Download ABA control of plant macroelement membrane transport systems in

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ABA control of plant macroelement membrane
transport systems in response to water deficit
and high salinity
Authors for correspondence:
Yuriko Osakabe
Tel: +81 29 836 4359
Email: [email protected]
Lam-Son Phan Tran
Tel: +81 45 503 9593
Email: [email protected]
Yuriko Osakabe1, Kazuko Yamaguchi-Shinozaki2, Kazuo Shinozaki1 and
Lam-Son Phan Tran3
1
Gene Discovery Research Group, RIKEN Center for Sustainable Resource Science, 3-1-1 Kouyadai, Tsukuba, Ibaraki 305-0074,
Japan; 2Graduate School of Agricultural and Life Sciences, University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan;
3
Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi, Yokohama
230-0045, Japan
Received: 11 September 2013
Accepted: 21 October 2013
Contents
IV.
The involvement of ion transport systems in the
maintenance of ion homeostasis during abiotic stress
42
V.
Conclusion
44
36
Acknowledgements
44
39
References
45
Summary
35
I.
Introduction
35
II.
Water deficit stress stimulates ABA biosynthesis
and transport
III.
ABA signal transductions control ion transport for
modulating stomatal aperture
Summary
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doi: 10.1111/nph.12613
Key words: abiotic stress, abscisic acid (ABA),
ion channel, phosphorylation, stomata,
transporter.
Plant growth and productivity are adversely affected by various abiotic stressors and plants
develop a wide range of adaptive mechanisms to cope with these adverse conditions, including
adjustment of growth and development brought about by changes in stomatal activity.
Membrane ion transport systems are involved in the maintenance of cellular homeostasis during
exposure to stress and ion transport activity is regulated by phosphorylation/dephosphorylation
networks that respond to stress conditions. The phytohormone abscisic acid (ABA), which is
produced rapidly in response to drought and salinity stress, plays a critical role in the regulation of
stress responses and induces a series of signaling cascades. ABA signaling involves an ABA receptor
complex, consisting of an ABA receptor family, phosphatases and kinases: these proteins play a
central role in regulating a variety of diverse responses to drought stress, including the activities of
membrane-localized factors, such as ion transporters. In this review, recent research on signal
transduction networks that regulate the function ofmembrane transport systems in response to
stress, especially water deficit and high salinity, is summarized and discussed. The signal
transduction networks covered in this review have central roles in mitigating the effect of stress by
maintaining plant homeostasis through the control of membrane transport systems.
I. Introduction
Plants sense environmental conditions and adjust their growth and
development accordingly through a wide range of physiological,
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biochemical and molecular responses that enable the plant to
survive and reproduce. Understanding how plants sense their
environment and adapt to adverse conditions is essential for
ensuring adequate and sustainable agricultural production under
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36 Review
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the conditions predicted as a result of global climate change –
elevated temperatures and increased drought. A considerable
amount of research in the past 20 yr has focused on elucidating the
various mechanisms plants have evolved to cope with unfavorable
environmental conditions (Wang et al., 2003; Vinocur & Altman,
2005; Tran & Mochida, 2010; Hadiarto & Tran, 2011). These
mechanisms are initiated and sustained by complex processes
controlled by signal transduction pathways activated by environmental stimuli (Tran et al., 2007, 2010a; Hirayama & Shinozaki,
2010; Osakabe et al., 2011, 2013b; Fujii & Zhu, 2012). The
signaling events regulating plant adaptation and survival in
response to environmental stresses have been extensively studied
(Shinozaki & Yamaguchi-Shinozaki, 2007; Munns & Tester,
2008; Tran et al., 2010a,b; Choudhary et al., 2012; Ha et al., 2012;
Jogaiah et al., 2013; Nishiyama et al., 2013).
Water deficit stress or drought stress, an abiotic stress commonly
encountered by plants, is detrimental to plant growth and
development, and thus plant productivity, by adversely affecting
plant photosynthesis. Drought stress tolerance and water use
efficiency (WUE) are important criteria for evaluating the quality
of and economic utility of new germplasm. Response to water
deficit stress is regulated by a highly orchestrated, complex signaling
network that is capable of cross-talk with many other signaling
pathways (Mittler, 2006; Ahuja et al., 2010). Water deficit stress
affects various cellular and molecular events, including stomatal
response, shifts in metabolism and the expression of a variety of
stress-responsive genes (Yamaguchi-Shinozaki & Shinozaki, 2006;
Urano et al., 2010; Thao & Tran, 2012; Jogaiah et al., 2013). In
sessile plants, membrane transport and perception systems have
essential roles in maintaining cellular homeostasis under adverse
environmental stresses, which involves the cell-to-cell and/or
organ-to-organ communication during a plant’s life (Fig. 1)
(Amtmann & Blatt, 2009; Hedrich, 2012; Osakabe et al., 2013b).
In response to low soil water potential, plants have evolved
several mechanisms to regulate NaCl accumulation using various
membrane transport systems (Fig. 1b) (Munns & Tester, 2008). In
Arabidopsis, the Na+/H+ antiporter Salt Overly Sensitive 1 (SOS1)
that functions in Na+ efflux from root cells and long-distance
transport from roots to shoots (Wu et al., 1996; Shi et al., 2002),
and the HKT1 transporter that functions in Na+ uptake in root
tissues (Uozumi et al., 2000; Rus et al., 2001) play important roles
in regulating Na+ accumulation in roots and shoots by unloading
Na+ from xylem cells to eliminate excessive accumulation of Na+ in
roots and shoots (Hauser & Horie, 2010).
