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MOLECULAR PLANT PATHOLOGY (2003) 4(1), 73–79
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Pathogen derived elicitors
Pathogen derived elicitors: searching for receptors in plants
M A R C O S M O N T E S A N O † , G Ü N T E R B RA D E R † A N D E . TA P I O PA L VA *
Department of Biosciences, Division of Genetics, and Institute of Biotechnology, University of Helsinki, FIN-00014, Helsinki, Finland
Recognition of potential pathogens is central to plants’ ability
to defend themselves against harmful microbes. Plants are able
to recognize pathogen-derived molecules; elicitors that trigger
a number of induced defences in plants. Microbial elicitors
constitute a bewildering array of compounds including different
oligosaccharides, lipids, peptides and proteins. Identifying the
receptors for this vast array of elicitors is a major research challenge. Only in a very few cases has the cognate receptor for a particular elicitor been identified. Biochemical studies have resulted
in the characterization of some elicitor binding proteins that may
be part of the recognition complex. Transmembrane receptor-like
protein kinases (RLKs) constitute one of the most likely categories
of receptors involved in pathogen perception. Some of these
serine/threonine kinases have been identified as resistance or R
genes, others as induced by pathogens or elicitors. One of the RLKs
belonging to a leucine rich repeat (LRR) class of putative receptor
kinases was recently identified as a receptor for bacterial flagellin,
and the underlying signal pathway leading to activation of defence
genes was elucidated. These and other recent studies have revealed
intriguing similarities in elicitor recognition and defence signalling processes in plant and animal hosts suggesting a common
evolutionary origin of eukaryotic defence mechanisms.
recognition of a potential pathogen results in several early
responses including rapid ion fluxes, activation of kinase cascades and the generation of reactive oxygen species (ROS). These
early events are followed by other defence responses including
induction of hypersensitive response (HR), a localized form of
programmed cell death (PCD) limiting pathogen spread, further
reinforcement of the cell walls, and production of antimicrobial
compounds such as defence proteins and phytoalexins. Many of
the plant defence responses are mediated by an interacting set
of endogenous signal molecules including jasmonic acid (JA),
ethylene (ET) and salicylic acid (SA). These signal molecules are part
of two major pathways in defence signalling, one SA-dependent,
the other SA-independent but involving JA and ET (Kunkel and
Brooks, 2002). However, these are not the only endogenous signals for defence gene activation but other molecules such as ROS
and nitric oxide (NO) appear also to be involved in plant defence
signalling.
Central to any inducible defence system is timely perception of
the pathogen. Plants are able to recognize compounds produced
or released by the aggressor (so-called elicitors) and employ
these to trigger defence signalling. Although a large array of
elicitor molecules have been characterized, only in a few cases has
the cognate receptor been identified. In this review we will briefly
discuss the current view on plant defence elicitors and recent
developments in elucidating the identity of plant receptors
involved in elicitor recognition.
I N T RO D U C T I O N
E L I C I T O RS O F D E F E N C E RE S P O N S E
To defend themselves against attack from the vast array of
viruses, bacteria, fungi, parasitic plants, nematodes and insects in
their environment, plants are equipped both with pre-formed,
constitutive chemical and mechanical barriers as well as with
inducible defence systems. Plants are normally capable of withstanding an attack by a potential pathogen and responding with
a local and systemic induction of a series of defences that prevent
or contain the infection and provide enhanced resistance to subsequent infections by the same or even unrelated pathogens. The
Originally the term elicitor was used for molecules capable of
inducing the production of phytoalexins, but it is now commonly
used for compounds stimulating any type of plant defence (Ebel
and Cosio, 1994; Hahn, 1996; Nürnberger, 1999). Eventually, the
induction of defence responses may lead to enhanced resistance.
This broader definition of elicitors includes both substances of
pathogen origin (exogenous elicitors) and compounds released
from plants by the action of the pathogen (endogenous elicitors)
(Boller, 1995; Ebel and Cosio, 1994).
Elicitors may be classified into two groups, ‘general elicitors’
and ‘race specific elicitors’. While general elicitors are able to trigger
defence both in host and non-host plants, race specific elicitors
SUMMARY
†Both authors contributed equally to this study.
*Correspondence: E-mail: [email protected]
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M. MONTESANO et al.
induce defence responses leading to disease resistance only in
specific host cultivars. A complementary pair of genes in a particular pathogen race and a host cultivar determines this cultivarspecific (gene-for-gene) resistance. Thus, a race specific elicitor
encoded by or produced by the action of an avirulence ( avr ) gene
present in a particular race of a pathogen will elicit resistance
only in a host plant variety carrying the corresponding resistance
(R ) gene. The absence of either gene product will often result in
disease (Cohn et al., 2001; Hammond-Kosack and Jones, 1997;
Luderer and Joosten, 2001; Nimchuk et al., 2001; Nürnberger
and Scheel, 2001; Tyler, 2002). In contrast, general elicitors signal
the presence of potential pathogens to both host and non-host
plants (Nürnberger, 1999). The nonspecific nature of general elicitors is relative, however, and some of these are only recognized
by a restricted number of plants (Shibuya and Minami, 2001).
