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A Successful Bacterial Coup
d’État: How Rhodococcus
fascians Redirects Plant
Development
Elisabeth Stes,1,2 Olivier M. Vandeputte,3
Mondher El Jaziri,3 Marcelle Holsters,1,2
and Danny Vereecke4,∗
1
Department of Plant Biotechnology and Genetics, Ghent University, 9052 Gent, Belgium;
email: [email protected], [email protected]
2
Department of Plant Systems Biology, VIB, 9052 Gent, Belgium
3
Laboratoire de Biotechnologie Végétale, Université Libre de Bruxelles, 6041 Gosselies,
Belgium; email: [email protected], [email protected]
4
Department of Plant Production, University College Ghent, Ghent University,
9000 Gent, Belgium; email: [email protected]
Annu. Rev. Phytopathol. 2011. 49:69–86
Keywords
The Annual Review of Phytopathology is online at
phyto.annualreviews.org
Actinomycete, autoregulation, cytokinin, auxin, polyamine,
organogenesis
This article’s doi:
10.1146/annurev-phyto-072910-095217
c 2011 by Annual Reviews.
Copyright All rights reserved
0066-4286/11/0908/0069$20.00
∗
Corresponding author
Abstract
Rhodococcus fascians is a gram-positive phytopathogen that induces differentiated galls, known as leafy galls, on a wide variety of plants, employing virulence genes located on a linear plasmid. The pathogenic
strategy consists of the production of a mixture of six synergistically
acting cytokinins that overwhelm the plant’s homeostatic mechanisms,
ensuring the activation of a signaling cascade that targets the plant cell
cycle and directs the newly formed cells to differentiate into shoot meristems. The shoots that are formed upon infection remain immature and
never convert to source tissues resulting in the establishment of a nutrient sink that is a niche for the epiphytic and endophytic R. fascians
subpopulations. Niche formation is accompanied by modifications of
the transcriptome, metabolome, physiology, and morphology of both
host and pathogen. Here, we review a decade of research and set the
outlines of the molecular basis of the leafy gall syndrome.
69
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INTRODUCTION
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Actinomycetales:
heterogeneous group
of gram-positive
bacteria with a high
G+C content and
prominent producers
of antibiotics and
other bioactive
secondary metabolites
Biotrophic: denotes
the dependency of
microbial organisms
on living hosts
Cytokinins: plant
hormones derived
from adenine
primarily involved in
cell division and
differentiation, axillary
bud growth, and leaf
senescence
Leafy gall syndrome:
disease caused by
Rhodococcus fascians,
characterized by
disorganized plant
growth and clusters of
tightly packed shoots
Meristem: organized,
undifferentiated plant
tissue of rapidly
dividing cells that
differentiates to form
new tissues or organs
70
In the order of the high G+C grampositive Actinomycetales, members of the
genus Rhodococcus are notorious for their medical, veterinary, environmental, and especially
industrial implications (11, 46, 50, 65, 96,
99). With an ever-growing number of new
and reclassified species assigned to the genus
Rhodococcus, the systematics of the genus remain cumbersome (38). However, despite the
expansion of the genus and several reports
documenting the plant-associated occurrence
of Rhodococcus species (6, 13, 30, 97), Rhodococcus fascians remains the only plant pathogenic
member.
R. fascians is a biotrophic phytopathogen
that causes hyperplastic outgrowths through
the production of cytokinins (90). Secretion of
phytohormones is a common strategy among
plant-associated microbes (3, 33, 98), and the
responsible genes are often located on large circular plasmids (67). However, to date, R. fascians is the only phytopathogen described that
harbors virulence genes on a linear plasmid
(17, 32). Moreover, R. fascians is unique among
the hyperplasia-inducing bacteria because it
provokes differentiated galls, known as leafy
galls (105). Other gall-inducing pathogens,
such as Agrobacterium tumefaciens, Pseudomonas
savastanoi, and Pantoea agglomerans pv. gypsophilae, cause the proliferation of undifferentiated tissues (4, 71, 75), whereas the leafy
galls incited upon R. fascians infection consist of multiple, partially expanded shoots
that arise from existing and newly induced
meristems (19, 20).
In this review, we address the conundrum of leafy gall formation by giving an
overview of the sequence of events that happens when plant and bacterium meet, initiate an interaction, and trigger the establishment of symptomatic tissues. We describe
the molecular crosstalk between both partners and the resulting physiological and morphological alterations that occur in plant and
bacterium.
Stes et al.
RHODOCOCCUS FASCIANS POSES
A THREAT TO THE
ORNAMENTALS INDUSTRY
Since the first report of fasciated peas (10), the
host range of R. fascians has expanded continuously (52, 60, 62, 80) and currently encompasses 164 species in 43 plant families. R. fascians
primarily affects dicotyledonous herbaceous
plants, but several woody and monocotyledonous plants are sensitive as well. Incidences
of infection have been recorded throughout the
world, mainly in temperate regions (24, 79).
Other than leafy galls, aerial malformations,
such as stunting, deformed leaves, witches’
brooms, and fasciated shoots, are commonly
observed on plants infected by R. fascians
(Figure 1a–e). When R. fascians hits ornamental plants, they lose their commercial value because symptomatic tissues are malformed compared to unaffected ones and flower formation
is impaired. Consequently, economic damage is
mainly situated in the globally expanding ornamentals industry (79). In this horticultural sector, R. fascians infections are a persistent problem because of the lack of efficient eradication
methods and little knowledge of the epidemiology of the disease (24). Indeed, leafy galls are
often mistakenly diagnosed as symptoms inflicted by A. tumefaciens, viruses, or eriophyid
mites, or as shoot proliferations caused by exposure to growth hormones or herbicides (24,
61, 77). Moreover, R. fascians can persist on the
plant surface for months before symptoms arise
and thus be established without the grower’s
awareness (16, 48). As a result, propagation of
(latently) infected plant material seems to be
the primary mode of transmission of the disease
(63). An early diagnosis of new plant material via
the polymerase chain reaction (PCR) (34, 59,
69, 85, 88), preferably combined with isolation
of the bacterium from PCR-positive plants, can
prevent introduction of R. fascians into greenhouses. Upon disease establishment, nurseries
have to rely on strict sanitary measures to control bacterial spreading (24, 63). Although the
increased incidence of R. fascians infections
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b
2 cm
e
c
d
2 cm
f
10 cm
g
4 mm
h
*
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*
2 cm
2 mm
10 µm
500 µm
Figure 1
Typical symptoms induced on ornamental plants and characteristic features of Rhodococcus fascians and the
interaction with its host. (a) Leafy gall (arrow) on Erysimum spp. (b) Leafy galls (arrows) on Viola spp.