It has been well established that the ABA signaling pathway
affects plant adaptation to stress by controlling the internal water
status in plants (Cutler et al., 2010; Raghavendra et al., 2010;
Hauser et al., 2011; Joshi-Saha et al., 2011; Fujii & Zhu, 2012). A
significant accumulation of ABA occurs in response to water deficit
stress and the increased ABA content in leaves induces stomatal
closure that decreases the rate of gas exchanges and thus results in
reduced photosynthetic activity. An increase in endogenous ABA
content also induces the expression of a number of stress-related
genes in plants (Hirayama & Shinozaki, 2007). Three types of ABA
transport systems, among which two members belong to the ATPbinding cassette transporter (ABCG25, ABCG40) family (Kang
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et al., 2010; Kuromori et al., 2010), and one member (AIT1/
NRT1.2/NPF4.6) to nitrate transporter family (Kanno et al.,
2012), have recently been identified. These transporters are
involved in ABA efflux and influx transport systems with tissuespecific expression. The efflux transporter ABCG25 is expressed
mainly in vascular tissues, while the ABACG40 and AIT1/NRT1.2/
NPF4.6 importers, are in guard cells and vascular tissues,
respectively (Boursiac et al., 2013). The ABA influx transporters
located in the plasma membrane are involved in a cytosolic ABAsignaling pathway by intracellular transportation of ABA (Boursiac
et al., 2013). When ABA is transported into cytosol, the basic core
of ABA signaling that involves an ABA receptor complex,
consisting of an ABA receptor family (PYR/PYL/RCAR), protein
phosphatases (PP2Cs) and Snf1-related protein kinase 2s
(SnRK2s), induces a variety of molecular events in the plant cells
(Cutler et al., 2010; Hubbard et al., 2010; Weiner et al., 2010;
Coello et al., 2011, 2012). The PYR/PYL/RCAR receptors bind to
ABA in response to drought stress and are thus activated (Weiner
et al., 2010; Joshi-Saha et al., 2011). The activation of the ABA
receptors leads to the inactivation of PP2Cs that interact with the
receptors, allowing the SnRK2s to phosphorylate target proteins,
such as the S-type slow anion channel, SLAC1, that controls
stomatal response (Geiger et al., 2009; Lee et al., 2009; Hubbard
et al., 2010; Lee & Luan, 2012). Leucine zipper (bZIP) transcription factors are also target proteins of SnRK2s and involved in
inducing downstream ABA-responsive gene expression (Yamaguchi-Shinozaki & Shinozaki, 2006; Cutler et al., 2010). These
studies indicate that the phosphorylation of target proteins by
SnRK2s acts as the molecular hub in ABA signaling in response to
water deficit stress. During drought stress, anions and cations, such
as Cl and K+, and water-transport systems in the plasma
membrane and tonoplast induce turgor pressure changes in guard
cells, which result in stomatal closure (Kim et al., 2010).
A number of recent studies have suggested that several channels/
transporters are also phosphorylation targets of the stress signaling
pathways that modify their activity, resulting in plant stress
tolerance (Fig. 1b) (Ho & Tsay, 2010; Kudla et al., 2010; BarbierBrygoo et al., 2011). In this review, the membrane transport
systems that maintain the plant tolerance to water-deficit and high
salinity stresses and the molecular mechanisms that regulate the
membrane transport systems in plant cells in response to the
stresses, including those implicated in the cell-to-cell and/or organto-organ communication and ion homeostasis, will be summarized. We will focus especially on the signaling networks associated
with abiotic stress responses mediated by ABA and the stress signals.
The phosphorylation/dephosphorylation cascades that control
membrane factors involved in plant stress signaling and that
maintain plant homeostasis in response to the environmental cues
will also be discussed throughout this review.
II. Water deficit stress stimulates ABA biosynthesis
and transport
It has been proposed that different types of endogenous signals act
as long-distance signals of drought stress from roots to shoots.
These include chemicals, such as phytohormones and pH,
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(a)
Fig. 1 Plant transport system and responses to
water deficit and high salinity stresses. (a)
Water deficit and salinity stresses decrease soil
water potential (w) and cause osmotic, ionic
and oxidative stresses. These stress signals
stimulate various downstream signaling
cascades and biochemical and physiological
processes in plants, including biosynthesis and
transport of plant hormones, such as abscisic
acid (ABA), triggering of signaling networks,
activation of membrane transport systems and
transcriptional activation of a number of
stress-responsive genes. These processes
control the plant cellular homoeostasis and
ability to survive under stress through the
activation of plant stress-responsive systems.
(b) The transport systems have important roles
as driving forces to switch on the flow to
enhance and accelerate the plant responses to
stress.
(b)
hydraulic and electrical signals (Schachtman & Goodger, 2008;
Perez-Alfocea et al., 2011; Christmann et al., 2013). The accumulation of the hormone ABA is a key response to water deficiency in
plants. During water deficit stress, ABA was suggested to act as a
long-distance signal between roots and shoots (Sauter et al., 2001;
Wilkinson & Davies, 2002; Jiang & Hartung, 2008). The first step
of ABA biosynthesis from carotenoids is rapidly induced in
response to the water deficit stress, in which the transcriptional
upregulation of the 9-cis-epoxycarotenoid dioxygenase 3 encoding
(NCED3) gene plays a key role. The Arabidopsis nced3 mutant
plants exhibit increased water loss and decreased drought tolerance
(Iuchi et al., 2001). Studies have indicated that the NCED3 gene
and its encoded protein are expressed and localized mainly in
vascular parenchyma of leaves (Cheng et al., 2002; Koiwai et al.,
2004; Endo et al., 2008). In addition, the recent studies suggested
that the ABA synthesized in shoots is postulated to represent the
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conversion of a long-distance hydraulic signal in xylem vessels
which induces stomatal closure in response to low soil water
potential (Fig. 1a) (Holbrook et al., 2002; Christmann et al., 2005,
2007, 2013). When water deficit stress was applied to roots, the
increased ABA content in the leaves resulted in reduced water status
in shoots (Christmann et al., 2005, 2007). Using grafted plants of
wild-type shoots and root stocks from wild-type or ABA-deficient
mutant aba2-1, Christmann et al. (2007) showed that the stomata
closing in both types of grafted plants responded similarly to water
deficit in the roots. Furthermore, when osmotic stress was applied
to roots without affecting the water status in shoots by providing
water directly to leaves during the stress, ABA contents and ABAdependent reporter in leaves were not changed (Christmann et al.,
2007). These studies suggested that ABA produced in leaves affects
mainly ABA signaling and stomatal closing in this organ and that
there appears to be no requirement for root–shoot delivery of ABA.
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ABA mainly produced in leaf vascular tissues in response to water
deficit stress is transported to guard cells where it induces stomatal
closure. ABA is supposed to be transported via passive diffusion
from a low to a high pH environment without the involvement of
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ABA transporters because ABA is a weak acid. ABA, however, can
also be transported by ABA transporters, particularly by the
members of the ABC subfamily G (Fig. 2a). Recently, two
membrane-localized ATP-binding cassette (ABC) transporter
(a)
(b)
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Fig. 2 Abscisic acid (ABA) transport system.
