MINI REVIEW ARTICLE

published: 13 March 2014

doi: 10.3389/fpls.2014.00086

Response of plants to water stress

Yuriko Osakabe1 *, Keishi Osakabe 2 , Kazuo Shinozaki 1 and Lam-Son P. Tran 3 *
1
Gene Discovery Research Group, RIKEN Center for Sustainable Resource Science, Tsukuba, Japan
2
Center for Collaboration among Agriculture, Industry and Commerce, The University of Tokushima, Tokushima, Japan
3
Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, Yokohoma, Japan

Edited by: Water stress adversely impacts many aspects of the physiology of plants, especially
Nobuyuki Uozumi, Tohoku University, photosynthetic capacity. If the stress is prolonged, plant growth, and productivity
Japan
are severely diminished. Plants have evolved complex physiological and biochemical
Reviewed by:
Christa Testerink, University of
adaptations to adjust and adapt to a variety of environmental stresses. The molecular and
Amsterdam, Netherlands physiological mechanisms associated with water-stress tolerance and water-use efficiency
Vasileios Fotopoulos, Cyprus have been extensively studied. The systems that regulate plant adaptation to water stress
University of Technology, Cyprus through a sophisticated regulatory network are the subject of the current review. Molecular
*Correspondence: mechanisms that plants use to increase stress tolerance, maintain appropriate hormone
Yuriko Osakabe, Gene Discovery
Research Group, RIKEN Center for
homeostasis and responses and prevent excess light damage, are also discussed. An
Sustainable Resource Science, 3-1-1 understanding of how these systems are regulated and ameliorate the impact of water
Koyadai, Tsukuba, Ibaraki 305-0074, stress on plant productivity will provide the information needed to improve plant stress
Japan tolerance using biotechnology, while maintaining the yield and quality of crops.
e-mail: [email protected];
Lam-Son P. Tran, Signaling Pathway Keywords: abiotic stress, biomass, drought stress, photosynthesis, reactive oxygen species, stomatal closure
Research Unit, RIKEN Center for
Sustainable Resource Science,
1-7-22 Suehiro-cho, Tsurumi,
Yokohama 230-0045, Japan
e-mail: [email protected]

INTRODUCTION factors (TFs) involved in the regulation of stomatal responses,

Plant growth and productivity are adversely affected by water all of which are integrated into orchestrated molecular networks,
stress. Therefore, the development of plants with increased sur- enabling plants to adapt and survive. Furthermore, recent findings
vivability and growth during water stress is a major objective on molecular mechanisms involved in protecting photosynthesis
in the breeding crops. Water use efficiency (WUE), a parame- in order to adjust plant growth during water stress are discussed.
ter of crop quality and performance under water deficit is an
important selection trait. In fact, plants have evolved various STOMATAL SIGNALING DURING WATER STRESS
molecular mechanisms to reduce their consumption of resources MEMBRANE TRANSPORT AND ABA SIGNALING IN STOMATAL
and adjust their growth to adapt to adverse environmental con- RESPONSES
ditions (Yamaguchi-Shinozaki and Shinozaki, 2006; Ahuja et al., Stomatal activity, which is affected by environmental stresses,
2010; Skirycz and Inze, 2010; Osakabe et al., 2011; Nishiyama et al., can influence CO2 absorption and thus impact photosynthesis
2013; Ha et al., 2014). and plant growth. In response to a water deficit stress, ion- and
Plant growth is anchored by photosynthesis; however, excess water-transport systems across membranes function to control
light (EL) can cause severe damage to plants. EL induces pho- turgor pressure changes in guard cells and stimulate stomatal
tooxidation, which results in the increased production of highly closure. Endogenous ABA is rapidly produced during drought,
reactive oxygen intermediates that negatively affect biological triggering a cascade of physiological responses, including stomatal
molecules and, if severe, a significant decrease in plant produc- closure, which is regulated by a signal transduction network. 9-cis-
tivity (Li et al., 2009). Water stress that induces a decrease in leaf epoxycarotenoid dioxygenase 3 (NCED3) in Arabidopsis catalyzes
water potential and in stomatal opening (Figure 1), leading to a key step in ABA biosynthesis, and NCED3 expression is rapidly
the down-regulation of photosynthesis-related genes and reduced induced by drought stress in a vascular tissue-specific manner
availability of CO2 , has been known as one of the major factors in (Iuchi et al., 2001; Endo et al., 2008; Behnam et al., 2013; Figure 2).
the EL stress (Osakabe and Osakabe, 2012). Mutations in nced3 reduced, while the overexpression of NCED3
Various molecular networks, including signal transduction, enhanced drought tolerance and/or increased WUE in several
are involved in stress responses (Osakabe et al., 2011, 2013b; plant species (Iuchi et al., 2001; Tung et al., 2008). During drought
Nishiyama et al., 2013). The elucidation of these networks is essen- stress, the accumulated ABA in the vascular tissue is transported
tial to improve the stress tolerance of crops. In this review, plant to guard cells via passive diffusion in response to pH changes
responses to water stress are summarized, revealing that they are and by specific transporters. Two members of the membrane-
controlled by complex regulatory events mediated by abscisic acid localized ABC transporter family, ABCG25 and ABCG40, and one
(ABA) signaling, ion transport, and the activities of transcription member from a nitrate transporter family, AIT1/NRT1.2/NPF4.6,