(c) Stunted growth on Iberis spp. (d ) Leaf deformation (arrow) in Ipomoea spp. (e) Fasciation (arrow) on Iberis
spp. ( f ) R. fascians orange-colored colonies. ( g) Epiphytic R. fascians colony covered by a slime layer on
tobacco; rod-shaped (asterisk) and elongated (arrow) bacteria are indicated. (h) Axillary activation (asterisk)
and de novo meristem formation (arrow ) in Arabidopsis thaliana.
in nurseries is best documented for the United
States (60, 78), the worldwide dispersal of
R. fascians and the extraordinarily wide host
range of this phytopathogen present a potential global threat in horticultural practices (24).
EPIPHYTIC COLONIZATION
INDUCES CHANGES IN THE
PRIMARY METABOLISM
OF THE PLANT
R. fascians has several characteristics that are
typical of a successful epiphyte. The orange
carotenoid pigments (76) (Figure 1f ) provide
protection against UV irradiation (91) during
the establishment of epiphytic colonies on the
stems and leaves of a host. Moreover, colonies
are often formed in excavations and epidermal cell wall junctions, thus evading harsh environmental conditions, whereas colocalization
with hydathode-rich leaf margins may be associated with nutrient availability (16, 53). R. fascians also produces indole-3-acetic acid (IAA)
(101), an auxin hormone that may trigger nutrient release from plant cells (53) and suppress
their defense responses (25), a strategy commonly deployed by biotrophic pathogens (5).
R. fascians is not motile and to facilitate spreading, epiphytic bacteria shift from initially rodshaped cells to extended hyphae-like cells (16)
(Figure 1g). The colonies resemble biofilms
in that they are covered by a slime layer
(Figure 1g) possibly improving attachment to
the plant surface, preventing desiccation, and
playing a role in epiphytic fitness (16). The epiphytic colonization capacity of nonvirulent linear plasmid-free strains is comparable to that
of wild-type strains (16), implying that all these
features are encoded by chromosomal genes.
Although symptom development is not
initiated during the initial epiphytic phase (16),
the plant responds to the bacterial presence by
modulating its primary metabolism (25). This
reaction occurs with pathogenic strains as well
as with their nonpathogenic derivatives, but it
is much stronger during colonization by the
virulent bacteria (25). The bacterial signals that
trigger this response have not yet been identified, but possibly they could be low levels of
phytohormones produced from chromosomal
www.annualreviews.org • Origin of the Leafy Gall Syndrome
IAA: indole-3-acetic
acid
Auxin: plant hormone
that promotes and
regulates growth and
development by
affecting cell division,
differentiation,
phototropism,
geotropism, and apical
dominance
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Autoregulation:
cell-to-cell
communication that
enables a population
density–based control
of gene transcription
via production, release,
and sensing of lowmolecular weight
compounds
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att: attenuation
12:43
genes (73, 101) or microbe-associated molecular patterns (8). In Arabidopsis thaliana, plant
metabolic processes are redirected upon
R. fascians infection toward an enhanced
synthesis of specific amino acids, such as
proline, valine, phenylalanine, and tryptophan,
and sugars, such as trehalose, glucose, and
fructose (25), likely providing extra carbon and
nitrogen sources for bacterial proliferation.
Moreover, increased tryptophan levels may
stimulate bacterial auxin biosynthesis and, thus,
epiphytic fitness because IAA biosynthesis by
R. fascians is tryptophan-dependent (101).
Other modifications include a downregulation
of arginine and ornithine levels and a rise in
succinate and pyruvate concentrations (25).
Together with the increased glucose, proline,
valine, and phenylalanine levels, a physiological
condition is created that is perceived by the
bacteria as a signal for the initiation of the
pathogenic life style by favoring the activation
of autoregulation processes for virulence (55).
AUTOREGULATION TRIGGERS
THE ONSET OF THE
PATHOLOGY
The success of pathogens often depends on the
coordinated expression of their virulence functions, allowing them to act as a community
rather than as single cells. This phenomenon,
known as quorum sensing, can be accomplished
attR
attX attA
AttR
AttX
AttA
AttB
AttC
AttD
AttE
AttF
AttG
AttH
attB
attC attD
attE
attF
attG
LysR-type regulator
Translocator
Argininosuccinate lyase
Argininosuccinate synthase
Formyltransferase
Enoyl-CoA hydratase/isomerase (CarB)
β-lactam synthetase (CarA)
Clavaminic acid synthase (CarC)
AMP-binding acetyl-CoA synthetase
Ornithine acetyltransferase
attH
fasR
mtr1
mtr2
FasR
Mtr1
Mtr2
FasA
FasB
FasC
FasD
FasE
FasF
by autoregulatory compounds, such as Nacyl homoserine lactones in gram-negative or
oligopeptides and γ-butyrolactones in grampositive bacteria. Typically, an autoregulatory
compound accumulates in the surroundings of
the growing bacterial population, and its concentration correlates positively with the cell
density. As soon as the extracellular concentration of the autoinducer is high enough, that
is, when a quorum is reached, concerted target gene expression occurs. Consequently, such
autoregulatory compounds can be detected in
spent medium of high-density bacterial cultures
(9, 68). Although in R. fascians positive autoregulation of virulence functions also takes places,
the process has not been described as genuine
quorum sensing because the presence of the
plant is required for an optimal production of
the autoregulatory compound (55).
Autoregulation of virulence in R. fascians
strain D188 is mediated by nine genes that
constitute the attenuation (att) operon, located
on the linear plasmid (55). The gene products
are homologous to proteins implicated in the
biosynthesis and secretion of arginine and βlactam–like compounds (Figure 2). Although
the structure of the att-autoregulatory molecule
remains to be determined, several data point to
a positively charged acylated cyclic amino acid
derivative (54, 55, 100, 104).
