Graduate School of Bio-Agricultural Sciences, Nagoya University, Chikusa, Nagoya 464-8601, Japan (e-mail: matsu{at}agr.nagoya-u.ac.jp)
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Summary |
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Key words: Peptide hormone, Receptor-like kinase, Plant, Leucine-rich repeat
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Introduction |
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To date, researchers have identified four peptide-ligand-receptor pairs in
plants (reviewed by Ryan et al.,
2002), which are involved in a variety of processes, such as wound
responses, cellular dedifferentiation, meristem organization and
self-incompatibility (Fig. 1,
Table 1). However, these must
be only part of the story, because plant genome sequencing has revealed many
genes predicted to encode small peptide ligands and receptor-like kinases,
whose functions remain to be uncovered
(The Arabidopsis Genome Initiative,
2000
; Shiu and Bleecker,
2001
). Furthermore, mutations in possible prohormone processing
proteases have been shown to disrupt plant growth and development. For
example, the Arabidopsis sdd1 mutant, which has a defect in a
subtilisin-like serine protease, shows stomatal clustering and an increase in
stomatal density (Berger and Altmann,
2000
). Arabidopsis amp1 mutants show pleiotropic
phenotypes, including altered shoot apical meristems, increased cell
proliferation, and increased cyclin expression. The AMP1 gene encodes
a protein with significant similarity to glutamate carboxypeptidases
(Helliwell et al., 2001
). In
addition, the ALE1 gene, which is required for proper differentiation
of epidermis, encodes a subtilisin-like serine protease
(Tanaka et al., 2001
). All
this evidence strongly suggests that a number of undiscovered peptide ligands
that are produced by proteolytic processing from larger proteins are involved
in plant growth and development.
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Here, I outline the roles of the four known ligand-receptor pairs in plant peptide signaling from a biochemical point of view, and discuss the current limitations of the methodology used in identifying new ligand-receptor pairs and possibilities for future studies.
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Systemins: systemic inducers of the plant wound response |
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Cloning of systemin cDNA revealed that the peptide is proteolytically
processed from the C-terminus of a 200-residue precursor called prosystemin
(McGurl et al., 1992). This
precursor, however, does not exhibit a signal sequence at its N terminus,
which suggests that it does not enter the secretory pathway but is probably
systhesized on free ribosomes in the cytosol. Prosystemin orthologs have also
been identified in other solanaceous species, such as potato, black nightshade
and bell pepper (Constabel et al.,
1998
), but not in tobacco. Two prosystemin isoforms produced by
alternative splicing of prosystemin pre-mRNA have been found, and both
isoforms are active as signals in the wound response pathway
(Li and Howe, 2001
). Promoter
analysis of the prosystemin gene indicates a low, constitutive level of
expression in unwounded leaves and the presence of wound-inducible elements
that can be activated in cells associated with the vascular bundles of
petioles (Jacinto et al.,
1997
). Although systemin peptide has been detected in the phloem,
how the systemin peptide is incorporated into this transport system and how it
is transported from the phloem to the outside of distal leaf cells to activate
defense genes have not been established.
The significance of systemin in the defense response was revealed by
experiments in which tomato plants were transformed with sense or antisense
prosystemin cDNAs under the control of the constitutive 35S promoter
(McGurl et al., 1994).
Overexpression of prosystemin resulted in constitutive expression of defense
response genes, as if the plant were in a permanently wounded state. In
addition, grafting of wild-type tomato plants onto root stocks overexpressing
the prosystemin gene caused the wild-type scions to express defense genes in
the absence of wounding. By contrast, transgenic plants expressing anti-sense
systemin transcripts showed a severe depression of systemic proteinase
inhibitor induction as well as decreased resistance towards herbivorous larvae
(Orozco-Cardenas et al.,
1993
).
Although several solanaceous species contain homologs of prosystemin genes,
no orthologous tobacco gene had been identified until recently. Pearce et al.,
however, have now isolated systemic hydroxyproline-rich glycopeptides
(TobHypSys I and II) from tobacco leaves by biochemical purification
(Pearce et al., 2001). Both
peptides contain 18 residues, although they share no sequence similarity with
tomato systemin, and have tobacco-trypsin inhibitor-inducing activity similar
to that of tomato systemin. District peptides might therefore serve the same
functions in different plant species. Interestingly, the tobacco peptides
arise from a single 165-residue precursor protein that has a signal sequence
at its N-terminus; such a scenario is common in peptide-ligand precursors in
animals (Fisher et al., 1988
).
Recently, Pearce and Ryan (Pearce and
Ryan, 2003
) reported the isolation of three hydroxyproline-rich
glycopeptides from tomato leaves, of 20, 18 and 15 amino acids in length, that
act as signals for activation of defense genes, and function similarly to the
systemin peptide. These three glycopeptides (TomHypSys I, TomHypSys II, and
TomHypSys III) are also encoded by a single precursor gene.
A systemin receptor was detected in plasma membranes from tomato cells
(Scheer and Ryan, 1999). A
mono-iodinated systemin analog rapidly, reversibly and saturably binds to the
receptor with nanomolar binding affinity. Scheer and Ryan have purified the
160 kDa receptor, SR160, from tomato plasma membranes
(Scheer and Ryan, 2002
). It
has a typical leucine-rich repeat receptor-like kinase (LRR-RLK) sequence,
including a putative signal sequence, a leucine zipper motif, 25 LRRs
interrupted by an island domain, a single transmembrane domain, and a protein
kinase domain (Fig. 2A).
Interestingly, SR160 has also been isolated as tBRI1 (tomato brassinosteroid
insensitive 1), a membrane receptor for the plant steroid hormone
brassinolide, which is essential for normal plant development
(Montoya et al., 2002
).