(a) Phylogenetic analysis of the subfamily G of
Arabidopsis ABC transporters (ABCG
subfamily) indicates that the ABCGs can be
classified into two groups. The WBC (white–
brown complex) is composed of one-half-size
ABC protein, possessing one transmembrane
domain (TMD) and one nucleotide binding
domain (NBD). The pleiotropic drug resistance
(PDR) complex is composed of full-size
(2 TMDs and 2 NBDs) ABC proteins. Several
ABC proteins have been reported to be
involved in the transport of hydrophobic
chemicals. 1, Kuromori et al. (2011b); 2,
Kuromori et al. (2011a); 3, Kuromori et al.
(2010); 4, Bird et al. (2007), Ukitsu et al.
(2007); 5, Panikashvili et al. (2011); 6,
McFarlane et al. (2010); 7, Kang et al. (2010);
8, Kretzschmar et al. (2012); 9, Xi et al.
(2012); 10, Alejandro et al. (2012). The amino
acid sequences of the Arabidopsis ABCGs
were aligned using ClustalW (Thompson
et al., 1994). Phylogenetic analysis based on
the neighbor-joining (NJ) method was
performed using the MEGA5 package
(Tamura et al., 2011). (b) In response to
dehydration stress, ABA is mainly synthesized
in leaf vascular tissue and then transported to
guard cells through the activity of ABA
transporters. The membrane-localized ATPbinding cassette (ABC) transporter ABCG25
localized in vascular tissues plays a role in ABA
export. The ABCG40 transporter found in
guard cells plays a role in the import of ABA.
AIT1/NRT1.2/NPF4.6 also has ABA importer
activity, implying that ABA uptake from the
site of ABA synthesis is important in regulating
stomatal closure.
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proteins, ABCG25 and ABCG40, have been identified as ABA
transporters in Arabidopsis by two independent studies (Kang
et al., 2010; Kuromori et al., 2010). Arabidopsis abcg25 and abcg40
mutant plants decreased the responses to ABA-induced dormancy
and stomatal closure (Kang et al., 2010; Kuromori et al., 2010).
The ABCG25 and ABCG40 transporters have been reported to
play a role in the export and import of ABA into plant cells,
respectively. The ABCG25gene is expressed mainly in vascular
tissues and is induced by ABA and drought stress (Kuromori et al.,
2010), whereas ABCG40 is expressed in guard cells (Kang et al.,
2010). These findings suggest an ABA transport model in leaves
where ABA is synthesized in vascular tissues in response to drought
stress. ABA is then transported outside of vascular cells by the
ABCG25 transporter and imported into leaf guard cells by the
ABCG40 transporter (Fig. 2b). Because the Arabidopsis ABAdeficit mutant plants display a more severe phenotype to drought
stress than abcg25 and abcg40 plants, additional transporters with
redundant functions might also be involved in the transport of
ABA. Alternatively, passive ABA transport by pH gradients may
play a major role (Seo & Koshiba, 2011).
More recently, NRT1.2/NPF4.6, which has been characterized
as a low-affinity nitrate transporter (Huang et al., 1999), was shown
to have ABA importer activity in Arabidopsis (Kanno et al., 2012).
Thus, it was renamed as ABA-IMPORTING TRANSPORTER 1
(AIT1) (Kanno et al., 2012). The authors used a modified yeast
two-hybrid screening system to isolate ABA transporters, where
Arabidopsis cDNAs were screened as components able to induce an
interaction between the ABA receptor PYR family members and
PP2Cs under a low concentration of ABA (Kanno et al., 2012).
ait1/nrt1.2/npf4.6 mutant showed decreased ABA response in seed
dormancy, reduced inhibition of post-germination growth and
decreased stomatal closure, whereas overexpression of AIT1
resulted in the enhanced response to ABA in transgenic Arabidopsis
plants. Additionally, the AIT1 gene was expressed mainly in
vascular tissues, the site of ABA biosynthesis. These results suggest
that AIT1 functions in the ABA transport from the vascular system
to other parts of the plant. Collectively, these findings indicate that
the function of AIT1 is to import ABA from the site of its synthesis
and that this function plays an important role in the regulation of
stomatal closure in response to water deficit stress.
Recently, cell-automonous ABA biosynthesis in guard cells has
been suggested to be required for the stomatal closure in response to
low humidity (Bauer et al., 2013). This system of ABA biosynthesis
may be required for rapid and adaptable responses in ABA signaling
to the low humidity stress. The different sites of ABA production in
plants, vasculature and stomata, may enable plants to control
properly osmotic adjustment and survivability to various modes of
stress.
III. ABA signal transductions control ion transport for
modulating stomatal aperture
Stomatal responses are coordinately regulated by macroelements
transported through various transport systems to efficiently control
the water status of plants. In response to water deficit, ABA is
accumulated in guard cells through its transport from the
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Review 39
biosynthesis sites (discussed in Water deficit stress stimulates
ABA biosynthesis and transport section), and induces a reduction
in their turgor and volume, resulting in stomatal closure
(MacRobbie, 1998; Hu et al., 2010) (Fig. 3). In the early phase
of stomatal closing, it has been shown that ABA induces reactive
oxygen species (ROS) production via NADPH oxidases, such as
respiratory burst oxidase homologs from Arabidopsis, AtRBOHD
and AtRBOHF (Kwak et al., 2003). The double mutant atrbohd/f
generated lower ABA-induced ROS and impaired the ABAactivated Ca2+ channels and stomatal closure, while the exogenous
application of H2O2 rescued these responses (Kwak et al., 2003),
suggesting that ROS acts as a second messenger in ABA signaling of
stomatal response (Wang & Song, 2008). ABA-induced ROS
triggers an increase in the concentration of cytoplasmic Ca2+
([Ca2+]cyt) that then activates two distinct types of anion channels:
a slow-activating sustained type (S-type) and a rapid-transient type
(R-type) (Kim et al., 2010). Anion efflux through these channels
induces membrane depolarization and leads to inhibition of inward
K+ channels (KAT1/KAT2) that control cell turgor during
stomatal opening.