Expression of the att genes is controlled by
a LysR-type transcriptional regulator, AttR,
fasA
fasB
fasC
fasD
AraC-type regulator
SAM-dependent methyltransferase
SAM-dependent methyltransferase
P450 monooxygenase
Ferredoxin/pyruvate decarboxylase α subunit
Pyruvate decarboxylase β subunit
Isopentenyltransferase
Cytokinin oxidase/dehydrogenase
Phosphoribohydrolase
Figure 2
Organization and homologies of the fas and att loci on pFiD188, the linear plasmid of Rhodococcus fascians strain D188.
72
Stes et al.
fasE
fasF
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IAA
12:43
*
* * * ** *
* at
att
* * * **
* fasA-E
fasA-F
fasA-E
CK
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b
Controlled
epiphytic
colonization
Modification of
primary metabolism
Succ, Pyr
Orn, Arg
Trp
Sugars
Autoregulation
IAA production
Initial defense
CK perception
CK homeostasis
Subset CKs
Put
Cell cycle activation
CYCD3
1
3
CK
fasA-E
fasA-F
Synergistic CK
action
CK maintenance
flow
fasA-F
Metabolic shift
toward C2
compounds in
endophytic
population
Controlled
endophytic
colonization
c
0
CK initiation
wave
fasA-F
CK
CK
Defense down
KNOX
Amino acids
Sugars
Strong transcriptome
modification
Sink/niche
establishment
Symptom onset
Days post-infection
7
Metabolic
habitat
modification
Controlled
bacterial cell
proliferation
Continuous
shoot formation
Established
leafy gall
14
21
Figure 3
Overview of the different steps of the Rhodococcus fascians–plant interaction leading to symptom development and niche establishment. A
detailed description of the events is given throughout the text. (a) Bacterial responses (epiphytic and endophytic bacteria are depicted in
orange and green, respectively); (b) molecular crosstalk between bacteria (orange text) and plant ( green text); (c) timeline and the
phenotypical responses in Arabidopsis.
and is activated in response to specific combinations of carbon and nitrogen sources that
reflect the physiological state of epiphytically
colonized plant tissues (Figure 3). An initially
low concentration of the att compound is
sufficient to activate the expression of the attbiosynthetic genes, thus mediating a positive
feedback mechanism that results in the production of high amounts of the att compound
required to trigger the expression of essential
virulence genes, including the fasciation ( fas)
genes for cytokinin production (55, 94). The
att compound is also involved—directly or
indirectly—in breaching the plant’s cuticula,
thus facilitating endophytic colonization (55).
As a result, few epidermis cells collapse and
large ingression sites are formed beneath the
epiphytic colonies on leaves, stems, and axils
(16, 90). During the endophytic colonization,
the bacteria undergo a series of adaptations to
the new environment (Figure 3). Their cell
wall is modulated (16) or even completely lost
(49), and their metabolism is shifted toward the
use of C2 compounds (31, 107). Surprisingly, in
the endophytic population, att gene expression
is shut down without affecting fas gene expression (15). This observation implies that, upon
invasion of the internal plant tissues, fas gene
regulation is controlled by other (unknown)
factors.
www.annualreviews.org • Origin of the Leafy Gall Syndrome
fas: fasciation
73
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IPT:
isopentenyltransferase
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CKX: cytokinin
oxidase/
dehydrogenase
12:43
Interestingly, the att compound appears to
be highly diffusible: It can be detected throughout the tissues of infected plants and even seems
to be exuded by the roots (100, 104). This feature could undoubtedly contribute to the aggressiveness of the R. fascians population as a
whole. Indeed, the att operon determines the
transition from a harmless epiphytic lifestyle
to a pathogenic endophytic one by controlling the onset of penetration and virulence (15)
(Figure 3). The significance of autoregulation
in the R. fascians pathology has recently been
documented in the incompatible interaction
between a tropical legume, Dalbergia pervillei,
and R. fascians. Although the recalcitrance of
this plant to R. fascians infection was found to be
multifactorial, an important cause for the lack
of symptom formation was the production of
perbergin, a newly identified prenylated isoflavanone that acts as a competitive inhibitor of
the natural autoinducer of AttR (81).
RHODOCOCCUS FASCIANS
PRODUCES A MIX OF
CYTOKININS THAT IS
PERCEIVED BY THE HOST AND
ACTIVATES HOMEOSTASIS
MECHANISMS
The major virulence strategy of R. fascians is the
production of shoot-inducing cytokinins (90).
Since the discovery of isopentenyladenin (iP) in
the supernatans of R. fascians (95), several other
cytokinin derivatives have been isolated from
different isolates grown under diverse culture
conditions (37). However, despite major efforts
by several generations of researchers (2, 28, 39,
47, 82, 84), a positive correlation between a specific cytokinin and virulence was not found (17,
28, 64). Undoubtedly, the very stringent regulation of fas gene expression contributes to this
problem. Indeed, fas expression is subjected to
the att compound (55) and other environmental
conditions (94) and controlled by two transcriptional regulators, AttR (72) and the AraC-type
regulator FasR (94), and an unidentified posttranscriptional mechanism (72, 94).
74
Stes et al.
