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Multi-tasking of somatic embryogenesis receptor-like
protein kinases
Jia Li
Receptor-like protein kinases (RLKs) are transmembrane
proteins crucial for cell-to-cell and cell-to-environment
communications. The extracellular domain of a RLK is
responsible for perception of a specific extracellular ligand to
trigger a unique intercellular signaling cascade, often via
phosphorylation of cellular proteins. The signal is then
transduced to the nucleus of a cell where it alters gene
expression. There are more than 610 RLKs in Arabidopsis
thaliana, only a handful of them have been functionally
characterized. This review focuses on recent advances in our
understanding of a small group of RLKs named somatic
embryogenesis receptor-like protein kinases (SERKs).
SERKs act as coreceptors in multiple signaling pathways via
their physical interactions with distinct ligand-binding RLKs.
Address
School of Life Sciences, Lanzhou University, Lanzhou 730000, People’s
Republic of China
Corresponding author: Li, Jia (lijia@lzu.edu.cn)
Current Opinion in Plant Biology 2010, 13:509–514
This review comes from a themed issue on
Cell signalling and gene regulation
Edited by Zhiyong Wang and Giltsu Choi
1369-5266/$ – see front matter
#2010 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2010.09.004
Introduction
Multicellular organisms utilize transmembrane recep-
tor-like protein kinases (RLKs) for cell-to-cell and cell-
to-environment communications during normal growth
and development. A typical plant RLK contains an
extracellular domain perceiving chemical signals from
surrounding environment, a single-pass transmembrane
domain anchoring the protein to the plasma membrane,
and a cytoplasmic kinase domain transducing extra-
cellular signals to intracellular processes via protein
phosphorylation. Plant RLKs were initially classified
as serine/threonine protein kinases [1], but recent stu-
dies indicate that some RLKs may have serine/threo-
nine and tyrosine dual kinase activities [2]. Arabidopsis
genome encodes at least 610 RLKs and receptor-like
cytoplasmic kinases (RLCKs), which lack extracellular
domains. RLKs and RLCKs belong to a large mono-
phyletic superfamily, representing nearly 2.5% of
proteins encoded in the Arabidopsis genome [3,4].
Based on their sequence and structure similarities,
RLKs were classified into more than 10 subfamilies,
among which the leucine-rich repeat (LRR) RLKs,
LRR-RLKs, belong to the largest subfamily containing
at least 223 members [5
].
A variety of approaches have been used to unfold the
biological functions of about 30 LRR-RLKs [5
], but the
roles of majority of LRR-RLKs are yet to be elucidated.
LRR-RLKs have been found to be crucial in regulating
numerous physiological processes such as microsporogen-
esis and male fertility [6–8], embryo pattern formation [9],
vascular tissue differentiation [10], organ shape and inflor-
escence architecture [11], maintenance of meristematic
cells [12], stomatal patterning and differentiation [13],
brassinosteroid (BR) signaling [14–16], floral organ abscis-
sion [17], cell death control [18
,19,20], and innate
immunity [21,22].
A surprising discovery from recent studies is that some
LRR-RLKs have dual or multiple roles. For example,
Arabidopsis SERKs were found to regulate distinct sig-
naling pathways mediating development and innate
immunity [23]. SERK was first isolated in Daucus carota
(carrot) as a marker gene to monitor the transition from
somatic to embryogenic cells in carrot cell culture [24]. In
Arabidopsis, there are five homologs of DcSERK, named
SERK1 to SERK5 [25]. SERK3 and SERK4 were also
named as brassinosteroid insensitive 1 (BRI1) associated
receptor kinase 1 (BAK1) and BAK1-like 1 (BKK1) due to
their functions in the BR signaling pathway [15,16,20].
Interestingly, members of SERKs showed both signifi-
cantly overlapped and divergent functions [23]. Identifi-
cation of multiple roles of SERKs raised interesting
questions about specificity of members of SERK sub-
family and crosstalk among SERK-mediated signaling
pathways. This review focuses on recent advances in
our understanding of the functions of SERKs in various
signaling pathways.