Recent studies have indicated remarkable similarities between
the defence mechanisms triggered by general elicitors and the
innate immunity of animals, and it is tempting to speculate that
the recognition of general elicitors subsequently leads to plant
innate immunity (Nürnberger and Brunner, 2002).
Elicitors do not have any common chemical structure, but
belong to a wide range of different classes of compounds including oligosaccharides, peptides, proteins and lipids, as summarized in Table 1. This vast array of elicitor compounds precludes
the presence of a common elicitor motif and suggests that plants
have the ability to recognize a number of structurally distinct
molecules as signals for pathogen defences. Elicitors act as signal
compounds at low concentrations, providing information for the
plant to trigger defence, distinguishing elicitors from toxins,
which may act only at higher concentrations and/or affect the
plant detrimentally without active plant metabolism (Boller,
1995). The terms are overlapping, however, as exemplified by certain fungal compounds like fumonisin B1. While fumonisin B1 can
be seen as a phytotoxin in the interaction of the necrotrophic
pathogen Fusarium verticillioides with its host maize (Desjardins
and Plattner, 2000), it acts as a elicitor switching on active plant
defence and cell death programmes in the model plant Arabidopsis
(Stone et al., 2000). Coronatine provides another example of a
compound with several identities. It is a phytotoxin produced by
certain races of the pathogen Pseudomonas syringae. It mimics
JA, acting as a plant hormone and disturbing the ‘appropriate’
response in Arabidopsis (Feys et al., 1994; Kloek et al., 2001). On
the other hand, isolated from the pathogen, coronatine does
nothing but elicit the expression of defence genes (e.g. THI2.1) in
Arabidopsis (Bohlmann et al., 1998). Thus, depending on the type
of interaction, coronatine can be seen as a toxin, elicitor or a
plant hormone.
What is the function of the elicitors in the pathogen life cycle?
Most elicitors seem to fall into two broad categories. Many of
them are constitutively present in the pathogen cell wall as structural components, e.g. glucan and chitin fragments as well as
bacterial flagellin and lipopolysaccharides (LPS). Another class of
elicitor plays a role as virulence determinants, e.g. harpins, products of avr genes (see Table 1), while the function of some elicitors remains elusive. In certain plant–pathogen interactions the
main elicitors for the plant response might be produced due to
the activity of plant cell wall-degrading enzymes. These enzymes
that are often essential virulence factors and provide the attacking pathogen with nutrients, also release pectic fragments (oligogalacturonides, OGAs) that can act as endogenous elicitors (Ebel
and Cosio, 1994; Shibuya and Minami, 2001).
The vast majority of elicitors described so far are produced by
fungi and bacteria, but elicitors present in viruses or produced by
insects have also been described (Table 1). Chewing insects
cause mechanical wounding activating ET/JA-mediated defence
responses, and additionally produce other, more specific elicitors
of plant defence. The best-characterized insect-derived elicitors
are fatty-acid-amino acid conjugates (FACs) from the caterpillar
Manduca sexta. Wounding, together with FACs, leads to increased
production of volatile compounds which trigger defence gene
activation but also act as an indirect defence by attracting predators of the caterpillar (Kessler and Baldwin, 2002).
Elicitor-like substances are involved in the symbiosis between
leguminous plants and rhizobia (Cullimore et al., 2001). The
bacterial partner produces chemical signals—nodulation (Nod)
factors—that are responsible for appropriate recognition of the
bacteria by the plant partner and subsequent nodulation. The
Nod factors are lipo-chitooligosaccharides and there are pieces
of evidence suggesting that the perception of Nod factors has
evolved from recognition of more general elicitors of plant
defence such as chitin fragments or LPS (Boller, 1995; Cullimore
et al., 2001). Interestingly, LPS from plant growth-promoting
rhizobacteria trigger induced systemic resistance (ISR) to subsequent infections of plant pathogens without eliciting the accumulation of PR proteins or phytoalexin (van Loon et al., 1998).
As discussed above, there are a several indispensable components that are present in a number of pathogens and are recognized by a wide variety of plants as general defence elicitors.
