorum-sensing regulatory system. J. Bacteriol.
182:17988
66. Li Y, Peng Q, Selimi D, Wang Q, Charkowski AO, et al. 2009. The plant phenolic compound p-coumaric
acid represses gene expression in the Dickeya dadantii type III secretion system. Appl. Environ. Microbiol.
75:12238
33
ARI
1 July 2013
18:30
67. Lintz MJ, Oinuma K, Wysoczynski CL, Greenberg EP, Churchill ME. 2011. Crystal structure of QscR,
a Pseudomonas aeruginosa quorum sensing signal receptor. Proc. Natl. Acad. Sci. USA 108:1576368
68. Lohrke SM, Yang H, Jin S. 2001. Reconstitution of acetosyringone-mediated Agrobacterium tumefaciens
virulence gene expression in the heterologous host Escherichia coli. J. Bacteriol. 183:370411
69. Lu SE, Scholz-Schroeder BK, Gross DC. 2002. Characterization of the salA, syrF, and syrG regulatory
genes located at the right border of the syringomycin gene cluster of Pseudomonas syringae pv. syringae.
Mol. Plant Microbe Interact. 15:4353
70. Lu SE, Wang N, Wang J, Chen ZJ, Gross DC. 2005. Oligonucleotide microarray analysis of the salA regulon controlling phytotoxin production by Pseudomonas syringae pv. syringae. Mol. Plant Microbe Interact.
18:32433
71. Lugtenberg B, Kamilova F. 2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63:541
56
72. Mae A, Montesano M, Koiv V, Palva ET. 2001. Transgenic plants producing the bacterial pheromone
N-acyl-homoserine lactone exhibit enhanced resistance to the bacterial phytopathogen Erwinia carotovora. Mol. Plant Microbe Interact. 14:103542
73. Maneeld M, Rasmussen TB, Henzter M, Andersen JB, Steinberg P, et al. 2002. Halogenated furanones
inhibit quorum sensing through accelerated LuxR turnover. Microbiology 148:111927
74. Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anolles G, et al. 2003. Extensive and specic
responses of a eukaryote to bacterial quorum-sensing signals. Proc. Natl. Acad. Sci. USA 100:144449
75. Melchers LS, Regensburg-Tuink AJ, Schilperoort RA, Hooykaas PJ. 1989. Specicity of signal molecules
in the activation of Agrobacterium virulence gene expression. Mol. Microbiol. 3:96977
76. Minogue TD, Wehland-von Trebra M, Bernhard F, von Bodman SB. 2002. The autoregulatory role of
EsaR, a quorum-sensing regulator in Pantoea stewartii ssp. stewartii: evidence for a repressor function.
Mol. Microbiol. 44:162535
77. Mo YY, Geibel M, Bonsall RF, Gross DC. 1995. Analysis of sweet cherry (Prunus avium L.) leaves for
plant signal molecules that activate the syrB gene required for synthesis of the phytotoxin, syringomycin,
by Pseudomonas syringae pv syringae. Plant Physiol. 107:60312
78. More MI, Finger LD, Stryker JL, Fuqua C, Eberhard A, Winans SC. 1996. Enzymatic synthesis of a
quorum-sensing autoinducer through use of dened substrates. Science 272:165558
79. Nair GR, Lai X, Wise AA, Rhee BW, Jacobs M, Binns AN. 2011. The integrity of the periplasmic
domain of the VirA sensor kinase is critical for optimal coordination of the virulence signal response in
Agrobacterium tumefaciens. J. Bacteriol. 193:143648
80. Nasser W, Reverchon S. 2007. New insights into the regulatory mechanisms of the LuxR family of
quorum sensing regulators. Anal. Bioanal. Chem. 387:38190
81. Newton JA, Fray RG. 2004. Integration of environmental and host-derived signals with quorum sensing
during plant-microbe interactions. Cell. Microbiol. 6:21324
82. Oger P, Kim K-S, Sackett RL, Piper KR, Farrand SK. 1998. Octopine-type Ti plasmids code for a
mannopine-inducible dominant-negative allele of traR, the quorum-sensing activator that regulates Ti
plasmid conjugal transfer. Mol. Microbiol. 27:27788
83. Ortz-Castro R, Diaz-Perez C, Martinez-Trujillo M, del Rio RE, Campos-Garcia J, Lopez-Bucio J.
2011. Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants. Proc.
Natl. Acad. Sci. USA 108:725358
84. Ortz-Castro R, Martnez-Trujillo M, Lopez-Bucio J. 2008. N-acyl-L-homoserine lactones: a class of
bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant
Cell Environ. 31:1497
85. Pappas KM, Winans SC. 2003. A LuxR-type regulator from Agrobacterium tumefaciens elevates Ti plasmid
copy number by activating transcription of plasmid replication genes. Mol. Microbiol. 48:105973
86. Patankar AV, Gonzalez JE. 2009. An orphan LuxR homolog of Sinorhizobium meliloti affects stress
adaptation and competition for nodulation. Appl. Environ. Microbiol. 75:94655
87. Patankar AV, Gonzalez JE. 2009. Orphan LuxR regulators of quorum sensing. FEMS Microbiol. Rev.
33:73956
88. Piper KR, Beck von Bodman S, Farrand SK. 1993. Conjugation factor of Agrobacterium tumefaciens
regulates Ti plasmid transfer by autoinduction. Nature 362:44850