Plasma membrane H+-ATPase plays the important roles in
creating electrical potential across the membrane (Shimazaki et al.,
2007). It has been shown that H+-ATPase is activated by blue light
Fig. 3 The signaling pathway and ion transport system involved in stomatal
closure. In response to dehydration stress, cytosolic abscisic acid (ABA),
imported via ABCG40, binds to the PYR/PYL receptor and forms a receptor
complex with PP2Cs, which acts as a negative regulator in the ABA signaling
pathway by inhibiting SRK2E/OST1 kinase activity. ABA-binding to the
receptor complex induces the dissociation of PP2Cs from SRK2E/OST1. The
activated SRK2E/OST1 then inhibits KAT1 and phosphorylates and activates
NADPH oxidase to produce H2O2 that acts as a second messenger to
promote Ca2+ release. Moreover, SRK2E/OST1 and CPK phosphorylate and
activate S-type anion channels, such as SLAC1 that triggers membrane
depolarization and induces the activation of the K+ outward rectifying
channel (GORK). KUP6 is also phosphorylated by SRK2E/OST1 and possibly
functions in K+ efflux. These ion transport activities regulate stomatal closure
in response to dehydration stress. MD, membrane depolarization.
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signal through the phosphorylation of its C-terminus (Shimazaki
et al., 1986). The activated H+-ATPase induces negative electric
potential gradient inside the plasma membrane. This in turn causes
a hyperpolarization of the plasma membrane and a subsequent
opening of voltage-regulated inward K+ channels, resulting in
stomatal opening (Shimazaki et al., 2007). During water deficit
stress, ABA inhibits the H+-ATPase activity by reducing the H+ATPase phosphorylation level, and this is important to maintain
membrane depolarization (Zhang et al., 2004; Hayashi et al.,
2011). The ost2-1 and ost2-2 dominant mutants of ARABIDOPSIS
H+ATPASE 1/OPEN STOMATA 2 (AHA1/OST2) exhibit constitutive H+-ATPase activity and impaired ABA-induced stomatal
closure, suggesting that the inhibition of H+-ATPase activity is one
of the important processes that control stomatal closing (Merlot
et al., 2007). On the other hand, during stress the anion-effluxinduced membrane depolarization activates outward K+ channels,
such as the GUARD CELL OUTWARD RECTIFYING K+
CHANNEL (GORK), making them open, resulting in stomatal
closure (Ache et al., 2000).
Recent studies at a molecular level have provided strong lines of
evidence on the central roles of ABA signaling system in the control
of channels in stomata closing. The phosphorylation of the
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C-terminal domain of KAT1 by SRK2E inhibits the KAT1 activity
(Sato et al., 2009), suggesting that the direct negative regulation of
KAT1 by SRK2E/OST1/SnRK2.6 can enhance the adaptative
responses to water-deficit stress (Sato et al., 2009) (Fig. 4a). It has
also been reported that the inhibition of Kin channel activity
responds to Ca2+, too, suggesting that the SRK2E calciumdependent kinases may function in KAT1 phosphorylation as well
(Li et al., 1998; Siegel et al., 2009). Moreover, selective endocytosis
of KAT1, which is stimulated by ABA and the recycling of KAT1
protein, suggested that another ABA-mediated mechanism controls the subcellular dynamics of K+ channel at plasma membrane
(Sutter et al., 2007). The controls of the Kin channel activity have
been shown to affect stomatal responses to various environmental
conditions. Kincless, a double mutant of the KAT2 gene disruption
and a dominant negative kat2, lacked Kin channel activity in guard
cells and stomatal opening for appropriate responding to changes in
various environmental conditions (Lebaudy et al., 2008b).
SLOW ANION CHANNEL-ASSOCIATED 1 (SLAC1) gene,
which was identified by screening Arabidopsis plants for ozonesensitive or CO2-insensitive mutants, is involved in anion efflux
guard cells (Negi et al., 2008; Vahisalu et al., 2008) (Fig. 3). SLAC1
has a structure similar to bacterial dicarboxylate/malate
(a)
(b)
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Fig. 4 Membrane ion transport systems
controlled by protein kinases during osmotic
stress. (a) Abscisic acid (ABA) signal
transduction, regulated by phosphorylation/
dephosphorylation, controls the anion and
potassium transport system in guard cells.
Both N-terminal and C-terminal portions of
the SLAC1 anion channel protein have been
identified as target sites for phosphorylation
(Geiger et al., 2009; Lee et al., 2009; Vahisalu
et al., 2010). The C-terminal region of KUP6 is
phosphorylated by SRK2E/OST1, implying
that this process might be involved in the
activation of KUP6 transport system.
Phosphorylation of an amino acid residue in
the C-terminal portion of KAT1 by SRK2E/
OST1 induces inactivation of the transporter.
(b) Na+ signaling system, composed of SOS2
and SOS3, controls a sodium/proton
antiporter, the SOS1. SOS3, a myristoylated
calcineurin B-like protein (CBL), plays a role in
sensing cytosolic Ca2+ under high salt stress,
and forms a signaling complex with the protein
kinase SOS2. The SOS2–SOS3 complex
phosphorylates the C-terminal portion of
SOS1 and controls its activity in response to
high salinity.
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transporters (Negi et al., 2008; Vahisalu et al., 2008). Using a
Xenopus oocyte system SLAC1 was shown to have anion channel
activity (Geiger et al., 2009; Lee et al., 2009). slac1 mutant plants
exhibited impaired stomatal closure in response to ABA, CO2, Ca2+
and ozone treatments. In addition, guard cells in the slac1 mutant
had impaired Ca2+ and ABA activation of S-type anion channels.
These findings suggested that SLAC1 is a major S-type anion
channel in guard cells (Vahisalu et al., 2008). Recently, direct
activation of S-type anion channels by ABA signaling has been
reported (Geiger et al., 2009; Lee et al., 2009) (Figs 3, 4a). SLAC1
is directly activated by SRK2E/OST1/SnRK2.6 that is involved in
core ABA signaling together with ABA receptor PYR family
members and PP2Cs (Geiger et al., 2009; Lee et al., 2009). SLAC1
is also regulated by the calcium-dependent protein kinases (CDPK/
CPK) CPK21 and CPK23 (Geiger et al., 2010) (Fig. 3). Both
kinases target the N-terminal domain of SLAC1 as a phosphorylation site. Recently, other CDPK members – namely CPK3 and
CPK6 – were also shown to activate SLAC1 by phosphorylation
(Brandt et al., 2012; Scherzer et al., 2012). Additionally, the double
knockout cpk3cpk6 mutant plants were reported to exhibit
decreased ABA-induced activation of Ca2+ channels and ABA/
Ca2+-induced activation of S-type anion channels, as well as
decreased stomatal closure (Mori et al., 2006). SLAH3, which is a
homologous protein for SLAC1 and functions in guard cells as the
S-type anion channel, was also shown to be stimulated by CPK3, 6,
21 and 23 (Geiger et al., 2011; Dreyer et al., 2012). These findings
demonstrate that various key signaling regulators control the
function of SLAC family proteins. Recently, ALMT12/QUAC1
(QUick Anion Channel 1), a member of the aluminum-activated
malate transporter (ALMT) family, has been characterized as a
malate-induced R-type anion channel in guard cells to control
stomatal responses (Meyer et al., 2010; Sasaki et al., 2010).