Recent advances in characterizing responses to one such elicitor,
bacterial flagellin, have been instrumental in understanding
plant immunity (Asai et al., 2002; Felix et al., 1999; Meindl et al.,
2000). Flagellin represents the protein building block of the flagellar filament of eubacteria. Flagellins from a series of Gramnegative bacteria have elicitor activity, except those from highly
specialized organisms like Rhizobium melioti and Agrobacterium
tumefaciens (Felix et al., 1999). First demonstrated with Pseudomonas syringae (Felix et al., 1999), flagellin was shown to elicit
medium alkalinization and ET production in tomato cell cultures
as well as callose deposition and defence gene activation in
Arabidopsis (Gómez-Gómez et al., 1999). The N-terminal part of
flagellin, containing 15–22 conserved amino acids is responsible
for the elicitor activity (Meindl et al., 2000). Flagellins as well as
MOLECULAR PLANT PATHOLOGY (2003) 4(1), 73–79 © 2003 BLACKWELL PUBLISHING LTD
Pathogen derived elicitors
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Table 1 Elicitors of defence and defence-like responses in plants. I = oligosaccharides; II = peptides and proteins; III = glycopeptides and -proteins; IV = glycolipids;
V = lipophilic elicitors
I
Elicitor*
Source
Function in producing organism
Type
Examples for effects in plants
Branched (1,3-1,6)-β-glucans;
active with DP ≥ 7 or 5,
depending on host
Chitin oligomers; active
with DP ≥ 4– 6, depending
on host
Phytophtora,
Pythium
Component of the
fungal cell wall
General
Phytoalexin in soybean,
rice
Higher fungi
Chitin (linear β-1,4-linked
polymer of N-acetylglucosamine) of the fungal
cell wall
General
Phytoalexin in rice;
lignification in wheat
leaves
I + II
Pectolytic enzymes degrading
plant cell walls and releasing
endogenous elicitors, e.g.
oligogalacturonides
Various fungi and
bacteria
Enzymes provide
nutrients for the
pathogen
General
Protein inhibitors and
defence genes in
Arabidopsis, tomato
II
Elicitor activity independent
from enzyme activity, e.g.
endoxylanase
Elicitins (10 kDa)
PaNie 25 kDa
Trichoderma viride
Enzyme of fungal
metabolism
Race specific
HR and defence genes
in tobacco
Phytophtora, Pythium
Pythium aphanidermatum
Cladosporium fulvum;
avr products also from
other fungi and bacteria
TMV
Sterol scavengers?
?
Narrow
General
Role in virulence?
Race specific
HR in tobacco
PCD and callose formation
in tobacco, carrot, Arabidopsis
HR in tomato
Structural component
Race specific
HR in tomato, tobacco
Involved in Type III
secretion. Exact function?
Part of bacterial
flagellum
Toxin for host plants
General
General
HR and defence genes in
tobacco and Arabidopsis
Callose deposition, defence
genes, ROS in Arabidopsis
PCD in oat
Phytophtora sojae
?
General
Phytoalexin and defence
genes in parsley
Yeast
Enzyme in yeast
metabolism
General
Defence genes and
ethylene in tomato
Pseudomonas
syringae pv.
Rhizobium and other
rhizobia
Signal compound for
the bacterium?
Signal in symbiosis
communication
Race specific
HR in soybean carrying
Rpg 4 resistance gene
Nod formation in legumes
but also alkalinization in
tomato cell cultures
FACs (fatty acid amino acid
conjugates)
Ergosterol
Various Lepidoptera
Bacterial toxins, e.g.
coronatine
Pseudomonas syringae
Sphinganine analogue
mycotoxins,
e.g. fumonisin B1
Fusarium moniliforme
Emulsification of lipids
during digestion?
Main sterol of higher
fungi
Toxin in compatible
interactions, disturbs
‘proper’ salicylic acid
response, mimics
jasmonate action
Toxin in necrotrophic
interaction; disturbs
sphingolipid metabolism
avr gene products, e.g.
AVR4, AVR9
Viral proteins, e.g. viral
coat protein
Harpins (kDa)
Flagellin (33 kDa); flg15 is
sufficient for activity
Protein or peptide toxins,
e.g. victorin
III
IV
Glycoproteins, e.g. a 42 kDa
protein where a Pep-13
fragment without
glycosylation site is sufficient
for elicitor function
Glycopeptide fragments of
invertase
Syringolids (acyl glycosides)
Nod factors (lipochitooligosaccharides)
V
Several Gram-negative
bacteria
Gram-negative bacteria
Helminthosporium
victoriae (rust)
Various fungi
Race specific
General
General
General
General
General
Monoterpenes in tobacco—
‘indirect’ defence
Alkalinization in tomato
cell cultures
Defence genes and defence
compounds in Arabidopsis,
Brassica
PCD and defence genes
in tomato, Arabidopsis
*DP = degree of polymerization.
Data from reviews (Boller, 1995; Cullimore et al., 2001; Ebel and Cosio, 1994; Hahn, 1996; Kessler and Baldwin, 2002; Leach and White, 1996; Nürnberger, 1999;
Ponchet et al., 1999; Shibuya and Minami, 2001; Tyler, 2002) and original articles (Asai et al., 2002; Bohlmann et al., 1998; Desjardins and Plattner, 2000; Felix
et al., 1999; Feys et al., 1994; Gómez-Gómez et al., 1999; Hanania and Avni, 1997; Kloek et al., 2001; Stone et al., 2000; Tada et al., 2001; Veit et al., 2001).
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other general plant defence elicitors are also recognized as
antigenic by animals. These molecules, referred to as pathogenassociated molecular patterns (PAMPs) trigger immune response
genes and the production of antimicrobial compounds in animals.
Thus similar elicitor molecules appear to trigger innate immunity
in animals and plants (Nürnberger and Brunner, 2002).
In nature, plants have to deal with various potential aggressors, all of them capable of exhibiting a specific ‘elicitor profile’.