Brassinolide, however, does not compete with systemin for binding to SR160. To
confirm that SR160/tBRI1 is a bona fide systemin receptor, it should be
determined whether tBRI1 mutants lack systemin-binding activity and exhibit
defective systemin signaling.
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Phytosulfokine: a key factor regulating cellular dedifferentiation and re-differentiation in plants |
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This growth factor has been purified from conditioned medium derived from
suspension culture of dispersed asparagus mesophyll cells
(Matsubayashi and Sakagami,
1996). It is a five-residue peptide that has the sequence
Tyr(SO3H)-Ile-Tyr(SO3H)-Thr-Gln, and because of the
presence of a sulfate ester, is named phytosulfokine (PSK). Sulfated tyrosine
residues are often found in secreted peptides in animals
(Huttner, 1982
) but, to date,
PSK is the only example of post-translational sulfation of tyrosine residues
in plants. PSK with an identical structure is present in conditioned medium
derived from many plant cell lines, including dicotyledons and monocotyledons,
which indicates the peptide is widely distributed in higher plants. PSK
induces dedifferentiation and callus growth of dispersed plant cells at low
nanomolar concentrations, even at initial cell densities as low as
300
cells/ml. Interestingly, it also stimulates tracheary element differentiation
of Zinnia mesophyll cells without intervening cell division
(Matsubayashi et al., 1999
)
and stimulates somatic embryogenesis in carrot
(Kobayashi et al., 1999
). Such
cellular dedifferentiation and re-differentiation, however, cannot be induced
by PSK alone, but require in addition certain ratios and concentrations of
auxin and cytokinin.
Organogenesis in vitro generally has three distinct phases, which were
revealed by the temporal requirements of explants for a specific balance of
phytohormones in the control of organogenesis
(Christianson and Warnick,
1985). In the first phase, explants acquire competence, which is
defined as the ability to respond to induction signals such as auxin and
cytokinin. These competent explants can then be canalized and analysed for
specific organ development under the influence of the auxin/cytokinin balance
through the second phase. During the third phase, morphogenesis proceeds
independently of exogenously supplied hormones. One possibility is that PSK
confers competence on individual cell plants and that auxin and cytokinin then
determine cell fate.
Five paralogous genes encoding 80-residue precursors of PSK have been
identified in Arabidopsis. Each predicted protein has a probable
secretion signal at the N-terminus and a single PSK sequence close to the
C-terminus (Yang et al.,
2001
). In addition, there are dibasic amino acid residues
immediately upstream from the PSK domain. It is generally accepted that, in
animal prohormone precursor proteins, the primary processing recognition
sequence for endoproteolysis is a pair of basic amino acid residues that
bracket the peptide hormone (Harris,
1989
). Gene families encoding putative PSK precursors also exist
in many other plant species, including rice, carrot and asparagus, but these
genes are extremely diverse, with only a few residues being conserved
throughout the family. PSK mRNAs are found not only in callus cells
but also in the leaves and roots of intact plants, indicating that
PSK expression is not limited to the region in which individual cells
actively divide. Overexpression of PSK genes slightly promotes callus
formation in the presence of auxin and cytokinin
(Yang et al., 2001
) but does
not affect growth of plants (Y.M., unpublished).
Acidic amino acid residues flanking the mature PSK sequence in PSK
precursors are suggested to be involved in tyrosine sulfation, which is
catalyzed by a tyrosylprotein sulfotransferase in the Golgi apparatus
(Hanai et al., 2000). Since
elimination of sulfate esters of tyrosine residues within the mature PSK
sequence abolishes its biological activities, tyrosylprotein sulfotransferase
must be a key enzyme in PSK biosynthesis.
Studies using radiolabelled PSK have provided evidence for the existence of
high-affinity binding sites for PSK in plant plasma membranes
(Matsubayashi et al., 1997;
Matsubayashi and Sakagami,
1999
). Photoaffinity labeling experiments have shown that 120 kDa
and 150 kDa glycosylated proteins are putative PSK receptors
(Matsubayashi and Sakagami,
2000
), and a PSK receptor has been purified from membrane
fractions of carrot cells (Matsubayashi et
al., 2002
). The cDNA encodes a typical LRR-RLK that has 21 LRRs
and a 36-residue island between the 17th and 18th LRRs
(Fig. 2B). Overexpression of
this receptor-like kinase in carrot cells enhances callus growth in response
to PSK and substantially increases the number of PSK-binding sites, indicating
that PSK and this receptor-like kinase act as a ligand-receptor pair.
Now that the in vitro function of PSK and the molecular basis of ligand-receptor interaction in PSK signaling have been established, the next phase of research is characterization of the in vivo role of PSK and its downstream signaling pathway in plants. The carrot PSK receptor shares significant sequence identity with At2g02220, an LRR receptor-like kinase found in Arabidopsis. The sequencing of the Arabidopsis genome is now complete, and large collections of gene-disruption lines are available. Once the PSK-binding activity of At2g02220 is confirmed, direct clues to in vivo function of PSK will be provided by the phenotypes of knockout mutants.
