Journal of Experimental Botany, Vol. 64, No. 2, pp. 445–458, 2013
doi:10.1093/jxb/ers354
Review paper
Sensing the environment: key roles of membrane-localized
kinases in plant perception and response to abiotic stress
Yuriko Osakabe1,*, Kazuko Yamaguchi-Shinozaki2,3, Kazuo Shinozaki1 and Lam-Son Phan Tran4,*
1 Gene Discovery Research Group, RIKEN Plant Science Center, 3-1-1 Koyadai, Tsukuba, Ibaraki 305-0074, Japan
Graduate School of Agricultural and Life Sciences, University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113–8657, Japan
3 Biological Resources and Post-harvest Division, Japan International Research Center for Agricultural Sciences, 1-1 Ohwashi, Tsukuba,
Ibaraki 305–8686, Japan
4 Signalling Pathway Research Unit, RIKEN Plant Science Center, 1-7-22, Suehiro-cho, Tsurumi, Yokohama 230-0045, Japan
2 * To whom correspondence should be addressed. E-mail: [email protected] or [email protected]
Received 21 September 2012; Revised 1 November 2012; Accepted 14 November 2012
Abstract
Adverse environmental conditions have negative effects on plant growth and development. Receptor proteins on
the plasma membrane sense various environmental stimuli and transduce them to downstream intra- and intercellular signalling networks. Receptor-like kinases (RLKs) play important roles in perceiving the extracellular ligands
and activating the downstream pathway via phosphorylation of intracellular serine/threonine kinase domains. The
Arabidopsis genome possesses >600 RLK-encoding genes, some of which are implicated in the perception of environmental signals during the life cycle of the sessile plants. Histidine kinases are also membrane-localized kinases
and perceive osmotic stress and plant hormones. In this review, we focus on the RLKs and histidine kinases that play
a role in plant response to abiotic stresses. We summarize our recent understanding of their specific roles in stress
responses and absicisic acid (ABA) regulation. Elucidation of the functions of these kinases in the osmotic stress
response will provide a better understanding of stress-sensing mechanisms in plants and help to identify potential
candidate genes for genetic engineering of improved stress-tolerant crops.
Key words: Abiotic stress, histidine kinase, hormone signalling, phosphorylation, receptor-like kinase, signal transduction, stress
signalling.
Introduction
Plants have evolved adaptive mechanisms that allow them
to survive in an ever-changing environment. Since plants are
sessile, they must be able to sense their natural environment
and undergo changes in their physiology and development
in response to those environmental cues whether they are
adverse or beneficial. External stimuli activate the receptor
molecules and initiate complex downstream signalling networks that exhibit cross-talk in order to respond to various
environmental and developmental cues in an appropriate and
integrated manner. Abiotic and biotic stresses often result in
significant decreases in the yield of native plants and economically important crop plants. Due to the negative impact on
growth and yield, the complex mechanisms involved in stress
response and adaptation, such as stress signalling and the regulation of gene expression, have been widely studied with the
aim of improving stress tolerance (Tran et al., 2007a, 2010a;
Baena-Gonzalez and Sheen, 2008; Manavalan et al., 2009;
Tran and Mochida, 2010; Hadiarto and Tran, 2011; Osakabe
et al., 2011, 2012; Jogaiah et al., 2012; Ma et al., 2012).
Plants need to allocate energy to reprogramme stress signalling networks that initiate adaptive responses to stress conditions (Ahuja et al., 2010; Skirycz and Inze, 2010; Thao and
Tran, 2012). Endogenous stimuli, such as plant hormones,
coordinate and modulate the molecular and biochemical
© The Author [2012]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
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446 | Osakabe et al.
mechanisms that provide increased stress tolerance and adjust
overall plant growth and development for greater survival
(Peleg and Blumwald, 2011; Choudhary et al., 2012a, b, c; Ha
et al., 2012; Le et al., 2012a). The external signals involved
in cell–cell signalling are also able to control molecular processes by activation of coordinated intercellular signalling
during growth and development and stress responses. The
pivotal role of cell–cell communication has been identified in
cell fate determination and organ development (Van Norman
et al., 2011). Signalling molecules involved in the cell–cell
communication include small organic molecules, small peptides, ions, and physical stimuli. These signals are initially
received by receptor proteins and sequentially transmitted to
target signalling elements.
Receptor-like kinases (RLKs), which form a large gene
family in plants, contain Ser/Thr kinase as a cytosolic domain
while having structural elements similar to animal receptor
tyrosine kinases (RTKs). RLKs convey signal to their target
proteins in the cytoplasm by catalytic processes of protein
kinase activity. In Arabidopsis, the RLK family includes >600
members, with the leucine-rich repeat RLKs (LRR-RLKs)
constituting the largest group among the RLKs (Shiu and
Bleecker, 2001a, b, 2003; Gish and Clark, 2011). These RLKs
regulate various plant processes of plant growth and development as well as homeostatic mechanisms underlying the
abiotic stress response. In addition, RLKs have been known
to have a major role in integrating environmental and plant
hormone signalling (Shiu and Bleecker, 2001b; Dievart and
Clark, 2004) (Fig. 1). Recent studies suggested that the rapid
evolution and diversification of RLK-encoding genes in the
plant genome might be enhanced by various environmental
associations (Alcazar et al., 2010; Smith et al., 2011). Natural
SAM
maintenance
SAM
cell
elongation
cell
proliferation
& organ growth
ERECTA
ERL1
ERL2
PSKR
OAK
BRI1
BAK1
FER
THE1
HERK1
WAK
stomatal
development
ERECTA
ERL1
ERL2
LP
L1
L2
L3
LP
CLV1
BAM1/2
SOL2
RPK2
anther development
& fertilization
FER
BAM1/2
EMS1
SERK1/2
RPK2
xylem
differentiation
abiotic stress
responses
PXY/TDR
biotic stress
responses
Na+
RPK1
PERK4
GHR1
CRK36
CRK
RLK7
FLS2
PEPR1/2
BAK1
Fig. 1. Overview of plant receptor-like kinases (RLKs) and their functions. The RLKs form a large gene family in plants and regulate
various plant processes, including growth and development and responses to biotic and abiotic stresses. The typical well-known RLKs
shown in the figure are also listed in Supplementary Table S1 at JXB online. The RLKs that control abiotic stress signallings are also listed
in Table 1.