Several SERKs interact with BRI1 to regulate
BR signaling pathway
The function of BAK1/SERK3 in regulating BR signaling
was independently identified via an activation tagging
genetic screen for extragenic suppressors of a weak Ara-
bidopsis BRI1 mutant named bri1–5[15,26], and by a
yeast two-hybrid screen for BRI1 interacting proteins
[16]. Recent studies demonstrated that the bona-fide
www.sciencedirect.com Current Opinion in Plant Biology 2010, 13:509–514
BR receptor BRI1 and coreceptor BAK1 follow a recipro-
cal and sequential phosphorylation model [27
]. The
BRI1 kinase domain can be activated via autophosphor-
ylation upon the binding of BR to the extracellular
domain of BRI1. The active BRI1 then recruits BAK1
to its protein complex likely forming a heterotetramer
[28]. Specific residues within the BAK1 activation loop
are therefore transphosphorylated by BRI1, resulting in
activation of BAK1. BAK1 transphosphorylates the Ser/
Thr residues in the juxtamembrane and C-terminal
domains of BRI1, enhancing the kinase activity of
BRI1. Genetic data obtained from bak1 bkk1 double
mutant plants suggested that BRI1 retains a basal activity
even without SERK proteins [27
]. Since SERK1 and
additional BAK1 paralogs are also likely involved in BR
signaling, the significance of SERKs in BR signaling still
needs to be reevaluated in mutant plants lacking BAK1
and all its functionally redundant genes.
SERKs bind to BIR1 to control plant cell death
The fact that the bak1 single mutant only shows subtle
bri1-like phenotype suggested that there must be other
BAK1-like genes playing functionally redundant roles
with BAK1. Among five Arabidopsis SERKs, SERK4
and SERK5 are the two closest paralogs of BAK1/
SERK3. The SERK4 and SERK5 genes are found as
a tandem repeat on chromosome 2. It is therefore
impractical to generate serk4 serk5 double or bak1 serk4
serk5 triple mutants in order to analyze the significance
of these presumed functionally redundant proteins in
regulating plant growth and development. In the Ara-
bidopsis accession Columbia (Col-0), but not in acces-
sion WS2, however, SERK5 bears a natural point
mutation which alters Arg401 to Leu within its con-
served ‘RD’ motif. This substitution may have abol-
ished the kinase activity of SERK5, as overexpression
of SERK4 but not SERK5 (from Col-0) can partially
suppress the defective phenotypes of bri1–5, similar to
that of BAK1 [20]. When Leu401 is mutagenized to Arg
in Col-0 SERK5, SERK5 can regain partial function in
the BR signaling pathway [20]. The bak1 bkk1 double
mutant is practically a bak1 bkk1 serk5 triple mutant in
Col-0 background.
Surprisingly, the double mutant did not show the
expected typical bri1-like defects. Instead, it exhibited
a seedling lethality phenotype due to constitutive
defense responses and spontaneous cell death [20].
The seedling lethality is salicylic acid (SA) and light
dependent [20,29]. These results suggest that BAK1
and BKK1 not only modulate cell elongation via their
function in BR signaling, but they also play critical roles in
a light-dependent cell death control process. Since BAK1
regulates BR signaling through its interaction with the
ligand-binding receptor BRI1, it is possible that BAK1
controls cell death via its interaction with another
unknown ligand-binding RLK [29].
In an attempt to identify genes important for innate
immunity response, Gao et al. [18
] used a systematic
reverse genetic approach to determine the functions of
genes whose expression levels are elevated upon treat-
ment with the bacterial pathogen Pseudomonas syringae pv.
Maculicola ES4326. A null mutant of a novel RLK gene
showed constitutive defense response, cell death, and
seedling lethality phenotypes similar to that of bak1 bkk1
double mutant. Using a co-immunoprecipitation
approach followed by a proteomic analysis, it was found
that this RLK interacts with BAK1 in vivo. The RLK was
therefore named as BAK1-interacting receptor-like
kinase 1 (BIR1) [18
]. BIR1 is a member of the LRR-
RLK X subfamily. Using bimolecular fluorescence com-
plementation (BiFC) approach, it was found that BIR1
interacts with BAK1 paralogs including SERK1, SERK2,
and BKK1/SERK4. The seedling lethality phenotype of
bir1 mutant is also SA dependent, as blocking SA bio-
synthesis can partially rescue the bir1 phenotype [18
].
The phenotypic similarity between bir1 and bak1 bkk1
mutants and the physical interaction of BAK1 and BIR1
suggest that bir1 and bak1 bkk1 may block the same
signaling pathway, which resulted in cell death. If this is
the case, it suggests that BIR1 is a ligand-binding RLK,
similar to BRI1 in the BRI1/BAK1-mediated BR signaling
pathway, which can sense the ‘surviving’ signal yet to be
determined. This notion is supported by the fact that BIR1
belongs to the same LRR-RLK X subfamily as known
ligand-binding LRR-RLKs such as BRI1 and EMS1/EXS
[6,14,30]. The extracellular domain of BRI1 perceives BRs,
whereas the extracellular domain of EMS1/EXS interacts
with a small secreted peptide TPD1 [31,32
]. The MAP
kinase cascade regulated by MEKK1, MKK1/MKK2, and
MPK4 may also be involved in the BIR1-midiated sig-
naling pathway. The mekk1 mutant shows a cell death
phenotype similar to bir1 [33]; and the defective pheno-
types of both mutants can be suppressed by higher
temperature. Whether the bak1 bkk1 double mutant phe-
notype can also be suppressed by higher temperature has
not yet been reported. Future identification of the ‘surviv-
ing’ signal as well as elucidation of the rest of the signaling
pathway should provide significant insight into mechan-
isms of RLK-mediated cell death control in plants.