More clarity came when the biosynthetic
pathway encoded by the six genes of the fas
operon (Figure 2) was solved for strain D188,
based on biochemical data and cytokinin profiles of several fas mutants (74). Instead of
producing a single cytokinin, the Fas proteins
proved to mediate the synthesis of six distinct cytokinin bases: iP, cis-zeatin (cZ), transzeatin (tZ), and their methylthio-derivatives
(2MeSiP, 2MeScZ, 2MeStZ) (73, 74) (Figure 3). The isopentenyltransferase (IPT) FasD,
the key enzyme of the pathway, synthesizes
iP (and possibly tZ) that is a precursor for
other Fas enzymes. FasA is a putative P450
monooxygenase hydroxylating iP to form tZ
and cZ. FasB is a putative bifunctional enzyme with a ferredoxin-like domain and a pyruvate decarboxylase α subunit domain, whereas
FasC is homologous to the β-subunit of pyruvate decarboxylase. It is hypothesized that
FasB and FasC are accessory proteins of FasA
and deliver the energy for the hydroxylation reaction by using pyruvate as an electron donor (18, 37). FasA can also hydroxylate chromosomally produced 2MeSiP, yielding 2MeScZ and probably 2MeStZ. The absolute requirement of FasA for virulence (18)
illustrates the central position of the Z-type
cytokinins in the modulation of plant development (73, 74). The enzymes involved in
the direct methylthiolation of iP, tZ, and cZ
to yield their 2MeS derivatives remain to be
identified. FasF, a prerequisite for symptom
maintenance, is a phosphoribohydrolase capable of releasing cytokinin bases directly from
their nucleotide precursors in a complementary
route for the production of Z-type cytokinins
(74). FasE is a cytokinin oxidase/dehydrogenase
(CKX) with a strong affinity for iP-type cytokinins and is probably required for the optimal functioning of the FasD enzyme (74).
A similar reaction mechanism presumably occurs in Streptomyces turgidiscabies, a scab-causing
phytopathogen that is the only other organism known until now to carry a fas operon
(see sidebar, Phytopathogenic Streptomycetes)
(42).
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Unexpectedly, the linear plasmid-free nonvirulent derivative of strain D188 secretes
the same array of cytokinins as the wildtype strain, albeit at much lower levels (73).
Whereas tRNA degradation is believed to be
the source of this basal level (1, 29, 57), the
increased pathogenicity-related levels are the
consequence of de novo biosynthesis by the Fas
machinery (74). These findings suggest that R.
fascians virulence depends on exposure of the
host to particular cytokinin concentrations and
ratios rather than on the production of specialized molecules (73, 74) and clarify why no specific virulence-associated cytokinins have been
identified.
At the onset of the interaction, bacterially produced cytokinins are perceived by
the plant (73) and trigger substantial transcriptomic and metabolomic changes (25). In
Arabidopsis, homeostatic mechanisms are activated that are directed toward the reduction
of the cytokinin levels in the infected tissues
(Figure 3). For instance, plant cytokinin
biosynthesis is switched off, as illustrated
by the downregulation of IPT3, IPT5, and
IPT7 expression and the decrease in cytokinin
monophosphates. Moreover, expression of all
CKX genes is induced correlating with a net
reduction of iP and N-glucosides at later time
points of the interaction (23). Also, in infected
peas cytokinin nucleotide levels are reduced
(28, 34), and in tobacco plants CKX gene expression is upregulated upon infection (35).
The modulation of the cytokinin metabolism
explains why no increased cytokinin levels have
been detected in infected tissues (20, 23, 34).
Importantly, however, because generally little
biological relevance had been attributed to cZ
and 2MeS-cytokinins, these compounds have
been overlooked in the past.
With the identification of the fas-produced
cytokinins and the recent development of very
sensitive analytical methods (92), the enigmatic
lack of an increased cytokinin content in infected plant tissues has been reassessed. As such,
depending on the plant species, specific fas
cytokinins have been found to accumulate in
symptomatic plants (73).
PHYTOPATHOGENIC STREPTOMYCETES
Just like Rhodococcus fascians, the genus Streptomyces belongs to the
high G+C gram-positive Actinomycetales. The majority of the
Streptomycetes are renowned producers of bioactive secondary
metabolites and antibiotics (12, 56). However, several species are
devastating phytopathogens that are neither host nor tissue specific (7). The most important global economical impact is caused
by potato scab, a disease characterized by the formation of lesions
resulting from the bacterial interference with the plant’s cellulose biosynthesis (45). Although the main pathogenicity factor is
the production of thaxtomin, a peptidic phytotoxin, Streptomyces
turgidiscabies also secretes cytokinins that are encoded by a fas
operon that is similar to that of R. fascians. Wild-type S. turgidiscabies strains do not induce shoot formation, but scab lesions
with an erumpent phenotype. In contrast, a thaxtomin-deficient
mutant induces leafy galls in tobacco (Nicotiana tabacum) and Arabidopsis thaliana that are indistinguishable from those induced by
R. fascians (42). The role of cytokinin in this pathosystem is postulated to be multifactorial, as an apoptosis inducer in the plant
and as a trigger of secondary metabolites in the pathogen.
THE TRICK-WITH-THECYTOKININ-MIX: THE
SYNERGISTIC ACTION OF
BACTERIALLY PRODUCED
CYTOKININS OVERTAKES
PLANT GENE EXPRESSION
AND CAUSES ECTOPIC AND
PERSISTENT PLANT
CELL DIVISIONS
Bacterial production of a mixture of cytokinins
instead of a large amount of a single cytokinin provides multiple advantages. First of
all, the generation of a cytokinin mixture ensures an enhanced in planta stability because of
the restricted substrate specificity of CKX enzymes in different plant tissues and species (36,
109). With the de novo production of 2MeScytokinins in addition to the classical iP and Z,
the cytokinin-degrading capacity of the plant is
challenged but defeated and hence, irrespective
of the host, always at least some of the bacterial cytokinins will accumulate in the infected
tissues (73) (Figure 3). Indeed, in Arabidopsis
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the activation of the apoplastic CKXs (CKX2,
CKX4, and CKX6) effectively reduces the in
planta levels of most of the bacterially produced
cytokinins, but these enzymes are unable to efficiently degrade cZ and 2MeScZ. In tobacco,
however, the CKX enzymes seem to be ineffective against iP (73).
Secondly, the R. fascians cytokinin mixtures modulate the sensitivity of plants for
these morphogens. In Arabidopsis, throughout the interaction, all secreted cytokinins
are perceived by ARABIDOPSIS HISTIDINE
KINASE (AHK) 3 (73, 74), a broad-spectrum
cytokinin receptor that plays an important role
in shoot development (83). However, at the onset of the interaction, iP strongly accumulates
and induces ectopic expression in the shoots
of the root-specific, narrow-spectrum cytokinin
receptor AHK4 (40, 73, 87). Consequently,
even with a relatively low amount of secreted
cytokinins, R. fascians manipulates the plant so
that its cytokinin sensitivity is the highest at the
moment when symptoms need to be initiated
(73, 74) (Figure 3).