Membrane-localized kinases in plant response to abiotic stress | 447
variations at the Strubbelig Receptor Family 3 (SRF3) in
Arabidopsis were able to change the early immune responses
and control immune-triggered incompatibilities between
the variations (Alcazar et al., 2010). OUTGROWTHASSOCIATED PROTEIN KINASE (OAK) alleles from
Arabidopsis accessions have been shown to cause a variety
of abnormal growth phenotypes and cell death responses
(Smith et al., 2011). The OAK gene belongs to a subgroup
of similar RLK genes which are composed of a tandem cluster in the Arabidopsis genome and vary between the natural
accessions. Furthermore, this gene was the causal gene for the
incompatibility of the accessions (Smith et al., 2011). These
RLK studies on plant self-incompatibility and innate immunity indicated that the molecular evolution and divergence of
RLKs play a major role in defining the diversity of environmental responses in the natural variations.
Typical molecular approaches, such as transcriptome analyses, also suggested that the RLKs can be considered as key
regulators in growth and developmental processes as well as
in various environmental stress responses (Chae et al., 2009;
Hwang et al., 2011; Marshall et al., 2012). The changes in
transcriptome in response to abiotic and biotic stresses have
been widely characterized, and the results suggested that
general regulatory pathways are involved in the processes of
gene expression during stresses (Kilian et al., 2007; Matsui
et al., 2008; Osakabe et al., 2011, 2012; Le et al., 2012b; Ma
et al., 2012). The transcription of various RLK genes is also
regulated and modulated in response to stresses at the levels of individual genes and/or subfamilies (Chae et al., 2009;
Tanaka et al., 2012).
Histidine kinases (HKs) localized to cellular membranes
or the endoplasmic reticulum were originally identified as
the first member of two-component systems that mediate
bacterial environmental signals to downstream members, the
response regulators (RRs) (Mizuno, 2005; Ha et al., 2012).
In plants, two-component systems or histidine-to-aspartate
(His–Asp) phosphorelays are involved in the regulation of
various biological processes, including the perception of
plant hormones, such as ethylene and cytokinins (CKs), and
responses to environmental stimuli. A typical, multistep His–
Asp phosphorelay consists of hybrid HKs, histidine phosphotransfer proteins (HPs), and RRs (Mochida et al., 2010;
Le et al., 2011; Schaller et al., 2011; Ha et al., 2012). Recently,
CK receptor AHKs were shown to act as negative regulators
in abiotic stress responses via a CK-mediated signalling pathway (Tran et al., 2007b, 2010b; Jeon et al., 2010; Nishiyama
et al., 2011, 2012). On the other hand, ATHK1/AHK1, a nonCK receptor kinase, was identified as an osmosensor acting
as a positive regulator of osmotic stress signal transduction
(Tran et al., 2007b; Wohlbach et al., 2008).
In this review, we will discuss the current knowledge of
membrane-bound receptor proteins that act as key regulators in the perception of environmental signals in plants.
The focus will be on RLKs and HKs, which perceive plant
hormones and small peptides and are involved in the regulation of plant abiotic stress responses. The elucidation of
how these membrane elements form a molecular connection
between an environmental stress response and the regulation
of plant growth will greatly enhance our understanding of
how plants control their adaptive response to adverse environmental conditions.
RLKs control plant growth during
environmental stresses
The membrane-localized RLKs have been shown to control
diverse signalling events (Fig. 1), and these RLKs constitute the largest gene family in various plant genomes, with
>600 members in Arabidopsis and 1100 members in rice,
and are classified based on their extracellular structures
(Supplementary Table S1 available at JXB online) (Shiu and
Bleecker, 2001a, b, 2003; Morillo and Tax, 2006; Gish and
Clark, 2011). The LRR-RLKs form a major RLK family,
which has >200 members and is classified into 15 subfamilies (LRR I–LRR XV) in Arabidopsis (Shiu and Bleecker,
2001a, b, 2003). These LRR-RLKs are implicated in diverse
signalling events (Figs 1, 2; Supplementary Table S1), such as
brassinosteroid (BR) perception by the BR INTENSITIVE
1 (BRI1) and BR1-ASSOCIATED RECEPTOR KINASE1
(BAK1) (Clouse, 2011; Choudhary et al., 2012a), meristem
size regulation as shown by the functions of CLAVATA1
(CLV1) involved in perception of the peptide hormone CLV3
(Deyoung and Clark, 2008; Muller et al., 2008; Ogawa et al.,
2008; Kinoshita et al., 2010), and in organ growth and stomatal cell differentiation by the ERECTA family and the EPF
(EPIDERMAL PATTERNING FACTOR) peptide receptors (Kim et al., 2012).