Additionally, the physical interaction between ALMT12/QUAC1
and SRK2E/OST1 was detected in oocytes by biomolecular
fluorescence complementation (BiFC), suggesting that ALMT12/
QUAC1 might be activated by SRK2E/OST1 (Imes et al., 2013).
These findings provide evidence that both S-type and R-type anion
channels are tightly controlled by the ABA core-signaling factors.
The ABC proteins AtMRP4 and 5 (MULTIDRUG RESISTANCE PROTEIN 5) are also involved in regulation of stomatal
responses (Gaedeke et al., 2001; Klein et al., 2003). It has been
reported that AtMRP4 and AtMRP5 have opposite roles in
stomatal opening and atmrp5 mutant plants exhibited decreased
responses to ABA-mediated stomatal closing (Gaedeke et al., 2001;
Klein et al., 2003). Although the biochemical characteristics of
AtMRP4 and 5 substrates have not been elucidated yet, it was
speculated that AtMRP5 functions as a membrane regulator of
several ion channels because it has roles in the regulation of anion
and Ca2+ channels at the plasma membrane of guard cells (Rea,
2007; Suh et al., 2007).
The guard cell vacuole plays important roles as an ion pool and
contributes to stomata responses. Compared to potassium and
chloride fluxes at the plasma membrane, these ion fluxes across the
vacuolar membrane during stomata responses have not been
elucidated well at the molecular level. A recent study showed that a
member of the chloride channel (CLC) family, the AtCLCc that is
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localized in the tonoplast and mainly expressed in guard cells and
roots, has a role in the anion fluxes that control stomatal movements
and high salinity tolerance in Arabidopsis (Jossier et al., 2010).
Additional electrophysiological experiments might characterize the
anion transport mechanisms mediated by the AtCLCc in these
physiological processes. More recently, AtALMT9, which acts as a
malate-induced chloride channel at the tonoplast, has been
identified in stomata opening (De Angeli et al., 2013). Identification of the molecular mechanisms involved in the inactivation of
AtALMT9 during water deficit stress, for example the presence of
an inactivation mechanism by ABA signaling, would be an
interesting objective for future research.
K+ is not only a macroelement with vital roles in plant growth
and development, but also a key player in the maintainance of
osmotic adjustment and cell turgor. In stomatal responses, the
outward shaker K+ channel GORK mediates K+ efflux from guard
cells and both anion and K+ effluxes induce a loss of guard cell
turgor, leading to stomatal closure (Fig. 3). GORK is expressed in
the guard cells and root epidermis. The GORK transcription is
highly upregulated by ABA and osmotic stress treatments (Becker
et al., 2003; Osakabe et al., 2013a). ABA responsiveness of GORK
expression was impaired in ABA INSENSITIVE 1 (abi1) and abi2
that encode PP2Cs, the core factors involved in the ABA perception
(Becker et al., 2003), indicating that GORK expression is regulated
by the ABA signaling pathway at the transcriptional level. In
agreement with this observation, the GORK promoter contains the
cis-acting ABA-RESPONSIVE ELEMENT (ABRE) ABRE that
together with several members of the basic leucine zipper (bZIP)
transcription factor family control the transcription of ABA/
stress-responsive genes in addition to the ABA-independent
DEHYDRATION-RESPONSIVE ELEMENT (DRE) cis-acting
sequence of the DREB-type transcription factors (YamaguchiShinozaki & Shinozaki, 2006) (Table 1). The GORK transcription
is also dependent on extracellular Ca2+ (Becker et al., 2003). The
loss-of-function of GORK results in defects in K+ efflux in guard
cells and causes lower rates of stomatal closure in comparison with
the wild-type plants (Hosy et al., 2003). The studies of the gork-1
mutant suggested the possibility that other K+ efflux systems are
involved in stomatal closing (Hosy et al., 2003). Recently, it has
been reported that a stress-responsive KUP/HAK/KT family
potassium transporter, KUP6, and its homologs (KUP8 and
KUP2/SHY3), from Arabidopsis are involved in water deficit stress
responses (Osakabe et al., 2013a) (Figs 3, 4a). The triple kup268
mutant and the combined double kup and ABA-responsive
potassium channel gork mutant (kup68gork) exhibited increased
sensitivity to drought stress (Osakabe et al., 2013a). The kup68gork
displayed impaired ABA-mediated stomatal closing, suggesting
that KUP6 and KUP8 may be involved in K+ efflux transport and
redundantly function with GORK in the stomatal responses
mediated by ABA signaling (Osakabe et al., 2013a). Furthermore,
kup268 exhibited enhanced lateral root formation. Because auxin
signaling is required for lateral root formation, the findings
suggested that these KUP family members function in an
antagonistic cross-talk pathway mediated by auxin and ABA. In
sum, the study by Osakabe et al. (2013a) indicated the regulation of
growth and water deficit stress responses by the KUP family in
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42 Review
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Table 1 Putative cis-regulatory sequences in the stress-responsive transporter gene promoters
Gene
ABRE (C/TACGTGG/T)
Nucleotide sequence
GORK
KUP6
830 ..
2130 ..
835a ( )b
2136 ( )
acgtgt
cacgtgg
ABCG25
SOS1
AtHKT1;1
1834 ..
111 ..
71 ..
277 ..
2307 ..
3060 ..
1840 ( )
117 ( )
77
283 ( )
2314 (+, )
3066 (+)
tacgtgt
cacgtgt
tacgtgt
cacgtgg
acacgtgt
cacgtgt
a
DRE/CRT (A/GCCGAC)
Nucleotide sequence
778.. 783 ( )
1814.. 1819 ( )
2254.. 2259 ( )
gtcggc
gccgac
gccgac
217.. 117 ( )
13.. 18 (+)
gccgac
accgac
position of cis-element upstream from +1 transcription start site.