How then does the plant perceive the given elicitor signal? The
elicitor may act directly as a ligand or release plant compounds
(endogenous elicitors) which interact with receptors. The elicitor
does not necessarily need to interact with a receptor but may, for
example form membrane pores or bilayer discontinuities that
elicit responses. These mechanisms of elicitor activity have been
suggested for peptides from the parasitic fungus Trichoderma
viridae (Engelberth et al. 2001), yeast elicitors (Klüsener and
Weiler, 1999), and the bacterial HR inducer harpin (Lee et al.,
2001a,b).
PE RC E P T I O N O F E L I C I T O RS
The successful activation of plant defence responses requires
timely perception of the aggressor, whether through recognition
of race-specific elicitors or general elicitors. While only a very few
receptors interacting with elicitors have been identified, recent
results have significantly improved our understanding of elicitor
perception and the development of disease resistance. Interestingly, in many race–cultivar specific interactions, especially those
involving bacteria, the recognition of the avr gene products by
R gene products appears to take place intracellularly (Bonas
and Lahaye, 2002; Nürnberger, 1999), often involving leucine
rich repeat (LRR)-containing proteins. Not all R proteins are
intracellular— some seem to act as cell-surface receptors. Plant
cell-surface receptors are key components that perceive extracellular stimuli from the environment, including both general and
race specific elicitors. Several high affinity binding sites for general
elicitors including oligosaccharides, glycopeptides and peptides
have been identified through biochemical approaches (Basse et al.,
1993; Cheong and Hahn, 1991; Cosio et al., 1990; Ito et al., 1997;
Mithöfer et al., 2000; Nürnberger et al., 1994; Umemoto et al., 1997).
For example, similar 75 kDa proteins associated with the plasma
membrane of Glycine max and Phaseolus vulgaris cells, bind βglucan elicitors from Phytophthora species with high affinity
(Mithöfer et al., 2000; Umemoto et al., 1997). However, none of
these proteins exhibit a signalling domain, suggesting that these
β-glucan binding proteins may interact with other components to
transduce the elicitor signal (Mithöfer et al., 2000).
Molecular approaches have led to the identification of several
types of putative receptors in plants. According to their structural
characteristics they have been classified into different categories,
including receptor-like protein kinases (RLKs), histidine kinase
receptors and receptors with different numbers of transmembrane domains (Grignon, 1999; Satterlee and Sussman, 1998;
Walker, 1994). Some of the best characterized but not directly
involved in pathogen perception are the ethylene receptor ETR1
and the cytokinin receptor CRE1, both of them histidine kinase
receptors (Bleecker and Kende, 2000; Inoue et al., 2001).
Of special interest in pathogen perception are the RLKs; there
are at least 340 genes encoding putative RLKs in the Arabidopsis
genome (The Arabidopsis Genome Initiative, 2000). RLKs are
characterized by an extracellular domain which is probably
involved in signal perception, a transmembrane domain and a
cytoplasmic kinase domain, which may initiate a signal transduction cascade into the cell. All plant RLKs identified are serinethreonine kinases and based on the structural characteristics of
the extracellular domain they have been divided into different
categories (Fig. 1) (Satterlee and Sussman, 1998; Shiu and Bleecker,
2001; Walker, 1994).
The diversity of plant RLKs and the large number of them
present in the Arabidopsis genome suggest that RLKs may be
involved in the perception of a wide range of stimuli, including
elicitors produced both during symbiosis (Endre et al., 2002;
Stracke et al., 2002) and in plant–pathogen interactions. Some
RLKs have been identified as R gene products, e.g. Xa21 (an LRR
type of RLK) from rice (Oryza sativa) that confer resistance to
Fig. 1 Schematic representation of plant receptor-like protein kinases (RLKs)
possibly associated with elicitor perception. All the RLK identified contain a
serine-threonine kinase domain and their extracellular domains exhibit
similarity to diverse sequence motifs. (A) Xa21 from rice contains leucine-rich
repeats (LRR) (Song et al., 1995). (B) AthLecRK1 from Arabidopsis contains
lectin-like motifs (Hervé et al., 1996). (C) PR5K from Arabidopsis exhibits
similarity to the PR protein thaumatin (Wang et al., 1996). (D) CHRK1 from
tobacco shows similarity to the PR protein chitinase (Kim et al., 2000). (E)
WAK1 from Arabidopsis contains epidermal growth factor-like (EGF) repeats
(He et al., 1999). (F) LRK10 from wheat do not exhibit homology to a particular
established sequence motif (Feuillet et al., 1997). (G) StPRKs from potato
exhibit a novel bimodular cysteine motif (Montesano et al., 2001).
MOLECULAR PLANT PATHOLOGY (2003) 4(1), 73–79 © 2003 BLACKWELL PUBLISHING LTD
Pathogen derived elicitors
Xanthomonas oryzae pv. oryzae (Song et al., 1995) and LRK10
from wheat (Triticum aestivum) that confer resistance to the
wheat rust fungus Puccinia recondita (Feuillet et al., 1997). Several R genes appear to encode cytoplasmic proteins related to
RLKs, including the Pto R gene product involved in resistance
against P. syringae (Shiu and Bleecker, 2001).