PY51CH02-Venturi
34
Venturi
Fuqua

PY51CH02-Venturi
ARI
1 July 2013
18:30
89. Piper KR, Beck von Bodman S, Hwang I, Farrand SK. 1999. Hierarchical gene regulatory systems arising
from fortuitous gene associations: controlling quorum sensing by the opine regulon in Agrobacterium.
Mol. Microbiol. 32:107789
90. Platt TG, Bever JD, Fuqua C. 2012. A cooperative virulence plasmid imposes a high tness cost under
conditions that induce pathogenesis. Proc. R. Soc. B 279:169199
91. Platt TG, Fuqua C, Bever JD. 2012. Resource and competitive dynamics shape the benets of public
goods cooperation in a plant pathogen. Evol. Int. J. Org. Evol. 66:195365
92. Quinones B, Dulla G, Lindow SE. 2005. Quorum sensing regulates exopolysaccharide production,
motility, and virulence in Pseudomonas syringae. Mol. Plant-Microbe Interact. 18:68293
93. Rahmati S, Yang S, Davidson AL, Zechiedrich EL. 2002. Control of the AcrAB multidrug efux pump
by quorum sensing regulator SdiA. Mol. Microbiol. 43:67785
94. Rajamani S, Bauer WD, Robinson JB, Farrow JM 3rd, Pesci EC, et al. 2008. The vitamin riboavin
and its derivative lumichrome activate the LasR bacterial quorum-sensing receptor. Mol. Plant-Microbe
Interact. 21:118492
95. Sarid S, Berger A, Katchalski E. 1959. Proline iminopeptidase. J. Biol. Chem. 234:174046
96. Schenk ST, Stein E, Kogel KH, Schikora A. 2012. Arabidopsis growth and defense are modulated by
bacterial quorum sensing molecules. Plant Signal. Behav. 7:17881
97. Schikora A, Schenk ST, Stein E, Molitor A, Zuccaro A, Kogel KH. 2011. N-acyl-homoserine lactone
confers resistance toward biotrophic and hemibiotrophic pathogens via altered activation of AtMPK6.
Plant Physiol. 157:140718
98. Schuhegger R, Ihring A, Gantner S, Bahnweg G, Knappe C, et al. 2006. Induction of systemic resistance
in tomato by N-acyl-L-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ. 29:909
18
99. Shadel GS, Young R, Baldwin TO. 1990. Use of regulated cell lysis in a lethal genetic selection in
Escherichia coli: identication of the autoinducer-binding region of the LuxR protein from Vibrio scheri
ATCC 7744. J. Bacteriol. 172:398087
100. Shaw PD, Ping G, Daly SL, Cha C, Cronan JE Jr., et al. 1997. Detecting and characterizing N-acylhomoserine lactone signal molecules by thin-layer chromatography. Proc. Natl. Acad. Sci. USA 94:6036
41
101. Shimoda N, Toyoda-Yamamoto A, Aoki S, Machida Y. 1993. Genetic evidence for an interaction between
the VirA sensor protein and the ChvE sugar-binding protein of Agrobacterium. J. Biol. Chem. 268:26552
58
102. Shiner EK, Rumbaugh KP, Williams SC. 2005. Inter-kingdom signaling: deciphering the language of
acyl homoserine lactones. FEMS Microbiol. Rev. 29:93547
103. Slock J, VanRiet D, Kolibachuk D, Greenberg EP. 1990. Critical regions of the Vibrio scheri LuxR
protein dened by mutational analysis. J. Bacteriol. 172:397479
104. Stachel SE, Nester EW, Zambryski PC. 1986. A plant cell factor induces Agrobacterium tumefaciens vir
gene expression. Proc. Natl. Acad. Sci. USA 83:37983
105. Stachel SE, Zambryski PC. 1986. virA and virG control the plant induced activation of the T-DNA
transfer process in A. tumefaciens. Cell 46:32533
106. Steindler L, Venturi V. 2007. Detection of quorum-sensing N-acyl homoserine lactone signal molecules
by bacterial biosensors. FEMS Microbiol. Lett. 266:19
107. Stevens AM, Greenberg EP. 1997. Quorum sensing in Vibrio scheri: essential elements for activation of
the luminescence genes. J. Bacteriol. 179:55762
108. Subramoni S, Gonzalez JF, Johnson A, Pechy-Tarr M, Rochat L, et al. 2011. Bacterial subfamily of
LuxR regulators that respond to plant compounds. Appl. Environ. Microbiol. 77:457988
109. Subramoni S, Venturi V. 2009. LuxR-family solos: bachelor sensors/regulators of signalling molecules.
Microbiology 155:137785
110. Tepfer D. 1984. Transformation of several species of higher plants by Agrobacterium rhizogenes: sexual
transmission of the transformed genotype and phenotype. Cell 37:95967
111. Teplitski M, Chen H, Rajamani S, Gao M, Merighi M, et al. 2004. Chlamydomonas reinhardtii secretes
compounds that mimic bacterial signals and interfere with quorum sensing regulation in bacteria. Plant