Increasing evidence suggests that RLKs regulate the
environmental stress response and play an essential role in
the resulting adaptive mechanisms. The RLKs regulate the
homeostatic mechanisms underlying abiotic and biotic stress
responses and have a major role in integrating environmental and plant hormone signallings. In the first two sections,
we focus on the RLK families that have important roles to
control water stress signalling and the adaptive responses
in plants. RLKs, such as RPK1, CYSTEINE-RICH RLK
(CRK36), PROLINE-RICH-EXTENSIN-LIKE RLK4
(PERK4), and GHR1 (GUARD CELL HYDROGEN
PEROXIDE-RESISTANT1), have been reported to control
water stress signalling directly in Arabidopsis (Osakabe et al.,
2005; Bai et al., 2009; Y. Osakabe et al., 2010; Lee et al., 2011;
Hua et al., 2012; Tanaka et al., 2012) (Fig. 2, Table 1). Many
aspects of stomatal morphology and vascular tissue structure
have evolved to optimize gas exchange, photosynthesis, and
water use efficiency (WUE) under various degrees of drought
stress (Bergmann and Sack, 2007; Casson and Hetherington,
2010; Yoo et al., 2010). The ERECTA (ER) family controls
stomatal differentiation and affects WUE in plants. Their
functions and the signal transduction pathways are also summarized in this section.
The ERECTA family
Stomatal differentiation in the epidermis of plants is initiated
by a series of asymmetric cell divisions and involves cell–cell
448 | Osakabe et al.
Fig. 2. The signaling networks of RLKs and histidine kinases (HKs) in plant stress responses. RLKs and HKs perceive peptidic ligands
or phytohormones to trigger the signalling cascades, leading to an adaptation to the adverse environmental changes. Downstream
pathways of several receptors have been studied in more detail. MAPK signalling cascades, ABA signalling pathway, reactive oxygen
species (ROS), and calcium ions are involved in the RLK downstream pathways and affect the various molecules and cellular events.
The region downstream of cytokinin HKs contains the His–Asp phosphorelay pathway composed of phosphotransfer proteins (HPs) and
response regulators (RRs).
communication to establish their number and arrangement
(Peterson et al., 2010). The ERECTA family of LRR-RLKs,
consisting of ERECTA (ER), ERECTA-LIKE1 (ERL1) and
ERL2, mediate various plant developmental processes, such
as cell fate specification including stomatal development
(Fig. 3) (Pillitteri and Torii, 2012). Disruption of the ER family produced a phenotype characterized by a high density of
mispatterned stomata (Shpak et al., 2005). The ER family
together with the LRR receptor-like protein TOO MANY
MOUTHS (TMM) control stomatal patterning in a synergistic manner (Guseman et al., 2010). Recent findings suggest
that the different types of receptor–ligand pairs between ER/
TMM and EPFs may specify the different steps of stomatal
development (Hara et al., 2007, 2009; Ohki et al., 2011; Lee
et al., 2012).
Mitogen-activated protein kinase (MAPK) cascades,
which include a MAPKKK YODA, MAPK kinases MKK4,
MKK5, MKK7, and MKK9, and MAPKs MPK3 and
MPK6, act as a potential downstream pathway for ER signalling (Wang et al., 2007). Basic helix–loop–helix (bHLH)
transcription factors control stomatal development by
serving as targets of MAPKs. Three paralogous bHLHs,
SPEECHLESS (SPCH), MUTE, and FAMA, are key factors regulating stomatal development (Peterson et al., 2010).
These bHLHs control the progression of the stomatal lineage
to generate a pair of guard cells that are sequentially differentiated from a protodermal cell, meristemoid mother cell, meristemoid cell, and guard mother cell. Other bHLHs involved
in modulation of stomatal development are ICE1/SCRM1
and SCRM2, which physically interact with SPCH, MUTE,
and FAMA (Peterson et al., 2010).
Environmental factors, such as light and carbon dioxide (CO2), have roles in stomatal development (Casson and
Hetherington, 2010). Stomatal density and the stomatal index
are affected by the amount of light energy present during stomatal development. Casson et al. (2009) suggested that the
Membrane-localized kinases in plant response to abiotic stress | 449
Table 1. Receptor-like kinases involved in regulation of plant responses to abiotic stresses.
Type of
RLK
Subfamily
Gene
name
Full name
Organism
LRR
LRR III
GHR1
Arabidopsis
LRRIX
SRLK
LRRXI
RLK7
GUARD CELL
HYDROGEN
PEROXIDERESISTANT1
SALT-INDUCED
RECEPTOR-LIKE
KINASE
RECEPTOR-LIKE
KINASE 7
LRRXIII
OsSIK1
O. SATIVA STRESSINDUCED PROTEIN
KINASE GENE 1
Oryza sativa
LRRXV
RPK1
RECEPTOR-LIKE
PROTEIN KINASE 1
Arabidopsis
Abiotic
stressinducible
PERK
PERK4
PROLINE-RICH
EXTENSIN-LIKE
RECEPTOR
KINASE 4
Arabidopsis
Abiotic
stressinducible
CRK/
DUF26
CRK36
CYSTEINE-RICH
RECEPTOR-LIKE
KINASE 36
Arabidopsis
Abiotic
stressinducible
RLCK
ARCK1
ABA- AND
OSMOTIC-STRESSINDUCIBLE
RECEPTOR-LIKE
CYTOSOLIC
KINASE 1
O. SATIVA
RECEPTOR-LIKE
CYTOSOLIC
KINASE 253
PHOSPHORUSSTARVATION
TOLERANCE 1
Arabidopsis
Abiotic
stressinducible
Oryza sativa
Oryza sativa
GsCBRLK
G. soja calmodulinbinding receptor-like
kinase
Glycine soja
CRLK1
Ca2+/CaM-regulated
RLK
Arabidopsis
OsRLCK253
PSTOL1
a
OX, overexpressor
Medicago
truncatula
Homologues
with known
function
BIR1
Arabidopsis
ERECTA
CRLK1
Expression
Function
References
Guard cells
Functions in ABA- and
H2O2-regulated activation
of S-type anion channels in
guard cells.