In addition to R gene products, several other RLKs have been
associated with plant defence responses to pathogens. In these
cases, the association is usually based on the expression pattern
certain RLKs exhibit in plants treated with elicitors, pathogens or
signal molecules related to defence responses such as SA. For
example, RLK3 from Arabidopsis is induced by oxidative stress,
SA and pathogen attack (Czernic et al., 1999), SFR1 (S domain
RLK) from Brassica oleracea is induced by wounding and bacterial infection (Pastuglia et al., 1997), and StPRKs (potato receptor
kinase) from potato (Solanum tuberosum) are induced by plant
cell wall-degrading enzymes from Erwinia carotovora and short
oligogalacturonides (Montesano et al., 2001). The StPRKs constitute a new group of RLKs with a bimodular cysteine motif in the
extracellular domain (Montesano et al., 2001). Another group of
pathogen-related receptor kinases is the WAK (wall associated
kinase) family that is induced by pathogens and SA and thought
to interact with cell wall pectin (He et al., 1999; Shiu and
Bleecker, 2001). The extracellular domain of the WAK from Arabidopsis contains epidermal growth factor-like (EGF) repeats (He
et al., 1999). Whether the elicitors inducing expression of the RLK
genes are ligands of these RLKs remains to be demonstrated.
Structural features of some RLKs suggest an elicitor receptor
function. Thus some RLKs contain extracellular domains with
similarity to pathogenesis-related (PR) proteins from plants.
Examples of this class are PR5K from Arabidopsis with similarity
to PR5 (thaumatin) (Wang et al., 1996) and CHRK1 from tobacco
with similarity to chitinase (Kim et al., 2000). It is tempting to
speculate that CHRK1 may be involved in the recognition of
pathogen-derived chitin oligosaccharides. Another class of RLKs
possibly involved in the perception of oligosaccharide elicitors
contains lectin-like motifs within their extracellular domain (Fig. 1).
Based on the sequence similarity to lectin proteins, the lectin
binding motifs of these RLKs are thought to bind sugars (Hervé
et al., 1996).
By far the best characterized receptor system for a general
pathogen elicitor is the flagellin receptor identified by the Boller
laboratory (Gómez-Gómez and Boller, 2000; Gómez-Gómez and
Boller, 2002). They employed a genetic screen for flagellin insensitive Arabidopsis mutants that mapped to a single locus FLS2.
This gene was shown to encode a LRR-containing transmembrane RLK, structurally similar to Xa21 (Fig. 1). The LRR regions
often participate in protein–protein interactions and evidence
suggests that the LRR domain of FLS2 indeed interacts with a
conserved domain of eubacterial flagellin (Bauer et al., 2001).
Interestingly, FLS2 exhibits a structural similarity to Drosophila
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Toll and mammalian TLRs (Toll like receptor), both of which are
LRR-type receptors involved in mediating the innate immune
responses in animals. Thus, both plants and animals appear to
have related receptors to the same elicitor, flagellin. Recent work
using transient assays in Arabidopsis protoplasts led to the
identification of a MAP kinase cascade and WRKY transcription
factors downstream of FLS2 (Asai et al., 2002). The similarity of this
signalling system to those in animals further suggests a common
evolutionary origin of innate immunity response in plants and
animals.
Although a direct receptor–elicitor interaction has been
demonstrated in some cases (as in the flagellin–FLS2 interaction),
the recognition event is often likely to be more complicated. For
example, the tomato protein kinase Pto requires an additional
NB-LRR protein (Prf ) to trigger a resistance response upon recognition of AvrPto (Oldroyd and Staskawicz, 1998). The elucidation
of such a type of Avr/R interactions led to the development of the
guard hypothesis (for review and possible mechanistic scenarios
see Dangl and Jones, 2001; Luderer and Joosten, 2001). Generally, the Avr product does not directly interact with an R-protein,
but at least three players are needed to trigger resistance. New
insights into the mechanisms involved here are provided by the
recent results of Mackey et al. (2002). Similar scenarios to those
described above are possible in general elicitor–RLK interactions,
where induction of the RLK defence cascade might require not
only the elicitor itself but also a guardee molecule forming a complex with the elicitor, which is thereafter recognized by the receptor.
These scenarios are hypothetical, but the lack of a direct R/Avr
interaction in several cases and the difficulty in finding receptors
for given general elicitors are indicators for such more complex
scenarios. An exciting task for the future will be the elucidation
of the nature of these putative recognition complexes.
ACKNOWLEDGEMENTS
Research in the laboratory of E.T.P. is supported by the Academy
of Finland, Biocentrum Helsinki and the Finnish Technical Development Board (TEKES).
R E F E RE N C E S
Asai, T., Tena, G., Plotnikova, J., Willmann, M.R., Chiu, W.-L., GómezGómez, L., Boller, T., Ausubel, F.M. and Sheen, J. (2002) MAP kinase
signalling cascade in Arabidopsis innate immunity. Nature, 415, 977–983.