Physiol. 134:13746
35
ARI
1 July 2013
18:30
112. Teplitski M, Robinson JB, Bauer WD. 2000. Plants secrete substances that mimic bacterial N-acyl
homoserine lactone signal activities and affect population densitydependent behaviors in associated
bacteria. Mol. Plant-Microbe Interact. 13:63748
113. Toth IK, Newton JA, Hyman LJ, Lees AK, Daykin M, et al. 2004. Potato plants genetically modied
to produce N-acylhomoserine lactones increase susceptibility to soft rot erwiniae. Mol. Plant-Microbe
Interact. 17:88087
114. Tzra T, Citovsky V, eds. 2008. Agrobacterium: From Biology to Biotechnology. New York: Springer
115. Tzra T, Li J, Lacroix B, Citovsky V. 2004. Agrobacterium T-DNA integration: molecules and models.
Trends Genet. 20:37583
116. Valdivia RH, Wang L, Winans SC. 1991. Characterization of a putative periplasmic transport system for
octopine accumulation encoded by Agrobacterium tumefaciens Ti plasmid pTiA6. J. Bacteriol. 173:6398
405
117. van Loon LC, Bakker PA, Pieterse CM. 1998. Systemic resistance induced by rhizosphere bacteria.
Annu. Rev. Phytopathol. 36:45383
118. Vannini A, Volpari C, Gargioli C, Muraglia E, Cortese R, et al. 2002. The crystal structure of the quorum
sensing protein TraR bound to its autoinducer and target DNA. EMBO J. 21:4393401
119. Von Bodman SB, Bauer WD, Coplin DL. 2003. Quorum sensing in plant-pathogenic bacteria. Annu.
Rev. Phytopathol. 41:45582
120. von Rad U, Klein I, Dobrev PI, Kottova J, Zazimalova E, et al. 2008. Response of Arabidopsis thaliana to
N-hexanoyl-DL-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere.
Planta 229:7385
121. Wang L, Helmann JD, Winans SC. 1992. The Agrobacterium tumefaciens transcriptional activator OccR
causes a bend at a target promoter, which is partially relaxed by a plant tumor metabolite. Cell 69:65967
122. Wang N, Lu SE, Wang J, Chen ZJ, Gross DC. 2006. The expression of genes encoding lipodepsipeptide
phytotoxins by Pseudomonas syringae pv. syringae is coordinated in response to plant signal molecules. Mol.
Plant-Microbe Interact. 19:25769
123. White CE, Winans SC. 2007. Cell-cell communication in the plant pathogen Agrobacterium tumefaciens.
Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 362:113548
124. Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP. 2001. Quorum-sensing in Gramnegative bacteria. FEMS Microbiol. Rev. 25:365404
125. Winans SC. 1990. Transcriptional induction of an Agrobacterium regulatory gene at tandem promoters by plant-released phenolic compounds, phosphate starvation, and acidic growth media. J. Bacteriol.
172:243338
126. Winans SC. 1991. An Agrobacterium two-component regulatory system for the detection of chemicals
released from plant wounds. Mol. Microbiol. 5:234550
127. Yamazaki A, Li J, Zeng Q, Khokhani D, Hutchins WC, et al. 2012. Derivatives of plant phenolic
compound affect the type III secretion system of Pseudomonas aeruginosa via a GacS-GacA two-component
signal transduction system. Antimicrob. Agents Chemother. 56:3643
128. Yang S, Peng Q, San Francisco M, Wang Y, Zeng Q, Yang CH. 2008. Type III secretion system genes
of Dickeya dadantii 3937 are induced by plant phenolic acids. PLoS ONE 3:e2973
129. Yao Y, Martinez-Yamout MA, Dickerson TJ, Brogan AP, Wright PE, Dyson HJ. 2006. Structure of
the Escherichia coli quorum sensing protein SdiA: activation of the folding switch by acyl homoserine
lactones. J. Mol. Biol. 355:26273
130. You YS, Marella H, Zentella R, Zhou Y, Ulmasov T, et al. 2006. Use of bacterial quorum-sensing
components to regulate gene expression in plants. Plant Physiol. 140:120512
131. Young JM. 2008. Agrobacterium: taxonomy of plant-pathogenic Rhizobium species. See Ref. 114, pp. 183
220
132. Yuan ZC, Liu P, Saenkham P, Kerr K, Nester EW. 2008. Transcriptome proling and functional analysis
of Agrobacterium tumefaciens reveals a general conserved response to acidic conditions (pH 5.5) and a
complex acid-mediated signaling involved in Agrobacterium-plant interactions. J. Bacteriol. 190:494507
133. Zamioudis C, Pieterse CM. 2012. Modulation of host immunity by benecial microbes. Mol. PlantMicrobe Interact. 25:13950