The RNAi prevents inhibition
of root growth in Medicago
under salt stress.
Involved in the control of
germination speed and the
tolerance to oxidant stress.
Rice OXa plants exhibited
tolerance to salt and drought
stresses with increased
levels of superoxide
dismutase and decreased
ROS accumulation.
Arabidopsis OXs showed
enhanced ABA sensitivity
and drought tolerance with
increased superoxide dismutase level and decreased
ROS accumulation.
Functions at early stage
of ABA signalling to inhibit
primary root cell elongation by perturbing Ca2+
homeostasis.
Forms a complex with
ARCK1 and negatively controls ABA and osmotic stress
signal transduction.
Forms a complex with
CRK36 and negatively controls ABA and osmotic stress
signal transduction.
Hua et al.
(2012)
–
Arabidopsis OX plants
have improved tolerance to
drought and salt stresses.
Giri et al.
(2011)
Abiotic
stressinducible
(P-deficient
conditions)
Abiotic
stressinducible
Root growth and grain yield
of rice OXs are enhanced in
P-deficient soil with constitutive up-regulation of drought
stress-responsive genes.
Arabidopsis OX plants have
enhanced tolerance to
high salinity and ABA with
increased expression levels
of stress-responsive genes.
Knock-out mutants exhibited
an increased sensitivity to chilling and freezing
temperatures.
Gamuyao et al.
(2012)
Abiotic
stressinducible
Abiotic
stressinducible
Abiotic
stressinducible
Abiotic
stressinducible
de Lorenzo
et al. (2009)
Pitorre et al.
(2010)
Ouyang et al.
(2010)
Y. Osakabe
et al. (2005,
2010)
Bai et al. (2009)
Tanaka et al.
(2012)
Tanaka et al.
(2012)
L. A. Yang
et al. (2010)
T. Yang et al.
(2010a)
450 | Osakabe et al.
Fig. 3. The model of ERECTA, BRI1, BAK1, and FLS signalling
pathways. The guard cell development controlled by the
ERECTA family (LRR-RLK) and its peptide ligands, EPFs, the
brassinosteroid signalling mediated by BRI1 (LRR-RLK), BAK1
(LRR-RLK), and BSK1 (RLCK), and the defence responses
controlled by flagellin receptor FLS2 (LRR-RLK), BAK1 (LRRRLK), and BIK1 (RLCK), involve cross-talk at the early steps in the
signalling cascades during various plant processes of growth and
stress responses.
photoreceptor PhyB and a bHLH transcription factor, PIF4,
might be the major factors involved in stomatal development
(Casson et al., 2009). Stomatal number is also affected by
the atmospheric concentration of CO2, and this association
has been established over millenia. An analysis of stomatal
characteristics and CO2 over long geological time periods
indicates that stomatal density negatively correlates with CO2
levels, whereas stomatal size is positively correlated (Franks
and Beerling, 2009; Lomax et al., 2009). The phytohomone
abscisic acid (ABA) mediates various physiological events
during water stress, including stomatal closing and stomatal
density. Lake and Woodward (2008) reported that aba mutant
plants, which are defective in ABA biosynthesis, display
higher stomatal densities (Lake and Woodward, 2008). The
regulation of stomatal conductance and transpiration rates
is linked to stomatal development, and systemic signalling
mediates stomatal development in response to environmental conditions (Casson and Hetherington, 2010). Although
the above-mentioned regulatory factors control stomatal
development under various environmental conditions, their
molecular relationship to the signalling cascades controlled
by EPFs, ER, MAPKs, and SPCH/MUTE/FAMA remain
largely unknown. Knowledge of how environmental signals
modulate these signalling pathways would help to clarify how
this process impacts the ability of plants to adapt to adverse
growth conditions.
Recent studies have provided evidence that ER is a major
genetic marker in various quantitative trait locus (QTL)
and expression QTL (eQTL) studies of plant development
and plant responses to environmental stresses. The molecular relationship between leaf production and leaf expansion
was determined by a quantitative genetic analysis using a set
of Arabidopsis recombinant inbred lines (RILs). One of the
QTLs at ER was identified in a heterozygous inbred family
as a control factor of both epidermal cell number and area
(Tisne et al., 2008). The QTLs for the different aspects of
plant growth-related traits, sugar and starch content, and
flowering time have been analysed using RILs derived from
Landsberg erecta (Ler) and Kondara (El-Lithy et al., 2010).
In their study, the authors detected co-locations of QTLs for
these various aspects mainly at the ER locus (El-Lithy et al.,
2010). ER was found as the major factor of transcriptional
regulation by conducting an eQTL analysis using the RILs of
Ler/Cape Verde Islands (Cvi). Additionally, candidate genes
in the downstream signalling pathway were identified where
ER has been linked to MAPK cascades and the WRKY
transcription factor family (Terpstra et al., 2010). Another
QTL analysis using the RILs of Ler/Cvi demonstrated that
ER controls ethylene-induced petiole angles and ethyleneindependent effects on initial angles (van Zanten et al., 2010).
Although it is not clear yet if ER is directly associated with
the factors involved in the regulation of these diverse plant
processes, these studies suggest that ER might be a key modulator of signalling pathways. This possibility, in which the ER
RLK family responds to a variety of ligands, might explain
the extensive diversity of their function.