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Three CLAVATA loci: genes encoding ligand-receptor pairs regulating meristem fate |
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CLV1 encodes a predicted 105 kDa RLK that has 21 extracellular
LRRs, a single transmembrane domain and an intracellular Ser/Thr kinase domain
(Clark et al., 1997)
(Fig. 2C). CLV3
encodes a 96-residue peptide containing an N-terminal secretion signal
(Fletcher et al., 1999
). The
protein does not contain a potential dibasic processing site that could be
recognized by a processing enzyme, and anti-CLV3 antibodies detect an
unprocessed polypeptide in Arabidopsis extracts, suggesting a lack of
further processing in CLV3 biosynthesis. Both CLV3 and CLV1
are expressed in shoot apical meristems, and there is a strong possibility
that CLV3 is a ligand for the CLV1 receptor-like kinase. An alternative
clv mutant, clv2, displays a phenotype that is weak but
similar to those of clv1 and clv3. CLV2 is structurally
similar to CLV1 but lacks a cytoplasmic kinase domain
(Jeong et al., 1999
)
(Fig. 2C).
Biochemical studies show that CLV1 exists in two distinct complexes of 185
kDa and 450 kDa (Trotochaud et al.,
1999). The 185 kDa molecule is proposed to be a disulfide-linked
heterodimer of CLV1 and CLV2. The larger 450 kDa complex contains, in addition
to the CLV1-CLV2 dimer, a Rho-GTPase-related protein (Rop)
(Trotochaud et al., 1999
) and
the kinase-associated protein phosphatase (KAPP)
(Stone et al., 1998
). Rop
represents a plant-specific subfamily of the RHO family of small GTPases, but
its function in CLV signaling is not known. KAPP is a type 2C protein
phosphatase, first isolated by screening an Arabidopsis cDNA
expression library for interactions with the cytoplasmic domain of
serine/threonine receptor-like kinase RLK5
(Stone et al., 1994
). In
clv3 mutants, CLV1 occurs only as the 185 kDa protein, which suggests
that formation of the 450 kDa complex requires CLV3. CLV3 and CLV1
coimmunoprecipitate in vivo, and yeast cells expressing CLV1 and CLV2 bind to
native CLV3 from meristem extracts
(Trotochaud et al., 2000
).
CLV3 associates with the active CLV1 protein complex but does not interact
with a mutated CLV1 lacking kinase activity. Kinase activity must therefore be
required for ligand binding. The CLV1 cytoplasmic domain has kinase activity
and phosphorylates both itself and KAPP. In contrast, KAPP binds and
dephosphorylates CLV1 (Williams et al.,
1997
). CLV3 peptide thus appears to bind to and activate the 185
kDa CLV1-CLV2 heterodimer, inducing its autophosphorylation and subsequent
formation of a 450 kDa complex including Rop and KAPP. KAPP functions as a
negative regulator of the CLV1 signal transduction pathway by
dephosphorylating the CLV1 cytoplasmic domain.
CLV3 is expressed specifically in the central zone of the
outermost meristem, whereas CLV1 mRNA accumulates in deeper cell
layers. CLV2 mRNA is detected in all tissues. It has been proposed
that the CLV3 protein is secreted from stem cells at the apex of the meristem,
travels through the extracellular space and interacts with the CLV1-CLV2
receptor complex at the plasma membrane of the underlying cells to restrict
the size of the stem cell population
(Fletcher et al., 1999). This
speculation is supported by the observation that a tagged CLV3 fusion protein,
which has the same biological activity as native CLV3, is localized to the
extracellular space (Rojo et al.,
2002
). Interestingly, database searches have revealed a large
family of genes that share homology with CLV3 in several plants
(Cock and McCormick, 2001
). The
majority of the predicted polypeptides have signal sequences in the N-terminal
and are actually exported to the extracellular space
(Sharma et al., 2003
). Because
CLV1 is a member of the LRR receptor-like kinase family, some of the CLV3
homologs are expected to be ligands for orphan LRR receptors.
In clv1 mutants, missense mutations within the LRR domain often
produce mutants that exhibit stronger phenotypes than null mutants, which
suggests they have dominant negative effects in these mutants. Recently, it
was confirmed that a chimeric CLV1 receptor kinase whose kinase domain is
replaced with that of another receptor kinase acts in a dominant negative
manner in the regulation of meristem development
(Diévart et al., 2003).
One possibility is that multiple receptor kinases that functionally overlap
act within the meristem.
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SCR/SP11 and SRK: determinants of Brassica self-incompatibility |
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Molecular and biochemical studies have identified two
S-locus-derived proteins, S-locus glycoprotein (SLG) and
S-locus receptor-like kinase (SRK), specifically expressed on the
stigma surface. SLG is a soluble extracellular glycoprotein containing several
N-linked sugar moieties, polymorphic regions and 12 conserved
cysteine residues (Takayama et al.,
1987; Nasrallah et al.,
1987
). SRK is a typical receptor-like kinase, consisting of an
SLG-like extracellular domain, a single transmembrane domain and a cytoplasmic
Ser/Thr kinase domain (Stein et al.,
1991
) (Fig. 2D).
Mutations within the SRK sequence block the SI response, suggesting that SRK
has a key role in SI signaling (Goring et
al., 1993
; Nasrallah et al.,
1994
). To determine directly the functions of SLG and SRK, each
gene has been independently introduced into Brassica plants.
Transformation with an SRK transgene results in acquisition of the
corresponding SI specificity, that is, rejection of pollen that has an
S haplotype the same as that of the transgene
(Takasaki et al., 2000
). In
contrast, transgenic plants expressing SLG alone showed no SI
specificity. The SLG transgene, however, enhances the SI response in
the presence of an SRK transgene derived from a plant with an
S haplotype the same as that of the SLG. These results
demonstrate that SRK alone regulates the female (stigmatic) SI
specificity and that SLG has an accessory role in SI. In some
Brassica species, there appears to be no SLG requirement for SI
(Suzuki et al., 2000
;
Suzuki et al., 2003
).