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Osakabe et al. Plant water stress response

role in K+ efflux. The anion and K+ efflux from guard cells

results in a reduction of guard cell turgor which causes stom-
atal closure (Schroeder and Hagiwara, 1989; Pei et al., 1997; Kwak
et al., 2003; Negi et al., 2008; Vahisalu et al., 2008). SLAC1 (SLOW
ANION CHANNEL-ASSOCIATED 1) functions as a major S-type
anion channel in guard cells (Negi et al., 2008; Vahisalu et al.,
2008), and is activated directly by a Snf1-related protein kinase
2 (SRK2E/OST1/SnRK2.6). This kinase is involved in the ABA-
signaling complex of the ABA receptor, PYR family and PP2Cs
(Geiger et al., 2009; Lee et al., 2009). S-type anion channels are
also activated by the calcium-dependent protein kinases CPK3,
CPK6, CPK21, and CPK23 (Geiger et al., 2010; Brandt et al., 2012).
KAT1 has also been shown to be a direct target of regulation by
ABA, since its activity is directly inhibited via phosphorylation by
an ABA-activated SRK2E (Sato et al., 2009). Recently, the activity
of KUP6, a KUP/HAK/KT family K+ transporter, has also been
shown to be involved in the direct regulation during drought stress
via phosphorylation by an ABA-activated SRK2E (Osakabe et al.,
2013a). These results suggest that the complicated, but direct, con-
trol of ion transport systems by ABA may play an important role
in stomatal responses that impact the tolerance of plants to water
stress and influence plant growth (Figure 2).

FIGURE 1 | Illustration of the response of plants to water stress. TRANSCRIPTION FACTORS

Stomatal response, ROS scavenging, metabolic changes, and The expression of various genes with functions in the water deficit
photosynthesis are all affected when plants are subjected to water stress.
These collective responses lead to an adjustment in the growth rate of
responses, are specifically induced during the stress. Transcrip-
plants as an adaptive response for survival. tomic and proteomic analyses in various species have identified
the involvement of general physiological processes associated
with drought-responsive gene expression (Molina et al., 2008;
have been independently isolated from Arabidopsis and reported Aprile et al., 2009; Walia et al., 2009; Abebe et al., 2010; Dugas
as ABA transporters (Kang et al., 2010; Kuromori et al., 2010; et al., 2011; Jogaiah et al., 2012; Le et al., 2012; Utsumi et al.,
Kanno et al., 2012; Figure 2). ABCG25 has a role in ABA export, 2012). These studies have identified the conserved, as well
whereas ABCG40 and AIT1 are involved in the import of ABA. as, species-specific regulatory and functional drought-responsive
ABA-induced stomatal closure and gene expression are reduced genes, including osmoprotectants and ABA biosynthesis, late
in the atabcg40 mutation, resulting in reduced drought tolerance embryogenesis abundant (LEA) and chaperone, ROS-related, ion
(Kang et al., 2010). These data indicate that the ABA transport sys- homeostasis, and signaling genes. Additionally, key TFs reg-
tem plays a significant role in water deficit tolerance and growth ulating drought-responsive gene transcription have also been
adjustment. Transcription of ABCG25 was induced by ABA and identified, such as MYB, MYC, DREB/CBF (drought-responsive
drought stress, and exhibited vascular tissue-specificity (Kuromori cis-element binding protein/C-repeat-binding factor), ABF/AREB,
et al., 2010). In contrast, ABCG40 was expressed in guard cells NAC, and WRKY TFs (Stockinger et al., 1997; Sakuma et al.,
(Kang et al., 2010), suggesting the possibility that the ABA syn- 2006; Tran et al., 2007b; Nakashima et al., 2009; Ishida et al.,
thesized in the vasculature during drought stress can be imported 2012; Figure 2). Corresponding cis-motifs, DRE/CRT and ABRE
into the guard cells via these transporters. The expression pattern (ABA-responsive cis-element), have also been discovered in the
of AIT1/NRT1.2/NPF4.6 was similar to ABCG25 and also showed promoters of many stress-responsive genes (Yamaguchi-Shinozaki
vascular tissue-specificity (Kanno et al., 2012). This finding sug- and Shinozaki, 2006).
gests that ABA import systems in vascular tissues may also play an ABA-responsive cis-element-mediated transcription via ABF/
important role in the regulation of water stress responses. AREB is directly regulated by an ABA receptor complex involving
In response to drought stress, ABA stimulates a signaling path- SnRK2 that activate ABF/AREBs by phosphorylation (Umezawa
way that triggers the production of reactive oxygen species (ROS), et al., 2010). The action of SnRK2 represents one of the impor-
which in turn induces an increase in cytosolic Ca2+ . Subsequently, tant mechanisms regulating the rapid, adaptive response of plants
two distinct types of anion channels, a slow-activating sustained to drought. DREB and AREB activate the transcription of var-
(S-type), and a rapid-transient (R-type), are activated and the ious genes that are expressed in variety tissues. Additionally,
anion efflux results in a depolarization of the plasma membrane. novel types of TFs, with critical functions in stomatal responses,
This leads to a decrease in the inward K+ channels (KAT1/KAT2) have also been identified. DST (drought and salt tolerance),
and H+ -ATPase, which are involved in stomatal opening, and a C2 H2 -type TF, controls the expression of genes involved in
the activation of outward K+ channels, including GUARD CELL H2 O2 homeostasis, and mediates ROS-induced stomatal clo-
OUTWARD RECTIFYING K+ CHANNEL (GORK) that has a sure and abiotic stress tolerance in rice (Huang et al., 2009).