Thirdly, the individual compounds appear
to act synergistically on plant development.
Bioassays that assess the activity of the six cytokinins secreted by R. fascians show that compared with an equal final concentration of the
individual molecules, an equimolar mix has a
stronger effect on proliferation of tobacco callus and in Arabidopsis, on cytokinin receptor activation, bleaching, anthocyanin accumulation,
de-etiolation, and shoot regeneration (73).
Moreover, the cytotoxicity of the 2MeScytokinins is considerably lower than that of the
classical cytokinins in a tobacco callus bioassay
(73). The continuous presence of the bacteria
is essential for sustaining symptoms (105) and
the constant secretion of cytokinins (15) possibly results in locally very high accumulation
levels. Therefore, the production of less active
and less toxic 2MeS-derivatives in addition to
iP, tZ, and cZ may be required to avoid deleterious effects on plant development.
Finally, the ratio of locally secreted cytokinins in the plant tissues is most probably
not the same throughout the interaction
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AHK:
ARABIDOPSIS
HISTIDINE
KINASE
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Stes et al.
because the cytokinin spectrum is produced
in a very controlled and dynamic fashion (74).
At the onset of symptom formation, R. fascians
launches a cytokinin initiation wave consisting
mainly of iP, tZ, and cZ via the combined
action of FasD and FasA. Later, the bacteria
shift their metabolism toward the production
of a cytokinin maintenance flow containing tZ,
2MeStZ, cZ, and 2MeScZ, through the action
of FasF (74). At the same time, the activated
CKX machinery of the plant contributes to
the relative concentrations of the six bacterial
cytokinins (73).
Altogether, the cytokinin mixture eventually
triggers a signal transduction cascade in the host
that leads to an elaborate modification of gene
expression. The effect on the transcriptome has
been assessed with different techniques, including differential display (70, 86, 102), cDNAamplified fragment length polymorphism (27,
103), and microarray hybridization (25), applied to different hosts, such as Atropa belladonna
(70), Arabidopsis (25), and tobacco plants (86)
and plant cell cultures (102, 103).
Because R. fascians infection leads to the
dedifferentiation and reactivation of cortical
cells to generate new shoot meristems (20),
the cell cycle genes have drawn a lot of
attention (Figure 3). Infection of Arabidopsis (105) and tobacco (20) reporter lines for
cell cycle markers illustrated the anticipated
stimulation of cell division. The effect of
R. fascians signals on cell cycle progression was
studied in greater detail in S-phase synchronized cell cultures of tobacco cv. Bright Yellow 2 (BY-2). Depending on the treatment,
an extended prophase, resulting in a widening of the mitotic index peak (93), or an acceleration of the progression of the plant cells
through the successive phases of the cell cycle
(103) were observed. Finally, the effect of R.
fascians on different phases of the cell cycle was
demonstrated in Arabidopsis. The induced transcription of the mitotic cyclin-dependent kinases (CDKs) CDKB1;1 and CDKA;1 and of the
cyclins CYCB1;1 and CYCA2;1 promotes the
G2-to-M phase transition, pushing progression
through mitosis (22). Additionally, the bacterial
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cytokinins are postulated to directly promote
the G2-to-M transition by dephosphorylating
CDKs (22). Moreover, transition through the
G1-to-S phase is stimulated via the transcriptional activation of the three CYCD3 genes
(22). The central position of the CYCD3 signal
transduction pathway in symptomatology has
been revealed by the strongly reduced response
of the Arabidopsis cycd3;1–3 triple knockout mutant toward infection (22).
DE NOVO SHOOT MERISTEM
FORMATION AND PREVENTION
OF TISSUE MATURATION LEAD
TO NICHE ESTABLISHMENT
One of the earliest visible symptoms of
R. fascians infection in many hosts is the activation of dormant axillary meristems (19, 20,
24, 77, 79, 105). This overruling of apical dominance has been correlated with a local upregulation of abscisic acid and gibberellic acid breakdown upon infection (86). Other than their
effect on the activity of existing meristems, the
induced hormone imbalances, together with
the secreted bacterial cytokinin mix, create
physiological conditions that are optimal for
the de novo formation of meristems (23, 86)
(Figure 3). Indeed, the reentry of cortical cells
into a stage of active cell division is followed
by their differentiation into shoot meristems
(20), but the newly formed shoots generated
from these meristems do not develop normally.
Analysis of the DNA ploidy level distribution
of symptomatic leaves of Arabidopsis demonstrated that most cells have a 2C content irrespective of their age, suggesting that the tissues retain a meristematic identity (22). Uninfected leaves grow in two phases: initially driven
by cell division and subsequently by cell expansion resulting from endoreduplication (26).
However, cell cycle gene expression profiles of
symptomatic leaves exhibited a biphasic pattern, indicating that endoreduplication does not
occur but is replaced by continuous growth
via cell proliferation (22). The undifferentiated
state of the symptomatic plant organs was illustrated by the ectopic expression of class I
KNOTTED-like homeobox (KNOX) genes,
such as SHOOT MERISTEMLESS (STM)
and BREVIPEDICELLUS/KNOTTED-LIKE1
(BP/KNAT1) (23) (Figure 3).
Analysis of infected Arabidopsis tissues by
microarray hybridization and primary metabolite profiling pointed to the establishment of
a niche. Because symptomatic tissues do not
mature, they remain sink tissues for photosynthates do not convert into source tissues. This
feature is demonstrated by an increased hexose/sucrose ratio and an enhanced invertase
gene transcription and enzyme activity in Arabidopsis (25). In accordance with the source-tosink transition, the photosynthetic activity in
the symptomatic leaves is repressed via endproduct inhibition (25) (Figure 3). Also, in infected tobacco BY-2 cells, an acidic invertase
gene is upregulated (103). Most likely, the accumulating hexoses serve as fuel for the energydemanding process of symptom formation and
for supporting bacterial growth (25). In addition to the modulation of the carbohydrate
profile of symptomatic tissues, a significant increase in the amino acid content has been measured, which may provide a nitrogen source for
the colonizing bacteria (25). Altogether, it is
clear that R. fascians infection strongly affects
the physiology of the plant to its advantage, an
aspect that has been termed metabolic habitat
modification (107) (Figure 3).