Basse, C.W., Fath, A. and Boller, T. (1993) High affinity binding of a
glycopeptide elicitor to tomato cells and microsomal membranes and
displacement by specific glycan suppressors. J. Biol. Chem. 268,
14724 –14731.
Bauer, Z., Gómez-Gómez, L., Boller, T. and Felix, G. (2001) Sensitivity
of different ecotypes and mutants of Arabidopsis thaliana toward the
bacterial elicitor flagellin correlates with the presence of receptorbinding sites. J. Biol. Chem. 276, 45669– 45676.
© 2003 BLACKWELL PUBLISHING LTD MOLECULAR PLANT PATHOLOGY (2003) 4(1), 73–79
78
M. MONTESANO et al.
Bleecker, A.B. and Kende, H. (2000) Ethylene: a gaseous signal molecule
in plants. Annu. Rev. Cell. Dev. Biol. 16, 1–18.
Bohlmann, H., Vignutelli, A., Hilpert, B., Miersch, O., Wasternack, C.
and Apel, K. (1998) Wounding and chemicals induce expression of the
Arabidopsis thaliana gene Thi2.1, encoding a fungal defense thionin, via
the octadecanoid pathway. FEBS Lett. 43, 281–286.
Boller, T. (1995) Chemoperception of microbial signals in plant cells. Annu.
Rev. Plant Physiol. Plant Mol Biol. 46, 189–214.
Bonas, U. and Lahaye, T. (2002) Plant disease resistance triggered by
pathogen-derived molecules: refined models of specific recognition.
Curr. Opin. Microbiol. 5, 44–50.
Cheong, J.-J. and Hahn, M.G. (1991) A specific, high-affinity binding site
for the hepta-β-glucoside elicitor exists in soybean membranes. Plant
Cell, 3, 137–147.
Cohn, J., Sessa, G. and Martin, G.B. (2001) Innate immunity in plants.
Curr. Opin. Immunol. 13, 55–62.
Cosio, E.G., Frey, T., Verduyn, R., van Boom, J. and Ebel, J. (1990)
High-affinity binding of a synthetic heptaglucoside and fungal glucan
phytoalexin elicitors to soybean membranes. FEBS Lett. 271, 223–226.
Cullimore, J.V., Ranjeva, R. and Bono, J.-J. (2001) Perception of lipochitooligosaccharidic Nod factors in legumes. Trends Plant Sci. 6, 24 –30.
Czernic, P., Visser, B., Sun, W., Savoure, A., Deslandes, L., Marco, Y.,
van Montagu, M. and Verbruggen, N. (1999) Characterization of an
Arabidopsis thaliana receptor-like protein kinase gene activated by
oxidative stress and pathogen attack. Plant J. 18, 321–327.
Dangl, J.L. and Jones, J.D.G. (2001) Plant pathogens and integrated
defence responses to infection. Nature, 411, 826–833.
Desjardins, A.E. and Plattner, R.D. (2000) Fumonisin B1-nonproducing
strains of Fusarium verticillioides cause maize (Zea mays) ear infection
and ear rot. J. Agric. Food Chem. 48, 5773–5780.
Ebel, J. and Cosio, E.G. (1994) Elicitors of plant defense responses. Int.
Rev. Cytol. 148, 1–36.
Endre, G., Kereszt, A., Kevei, Z., Mihacea, S., Kaló, P. and Kiss, G.B.
(2002) A receptor kinase gene regulating symbiotic nodule development.
Nature, 417, 962–966.
Engelberth, J., Koch, T., Schüler, G., Bachmann, N., Rechtenbach, J.
and Boland, W. (2001) Ion channel-forming alamethicin is a potent
elicitor of volatile biosynthesis and tendril coiling. Crosstalk between
jasmonate and salicylate signaling in lima bean. Plant Physiol. 125,
369–377.
Felix, G., Duran, J.D., Volko, S. and Boller, T. (1999) Plants have a
sensitive perception system for the most conserved domain of bacterial
flagellin. Plant J. 18, 265–276.
Feuillet, C., Schachermayr, G. and Keller, B. (1997) Molecular cloning of
a new receptor-like kinase gene encoded at the Lr10 disease resistance
locus of wheat. Plant J. 11, 45–52.
Feys, B.J.F., Benedetti, C.E., Penfold, C.N. and Turner, J.G. (1994)
Arabidopsis mutants selected for resistance to the phytotoxin coronatine
are male sterile, insensitive to methyl jasmonate, and resistant to a
bacterial pathogen. Plant Cell, 6, 751–759.
Gómez-Gómez, L. and Boller, T. (2000) An LRR- receptor-like kinase
involved in the perception of bacterial elicitor flagellin in Arabidopsis.
Mol. Cell, 5, 1003–1011.
Gómez-Gómez, L. and Boller, T. (2002) Flagellin perception: a paradigm
for innate immunity. Trends Plant Sci. 7, 251–256.
Gómez-Gómez, L., Felix, G. and Boller, T. (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J. 18,
277–284.
Grignon, C. (1999) Recent advances on proteins of plant terminal membranes. Biochimie, 81, 577–596.