PY51CH02-Venturi
36
Venturi
Fuqua
PY51CH02-Venturi
ARI
1 July 2013
18:30

134. Zhang L, Jia Y, Wang L, Fang R. 2007. A proline iminopeptidase gene upregulated in planta by a
LuxR homologue is essential for pathogenicity of Xanthomonas campestris pv. campestris. Mol. Microbiol.
65:12136
135. Zhang L, Murphy PJ, Kerr A, Tate ME. 1993. Agrobacterium conjugation and gene regulation by Nacyl-L-homoserine lactones. Nature 362:44648
136. Zhang RG, Pappas KM, Brace JL, Miller PC, Oulmassov T, et al. 2002. Structure of a bacterial quorumsensing transcription factor complexed with pheromone and DNA. Nature 417:97174
137. Zhu J, Oger PM, Schrammeijer B, Hooykaas PJJ, Farrand SK, Winans SC. 2000. The bases of crown
gall tumorigenesis. J. Bacteriol. 182:388595
138. Zhu J, Winans SC. 2001. The quorum-sensing transcriptional regulator TraR requires its cognate
signaling ligand for protein folding, protease resistance, and dimerization. Proc. Natl. Acad. Sci. USA
98:150712
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Contents
Annual Review of
Phytopathology
Volume 51, 2013
Will Decision-Support Systems Be Widely Used for the Management