KNOX:
KNOTTED-like
homeobox
Niche: place and
role occupied by an
organism or
population within an
ecological community
Putrescine: a diamine
that is the precursor of
the higher polyamines
spermidine, spermine,
and thermospermine,
implicated in growth
and development
CYTOKININ-ACTIVATED
SIGNALING IS AMPLIFIED BY
PLANT-DERIVED PUTRESCINE
Although the dominant role of cytokinins in
symptom development is obvious and the advantageous production of a mixture of cytokinins may be the reason for the significant
impact of bacterial infection on plant development, metabolite profiling revealed the accumulation of putrescine and trehalose, two
potential secondary signaling molecules (25).
This observation implies the intriguing alternative (although not mutually exclusive)
possibility that plant messengers may reinforce the pathology by amplification of the
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cytokinin signaling. Recent research in Arabidopsis showed that upon perception of the
R. fascians cytokinins, the transcription of
ARGININE DECARBOXYLASE (ADC) genes
is induced. Because ADC enzymes mediate the
rate-limiting step of polyamine biosynthesis,
this overexpression results in the accumulation of the diamine putrescine (89). Interestingly, the plant growth stimulation obtained
by exogenous putrescine seems to be accomplished by the direct stimulation of the cell cycle through the activation of CYCD3;1 expression (89). Because the CYCD3 genes are also
the primary targets of the bacterial cytokinins
(22), R. fascians–induced putrescine production
feeds into the same signal transduction pathway
(Figure 3). The importance of the additional putrescine signaling is evidenced
by the strongly reduced response toward
R. fascians infection of plants treated with inhibitors of polyamine biosynthesis. Moreover,
exogenously applied putrescine significantly
enhances R. fascians–induced symptom development (89). Consequently, the strong effect
of R. fascians infection on plant development
would not only be achieved through the production of a mixture of synergistically acting
cytokinins, but also through deviation of the
plant metabolism to reinforce the proliferative
and organogenic effect of its morphogens.
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PATHOGEN AND HOST
CONTRIBUTE TO NICHE
MAINTENANCE
The role of plant-derived putrescine in the
establishment of the niche illustrates that
both pathogen and host play an active role in
symptom development and maintenance. An
intriguing observation is that whereas decaying
leaves are quickly macerated, R. fascians is
unable to overgrow healthy symptomatic plant
tissue (16). Therefore, the plant seems to control the bacterial multiplication. Indeed, after
the primary epiphytic colonization, the bacteria
penetrate through the cuticula, proliferate in
the epidermal cells, and spread from there,
mainly intercellularly, in a few cortical cell
78
Stes et al.
layers. The colonization of the internal tissues
is accompanied by an increased tissue autofluorescence, indicative of a mild defense reaction
(16), which is confirmed by microarray hybridization (25). However, no extensive tissue
necrosis occurs (16), and there is no hypersensitive reaction to prevent bacterial spread (66).
Although an initial defense reaction is mounted,
it is very quickly alleviated and eventually suppressed (25). Interestingly, ectopic expression
of BP/KNAT1 is known to decrease cell wall lignification (58) and consequently, the cytokinininduced ectopic KNOX gene expression upon
R. fascians infection has been postulated to contribute to the formation of ingression sites (23).
Whereas this is an appealing hypothesis, the
timing of this expression suggests a role rather
late in the interaction, but formation of secondary ingressions sites at later time points cannot be ruled out. Altogether, these observations
suggest that pathogen and host balance each
other’s responses from the beginning of their
encounter. Moreover, in the only reported example of an incompatible interaction, Dalbergia
tissues contain perbergin, a prenylated isoflavanone that specifically inhibits AttR functioning and, therefore, onset of virulence gene expression and symptom development (81). Thus,
plants apparently manage R. fascians activity
despite its very broad host range (Figure 3).
Because symptomatic tissues never mature,
they remain sinks and thus represent a nutrientrich niche for R. fascians (22, 25). Whereas
the epiphytic subpopulation profits from the
accumulating hexoses and amino acids, the
endophytic subpopulation responds to this
metabolic habitat modification by converting
its metabolism toward the use of C2 compounds
as specific carbon and nitrogen sources (31,
107). Indeed, for endophytic survival, R. fascians requires a functional malate synthase encoded by the chromosomal vicA gene (Figure
3). Together with isocitrate lyase, the VicA protein forms the glyoxylate shunt of the Krebs
cycle (107). Moreover, downregulation of two
Krebs cycle genes, pyruvate dehydrogenase and
fumarate hydratase, in R. fascians grown on leafy
gall extract supports the metabolic shift toward
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the glyoxylate shunt (31). Interestingly, in the
related animal pathogen Mycobacterium tuberculosis, an operational glyoxylate pathway is also
needed for persistence because it allows the
pathogen to feed on the abundant fatty acids
of the host (41). As it is unlikely that R. fascians uses the rather scarce fatty acids from
plants, it has been proposed that the intercellular population would utilize photorespiration
intermediates, such as glycine, glycolate, and
glyoxylate (106). In support of this hypothesis,
a glycine dehydrogenase gene residing in the
same chromosomal locus as vicA is also necessary for full virulence (14, 107) and metabolic
and transcriptional analysis in Arabidopsis and
tobacco suggest the acceleration of photorespiration in symptomatic plants (25, 103). Importantly, symptoms are not maintained when
the endophytic population deteriorates (105),
implying that bacterial cytokinin production
by this subpopulation is essential for symptom
persistence.