(+) and ( ) indicate the DNA plus and minus strands, respectively.
b
Arabidopsis. Furthermore, KUP6 was shown to physically interact
with SRK2E and the phosphorylation site of SRK2E was identified
in the KUP6 C-terminal domain (Osakabe et al., 2013a). The data
indicate that KUP6 represents a newly discovered SnRK2 substrate,
whose function is directly regulated by the ABA signaling complex
(Osakabe et al., 2013a) (Fig. 4a). These findings also suggest that
mechanisms directly controlling ion transport systems via the core
ABA signaling complex play an important role in enhancing the
KUP transport system that controls water deficit stress responses.
K+ channel/transporters localized in the tonoplast were also
shown to be involved in stomatal closure via K+ release from
vacuoles (Ward & Schroeder, 1994). TWO PORE K+ CHANNEL
1 (TPK1) mediates vacuolar K+ tonoplast channel currents in guard
cells, and a mutation in tpk1 resulted in a decrease in ABA-induced
stomatal closure (Gobert et al., 2007). More recently, Na+/H+
exchangers, namely the NHX1 and NHX2, have been identified as
being involved in K+ uptake at the tonoplast for stomatal function
and turgor regulation (Barragan et al., 2012). One member of the
cation-H+ exchanger (CHX) family of transporters that control pH
and cation homeostasis in plant cells, the CHX20, which is
localized in the endomembrane of Arabidopsis mesophyll protoplasts, has been shown to be involved in K+ transport, turgor
regulation and stomatal responses (Padmanaban et al., 2007).
These transport systems coordinately regulate stomatal movement
in response to environmental stresses in plants.
IV. The involvement of ion transport systems in the
maintenance of ion homeostasis during abiotic stress
The control of ion flux, including ion uptake, efflux and
compartmentation, in maintaining an appropriate level of ion
homeostasis is one of the important mechanisms which plants use
to enhance their adaptation to osmotic stresses, particularly high
salinity stress. Plant cells use various ion transport systems,
controlled by several signal transduction pathways, to avoid Na+
toxicity (Munns & Tester, 2008). Thus, the specific functions of
these transport systems in maintaining the ion homeostasis balance
between tissues and cells warrant deeper discussion. Because a high
Na+/K+ ratio causes ion toxicity under high salinity stress, the
maintenance of Na+/K+ homeostasis is important for plants to
adapt to and tolerate high salinity stress (Zhu et al., 1998; Maathuis
& Amtmann, 1999). The NHX family plays a major role in the
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maintenance of an appropriate pH and K+ concentrations to help
mitigate the adverse effect of high salinity, thus enabling plants to
adapt to salt stress. The NHX family belongs to the monovalent
cation-proton antiporter (CPA) superfamily, which includes the
NHX, K+ efflux family (KEA), and CHX family of transporters that
control pH and cation homeostasis in plant cells (Sze et al., 2004;
Manohar et al., 2011; Chanroj et al., 2012). Salt Overly Sensitive 1
(SOS1)/NHX7, a member of the Na+/H+ antiporter (NHX)
family, was identified by screening Arabidopsis mutants for salt
sensitivity. SOS1 is localized at the plasma membrane and has an
important role in high Na+ tolerance by regulating Na+ extrusion. It
is involved in Na+ efflux from cytosol to the surrounding medium
across the plasma membrane to maintain a low concentration of
Na+ (Wu et al., 1996; Shi et al., 2002). SOS1 is controlled by the
Na+ signaling system composed of SOS2 and SOS3 (Qiu et al.,
2002; Zhu, 2003) (Fig. 4b). The SOS3 gene encodes a myristoylated calcium-binding protein that functions in the sensing of
cytosolic Ca2+ in cells under salt stress. SOS2 encodes a SnRK3
protein kinase that together with SOS3 forms a signaling complex
to phosphorylate and control SOS1 function in response to high
salinity. SOS1 possesses a long cytosolic-oriented C-terminal
domain (c. 700 amino acids) that can interact with and phosphorylated by SOS2. When its binding to cytosolic Ca2+ is induced by
high Na+, SOS3 is able to interact with and activate SOS2, and the
SOS2–SOS3 complex recruits SOS2 to the plasma membrane to
phosphorylate and activate SOS1 (Qiu et al., 2002; Quintero et al.,
2002). The post-translational modification of the cytosolic regions
of transporter/channel proteins is one of the important mechanisms in the control of their functions. The phosphorylation of the
cytosolic regions of the transporter/channels as mentioned above is
directed by the signaling cascade in response to stress signals and
causes the conformational changes of the transporter/channel
proteins, thereby initiating their activity. In the SOS1 phosphorylation by SOS2 kinase, two serine residues (S1136 and S1138) in the
C-terminal RIDSPSK motif (S1138 underlined) of SOS1 have been
shown to be essential for the SOS1 activation. S1138 is phosphorylated by SOS2, whereas S1136 is essential for substrate recognition
by the SOS2 protein kinase (Quintero et al., 2011) (Fig. 4b). In
another independent study, the C-terminal of SOS1 was also
shown to be phosphorylated by the MAP kinase MPK6 that is
activated by NaCl-induced phosphatidic acid (Yu et al., 2010). The
SOS1 C-terminal contained the target sites of two kinases,
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suggesting that two different types of signaling pathways regulate
SOS1 activity. The SOS3-like SCaBP8 (CBL10) has also been
identified to interact with SOS2 to form a complex and regulate
SOS1 activity in the plasma membrane of the shoots (Quan et al.,
2007; Lin et al., 2009). Recently, GIGANTEA (GI) that functions
in the photoperiod-dependent flowering and circadian clock switch
has been shown to interact with the SOS pathway (Kim et al.,
2013). GI physically interacts with SOS2 to inhibit the activation
of SOS1 in the absence of stress, and thus GI functions as a negative
regulator of the SOS pathway (Kim et al., 2013). Under stress, GI is
degraded and free SOS2 forms a protein complex with SOS1 and
SOS3 to activate the SOS1, suggesting that there is a salt stress
signaling pathway controlling the GI protein stability. Additionally, RCD1 (RADICAL-INDUCED CELL DEATH) identified
as an important regulator of oxidative stress response (KatiyarAgarwal et al., 2006; Quintero et al., 2011) was reported to interact
with SOS1, indicating that the increased sensitivity of Arabidopsis
sos1 mutant plants to oxidative stresses might be mediated by
RCD1 (Katiyar-Agarwal et al., 2006).
