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ANNUAL
REVIEWS
1 July 2013
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Further
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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
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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.
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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).
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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.
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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.
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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
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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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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.
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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.
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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.
Annu. Rev. Phytopathol. 2013.51:17-37. Downloaded from www.annualreviews.org
by Royal Melbourne Institute of Technology (RMIT) on 08/07/13. For personal use only.
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.
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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).
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Contents
Annual Review of
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