At the late stages of infection, bacterial
proliferation remains tightly controlled by the
plant even though transcript profiling has
shown that defense-related genes, typically upregulated during biotic interactions (21, 43),
are downregulated upon symptom establishment in R. fascians–infected Arabidopsis plants
(25). Moreover, no signs of plant defense reactions have been observed by microscopic analysis of infected tobacco and Arabidopsis plants (19,
20), and no relevant differences in secondary
metabolite production have been detected upon
infection of Pratia nummularia (51). In contrast, a few reports point to some level of defense activation in infected plants. For instance,
the phenolic profile of tobacco leafy galls differs from that of control plants and although
none of the identified compounds seemed to be
toxic to R. fascians grown in culture media (108),
it cannot be ruled out that they affect the epiphytic and/or endophytic population. In Atropa
belladonna leafy galls, the expression reduction
of three genes possibly involved in plant defense has been correlated with bacterial colonization (70). Finally, in tobacco the upregulation of an annexin during leafy gall formation
has been linked to stress responses (and/or plant
development) (102). These seemingly conflicting observations may indicate that a moderate defense reaction occurs throughout the
R. fascians pathology and that its main function
is to keep the bacterial population size within
limits (Figure 3). However, no full defense response seems to be set up that would eliminate
the bacteria. Auxin, from bacterial or plant origin, is a plausible candidate to be implicated in
this process. Indeed, increased auxin signaling
has long been recognized as a downregulator of
plant defense (5).
CONCLUDING REMARKS
AND PERSPECTIVES
In the past decade, a lot has been unraveled
about the mechanisms that lead to the formation of a leafy gall. Nevertheless, several
important questions remain to be answered.
The shooty phenotype of the induced malformations is clearly caused by the bacterial cytokinin mixture, but the regulation of fas gene
expression remains largely unsolved, as does the
question as to which genes are involved in the
de novo biosynthesis of the 2MeS-cytokinins.
Upstream of the fas operon, two genes are
present that are homologous to methyltransferases (MTRs) (Figure 2) and these genes are
conserved in the fas operon of S. turgidiscabies
(42). Interestingly, mtr mutants of R. fascians
are nonpathogenic, implying a role in cytokinin
biosynthesis (72). The possibility that R. fascians
produces highly modified adenine derivatives
has been opted for in the past (34, 37), so one can
speculate that something has been overlooked
or missed. Cytokinin profiling of infected tissues of different hosts and of S. turgidiscabies
may shed more light on these issues.
One can also wonder if leafy gall formation
is really only about cytokinins. R. fascians produces a considerable amount of IAA via chromosomally located genes under control of the
linear plasmid (101). A dual function for auxin
has been postulated in epiphytic fitness and as
a virulence factor (101), but the auxin biosynthesis genes await identification. To clarify the
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role of bacterial auxin production in the interaction, a bacterial IAA mutant needs to be generated and its virulence and colonization capacity
investigated.
The very broad host range of R. fascians
implies that it can efficiently suppress the defense systems of an extensive variety of plants.
The question as to which strategy the pathogen
employs to avoid plant defense remains open.
Possibly, R. fascians modulates the plant’s auxin
metabolism to achieve this goal, as reported for
other plant microbial pathosystems (44).
Finally, plants that do not respond to
R. fascians merit more attention because they
are potential sources of antivirulence or antidis-
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PY49CH05-Vereecke
ease compounds. As currently no eradication
methods exist for R. fascians, molecules such as
perbergin isolated from Dalbergia species (81)
could be developed as control agents to manage
plant damage in infested ornamentals nurseries.
In conclusion, in Figure 3 we summarize
the R. fascians story and provide an overview of
the molecular, physiological, and morphological changes in pathogen and host at the different
stages of leafy gall formation. Although the major steps of symptom development have probably been outlined, with the genome sequence of
strain D188 under way, the study of the more
subtle aspects of this intriguing pathosystem are
within reach.
SUMMARY POINTS
1. Although phytohormones and plasmids seem to be used by many, R. fascians is unique
among the phytopathogens because it induces the neoformation of differentiated tissues,
collectively called the leafy gall syndrome, through the activity of linear plasmid-encoded
virulence factors.
2. The interaction starts with the epiphytic nonpathological colonization of the host that
triggers the modification of the plant’s primary metabolism, which, in turn, signals to
the bacteria when conditions are appropriate to initiate the expression of the virulence
genes.
3. The transition from an epiphytic life style to an endophytic pathogenic one is controlled
by autoregulation via the att operon. Interference with optimal functioning of the Att
mechanism strongly impedes virulence.
4. Pathogenicity strictly relies on the fas operon that codes for the production of a mixture
of six synergistic cytokinin bases: isopentenyladenine, cis-zeatin, trans-zeatin, and their
methylthio-derivatives. The trick-with-the-cytokinin-mix has several advantages, such
as a high in planta stability, the broad recognition by the cytokinin receptors, and the
overruling of the host’s cytokinin-degrading mechanisms, assuring the activation of a
signal transduction pathway leading to shoot formation.
5. The bacterially produced cytokinins, reinforced by secondary signals from the host, target
key cell cycle genes, such as CDKs and cyclins, reactivating the cell division machinery in
differentiated cortical cells. The newly dividing cells develop into shoot meristems that
produce shoots in which the continuous expression of the CYCD3 signal transduction
pathway prevents tissue maturation and the concomitant sink-to-source transition.
6. The establishment of the leafy gall is mediated by significant alterations of the transcriptome and the metabolome of the host. These changes modify the metabolic habitat in
which carbon and nitrogen sources accumulate providing a nutrient-rich niche for the
inhabiting R. fascians population.
80
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7. Whereas the epiphytic bacterial subpopulation triggers the onset of symptom development, the maintenance of the symptoms depends on the endophytic population. During
niche formation, the bacteria that colonize the plant’s apoplast adapt to the changing
environment by modifying their cell wall, transcriptome, and metabolism.
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FUTURE ISSUES
1. Analysis of the fas operon and the produced cytokinins of S. turgidiscabies should confirm
and complete the knowledge obtained with R. fascians on the composition and generation
of the cytokinin mixture.
2. R. fascians has a very important impact on the development of an extremely broad range
of plants, whereas the plant is seemingly unable to protect or inefficiently defend itself
against the activity of the virulence factors. Which are the bacterial signals that mediate
the apparent defense suppression? Investigation of the role of the bacterial auxin or of
the putative modulation of the plant auxin metabolism would shed more light on this
important issue.