A significant number of studies also reported the functions of
other Arabidopsis NHX family members, namely the NHX1–6
and 8 that are localized in intracellular and plasma membranes,
respectively, in catalyzing cation (K+, Na+ or Li+)/proton exchange
(Shi et al., 2002; Yokoi et al., 2002; An et al., 2007; Bassil et al.,
2011; Chanroj et al., 2012). For example, the intracellular Na+/K+
antiporters NHX5 and 6 play important roles in cellular Na+/K+
homeostasis and pH balance as the nhx56 double knockout mutant
showed an increased sensitivity to high salinity stress (Bassil et al.,
2011). The nhx56 mutant plants exhibited decreased leaf cell size
and cell number, resulting in the small plant body under normal
growth conditions.
The long-distance transport of ions through plant tissues has
important roles in the maintenance of ion homeostasis in plant
body. In plants, the vascular tissues play the main roles in the longdistance transport of the substances between organs and tissues.
The vascular tissue-expressed K+ channels, such as Stelar K+
Outward Rectifier (SKOR), AKT2 and KAT2, are known to be
implicated in K+ homeostasis. The K+ outward rectifying channel
SKOR is expressed in pericycle and xylem parenchyma cells in
Arabidopsis (Gaymard et al., 1998). Because the knockout mutant
of skor showed the low K+ content in both shoots and xylem sap,
SKOR is likely involved in K+ release into xylem sap and K+
translocation toward to the shoot (Gaymard et al., 1998). On the
other hand, AKT2 and KAT2 encoding two K+ inward-rectifying
channels have been shown to be expressed in phloem tissues
(Marten et al., 1999; Pilot et al., 2001; Xicluna et al., 2007;
Lebaudy et al., 2010). AKT2 is expressed in phloem of both roots
and shoots. Loss-of-function of AKT2 exhibited a reduced reuptake
of photoassimilates leaked from the phloem (Deeken et al., 2002),
suggesting that AKT2 is involved in controlling K+ uploading in
sources and K+ unloading in sinks (Marten et al., 1999; Lacombe
et al., 2000; Gajdanowicz et al., 2011). KAT2 is expressed mainly in
leaves and its expression patterns might provide a hint that KAT2
was involved in K+ loading in sources (Pilot et al., 2001; Lebaudy
et al., 2010). Furthermore, it was suggested that the heterotetrameric structure of inward Shaker K+ channels (AKT1, AKT2,
Ó 2013 The Authors
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Review 43
KAT1, KAT2 and AtKC1) could contribute to the regulation of K+
channel activity (Xicluna et al., 2007; Lebaudy et al., 2008a, 2010;
Jeanguenin et al., 2011), indicating that the hetrodimerization of
the K+ channels in vascular tissues might affect the long-distance K+
transport required to maintain plant growth. During dehydration
and high salinity stresses, ABA stimulates the induction of AKT2
expression (Marten et al., 1999; Lacombe et al., 2000; Deeken
et al., 2002), whereas decreases SKOR expression (Gaymard et al.,
1998). Additionally, the interaction of PP2CA and the AKT2 was
evidenced (Cherel et al., 2002), which might link ABA signaling to
the control of AKT2 phosphorylation status during the stress.
Under high salinity stress, AtHKT1, a vascular specific transporter, has an essential role in the tolerance of the plants (Kato et al.,
2001; Rus et al., 2001). AtHKT1 is a plasma membrane-localized
sodium ion transporter and is encoded in the Arabidopsis genome
by a single copy of an HKT/Ktr/Trk gene that is expressed in
vascular tissues (Kato et al., 2001; Rus et al., 2001). Under salt
stress, hkt1-1 mutant plants showed a decrease in Na+ concentration in the phloem sap and displayed a NaCl-sensitive phenotype
resulting from Na+ overaccumulation in shoots (Berthomieu et al.,
2003). AtHKT1 function putatively involves the extraction of Na+
from xylem vessels, thereby mitigating salt stress, suggesting that
AtHKT1 controls root/shoot Na+ translocation and leaf Na+
accumulation (Sunarpi et al., 2005; Horie et al., 2007; Moller et al.,
2009). Natural variants of AtHKT1 were reported to enhance Na+
accumulation in two wild populations of Arabidopsis (Rus et al.,
2006; Baxter et al., 2010). Natural variation in the HKT1 gene has
also been identified in crop plants (Rus et al., 2006; Munns et al.,
2012). The improved productivity of a commercial durum wheat
cultivar grown on saline soils was shown to be due to Nax2, the
ancestral Na+ transporter gene encoding a HKT1 (TmHKT1;5-A).
Nax2 was identified in the wheat relative, Triticum monococcum,
and introduced into the commercial durum wheat (Munns et al.,
2012). TmHKT1;5-A is located on the plasma membrane of root
cells surrounding xylem vessels, and putatively functions in
extracting Na+ from the xylem and reducing Na+ transport from
roots to leaves (Munns et al., 2012). TaHKT2;1, another type of
the HKT family from wheat Triticum aestivum L., was reported to
have a role in Na+ and K+ co-transport and the knockout of this
gene enhanced high NaCl tolerance (Schachtman & Schroeder,
1994; Laurie et al., 2002). This type of HKTs functions in K+
transport under high NaCl stress, especially in the holophytic
plants that have a stronger selectivity for K+ than Na+ (Liu et al.,
2001; Ardie et al., 2009; Ali et al., 2012). For instance, TsHKT1;2
from a model halophyte (Thellungiella salsuginea), EcHKT1;2
from Eucalyptus camaldulensis, and PutHKT2;1 from Puccinellia
tenuiflora were shown to mediate K+ transport in the presence of
NaCl (Liu et al., 2001; Ardie et al., 2009; Ali et al., 2012). These
studies suggested that the halophytes have an ability to adapt to high
NaCl stress by maintaining K+/Na+ balance through the function
of these HKT transporters.
In addition, with regard to the transcriptional regulation of Na+
transporters, such as the SOS1 and AtHKT1, not only is the tissuespecific expression crucial, but also the responsiveness to high
salinity stress is one of the most important mechanisms underlying
the function of these transporters under stress conditions (Shi et al.,
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44 Review
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2000; Jha et al., 2010). In roots, SOS1 is mainly expressed in the
epidermis at root tips and in the adjacent cells to vascular tissues
(Shi et al., 2002), and this specificity was retained under the high
salinity stress; that is, the salt stress-responsive induction of SOS1
was observed in the epidermal tissues (Dinneny et al., 2008). The
upregulation of SOS1 and AtHKT1 also dictates those traits
concerning salinity tolerance in natural variation of Arabidopsis.