SERKs are crucial in regulating anther
development
Because the carrot SERK is transcriptionally induced
during the transition to somatic embryogenesis, Arabi-
dopsis SERK1 was thought to be involved in embryogen-
esis. Overexpression of SERK1 can efficiently increase
the initiation of somatic embryogenesis [25], although no
role in embryogenesis has been determined through loss-
of-function genetic analyses. In order to analyze the
biological functions of SERK1 and its closest paralog
SERK2, two independent groups generated serk1 and
serk2 single and serk1 serk2 double mutants. Neither serk1
510 Cell signalling and gene regulation
Current Opinion in Plant Biology 2010, 13:509–514 www.sciencedirect.com
nor serk2 showed any obvious morphological phenotypes,
but the double mutant is sterile due to lack of mature
pollen grains [7,8]. Detailed analysis found that the
double mutant does not contain the characteristic tapetal
cell layer which is essential for anther development. The
double mutant produces more sporogenous cells that fail
to develop into mature pollen grains after meiosis. These
phenotypic defects are consistent with the expression
patterns of SERK1 and SERK2. Although both genes
have a broad expression patterns in locules at an early
anther developmental stage (stage 5), their expression is
restricted to the tapetal cell layer at a later developmental
stage (stage 9) [7,8].
The phenotypes of serk1 serk2 double mutant are similar
to ems1/exs and tpd1 mutants. EMS1/EXS encodes an
LRR-RLK of LRR-RLK X subfamily, whereas TPD1
encodes a secreted small protein, which can directly bind
to the extracellular domain of EMS1/EXS [32
]. The
phenotypic similarity of the mutants raised an intriguing
question: do these three different genes control the same
signaling pathway? If this is the case, we would expect a
ligand (TPD1)-dependent interaction between EMS1/
EXS and SERK1 or SERK2. This is indeed a tempting
hypothesis to be tested in the future.
SERKs associate with a number of pattern
recognition receptors to modulate multiple
plant innate immunity responses
There are at least two layers of plant defense responses
against pathogens. One involves the pattern recognition
receptors (PRRs) which perceive the pathogen associated
molecular patterns (PAMPs). Perception of PAMPs by
PRRs can trigger a basic but weak defense response. The
second layer of innate immunity is the classic gene-for-
gene defense. Once a pathogen breaks down the first
layer of defense, it may release species-specific effectors
into the cytoplasm of a plant cell via a type III secretion
system (TTSS). If a plant has a dominant resistant gene,
R gene, its product may interact directly or indirectly with
the pathogen effectors, which can trigger a more intensive
defense response named hypersensitive response. Such
an immunity response is also called effector-triggered
immunity (ETI) [34].
Kemmerling et al. showed that bak1 single mutant exhib-
ited a spreading necrosis phenotype due to uncontrolled
cell death triggered by the pathogen infection [19]. This
result clearly suggested that BAK1 may act as PRRs or
coreceptors of PRRs to control innate immunity responses.
The best characterized PRRs are FLS2 and EFR [21,22].
Both RLKs are members of the LRR-RLK XII subfamily.
FLS2 and EFR sense the conserved22-amino acid epitope
of bacterial flagellin, named flg22, and the N-terminal
portion of elongation factor Tu (EF-Tu) called elf18/
elf26, respectively. Recent reports demonstrated that
FLS2 can heteromerize with BAK1 [35,36]. The inter-
action is ligand dependent, reminiscent of the interaction
between BAK1 and BRI1 [37]. Without the stimulation of
flg22, FLS2 and BAK1 are not associated with each other
[35,36]. Upon the stimulation by flg22 for only seconds,
these two LRR-RLKs can form a protein complex almost
instantaneously and transphosphorylate each other, which
subsequently initiate a defense signaling cascade including
MAPK activation [38
]. BAK1 is a positive regulator of
PAMP signaling pathways shared by different plant
species. In Arabidopsis, two BAK1 T-DNA insertion
mutants, bak1–3and bak1–4, showed drastically reduced
defense responses such as seedling growth inhibition,
oxidative burst, and MAPK activation upon treatments
with flg22 and elf18. The responsiveness of bak1–3is
slightly more than that of bak1–4because bak1–3is a leaky
mutant expressing trace amounts of wild-type BAK1,
whereas bak1–4is a true null allele (our unpublished data).