An alternative target in SI research is the identification of a male
(pollen) determinant. Extensive work by two groups has identified a highly
polymorphic small gene located between SRK and SLG at the
S-locus (Schopfer et al.,
1999; Takayama et al.,
2000
). This gene, designated S locus cysteine-rich
protein (SCR) or S locus protein 11 (SP11),
encodes a highly polymorphic peptide containing a putative signal peptide
cleavage site and is expressed predominantly in the anther. Transformation of
Brassica plants homozygous for one S haplotype with an
SCR/SP11 gene derived from another haplotype results in acquisition
by transgenic pollen of the SI specificity encoded by the transgene.
Furthermore, addition of bacterially expressed SP11 protein to the stigma
induced S-haplotype-specific inhibition of pollen
(Takayama et al., 2000
). These
experiments have confirmed that the SCR/SP11 gene product is
necessary and sufficient to determine pollen SI. Immunohistochemical
experiments suggested that SP11 is secreted from the tapetal cell into the
anther locule as a cluster and translocated to the pollen surface at the early
developmental stage of the anther. During the pollination process, SP11 is
translocated from the pollen surface to the papilla cell and then penetrates
the cuticle layer of the papilla cell to diffuse across the pectin cellulose
layer (Iwano et al.,
2003
).
S-haplotype-specific ligand-receptor interactions between SCR/SP11
and SRK were directly demonstrated by experiments that used synthetic
radiolabeled SP11 (Takayama et al.,
2001). Ligand-binding assays indicated the presence of high- and
low-affinity binding sites in the stigmatic membranes of the cognate
S-haplotype. The labeled SP11 could be specifically crosslinked to
the 120 kDa SRK and a 65 kDa protein that might correspond to SLG or a
truncated SRK produced by alternative splicing. In addition, synthetic SP11
induced autophosphorylation of SRK in an S-haplotype-specific manner.
Specific ligand-receptor interactions have also been detected by experiments
using bacterial recombinant SCR and native stigma SRK
(Kachroo et al., 2001
).
The next phase of SI research will be to focus on identifying components of
the SRK-mediated signaling cascade. The low efficiency of transformation and
lack of a genome database for Brassica, however, are making further
studies of SI responses difficult. To overcome these problems, a
self-incompatible Arabidopsis plant in which the SRK and SCR genes
are incorporated has been established
(Nasrallah et al., 2002).
A. thaliana is normally a self-fertilizing plant, but successful
complementation studies demonstrate that the signaling cascade leading to
rejection of self-related pollen is nevertheless present. Analysis of SI
responses will be facilitated by the availability of the complete genome
sequence of this species.
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Perspectives |
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There are several ways to identify ligand-receptor pairs in plants. The
most general approach is extensive screening of mutants on the basis of their
phenotype. Once a large collection of mutant lines showing a unique phenotype
is assembled, there is a chance that one can identify the ligand-receptor
pairs in a particular peptide signaling pathway. A successful precedent for
this approach, however, is found only in the CLV signaling pathway, suggesting
limitations in the genetic approach. The main difficulty in finding mutant
lines that have informative phenotypes may be due to functional redundancy
arising from the genome structure of Arabidopsis. Indeed, although
Arabidopsis, Drosophila and C. elegans share a similar
number of gene types, multigene families, present as clustered and dispersed
copies, are particularly frequent in Arabidopsis
(The Arabidopsis Genome Initiative,
2000). In fact, five paralogous genes encoding precursors of PSK
have been identified in Arabidopsis, and loss-of function approaches
have not given rise to visible, directly informative phenotypes; this suggests
functional redundancy among these five PSK precursor genes. The same may be
true of the members of the LRR-RLK family. There are three BRI1-like receptor
proteins in Arabidopsis, two of which actually show specific binding
to brassinolide (Yin et al.,
2002
). The existence of an additional receptor kinase(s) that has
a functional overlap with CLV1 is also suggested by the analysis of dominant
negative mutants (Diévart et al.,
2003
). In this context, definitive phenotypes may only emerge when
combinations of knockouts for all homologous redundant genes are
available.
The classical methodologies for receptor cloning are those based on direct
ligand-receptor binding. A key factor in the use of ligand-based affinity
chromatography is the ability to derivatize peptide ligands without loss of
functional binding activity. In PSK receptor studies, the finding that
[Lys5]PSK retains significant activity after derivatization of the
side chain of Lys5 provided the breakthrough in a series of
experiments aimed at visualization and purification of PSK receptors.
Similarly, receptor-based affinity chromatography has also been used for
ligand-fishing experiments. Bartley et al. isolated a protein ligand for the
ECK receptor protein-tyrosine kinase by using the extracellular domain of the
receptor as an affinity reagent in a single-step purification
(Bartley et al., 1994). In
addition, progress in biosensor technology, based on surface plasmon
resonance, has had a great impact on the ability to detect and measure
biospecific interactions in real time. Davis et al., for example, constructed
a probe consisting of the extracellular domain of the receptor-like tyrosine
kinase, TIE2, fused to the Fc portion of human IgG, and coupled this to the
surface of a BIAcore sensor chip, which they then used to screen conditioned
media from a variety of cell lines for specific binding to TIE2
(Davis et al., 1996
). Once
tagged versions of the plant receptor-like Ser/Thr kinases are functionally
expressed and immobilized on such a biosensor chip, this biochemical system
should offer the most direct approach for ligand fishing in plants.