Hahn, M.G. (1996) Microbial elicitors and their receptors in plants. Annu.
Rev. Phytopathol. 34, 387–412.
Hammond-Kosack, K.E. and Jones, J.D.G. (1997) Plant disease resistance
genes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 575–607.
Hanania, U. and Avni, A. (1997) High-affinity binding site for ethyleneinducing xylanase elicitor on Nicotiana tabacum membranes. Plant J. 12,
113–120.
He, Z.-H., Cheeseman, I., He, D. and Kohorn, B.D. (1999) A cluster of five
cell wall-associated receptor kinases, Wak1–5, are expressed in specific
organs of Arabidopsis. Plant Mol. Biol. 39, 1189–1999.
Hervé, C., Dabos, P., Galaud, J.-P., Rouge, P. and Lescure, B. (1996)
Characterization of an Arabidopsis thaliana gene that defines a new
class of putative plant receptor kinases with an extracellular lectin-like
domain. J. Mol. Biol. 258, 778–788.
Inoue, T., Higuchi, M., Hashimoto, Y., Seki, M., Kobayashi, M., Kato, T.,
Tabata, S., Shinozaki, K. and Kakimoto, T. (2001) Identification of CRE1
as a cytokinin receptor from Arabidopsis. Nature, 409, 1060–1063.
Ito, Y., Kaku, H. and Shibuya, S. (1997) Identification of a high-affinity
binding protein for N-acetylchitooligosacharide elicitor in the plasma
membrane of suspension-cultured rice cells by affinity labeling. Plant J.
12, 347–356.
Kessler, A. and Baldwin, I.T. (2002) Plant responses to insect herbivory:
The emerging molecular analysis. Annu. Rev. Plant Biol. 53, 299–328.
Kim, Y.S., Lee, J.H., Yoon, G.M., Cho, H.S., Park, S.-W., Suh, M.C., Choi,
D., Ha, H.J., Liu, J.R. and Pai, H.-S. (2000) CHRK1, a chitinase-related
receptor-like kinase in tobacco. Plant Physiol. 123, 905–915.
Kloek, A.P., Verbsky, M.L., Sharma, S.B., Schoelz, J.E., Vogel, J.,
Klessig, D.F. and Kunkel, B.N. (2001) Resistance to Pseudomonas
syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1)
mutation occurs through two distinct mechanisms. Plant J. 26, 509–522.
Klüsener, B. and Weiler, E.W. (1999) Pore-forming properties of elicitors
of plant defense reactions and cellulolytic enzymes. FEBS Lett. 459, 263–
266.
Kunkel, B.N. and Brooks, D.M. (2002) Cross talk between signaling
pathways in pathogen defense. Curr. Opin. Plant Biol. 5, 325–331.
Leach, J.E. and White, F.F. (1996) Bacterial avirulence genes. Annu. Rev.
Phytopathol. 34, 153–179.
Lee, J., Klessig, D.F. and Nürnberger, T. (2001a) A harpin binding site in
tobacco plasma membranes mediates activation of the pathogenesisrelated gene HIN1 independent of extracellular calcium but dependent
on mitogen-activated protein kinase activity. Plant Cell, 13, 1079–1093.
Lee, J., Klüsener, B., Tsiamis, G., Stevens, C., Neyt, C., Tampakaki,
A.P., Panopoulos, N.J., Nöller, J., Weiler, E.W., Cornelis, G.R.,
Mansfield, J.W. and Nürnberger, T. (2001b) HrpZPsph from the plant
pathogen Pseudomonas syringae pv. phaseolicola binds to lipid bilayers
and forms an ion-conducting pore in vitro. Proc. Natl Acad. Sci. USA,
98, 289–294.
van Loon, L.C., Bakker, P.A.H.M. and Pieterse, M.J. (1998) Systemic
resistance induced by rhizosphere bacteria. Annu. Rev. Phytopatol. 36,
453–483.
Luderer, R. and Joosten, M.H.A.J. (2001) Avirulence proteins of plant
pathogens: Determinants of victory and defeat. Mol. Plant Path. 2, 355–
364.
Mackey, D., Holt III, B.F., Wiig, A. and Dangl, J.L. (2002) RIN4 interacts
with Pseudomonas syringae Type III effector molecules and is required for
RPM1-mediated resistance in Arabidopsis. Cell, 108, 743–754.
MOLECULAR PLANT PATHOLOGY (2003) 4(1), 73–79 © 2003 BLACKWELL PUBLISHING LTD
Pathogen derived elicitors
Meindl, T., Boller, T. and Felix, G. (2000) The bacterial elicitor flagellin
activates its receptor in tomato cells according to the address-message
concept. Plant Cell, 12, 1783–1794.
Mithöfer, A., Fliegmann, J., Neuhaus-Uri, G., Schwarz, H. and Ebel, J.
(2000) The hepta-β-glucoside elicitor-binding proteins from legumes
represent a putative receptor family. Biol. Chem. 381, 705–713.
Montesano, M., Kõiv, V., Mäe, A. and Palva, E.T. (2001) Novel receptorlike protein kinases induced by Erwinia carotovora and short oligouronides in potato. Mol. Plant Pathol. 2, 339–346.