of Plant Diseases?
Dani Shtienberg p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Chemical Signaling Between Plants and Plant-Pathogenic Bacteria
Vittorio Venturi and Clay Fuqua p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p17
Biology, Epidemiology, and Control of Heterobasidion
Species Worldwide
Matteo Garbelotto and Paolo Gonthier p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p39
Pine Wood Nematode, Bursaphelenchus xylophilus
Kazuyoshi Futai p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p61
The Life History of Pseudomonas syringae: Linking Agriculture
to Earth System Processes
Cindy E. Morris, Caroline L. Monteil, and Odile Berge p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p85
Trichoderma Research in the Genome Era
Prasun K. Mukherjee, Benjamin A. Horwitz, Alfredo Herrera-Estrella,
Monika Schmoll, and Charles M. Kenerley p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 105
Experimental Measures of Pathogen Competition and Relative Fitness
Jiasui Zhan and Bruce A. McDonald p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 131
Quiescent and Necrotrophic Lifestyle Choice During Postharvest
Disease Development
Dov Prusky, Noam Alkan, Tesfaye Mengiste, and Robert Fluhr p p p p p p p p p p p p p p p p p p p p p p p p 155
Status and Prospects of Plant Virus Control Through Interference
with Vector Transmission
C. Bragard, P. Caciagli, O. Lemaire, J.J. Lopez-Moya, S. MacFarlane, D. Peters,
P. Susi, and L. Torrance p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 177
Diversity and Evolution of Root-Knot Nematodes, Genus Meloidogyne:
New Insights from the Genomic Era
Philippe Castagnone-Sereno, Etienne G.J. Danchin, Laetitia Perfus-Barbeoch,
and Pierre Abad p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 203
PY51-FrontMatter
ARI
14 July 2013
9:7
Antimicrobial Defenses and Resistance in Forest Trees:

Challenges and Perspectives in a Genomic Era
Andriy Kovalchuk, Susanna Kerio, Abbot O. Oghenekaro, Emad Jaber,
Tommaso Raffaello, and Fred O. Asiegbu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 221
MAPK Cascades in Plant Disease Resistance Signaling
Xiangzong Meng and Shuqun Zhang p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 245
The Use and Role of Predictive Systems in Disease Management
David H. Gent, Walter F. Mahaffee, Neil McRoberts, and William F. Pfender p p p p p p p 267

Impacts of Resistance Gene Genetics, Function, and Evolution

on a Durable Future
Richard W. Michelmore, Marilena Christopoulou, and Katherine S. Caldwell p p p p p p p p p 291
Virus-Based Transient Expression Vectors for Woody Crops: A New
Frontier for Vector Design and Use
William O. Dawson and Svetlana Y. Folimonova p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 321
Paradigms: Examples from the Bacterium Xylella fastidiosa
Alexander Purcell p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 339
Advances in Understanding Begomovirus Satellites
Xueping Zhou p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 357
Engineering Plant Disease Resistance Based on TAL Effectors
Sebastian Schornack, Matthew J. Moscou, Eric R. Ward, and Diana M. Horvath p p p p 383
Nonhost Resistance Against Bacterial Pathogens: Retrospectives
and Prospects
Muthappa Senthil-Kumar and Kirankumar S. Mysore p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 407
The Role of Prophage in Plant-Pathogenic Bacteria
Alessandro M. Varani, Claudia Barros Monteiro-Vitorello, Helder I. Nakaya,
and Marie-Anne Van Sluys p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 429
Considerations of Scale in the Analysis of Spatial Pattern
of Plant Disease Epidemics
William W. Turechek and Neil McRoberts p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 453
Pseudomonas syringae pv. tomato DC3000: A Model Pathogen for
Probing Disease Susceptibility and Hormone Signaling in Plants
Xiu-Fang Xin and Sheng Yang He p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 473
Diseases in Intercropping Systems
Mark A. Boudreau p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 499
Manipulation of Host Proteasomes as a Virulence Mechanism of Plant
Pathogens
Robert Dudler p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 521
vi
Contents
PY51-FrontMatter
ARI
14 July 2013
9:7
Centrality of Host Cell Death in Plant-Microbe Interactions