Although ligand-receptor binding depends on a large interacting surface
between two essentially correctly folded and disulfide-paired proteins, which
usually occurs efficiently only in the secretory pathway, the yeast two-hybrid
system, which detects protein-protein interactions that can occur within the
reducing environment of the yeast cell cytoplasm, may, in some cases, be a
sensitive tool for studying ligand-receptor interactions. To find the ligands
for pollen-specific RLKs, LePRKs, Tang et al. conducted a yeast two-hybrid
screen using the extracellular domains of LePRKs as bait to search for
interacting proteins encoded by a pollen cDNA library
(Tang et al., 2002). They
identified numerous secreted and plasma-membrane-bound candidate ligands. One
of these, the Cys-rich protein LAT52, is known to be essential during pollen
hydration and pollen tube growth (Twell et
al., 1989
; Muschietti et al.,
1994
). In vivo coimmunoprecipitation demonstrates that LAT52 is
capable of forming a complex with LePRK2 in pollen and that the extracellular
domain of LePRK2 is sufficient for the interaction. Although there is much to
be done, interactions between LePRK2 and LAT52 might represent an autocrine
pollen signaling system that plays a vital role in regulating the initiation
and maintenance of pollen tube growth.
Despite the large numbers of putative RLKs encoded in the genomes of
plants, a general model for how these receptors carry out signal transduction
has yet to be determined. To overcome this problem, the chimeric receptor
approach has been used for the characterization of a brassinosteroid receptor,
BRI1, one of the LRR-RLKs in plants (He et
al., 2000). A rice LRR-RLK named XA21
(Song et al., 1995
) confers
resistance to Xanthomonas oryzae pv. oryzae, and activation
of XA21 signaling leads to rapid and strong induction of transcription of the
rice defense genes chitinase RCH10 and phenylalanine ammonia lyase.
Interestingly, a chimeric receptor, consisting of the extracellular and
transmembrane domains of BRI1 and 65 amino acids of a juxtamembrane domain
fused to the kinase domain of XA21 is able to elicit cell death, an oxidative
burst, and the defense pathway, suggesting that a mechanism of signaling
conserved between BRI1 and XA21 may be extrapolated to the large number of
LRR-RLKs found in plant genomes. This chimeric receptor approach, using the
XA21 signaling outputs, should provide an alternative: an assay system that is
applicable to the discovery of ligands for the LRR-RLKs.
For many years, peptide signaling, despite its overwhelming importance in animals, has been largely neglected because six lipophilic non-peptide plant hormones play various roles in plant growth and development. Now, we are beginning to be aware of the possibility that some of the cell-to-cell interactions in plants are mediated by small hydrophilic ligands such as peptides. Our continued efforts to identify novel peptide ligands and their receptors should eventually yield a paradigm for local intercellular communication in plants and will clarify both distinct and similar aspects of peptide signal transduction in plants and animals.
Note added in proof
Recently, Clark and co-workers retracted their previous report regarding
CLV3 protein [Trotochaud, A. E., Jeong, S. and Clark, S. E. (2000). CLAVATA3,
a multimeric ligand for the CLAVATA1 receptor-like kinase. Science
289, 613-617]. In this paper they concluded that CLV3 acted as a ligand
for the CLV1 receptor kinase based on immunoprecipitation and western blots
using polyclonal antibodies to CLV3. However, subsequent examination by Clark
et al. revealed that these polyclonal antibodies can detect neither native
CLV3 nor bacterially expressed CLV3. Thus, there is currently no evidence for
the ligand-receptor interaction between CLV1 and CLV3 [Nishihama, R., Jeong,
S., DeYoung, B. and Clark, S. E. (2003). Retraction. Science
300, 1370].
Recently, it has been confirmed that systemin binds SR160 expressed in tobacco suspension-cultured cells. In addition, it has been reported that cu-3, a SR160/tBRI1 null mutant in tomato, exhibits a severely reduced response to systemin. These results indicate that SR160/tBRI1 is a component of the functional systemin receptor in tomato [Scheer, J. M., Pearce, G. and Ryan C. A. (2003). Generation of systemin signaling in tobacco by transformation with the tomato systemin receptor kinase gene. Proc. Natl. Acad. Sci. USA 100, 10114-10117].
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Acknowledgments |
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References |
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Bartley, T. D., Hunt, R. W., Welcher, A. A., Boyle, W. J., Parker, V. P., Lindberg, R. A., Lu, H. S., Colombero, A. M., Elliott, R. L., Guthrie, B. A. et al. (1994). B61 is a ligand for the ECK receptor protein-tyrosine kinase. Nature 368, 558-560.[CrossRef][Medline]
Bateman, A. J. (1955). Self-incompatibility systems in angiosperms. III. Cruciferae. Heredity 9, 52-68.
Bellincampi, D. and Morpurgo, G. (1987). Conditioning factor affecting growth in plant cells in culture. Plant Sci. 51, 83-91.
Berger, D. and Altmann, T. (2000). A
subtilisin-like serine protease involved in the regulation of stomatal density
and distribution in Arabidopsis thaliana. Genes
Dev. 14,
1119-1131.
Christianson, M. L. and Warnick, D. A. (1985). Temporal requirement for phytohormone balance in the control of organogenesis in vitro. Dev. Biol. 112, 494-497.
Clark, S. E., Running, M. P. and Meyerowitz, E. M.
(1993). CLAVATA1, a regulator of meristem and flower
development in Arabidopsis. Development
119,
397-418.
Clark, S. E., Running, M. P. and Meyerowitz, E. M.
(1995). CLAVATA3 is a specific regulator of shoot and
floral meristem development affecting the same processes as CLAVATA1.
Development 121,
2057-2067.
Clark, S. E., Williams, R. W. and Meyerowitz, E. M. (1997). The CLAVATA1 gene encodes a putative receptor-like kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89, 575-585.[Medline]
Cock, J. M. and McCormick, S. (2001). A large
family of genes that share homology with CLAVATA3. Plant
Physiol. 126,
939-942.