Nimchuk, Z., Rohmer, L., Chang, J.H. and Dangl, J.L. (2001) Knowing
the dancer from the dance: R-gene products and their interactions with
other proteins from host and pathogen. Curr. Opin. Plant Biol. 4, 288–
294.
Nürnberger, T. (1999) Signal perception in plant pathogen defense.
Cell. Mol. Life Sci. 55, 167–182.
Nürnberger, T. and Brunner, F. (2002) Innate immunity in plants and
animals: emerging parallels between the recognition of general elicitors
and pathogen-associated molecular patterns. Curr. Opin. Plant Biol. 5,
318–324.
Nürnberger, T., Nennstiel, D., Jabs, T., Sacks, W.R., Hahlbrock, K. and
Scheel, D. (1994) High affinity binding of a fungal oligopeptide elicitor
to parsley plasma membranes triggers multiple defense responses. Cell,
78, 449–460.
Nürnberger, T. and Scheel, D. (2001) Signal transmission in the plant
immune response. Trends Plant Sci. 6, 372–379.
Oldroyd, G.E.D. and Staskawicz, B.J. (1998) Genetically engineered
broad-spectrum disease resistance in tomato. Proc. Natl Acad. Sci. USA,
95, 10300–10305.
Pastuglia, M., Roby, D., Dumas, C. and Cock, M. (1997) Rapid induction
by wounding and bacterial infection of a S gene family receptor-like
kinase gene in Brassica oleracea. Plant Cell, 9, 49–60.
Ponchet, M., Panabieres, F., Milat, M.L., Mikes, V., Montillet, J.L.,
Suty, L., Triantaphylides, C., Tirilly, Y. and Blein, J.P. (1999) Are
elicitins cryptograms in plant-Oomycete communications? Cell. Mol. Life
Sci. 56, 1020–1047.
Satterlee, J.S. and Sussman, M.R. (1998) Unusual membrane-associated
protein kinases in higher plants. J. Membr. Biol. 164, 205–213.
79
Shibuya, N. and Minami, E. (2001) Oligosaccharide signalling for defence
responses in plant. Physiol. Mol. Plant Pathol. 59, 223–233.
Shiu, S.-H. and Bleecker, A.B. (2001) Plant receptor-like kinase gene
family: diversity, function, and signaling. Sci. STKE 113, RE22.
Song, W.-Y., Wang, G.-L., Chen, L.-L., Kim, H.-S., Pi, L.-Y., Holsten, T.,
Gardner, J., Wang, B., Zhai, W.-X., Zhu, L.-H., Fauquet, C. and Ronald, P. (1995) A receptor kinase-like protein encoded by the rice disease
resistance gene Xa21. Science, 270, 1804–1806.
Stone, J.M., Heard, J.E., Asai, T. and Ausubel, F.M. (2000) Simulation of
fungal-mediated cell death by fumonisin B1 and selection of fumonisin
B1-resistant (fbr) Arabidopsis mutants. Plant Cell, 12, 1811–1822.
Stracke, S., Kistner, C., Yoshida, S., Mulder, L., Sato, S., Kaneko, T.,
Tabata, S., Sandal, N., Stougaard, J., Szczyglowski, K. and Parniske, M. (2002) A plant receptor-like kinase required for both bacterial
and fungal symbiosis. Nature, 417, 959–962.
Tada, Y., Hata, S., Takata, Y., Nakayashiki, H., Tosa, Y. and Mayama,
S. (2001) Induction and signaling of an apoptotic response typified by
DNA laddering in the defense response of oats to infection and elicitors.
Mol. Plant-Microbe Interact. 14, 477–486.
The Arabidopsis Genome Initiative (2000) Analysis of the genome
sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796–815.
Tyler, B.M. (2002) Molecular basis of recognition between Phytophtora
pathogens and their hosts. Annu. Rev. Phytopathol. 40, 137–167.
Umemoto, N., Kakitani, M., Iwamatsu, A., Yoshikawa, M., Yamaoka, N.
and Ishida, I. (1997) The structure and function of a soybean beta
glucan elicitor binding protein. Proc. Natl Acad. Sci. USA, 94, 1029–
1034.
Veit, S., Worle, J.M., Nürnberger, T., Koch, W. and Seitz, H.U. (2001) A
novel protein elicitor (PaNie) from Pythium aphanidermatum induces
multiple defense responses in carrot, Arabidopsis, and tobacco. Plant
Physiol. 127, 832–841.
Walker, J.C. (1994) Structure and function of the receptor-like protein
kinase of higher plants. Plant Mol. Biol. 26, 1599–1609.
Wang, X., Zafian, P., Choudhary, M. and Lawton, M. (1996) The PR5K
receptor protein kinase from Arabidopsis thaliana is structurally related
to a family of plant defense proteins. Proc. Natl Acad. Sci. USA. 93,
2598–2602.
© 2003 BLACKWELL PUBLISHING LTD MOLECULAR PLANT PATHOLOGY (2003) 4(1), 73–79