For instance, SOS1 mRNA is accumulated greatly higher in the
salt-tolerant halophyte T. salsuginea than in Arabidopsis (Oh et al.,
2009). Furthermore, Rus et al. identified two coastal accessions of
Arabidopsis, Ts-1 and Tsu-1, which super-accumulated Na+ in
shoots. The causal locus of Na+ high accumulation was found to be
AtHKT1, whose expression levels were reduced in these accessions
(Rus et al., 2006). The authors also found that a deletion in the
AtHKT1 promoter region was responsible for the reduction of
AtHKT1 expression levels. The tandem repeats located in the c.
3.9 kb upstream of AtHKT1 strongly influence the AtHKT1
expression as an enhancer element, thereby playing an important
role in plant tolerance to high salinity stress (Rus et al., 2006; Baek
et al., 2011). We analyzed the cis-regulatory elements in the
promoter regions of these transporters to gain an insight into their
regulatory mechanisms (Table 1). Both SOS1 and AtHKT1 have
the ABRE and DRE elements in their promoter regions, suggesting
that they may also be the target genes of the bZIP- and AP2-type
transcription factors under stresses (Table 1). The finding of ABRE
suggests that expression of SOS1 and AtHKT1 might be under the
regulation of ABA signaling. However, several studies and the
public expression databases show that expression of both SOS1 and
AtHKT1 are not induced by ABA treatment (Shi et al., 2000). This
result would indicate that expression of these genes might be
regulated by an ABA-independent pathway, such as the DREDREB pathway (Yamaguchi-Shinozaki & Shinozaki, 2006), rather
than an ABA-dependent pathway. However, a recent study by
Shkolnik-Inbar et al. provided evidence for the involvement of the
ABA signaling pathway in regulation of AtHKT1 transcription.
The authors reported that the expression of the AtHKT1 gene was
upregulated in abi4 mutant plants of an AP2-type transcription
factor, the ABSCISIC ACID INSENSITIVE4 (ABI4) (ShkolnikInbar et al., 2013). In-depth studies are required to dissect this
regulatory mechanism and its physiological importance.
V. Conclusion
During stress, transport systems play important roles in maintaining physiological and biochemical balances between cells, tissues
and organs, enabling plants to adapt better to adverse conditions. In
the early phase of a stress period, transport systems may serve as a
driving force that switches on the flow to enhance and accelerate
plant responses (Fig. 1b). The stress-responsive expression patterns
and tissue specificities of genes encoding ion transporters and
channel proteins provide important information that can be used to
help determine their physiological functions in plant cells. Recent
transcriptomic studies have provided data indicating that many
transporter/channel encoding genes are expressed in specific tissue
or cells and/or induced by various environmental stimuli (Aleman
et al., 2011; Tsay et al., 2011; Wang et al., 2012; Boursiac et al.,
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2013). These genes encode proteins that form transport systems for
various compounds and ions, including phytohormones (Kuromori & Shinozaki, 2010), sugars (Rolland et al., 2006; Yamada
et al., 2010, 2011), amino acids (Tegeder, 2012), potassium
(Becker et al., 2003; Osakabe et al., 2013b; Wang & Wu, 2013),
iron (Walker & Connolly, 2008), nitrate (Wang et al., 2012),
boron (Miwa & Fujiwara, 2010), and silicon (Ma & Yamaji,
2006). Recent reports have also demonstrated that post-translational regulation of membrane transport systems plays a major role
in regulating transport activity in response to environmental cues
and/or adverse growth conditions (Li et al., 2006; Xu et al., 2006;
Lee et al., 2007, 2009; Geiger et al., 2009, 2010; Sato et al., 2009;
Osakabe et al., 2013b). Post-translational regulation of transport
activity involves the phosphorylation/dephosphorylation of potassium transporter/channel proteins by members of the CDPKSnRK superfamily of protein kinases. The extended intracellular,
cytosolic-oriented portions of the transporter/channels have been
shown to have regulatory domains and targets for phosphorylation
by kinases. The membrane protein dynamics also affect their
functions; thus several membrane proteins, such as KAT1 (Sutter
et al., 2007) and BOR1 (Takano et al., 2010), which function at the
appropriate membrane sites, are inactivated and/or downregulated
by the membrane dynamics. Further studies, such as the in-depth
characterization of these post-translational modifications and
regulation of proteins and protein degradation, need to be carried
out in order to gain a comprehensive understanding of the
molecular functions of transporter systems in plants. A systems
biology evaluation of gene transcriptional control, and genome
modification and evolution, not only helps to develop a more
complete understanding to the structure of transport systems, but
also creates essential avenues of future research. The selection and
investigation of natural variations, including those of crop species,
under conditions close to natural field conditions in terms of soil
water and nutrient contents, will also improve our understanding of
key responses in actual conditions. Recently this approach has been
used to identify the correlation between the activity of molybdenum transporter MOT1 in natural accessions of Arabidopsis and
the molybdenum availability in native soil (Poormohammad Kiani
et al., 2012). There are myriad types of soil conditions over the
world, such as acidic and salty soils, and the improvement of
membrane transport systems could be used to enhance the crop
quality and yields under these adverse conditions (Schroeder et al.,
2013). It has been recently reported that genome editing is also a
potentially powerful tool to improve crops (Osakabe et al., 2010;
Zhang et al., 2010; Voytas, 2013). These approaches together will
require a concerted effort from the research community if the
significant improvement in plant stress tolerance and adaptability
required to address the potential impact of global climate change on
productivity is to be achieved.
The genes discussed in this review are listed in Supporting
Information Table S1.
Acknowledgements
This work was supported by the Program for Promotion of Basic
and Applied Researches for Innovations in the Bio-Oriented
Ó 2013 The Authors
New Phytologist Ó 2013 New Phytologist Trust
New
Phytologist
Industry of Japan (Y.O., K.Y-S., and K.S.). Research in L-S.P.T.’s
laboratory is supported by a Grant (no. AP24-1-0076) from
RIKEN Strategic Research Program for R&D.
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Supporting Information
Additional supporting information may be found in the online
version of this article.
Table S1 Genes discussed in the review and their Arabidopsis
Genome Initiative (AGI) code
Please note: Wiley Blackwell are not responsible for the content or
functionality of any supporting information supplied by the
authors. Any queries (other than missing material) should be
directed to the New Phytologist Central Office.
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