Constabel, C. P., Yip, L. and Ryan, C. A. (1998). Prosystemin from potato, black nightshade, and bell pepper: Primary structure and biological activity of predicted systemin polypeptides. Plant Mol. Biol. 36, 55-62.[CrossRef][Medline]
Davis, S., Aldrich, T. H., Jones, P. F., Acheson, A., Compton, D. L., Jain, V., Ryan, T. E., Bruno, J., Radziejewski, C., Maisonpierre, P. C. and Yancopoulos, G. D. (1996). Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell 87, 1161-1169.[Medline]
Diévart, A., Dalal, M., Tax, F. E., Lacey, A. D., Huttly,
A., Li, J. and Clark, S. E. (2003). CLAVATA1
dominant-negative alleles reveal functional overlap between multiple receptor
kinases that regulate meristem and organ development. Plant
Cell 15,
1198-1211.
Fisher, J. M., Sossin, W., Newcomb, R. and Scheller, R. H. (1988). Multiple neuropeptides derived from a common precursor are differentially packaged and transported. Cell 54, 813-822.[Medline]
Folling, M., Madsen, S. and Olesen, A. (1995). Effect of nurse culture and conditioned medium on colony formation and plant regeneration from Lolium perenne protoplasts. Plant Sci. 108, 229-239.[CrossRef]
Fletcher, J. C., Brand, U., Running, M. P., Simon, R. and
Meyerowitz, E. M. (1999). Signaling of cell fate decisions by
CLAVATA3 in Arabidopsis shoot meristems.
Science 283,
1911-1914.
Gomez-Gomez, L. and Boller, T. (2000). FLS2: an LRR receptor-like kinase involved in the perception of the bacterial receptor flagellin in Arabidopsis. Mol. Cell 5, 1003-1011.[Medline]
Goring, D. R., Glavin, T. L., Schafer, U. and Rothstein, S.
J. (1993). An S receptor kinase gene in
self-compatible Brassica napus has a 1-bp deletion. Plant
Cell 5,
531-539.
Green, T. R. and Ryan, C. A. (1972). Wound-induced proteinase inhibitor in plant leaves: A possible defense mechanism against insects. Science 175, 776-777.
Hanai, H., Nakayama, D., Yang, H., Matsubayashi, Y., Hirota, Y. and Sakagami, Y. (2000). Existence of a plant tyrosylprotein sulfotransferase: novel plant enzyme catalyzing tyrosine O-sulfation of preprophytosulfokine variants in vitro. FEBS Lett. 470, 97-101.[CrossRef][Medline]
Harris, R. B. Processing of pro-hormone precursor proteins. (1989). Arch Biochem Biophys 275, 315-333.[Medline]
He, Z., Wang, Z. Y., Li, J., Zhu, Q., Lamb, C., Ronald, P. and
Chory, J. (2000). Perception of brassinosteroids by the
extracellular domain of the receptor-like kinase BRI1.
Science 288,
2360-2363.
Helliwell, C. A., Chin-Atkins, A. N., Wilson, I. W., Chapple,
R., Dennis, E. S. and Chaudhury, A. (2001). The
Arabidopsis AMP1 gene encodes a putative glutamate carboxypeptidase.
Plant Cell 13,
2115-2125.
Huttner, W. B. (1982). Sulphation of tyrosine residues, a widespread modification of proteins. Nature 299, 273-276.[Medline]
Iwano, M., Shiba, H., Funato, M., Shimosato, H., Takayama, S.
and Isogai, A. (2003). Immunohistochemical studies on
translocation of pollen S-haplotype determinant in self-incompatibility of
Brassica rapa. Plant Cell Physiol.
44,
428-436.
Jacinto, T., McGurl, B., Franceschi, V., Delano-Freier, J. and Ryan, C. A. (1997). Tomato prosystemin promoter confers wound-inducible vascular bundle-specific expression of the ß-glucuronidase gene in transgenic tomato plants. Planta 203, 406-412.[CrossRef]
Jeong, S., Trotochaud, A. E. and Clark, S. E.
(1999). The Arabidopsis CLAVATA2 gene encodes a
receptor-like protein required for the stability of the CLAVATA1
receptor-like kinase. Plant Cell
11,
1925-1933.
Jorgensen, R. B., Andersen, B. and Andersen, J. M. (1992). Effects and characterization of the conditioning medium that increase colony formation from barley (Hordeum vulgare L.) protoplasts. J. Plant Physiol. 140, 328-333.
Kachroo, A., Schopfer, C. R., Nasrallah, M. E. and Nasrallah, J.
B. (2001). Allele-specific receptor-ligand interactions in
Brassica self-incompatibility. Science
293,
1824-1826.
Kanno, T. and Hinata, K. (1969). An electron microscopic study of the barrier against pollen-tube growth in self-incompatible Cruciferae. Plant Cell Physiol. 10, 213-216.
Kobayashi, T., Eun, C.-H., Hanai, H., Matsubayashi, Y.,
Sakagami, Y. and Kamada, H. (1999). Phytosulfokine-, a
peptidyl plant growth factor, stimulates somatic embryogenesis in carrot.
J. Exp. Botany 50,
1123-1128.[Abstract]
Kobe, B. and Deisenhofer, J. (1995). Proteins with leucine-rich repeats. Curr. Opin. Struct. Biol. 5, 409-416.[CrossRef][Medline]
Li, J. and Chory, J. (1997). A putative leucine-rich repeat receptor-like kinase involved in brassinosteroid signal transduction. Cell 90, 929-938.[Medline]
Li, L. and Howe, G. A. (2001). Alternative splicing of prosystemin pre-mRNA produces two isoforms that are active as signals in the wound response pathway. Plant Mol. Biol. 46, 409-419.[CrossRef][Medline]
Li, J., Lease, K. A., Tax, F. E. and Walker, J. C.