The BRASSINOSTEROID INSENSITIVE 1 (BRI1) kinase
BRs are plant hormones involved in the regulation of various
aspects of plant growth and development, as well as responses
to both abiotic and biotic stresses (Divi and Krishna, 2009;
Wolters and Jurgens, 2009; Choudhary et al., 2012c; Wang,
2012). BRs negatively regulate stomatal development mediated by upstream signalling components including the
BR receptor RLK BRI1, the protein phosphatase BRI1
SUPPRESSOR1 (BSU1), the BR SIGNALLING KINASE
1 (BSK1), and the GSK3-like kinase BRASSINOSTEROIDINSENSITIVE 2 (BIN2) (Tang et al., 2008). When the BR
level is low, BIN2 directly interacts with MAPKKK YODA
and phosphorylates YODA, thereby inactivating it (Fig. 3).
Inactivation of YODA by BIN2 in turn leads to de-repression
of SPCH, allowing SPCH to initiate stomatal development.
Membrane-localized kinases in plant response to abiotic stress | 451
When BR is high, the MAPKKK YODA pathway is activated
by inactivation of BIN2 through BRI1, BSK1, and BSU1,
thereby inhibiting stomatal development. BRs have also been
shown to repress light-responsive gene expression and chloroplast development mainly through the BRASSINAZOLE
RESISTANT 1 (BZR1)-mediated transcriptional network
(Luo et al., 2010; Sun et al., 2010). Additionally, recent
reports indicate that appropriate genetic engineering of BR
signalling can lead to abiotic and/or biotic stress tolerance
(Divi and Krishna, 2009; Wang, 2012). These reports indicate that BR and the EPF signalling systems work together to
mediate signalling networks to optimize photosynthesis and
WUE. The multifunctional roles of RLKs in various plant
signalling pathways were shown through studies of BAK1
(Clouse, 2011). BRI1 requires BAK1 as a co-receptor to
execute BR signalling. Another RLK, the flagellin receptor
FLS2, was shown to act in concert with BAK1 in FLS2 signalling to regulate plant innate immunity (Wang, 2012) (Figs
2, 3). BAK1 belongs to the SOMATIC EMBRYOGENESIS
RECEPTOR-LIKE KINASE (SERK) family. Increasing
evidence has demonstrated that the SERKs can act as coreceptors in multiple independent signalling pathways by
their association with different RLKs (Li, 2010).
Function of RLKs in environmental stress
responses
To explore the novel stress-responsive RLKs in plants, comprehensive studies of the transcriptional profiles of the RLK
genes in environmental stresses have been performed (Chae
et al., 2009; Lehti-Shiu et al., 2009; Hwang et al., 2011;
Marshall et al., 2012). These studies indicated that the transcription of a number of RLK genes is controlled and modulated by various environmental cues, implying their important
roles in stress responses.
Various RLKs that control biotic stress responses have been
identified from several plant species (Supplementary Table S1
at JXB online). The bacterial flagellin fragment (Flg22) was
recognized by an LRR-RLK, the FLAGELLIN SENSING2
(FLS2), which mediates defence responses in plants (Figs 2, 3)
(Wang, 2012). FLS2 interacts with BAK1 and phosphorylates
the cytoplasmic kinase BIK1 that is able to control the FLS2
signalling as a positive regulator (Lu et al., 2009) (Fig. 3). In
addition, transcriptome analyses show that a number of RLK
genes are also up-regulated by biotic stresses, suggesting their
important roles in regulation of biotic responses (Chae et al.,
2009; Lehti-Shiu et al., 2009). There is also a significant overlap among RLK genes induced by biotic and abiotic stresses
(Chae et al., 2009; Lehti-Shiu et al., 2009), indicating that the
RLKs might mediate the cross-talk between biotic and abiotic stress responses.
Likewise, the RLKs involved in sensing environmental signals and in abiotic stress signalling pathways have been identified in various plant species, such as Arabidopsis (Yang et al.,
2004; Osakabe et al., 2005; Bai et al., 2009; Y. Osakabe et al.,
2010; Lee et al., 2011; Tanaka et al., 2012), rice (Oryza sativa)
(Ouyang et al., 2010), Medicago truncatula (de Lorenzo
et al., 2009), and Glycine soja (L.A. Yang et al., 2010) (Fig. 2,
Table 1; Supplementary Table S1 at JXB online). These RLKs
have a variety of extracellular domains, such as an LRR, an
extensin-like, or a cysteine-rich domain, suggesting that various environmental stimuli may activate the signalling pathways mediated by RLKs. Increasing evidence suggests that
RLKs can have either a positive or a negative regulatory role
in abiotic stress response.
LRR-RLKs involved in water stress responses
RECEPTOR-LIKE PROTEIN KINASE1 (RPK1) is an
LRR-RLK whose expression is induced by ABA, dehydration, high salt, and low temperature. Loss of function of
RPK1 resulted in ABA insensitivity and reduced expression levels of various water stress-responsive genes, indicating that RPK1 positively regulates ABA/stress signalling.