More recently, using a yeast two-hybrid approach, BAK1
was identified as a coreceptor of two additional LRR-
RLKs, PEPR1 and its closest homolog PEPR2, implicat-
ing BAK1 in a general activation role in diversified plant
immunity responses [39
]. PEPR1 and PEPR2 are mem-
bers of LRR-RLK XI subfamily which consists of at least
26 genes [40]. The ligand for PEPR1, AtPEP1, is a
wound-induced and plant-derived endogenous peptide,
which differs from pathogen-derived elicitors such as
flg22 and elf18/elf26. Recognition of AtPEP1 by PEPR1
triggers plant immunity response and enhances plant
resistance against Pytium irregulare infection [41,42].
The detailed molecular mechanisms of BAK1 in regulat-
ing PEPR1 and PEPR2-mediated responses need to be
elucidated in the future. These results suggest that BAK1
may interact with numerous ligand-binding PRRs in
controlling a wide range of microbes [36].
BAK1 is a common coreceptor for a number of PAMPs.
Interestingly, pathogens evolved unique strategies to
target such general defense component to weaken the
PRR-associated plant immunity in order to successfully
invade plant cells. A recent report provides an excellent
example for such unique tactics pathogens use for their
successful attacking purposes [43
]. During the infection
process, two sequence-distinct Pseudomonas syringae
effectors AvrPto and AvrPtoB are injected into plant cells
and interact with BAK1. The interaction between AvrPto/
AvrPtoB and BAK1 interferes with the associations of
BAK1 with different PRRs and with BRI1 [43
].
Conclusions
There is clear evidence that SERKs are able to regulate
many developmental and innate immunity signaling
pathways (Figure 1). In cases that have been studied in
details, SERKs act as coreceptors rather than ligand-
binding receptors. The first obvious question would be
how the specificity of each of the SERK-mediated sig-
naling pathways is controlled. From the story of BRI1 and
Multi-tasking of somatic embryogenesis receptor-like protein kinases Li 511
www.sciencedirect.com Current Opinion in Plant Biology 2010, 13:509–514
BSKs [44], it can be concluded that the determination of a
signaling pathway may rely more on the ligand-binding
receptors rather than the shared coreceptors. The second
apparent question would be why in some cases members
of SERKs exhibit divergent biological functions. Indirect
evidence from previous studies suggested that members
of SERKs may possess different biochemical properties
[23]. In addition, expression patterns of SERK members
are not always overlapped in some tissues [45]. A recent
report on genome-wide cloning and sequence analysis of
LRR-RLK cDNAs illustrated that more than 30 RLKs
have alternatively spliced forms [5
]. It is very likely that
the alternatively spliced forms represent another regulat-
ory mechanism to determine specificity of RLK-associ-
ated signaling pathways. So far all known SERK/ligand-
binding receptor pair showed ligand-dependent associ-
ation. It is yet to be tested whether reciprocal and
sequential phosphorylation of SERKs with their partner
RLKs represents a common mechanism in all SERK-
related signaling pathways.
Proteomic approaches have been widely used to identify
signaling components involved in RLK related signaling
pathways [46]. In the future, identification of other
SERK interacting RLKs may help to reveal additional
roles of SERKs. LRR-RLK II subfamily contains 14
members, but studies have been mainly focused on 5
SERKs. It is likely that other members of LRR-RLK II
or members of other RLK families may also serve as
coreceptors in many unknown signaling pathways mod-
ulating plant growth, development, and immunity
responses.
Acknowledgements
I apologize for not being able to cite all excellent papers published by
colleagues due to space limitation. The work of my research group is
currently supported by a grant from National Natural Science Foundation of
China (90917019 to JL), and by a grant from The Ministry of Agriculture of
the People’s Republic of China (2009ZX08009-029B). I would like to thank
Dr. Xiaoping Gou for helping to prepare the references and Figure 1.Iam
grateful to Frans Tax and Adriana Racolta for their invaluable comments on
the manuscript.
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512 Cell signalling and gene regulation
Figure 1
SERKs interact with multiple ligand-binding LRR-RLKs and control multiple developmental and defense-related signaling pathways. The interactionof
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514 Cell signalling and gene regulation
Current Opinion in Plant Biology 2010, 13:509–514 www.sciencedirect.com