(2001). BRS1, a serine carboxypeptidase, regulates BRI1 signaling
in Arabidopsis thaliana. Proc. Natl. Acad. Sci.
USA 98,
5916-5921.
Matsubayashi, Y. and Sakagami, Y. (1996).
Phytosulfokine, sulfated peptides that induce the proliferation of single
mesophyll cells of Asparagus officinalis L. Proc. Natl.
Acad. Sci. USA 93,
7623-7627.
Matsubayashi, Y. and Sakagami, Y. (1999).
Characterization of specific binding sites for a mitogenic sulfated peptide,
phytosulfokine-, in the plasma membrane fraction derived from Oryza
sativa L. Eur. J. Biochem.
262,
666-671.
Matsubayashi, Y. and Sakagami, Y. (2000). 120-
and 160-kDa receptors for endogenous mitogenic peptide,
phytosulfokine-, in rice plasma membranes. J. Biol.
Chem. 275,
15520-15525.
Matsubayashi, Y., Takagi, L. and Sakagami, Y.
(1997). Phytosulfokine-, a sulfated pentapeptide,
stimulates the proliferation of rice cells by means of specific high- and
low-affinity binding sites. Proc. Natl. Acad. Sci. USA
94,
13357-13362.
Matsubayashi, Y., Takagi, L., Omura, N., Morita, A. and
Sakagami, Y. (1999). The endogenous sulfated pentapeptide
phytosulfokine- stimulates tracheary element differentiation of
isolated mesophyll cells of Zinnia. Plant
Physiol. 120,
1043-1048.
Matsubayashi, Y., Ogawa, M., Morita, A. and Sakagami, Y.
(2002). An LRR receptor-like kinase involved in perception of a
peptide plant hormone, phytosulfokine. Science
296,
1470-1472.
McGurl, B., Pearce, G., Orozco-Cardenas, M. and Ryan, C. A. (1992). Structure, expression, and antisense inhibition of the systemin precursor gene. Science 255, 1570-1573.[Medline]
McGurl, B., Orozco-Cardenas, M., Pearce, G. and Ryan, C. A.
(1994). Overexpression of the prosystemin gene in transgenic
tomato plants generates a systemic signal that constitutively induces
proteinase inhibitor synthesis. Proc. Natl. Acad. Sci.
USA 91,
9799-9802.
Montoya, T., Nomura, T., Farrar, K., Kaneta, T., Yokota, T. and
Bishop, G. J. (2002). Cloning the tomato curl3 gene
highlights the putative dual role of the leucine-rich repeat receptor kinase
tBRI1/SR160 in plant steroid hormone and peptide hormone signaling.
Plant Cell 14,
3163-3176.
Muschietti, J., Dircks, L., Vancanneyt, G. and McCormick, S. (1994). LAT52 protein is essential for tomato pollen development: pollen expressing antisense LAT52 RNA hydrates and germinates abnormally and cannot achieve fertilization. Plant J. 6, 321-338.[CrossRef][Medline]
Nasrallah, J. B., Kao, T.-h., Chen, C.-H., Goldberg, M. L. and Nasrallah, M. E. (1987). Amino-acid sequence of glycoproteins encoded by three alleles of the S locus of Brassica oleracea. Nature 326, 617-619.[CrossRef]
Nasrallah, J. B., Rundle, S. J. and Nasrallah, M. E. (1994). Genetic evidence for the requirement of the Brassica S-locus receptor kinase gene in the self-incompatibility response. Plant J. 5, 373-384.
Nasrallah, M. E., Liu, P. and Nasrallah, J. B.
(2002). Generation of self-incompatible Arabidopsis
thaliana by transfer of two S locus genes from A.
lyrata. Science
297,
247-249.
Orozco-Cardenas, M., McGurl, B. and Ryan, C. A.
(1993). Expression of an antisense prosystemin gene in tomato
plants reduces resistance toward Manduca sexta larvae.
Proc. Natl. Acad. Sci. USA
90,
8273-8276.
Pearce, G. and Ryan, C. A. (2003). Systemic signaling in tomato plants for defense against herbivores: Isolation and characterization of three novel defense-signaling glycopeptide hormones coded in a single precursor gene. J. Biol. Chem. May 14 [Epub ahead of print].
Pearce, G., Strydom, D., Johnson, S. and Ryan, C. A. (1991). A polypeptide from tomato leaves activates the expression of proteinase inhibitor genes. Science 253, 895-898.
Pearce, G., Moura, D. S., Stratmann, J. and Ryan, C. A. (2001). Production of multiple plant hormones from a single polyprotein precursor. Nature 411, 817-820.[CrossRef][Medline]
Rojo, E., Sharma, V. K., Kovaleva, V., Raikhel, N. V. and
Fletcher, J. C. (2002). CLV3 is localized to the
extracellular space, where it activates the Arabidopsis CLAVATA stem
cell signaling pathway. Plant Cell
14,
969-977.
Ryan, C. A., Pearce, G., Scheer, J. and Moura, D. S.
(2002). Polypeptide hormones. Plant Cell
14,
S251-S264.
Scheer, J. M. and Ryan, C. A. (1999). A 160-kD
systemin receptor on the surface of Lycopersicon peruvianum
suspension-cultured cells. Plant Cell
11,
1525-1536.
Scheer, J. M. and Ryan, C. A. (2002). The
systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR
receptor-like kinase family. Proc. Natl. Acad. Sci.