Microarray analysis of the Arabidopsis RPK1 loss-of-function mutant identified a number of down-regulated stressrelated genes, including reactive oxygen species (ROS)-related
genes (Osakabe et al., 2005). ROS production is activated
during both biotic and abiotic stresses, including pathogen
attack, high light, osmotic stress, heavy metal stress, and herbicides. ROS are important second messengers for stress signal transduction pathways (Gill and Tuteja, 2010; Le et al.,
2010; Takahashi et al., 2011; Choudhary et al., 2012c). Many
water stress-responsive genes were consistently up-regulated
in Arabidopsis RPK1-overexpressing plants, including ROSrelated genes (Y. Osakabe et al., 2010). RPK1 transgenic
plants exhibited increased tolerance to both drought and
oxidative stress, suggesting that RPK1 controls ROS homeostasis and mechanisms regulating both the water and oxidative stress response in Arabidopsis. In an independent study,
Lee et al. (2011) reported that RPK1 functions in ABAdependent leaf senescence as well. RPK1 has been primarily
identified in the genomes of Brassica species, suggesting that
RPK1 might play a specific regulatory role in Brassica species,
whereas the Arabidopsis RPK1 homologous protein, RPK2/
TOAD2, with high similarity in the kinase domain of RPK1,
was identified in diverse plant species (Sawa and Tabata,
2011) (Fig. 2). RPK2 controls cell fate in anthers (Mizuno
et al., 2007), embryo development (Nodine et al., 2007), and
stem cell homeostasis in the shoot apical meristem through
the mediation of CLV3 (Kinoshita et al., 2010; Betsuyaku
et al., 2011). These studies indicate that RPK2 is one of the
important RLKs governing plant development in various
species. RLK7, an LRR-RLK member of the LRR XI subfamily, was identified as an important regulator in oxidative
stress responses and shown to be involved in maintaining
seed longevity (Pitorre et al., 2010). Recently, an LRR-RLK
that controls ABA- and H2O2-regulated activation of S-type
anion channels in guard cells has been identified (Hua et al.,
2012). This RLK, named GUARD CELL HYDROGEN
PEROXIDE-RESISTANT1 (GHR1), physically interacted
with and activated the S-type anion channel SLOW ANION
CHANNEL-ASSOCIATED1 (SLAC1) by phosphorylation,
resulting in stomatal closing in response to drought stress.
The ligands of these RLKs have not been resolved yet, and
452 | Osakabe et al.
further studies would elucidate the whole picture of the signalling mechanisms.
A number of reports have demonstrated that RLKs from
legume and crop plants regulate the abiotic stress response
(de Lorenzo et al., 2009; Ouyang et al., 2010; L.A. Yang et al.,
2010; Giri et al., 2011; Gamuyao et al., 2012) (Table 1). A salt
stress-inducible LRR-RLK gene, SRLK, identified from the
legume M. truncatula was reported to be involved in adaptation to salt stress (de Lorenzo et al., 2009). Root growth inhibition by high salinity stress was alleviated in SRLK RNA
interference (RNAi) transgenic Medicago roots. Epidermal
cell-specific expression of the SRLK gene was observed in
roots under salt stress, and SRLK was shown to control the
expression level of several salt-responsive genes. These findings suggest that SRLK activates the signalling pathway
involved in the adaptive response of Medicago roots to salt
stress.
Over 1000 RLK genes have been identified in the rice
genome. Among 267 abiotic stress-responsive RLK genes
in rice, Oryza sativa stress-induced protein kinase gene 1
(OsSIK1), which is induced by salt, drought, and oxidative
stresses, was selected for functional analysis (Ouyang et al.,
2010). OsSIK1-overexpressing transgenic rice plants exhibited increased salt and drought tolerance, whereas the loss of
function of OsSIK1 resulted in sensitivity to these stresses.
Increased activity of peroxidases, superoxide dismutases,
and catalases was found in the OsSIK1-overexpressing
transgenic plants, and ROS accumulation was decreased in
their leaves. The OsSIK1 kinase domain has high similarity
to the kinase domains of the Arabidopsis ER family, and
OsSIK1 affects stomatal density. These findings indicate
that OsSIK1 plays an important role in water stress tolerance in rice.
Collectively, the reports on the functions of LRR-RLKs
in water stress responses demonstrate the diversity of the
receptor domains. Further studies to identify their ligands
and kinase functions are required to elucidate how the RLKs
integrate their individual roles in controlling water stress
responses.
PERK family
A member of the proline-rich extensin-like receptor kinase
family, PERK4, was identified as a positive regulator in ABA
responses (Bai et al., 2009). Decreased sensitivity to ABA with
respect to seed germination, seedling growth, and root tip
growth was observed in perk4 mutant plants. ABA-induced
elevation of the concentration of cytosolic free calcium
and Ca2+ channel activity were impaired in perk4 root cells.
PERK4 was shown to be an ABA- and Ca2+-activated protein kinase that functions at an early stage of ABA signalling
involved in the inhibition of root cell elongation (Bai et al.,
2009), suggesting that PERK4 may perceive changes in the
levels of ABA. The PERK family is predicted to have similar
functions to cell wall-associated kinases (WAKs) which serve
as cell wall receptors and also bind to pectin (Nakhamchik
et al., 2004). Furthermore, Bai et al. (2009) demonstrated that
PERK4 may also perceive changes in the cell wall.
CRR-RLK (CRK) family
A cysteine-rich RLK (CRK), CRK36, has recently been
identified in Arabidopsis that acts as a negative regulator
in osmotic stress and ABA signalling (Tanaka et al., 2012).
CRK36, an abiotic stress-inducible CRK (Wrzaczek et al.,
2010), was first identified by co-expression analyses and yeast
two-hybrid screening as a potential interacting factor with
ARCK1, which encodes a receptor-like cytoplasmic kinase
(RLCK). CRK36 can physically interact with and phosphorylate ARCK1. The knock-down of CRK36 in transgenic
Arabidopsis resulted in increased sensitivity to ABA and
osmotic stress during post-germinative growth, and the upregulation of ABA-responsive genes, such as LEA genes, oleosin, ABA-INSENSITIVE 4 (ABI4), and ABI5. Collectively,
these results suggest that CRK36 and ARCK1 form a complex and function in a negative feedback mechanism regulating ABA and osmotic stress responses (Tanaka et al., 2012).
RLCK family
Calcium-mediated signalling plays a pivotal role in plant
responses to abiotic stresses, including cold and drought
stress. Calcium/calmodulin-regulated RLCKs have been
shown to be involved in abiotic stress signalling. For instance,
the cold-responsive CRLK1, which encodes an RLCK with
two sites for calcium/calmodulin binding to stimulate kinase
activity, was reported to regulate cold stress signalling (T.