Martin B. Dickman and Robert Fluhr p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 543
Continuous and Emerging Challenges of Potato virus Y in Potato
Alexander V. Karasev and Stewart M. Gray p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 571
Communication Between Filamentous Pathogens and Plants at the
Biotrophic Interface
Mihwa Yi and Barbara Valent p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 587

Errata
An online log of corrections to Annual Review of Phytopathology articles may be found at
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Contents
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Annual Review of Phytopathology Volume 51 Issue 1 2013 (Doi 10.1146/annurev-Phyto-082712-102239) Venturi, Vittorio Fuqua, Clay - Chemical Signaling Between Plants and Plant-Pathogenic Bacteria

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Annual Review of Phytopathology Volume 51 Issue 1 2013 (Doi 10.1146/annurev-Phyto-082712-102239) Venturi, Vittorio Fuqua, Clay - Chemical Signaling Between Plants and Plant-Pathogenic Bacteria

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Chemical Signaling Between

Annu. Rev. Phytopathol. 2013. 51:1737

The Annual Review of Phytopathology is online at

plant-bacteria interactions, interkingdom signaling, plant phenolic

This articles doi:

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It is estimated that land plants evolved more

metabolites that can serve as chemical signals

Annu. Rev. Phytopathol. 2013.51:17-37. Downloaded from www.annualreviews.org

Features of Quorum Sensing LuxR

region (17, 18). LuxR-type proteins bind to

proteins with different cognate AHL ligands

Annu. Rev. Phytopathol. 2013.51:17-37. Downloaded from www.annualreviews.org

LuxR Solos and Bacterial Response to

OryR of the Rice Pathogen

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rice is provided to the media, indicating that the

XccR of the Crucifer Pathogen

XagR of the Soybean Pathogen

adjacent pip gene (15). Both xagR and pip have

The LuxR-Solo Family Responding to

sativus), indicating some level of specicity.

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N-Acylhomoserine Lactones as Signals

AHL concentrations (10 nM2000 nM), and

genes. An earlier study reported that foliar

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N-Acylhomoserine Lactones and

chains ranging in size from 6 to 12 carbons.

N-Acylhomoserine Lactones Affect

resulted in a signicant increase in root and

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Transgenic Plants Producing

Plant Interference of Bacterial

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AHL compounds and interfere with bacterial

species of Sinorhizobium, Mesorhizobium, and

infection site as sources of carbon, nitrogen,

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Activation of Virulence Functions

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and contains a conserved aspartate (D) residue.

sequences, but PhoR-PhoB-dependent regulation has never been established, probably

Opine Signals Activate

plasmid from Ti-harboring strains to recipient

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the mannityl opines that are also specied by

PLANT PHENOLICS AS SIGNALS

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syr and syp genes. This model has several points

www.annualreviews.org Chemical Signaling

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Annu. Rev. Phytopathol. 2013.51:17-37. Downloaded from www.annualreviews.org

Annu. Rev. Phytopathol. 2013.51:17-37. Downloaded from www.annualreviews.org

Annu. Rev. Phytopathol. 2013.51:17-37. Downloaded from www.annualreviews.org

Annu. Rev. Phytopathol. 2013.51:17-37. Downloaded from www.annualreviews.org

Annu. Rev. Phytopathol. 2013.51:17-37. Downloaded from www.annualreviews.org

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www.annualreviews.org Chemical Signaling

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