USA 99,
9585-9590.
Schopfer, C. R., Nasrallah, M. E. and Nasrallah, J. B.
(1999). The male determinant of self-incompatibility in
Brassica. Science
286,
1697-1700.
Sharma, V. K., Ramirez, J. and Fletcher, J. C. (2003). The Arabidopsis CLV3-like (CLE) genes are expressed in diverse tissues and encode secreted proteins. Plant Mol. Biol. 51, 415-425.[CrossRef][Medline]
Shiu, S. H. and Bleecker, A. B. (2001).
Receptor-like kinases from Arabidopsis form a monophyletic gene family related
to animal receptor-like kinases. Proc. Natl. Acad. Sci.
USA 98,
10763-10768.
Skoog, F. and Miller, C. O. (1957). Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp. Soc. Exp. Biol. 11, 118-131.
Somers, D. A., Birnberg, P. R., Petersen, W. L. and Brenner, M. L. (1985). The effect of conditioned medium on colony formation from Black Mexican sweet corn protoplasts. Plant Cell Rep. 4, 155-157.
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. et al. (1995). A receptor-like protein encoded by the rice disease resistance gene, Xa21. Science 270, 1804-1806.[Abstract]
Stein, J. C., Howlett, B., Boyes, D. C., Nasrallah, M. E. and Nasrallah, J. B. (1991). Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc. Natl. Acad. Sci. USA 88, 8816-8820.[Abstract]
Stone, J. M., Collinge, M. A., Smith, R. D., Horn, M. A. and Walker, J. C. (1994). Interaction of a proteinphosphatase with an Arabidopsis serinethreonine receptor-like kinase. Science 266, 793-795.[Medline]
Stone, J. M., Trotochaud, A. E., Walker, J. C. and Clark, S.
E. (1998). Control of meristem development by CLAVATA1
receptor-like kinase and kinase-associated protein phosphatase interactions.
Plant Physiol. 117,
1217-1225.
Suzuki, T., Kusaba, M., Matsushita, M., Okazaki, K. and Nishio, T. (2000). Characterization of Brassica S-haplotypes lacking S-locus glycoprotein. FEBS Lett. 482, 102-108.[CrossRef][Medline]
Suzuki, G., Kakizaki, T., Takada, Y., Shiba, H., Takayama, S., Isogai, A. and Watanabe, M. (2003). The S haplotypes lacking SLG in the genome of Brassica rapa. Plant Cell Rep. 21, 911-915.[Medline]
Takasaki, T., Hatakeyama, K., Suzuki, G., Watanabe, M., Isogai, A. and Hinata, K. (2000). The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 403, 913-916.[CrossRef][Medline]
Takayama, S., Isogai, A., Tsukamoto, C., Ueda, Y., Hinata, K., Okazaki, K. and Suzuki, A. (1987). Sequences of S-glycoproteins, products of Brassica campestris self-incompatibility locus. Nature 326, 102-105.[CrossRef]
Takayama, S., Shiba, H., Iwano, M., Shimosato, H., Che, F.-S.,
Kai, N., Watanabe, M., Suzuki, G., Hinata, K. and Isogai, A.
(2000). The pollen determinant of self-incompatibility in
Brassica campestris. Proc. Natl. Acad. Sci.
USA. 97,
1920-1925.
Takayama, S., Shimosato, H., Shiba, H., Funato, M., Che, F-S., Watanabe, M., Iwano, M. and Isogai, A. (2001). Direct ligand-receptor complex interaction controls Brassica self-incompatibility. Nature 413, 534-538.[CrossRef][Medline]
Tanaka, H., Onouchi, H., Kondo, M., Hara-Nishimura, I.,
Nishimura, M., Machida, C. and Machida, Y. (2001). A
subtilisin-like serine protease is required for epidermal surface formation in
Arabidopsis embryos and juvenile plants.
Development 128,
4681-4689.
Tang, W., Ezcurra, I., Muschietti, J. and McCormick, S.
(2002). A cysteine-rich extracellular protein, LAT52, interacts
with the extracellular domain of the pollen receptor-like kinase LePRK2.
Plant Cell 14,
2277-2287.
The Arabidopsis Genome Initiative (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815.[CrossRef][Medline]
Trotochaud, A. E., Hao, T., Wu, G., Yang, Z. and Clark, S.
E. (1999). The CLAVATA1 receptor-like kinase requires
CLAVATA3 for its assembly into a signaling complex that includes KAPP and a
Rho-related protein. Plant Cell
11,
393-406.
Trotochaud, A. E., Jeong, S. and Clark, S. E.
(2000). CLAVATA3, a multimeric ligand for the CLAVATA1
receptor-like kinase. Science
289,
613-617.
Twell, D., Wing, R., Yamaguchi, J. and McCormick, S. (1989). Isolation and expression of an anther-specific gene from tomato. Mol. Gen. Genet. 217, 240-245.[Medline]
Williams, R. W., Wilson, J. M. and Meyerowitz, E. M.
(1997). A possible role for kinase-associated protein phosphatase
in the Arabidopsis CLAVATA1 signaling pathway. Proc. Natl.
Acad. Sci. USA 94,
10467-10472.
Yang, H., Matsubayashi, Y., Nakamura, K. and Sakagami, Y.
(2001). Diversity of Arabidopsis genes encoding
precursors for phytosulfokine, a peptide growth factor. Plant
Physiol. 127,
842-851.
Yin, Y., Wu, D. and Chory, J. (2002). Plant
receptor-like kinases: systemin receptor identified. Proc. Natl.
Acad. Sci. USA 99,
9090-9092.