Yang et al., 2010a). The crlk1 knock-out mutant plants exhibited an increased sensitivity to chilling and freezing stress, and
cold-responsive genes were down-regulated in crlk1 mutants
(T. Yang et al., 2010a). Further analysis revealed that CRLK1
interacts with MEKK1, a member of the MAPKKK family,
both in vitro and in planta (T. Yang et al., 2010b). MAPK activation by cold treatment was abolished in the crlk1 mutant,
and the expression levels of cold-inducible genes involved in
MAPK signalling were altered. Calcium-dependent calmodulin-binding RLCKs have also been isolated from Glycine
max (GmCaMK1) (DeFalco et al., 2010) and Glycine soja
(GsCBRLK) (L.A. Yang et al., 2010). Although GmCaMK1
was identified as a homologue of Arabidopsis CRLK1, the
function of GmCaMK1in the cold stress response is still
unclear. GsCBRLK activity is regulated by its calcium/
calmodulin binding, and the overexpression of GsCBRLK
in transgenic Arabidopsis enhanced plant tolerance to high
salinity and ABA, as well as increasing the expression level of
stress marker genes.
Perception and cross-talk of osmotic
stress signalling by non-ethylene histidine
kinases
The His–Asp phosphorelay is involved in the regulation of
responses to various abiotic stresses, including drought, high
salinity, and cold (Tran et al., 2007b, 2010b; Wohlbach et al.,
2008; Jeon et al., 2010; Ha et al., 2012; Pham et al., 2012).
The Arabidopsis genome contains eight HK members. Five
Membrane-localized kinases in plant response to abiotic stress | 453
HK members (ETR1, ERS1, AHK2, AHK3, and AHK4) are
implicated in the perception of two plant hormones, ethylene and CKs (Schaller et al., 2008). The CK receptor AHKs,
AHK2, AHK3, and AHK4, are involved in phosphorelay
along with five AHPs and numerous type-B ARRs which
control the transcription of certain type-A ARR genes (Tsai
et al., 2012) (Fig. 4). On the other hand, type-A ARR genes,
whose expression is rapidly induced by CKs for negative
feedback regulation, were reported to regulate the activity of
type-B ARRs indirectly via a negative feedback loop (Muller
and Sheen, 2007; Ha et al., 2012) (Fig. 4).
Among the non-hormonal receptor HKs (AHK1, AHK5,
and CKI1), AHK1 was identified as a unique osmosensor
with in planta positive regulatory function in the osmotic
stress response (Tran et al., 2007b; Wohlbach et al., 2008).
AHK1 complements a deletion of SLN1, an osmosensor HK
in yeast, and acts as an osmosensor by activating downstream
cascades in yeast cells (Urao et al., 1999). Overexpression
of AHK1 in Arabidopsis resulted in increased tolerance to
osmotic stress, whereas the ahk1 knock-out mutant plants
exhibited enhanced sensitivity to osmotic stress (Tran et al.,
Fig. 4. Schematic model of cytokinin and osmotic stress signal
transduction pathways via a His–Asp phosphorelay in Arabidopsis.
The activated HKs transfer the phosphoryl group to AHPs which
are subsequently activated. Activated AHPs then transport the
signals to type-B ARRs, which act as transcriptional factors, in the
nucleus. The target genes of the type-B ARRs contain type-A ARR
genes that function as negative regulators in cytokinin signalling
in a negative feedback loop. The osmotic stress signalling that is
controlled by AHK1 and the cytokinin signalling mediated via the
His–Asp phosphorelay have antagonistic functions in the control of
the osmotic stress responses.
2007b; Wohlbach et al., 2008). Additionally, ahk1 mutants
exhibited decreased sensitivity to ABA, and expression levels of ABA and/or stress-responsive genes were down-regulated. These studies indicate that the osmosensor AHK1
acts as a positive regulator in osmotic stress signalling and
regulates the expression of downstream genes in both an
ABA-dependent and ABA-independent manner (Tran et al.,
2007b; Wohlbach et al., 2008). While downstream cascades
are potentially controlled by AHPs and ARRs in the multiple His–Asp phosphorelay, the factors that receive the signals
from AHK1 and the identification of the precise signalling
cascades remain to be determined. AHK5, which is localized to the plasma membrane, was identified as a regulator of
stomatal closure in response to ROS (H2O2) (Desikan et al.,
2008). Guard cells of ahk5 mutant plants exhibited reduced
sensitivity to the ROS-induced stomatal closure response but
were not significantly altered in their response to ABA, suggesting that AHK5 regulates the H2O2 response in an ABAindependent manner (Desikan et al., 2008). Recently, the
same group provided evidence showing that AHK5 acts as
a negative regulator of the salt stress response during seed
germination and growth of both young seedlings and mature
plants in Arabidopsis (Pham et al., 2012).
Among the hormonal receptor HKs, AHK2, AHK3, and
AHK4 were shown to negatively regulate ABA and stress signalling (Tran et al., 2007b, 2010b; Jeon et al., 2010) (Fig. 4).