3. Is the plant really a defenseless victim surrendered to the will of R. fascians? The restriction
of bacterial proliferation throughout the interaction may suggest that the plant has some
level of control over the bacteria. By assessing the responsiveness of plants with defective
defense pathways, a better insight would be obtained into the relevance of the transient
induction of defense genes.
4. The expansion in global movement of ornamentals and the lack of eradication methods
increase the threat posed by R. fascians to horticultural practices. Therefore, from a
practical point of view, it would be interesting to explore the mechanisms of recalcitrance
toward R. fascians infection.
5. Determination of the genomic sequence of R. fascians will allow a thorough investigation
of all uncovered secrets of this pathogen.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
We thank Tita Ritsema for the scanning electron microscope pictures, Melodie Putnam for the
images of symptomatic ornamental plants, Karel Spruyt for the photography of Arabidopsis, and
Martine De Cock for help in preparing the manuscript. E.S. is a research fellow of the Research
Foundation-Flanders. O.M.V. is a postdoctoral researcher of the Fonds de la Recherche Scientifique (F.R.S.-F.N.R.S., Belgium).
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whereas maturation via
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inhibited.
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www.annualreviews.org • Origin of the Leafy Gall Syndrome
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73. Unequivocal
confirmation of the
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cytokinins during the
Rhodococcus fascians–
plant interaction.
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79. Specific, detailed
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Phytopathology
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Contents
Volume 49, 2011
Not As They Seem
George Bruening p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 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
Norman Borlaug: The Man I Worked With and Knew
Sanjaya Rajaram p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 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
Chris Lamb: A Visionary Leader in Plant Science
Richard A. Dixon p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p31
A Coevolutionary Framework for Managing Disease-Suppressive Soils
Linda L. Kinkel, Matthew G. Bakker, and Daniel C. Schlatter p p p p p p p p p p p p p p p p p p p p p p p p p p p47
A Successful Bacterial Coup d’État: How Rhodococcus fascians Redirects
Plant Development
Elisabeth Stes, Olivier M. Vandeputte, Mondher El Jaziri, Marcelle Holsters,
and Danny Vereecke p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p69
Application of High-Throughput DNA Sequencing in Phytopathology
David J. Studholme, Rachel H. Glover, and Neil Boonham p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p87
Aspergillus flavus
Saori Amaike and Nancy P. Keller p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 107
Cuticle Surface Coat of Plant-Parasitic Nematodes
Keith G. Davies and Rosane H.C. Curtis p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 135
Detection of Diseased Plants by Analysis of Volatile Organic
Compound Emission
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Diverse Targets of Phytoplasma Effectors: From Plant Development
to Defense Against Insects
Akiko Sugio, Allyson M. MacLean, Heather N. Kingdom, Victoria M. Grieve,
R. Manimekalai, and Saskia A. Hogenhout p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 175
Diversity of Puccinia striiformis on Cereals and Grasses
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and Annemarie F. Justesen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 197
v
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Emerging Virus Diseases Transmitted by Whiteflies
Jesús Navas-Castillo, Elvira Fiallo-Olivé, and Sonia Sánchez-Campos p p p p p p p p p p p p p p p p p 219
Evolution and Population Genetics of Exotic and Re-Emerging
Pathogens: Novel Tools and Approaches
Niklaus J. Grünwald and Erica M. Goss p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 249
Evolution of Plant Pathogenesis in Pseudomonas syringae:
A Genomics Perspective
Heath E. O’Brien, Shalabh Thakur, and David S. Guttman p p p p p p p p p p p p p p p p p p p p p p p p p p p 269
Hidden Fungi, Emergent Properties: Endophytes and Microbiomes
Andrea Porras-Alfaro and Paul Bayman p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 291
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Hormone Crosstalk in Plant Disease and Defense: More Than Just
JASMONATE-SALICYLATE Antagonism
Alexandre Robert-Seilaniantz, Murray Grant, and Jonathan D.G. Jones p p p p p p p p p p p p p 317
Plant-Parasite Coevolution: Bridging the Gap between Genetics
and Ecology
James K.M. Brown and Aurélien Tellier p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 345
Reactive Oxygen Species in Phytopathogenic Fungi: Signaling,
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Jens Heller and Paul Tudzynski p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 369
Revision of the Nomenclature of the Differential Host-Pathogen
Interactions of Venturia inaequalis and Malus
Vincent G.M. Bus, Erik H.A. Rikkerink, Valérie Caffier, Charles-Eric Durel,
and Kim M. Plummer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 391
RNA-RNA Recombination in Plant Virus Replication and Evolution
Joanna Sztuba-Solińska, Anna Urbanowicz, Marek Figlerowicz,
and Jozef J. Bujarski p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 415
The Clavibacter michiganensis Subspecies: Molecular Investigation
of Gram-Positive Bacterial Plant Pathogens
Rudolf Eichenlaub and Karl-Heinz Gartemann p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 445
The Emergence of Ug99 Races of the Stem Rust Fungus is a Threat
to World Wheat Production
Ravi P. Singh, David P. Hodson, Julio Huerta-Espino, Yue Jin, Sridhar Bhavani,
Peter Njau, Sybil Herrera-Foessel, Pawan K. Singh, Sukhwinder Singh,
and Velu Govindan p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 465
The Pathogen-Actin Connection: A Platform for Defense
Signaling in Plants
Brad Day, Jessica L. Henty, Katie J. Porter, and Christopher J. Staiger p p p p p p p p p p p p p p p 483
vi
Contents
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Understanding and Exploiting Late Blight Resistance in the Age
of Effectors
Vivianne G.A.A. Vleeshouwers, Sylvain Raffaele, Jack H. Vossen, Nicolas Champouret,
Ricardo Oliva, Maria E. Segretin, Hendrik Rietman, Liliana M. Cano,
Anoma Lokossou, Geert Kessel, Mathieu A. Pel, and Sophien Kamoun p p p p p p p p p p p p p p p 507
Water Relations in the Interaction of Foliar Bacterial Pathogens
with Plants
Gwyn A. Beattie p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 533
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What Can Plant Autophagy Do for an Innate Immune Response?
Andrew P. Hayward and S.P. Dinesh-Kumar p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 557
Errata
An online log of corrections to Annual Review of Phytopathology articles may be found at
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vii