Mutations of ahk2, ahk3, and ahk4 in various combinations
resulted in increased sensitivity to ABA and tolerance to abiotic stresses including cold, salt, and drought (Tran et al.,
2007b; Jeon et al., 2010). The expression levels of ABA and/or
stress-responsive genes were up-regulated in ahk2ahk3 mutant
plants. These studies suggest that cross-talk exists among ABA,
CK, and stress signalling pathways. The ability of CKs to have
an impact on the negative regulatory function of AHK4 suggests the involvement of CKs as a negative regulator of the
stress response (Tran et al., 2007b). This has been recently
verified by a series of molecular analyses of CK-deficient
mutants subjected to drought and salt stress (Nishiyama et al.,
2011, 2012). Reduced CK content found under drought and
salt stresses may help plants adapt to these stresses through
a leaf senescence strategy (Guo and Gan, 2007; Nishiyama
et al., 2011; Ha et al., 2012). However, the conditional and
stage-specific stimulation of CK biosynthesis by stress-inducible promoter(s) may delay the stress-induced acceleration of
leaf senescence and enable the maintenance of photosynthetic
activity under stress conditions, providing an effective biotechnological strategy for agricultural applications (Rivero et al.,
2007; Peleg et al., 2011). For instance, the overexpression of
a CK biosynthetic gene, an isopentenyltransferase (IPT) gene
derived from Agrobacterium tumefaciens, under the control of
a drought- and senescence-inducible promoter was reported to
enhance both plant longevity and stress tolerance in tobacco
(Nicotiana tabacum) and rice. The transgenic plants exhibited
increased ROS scavenging and photosynthetic capacity as well
as the ability to maintain homeostasis under stress conditions
(Rivero et al., 2007; Peleg et al., 2011).
Several downstream components of CK signalling have also
been shown to be involved in the stress response. For instance,
454 | Osakabe et al.
loss of function of ARR5, ARR6, or ARR7 improved cold
tolerance (Jeon et al., 2010), while that of ARR1 and ARR12
enhanced salt tolerance (Mason et al., 2010). Additionally,
altered expression of phosphorelay components by abiotic
stresses has been reported in various plant species, including
Arabidopsis, rice, and soybean (Osakabe et al., 2002; Tran
et al., 2007b; Karan et al., 2009; Jeon et al., 2010; Le et al.,
2011). Overall, the collective reports support the premise that
cross-talk between hormone and stress signalling networks
plays an important role in plant stress response.
Conclusions and future perspectives
Plants have evolved the ability to adapt to and tolerate natural environmental stresses. Tolerance mechanisms are constructed of complex processes involving various signalling
pathways. Changes in surrounding environmental conditions,
sensed by molecular sensors, can activate cellular signalling
events that control plant homeostasis in an effort to maintain
‘normal’ growth and development (Fig. 3). HKs involved in
the His–Asp signalling systems have been identified in many
plant species, indicating that the fundamental roles of HKs in
stress responses are conserved. In planta elucidation of each
member of the phosphorelay and their downstream genes will
provide a greater insight into the functions of the phosphorelay and the cross-talk that exists among various hormones
involved in stress responses.
The large RLK family, which has evolved during plant
evolutionary history, may enable RLKs to recognize a wide
range of environmental signals. This premise implies that the
diverse functions of RLKs are critical to maintaining ‘normal’ plant growth and development under various conditions.
Due to the multiple functions of RLKs in the abiotic stress
response, signalling networks governing plant responses to
stress are complex. The reports discussed in this review suggest that various abiotic stresses serve as signals to trigger the
activity of RLKs. These stress-specific ‘ligands’ and RLKs
coordinately control various molecular events and downstream cascades, such as phosphorylation cascades, activation of secondary messengers, gene expression, and protein
dynamics. Further analyses of tissue- and/or cellular-specific
responses, as well as developmentally regulated events, will
provide new insights into the integrated molecular relationship of these signalling pathways. The study of cross-talk
between regulatory pathways involving different plant hormones and/or biotic stresses will also help to identify the
specific molecular cascades that control plant homeostasis.
The precise ligands and the downstream signalling molecules
sensed by RLKs remain to be identified. Extracellular signals, such as hormones, small peptides, small chemical molecules, and physical stimuli, are all potential candidates. The
intracellular events downstream of RLKs may include kinase
cascades (e.g. MAPK), Ca2+ ions, ROS signalling, metabolic
adjustments, and membrane dynamics. It will be important to
analyse the cellular or tissue-specific events in stress responses
as well as growth, developmental, and ageing stage-specific
events to understand precisely the signalling pathways
controlled by RLKs, especially those involved in cell–cell
communication. These efforts will provide new insights that
will enable us to better understand the complex and wellcoordinated strategies that plants have evolved to adapt to
adverse environmental conditions.
Environmental stress tolerance is an important agronomic
trait and is essential for maintaining high yield under adverse
conditions. It is important to understand how plants sense the
environment and regulate signalling networks. This knowledge
will provide important information on how plants attempt to
maintain ‘normal’ growth and development under suboptimal environmental conditions. Genetic engineering of plant
membrane signalling factors, including RLKs and HKs, can
have a positive impact on stress tolerance by influencing many
downstream signalling factors. Furthermore, emerging technologies utilizing synthetic restriction endonucleases (Shukla
et al., 2009; K. Osakabe et al., 2010; Zhang et al., 2010) will
enable genome editing of RLKs and HKs, which will help to
elucidate how these kinases have evolved to control downstream signalling pathways in various plant species. A more
precise knowledge of how signalling networks function and
are regulated, their impact on the physiology and biochemistry of a plant, and how different signalling networks are
integrated to maintain plant homeostasis (i.e. normal growth
and development) will increase our ability to produce superior
plant genotypes that exhibit high levels of productivity in a
rapidly changing and ever more stressful environment.
Supplementary data
Supplementary data are available at JXB online.
Table S1. Plant receptor-like kinases that control plant
growth and development and plant responses to stresses.
Acknowledgements
This work was supported by the RIKEN Strategic Research
Program for R & D (no. AP24-1-0076) of Japan to L-ST
and by the Program for Promotion of Basic and Applied
Researches for Innovations in Bio-oriented Industry to YO,
KY-S, and KS.
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