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Osakabe et al. Plant water stress response

FIGURE 2 | Model for the role of signaling factors in stomatal closure and retrograde signaling during water stress.

Drought-inducible nuclear TF, NFYA5, was reported to control mediates osmotic-stress signaling in prokaryotes and has been
stomatal aperture and play a role in drought tolerance in Ara- shown to function as an osmosensor. Overexpression of AHK1
bidopsis (Li et al., 2008). SNAC1 (STRESS-RESPONSIVE NAC1) enhanced drought tolerance in Arabidopsis (Urao et al., 1999; Tran
is expressed in rice guard cells, and overexpression of this gene et al., 2007a). ahk1 mutants exhibited decreased sensitivity to
enhanced ABA sensitivity, stomatal closure, and both DST in rice ABA and the downregulation of ABA- and/or stress-responsive
(Hu et al., 2006). AtMYB60 and AtMYB61 are expressed mainly in genes, indicating that AHK1 acts as an osmosensor and func-
guard cells, and important TFs regulating stomatal aperture and tions as a positive regulator of osmotic-stress signaling (Tran
drought tolerance in plants (Cominelli et al., 2005). AtMYB60 is et al., 2007a; Wohlbach et al., 2008). Downstream AHK1 cascades
a negative regulator of stomatal closure (Cominelli et al., 2005; appear to be controlled by AHPs and ARRs as part of a mul-
Liang et al., 2005). Further studies to determine the molecu- tiple His-Asp phosphorelay. However, the factors that receive
lar targets and signaling systems associated with these TFs in signals from AHK1, and also the precise composition of the
stomatal responses will increase our understanding of the regu- signaling cascades, remain to be determined. In contrast, in
latory networks controlling plant drought responses and growth Arabidopsis, the cytokinin (CK) receptor HKs, AHK2, AHK3,
adjustment. and AHK4, have been shown to negatively regulate ABA and
drought signaling (Tran et al., 2007a, 2010). Multiple mutants of
EARLY WATER STRESS RESPONSE AND SIGNAL ahk2, ahk3, and ahk4 display increased sensitivity to ABA and
TRANSDUCTION PATHWAYS enhanced tolerance to drought (Tran et al., 2007a; Jeon et al.,
Receptor and sensor proteins localized to membranes play impor- 2010). These findings indicate the existence of crosstalk among
tant roles in various signaling pathways, conveying information ABA, CK, and stress-signaling pathways (Nishiyama et al., 2011;
to their cytoplasmic target proteins via catalytic processes, such as Ha et al., 2012).
phosphorylation. Plasma membrane signaling has been hypoth- In Arabidopsis, the receptor-like kinase (RLK) family includes
esized to be involved in the initial process of water status more than 600 members, with the leucine rich-repeat (LRR)-RLKs
perception outside the cell (Maathuis, 2013). AHK1, an Ara- constituting the largest subgroup (Gish and Clark, 2011). Sev-
bidopsis histidine kinase (HK) localized to the plasma membrane eral RLKs localized to the plasma membrane are known to be

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Osakabe et al. Plant water stress response

involved in the early steps of osmotic-stress signaling in a variety APXs (Rizhsky et al., 2004; Davletova et al., 2005; Rossel et al.,
of plant species (Osakabe et al., 2013b). These stress-related RLKs 2007). Several transgenic lines that overexpressed ZAT10 exhib-
possess a number of different extracellular domains (e.g., LRR, ited enhanced drought stress tolerance (Sakamoto et al., 2004).
an extensin-like domain, or a cysteine-rich domain; Bai et al., ZAT10 and ZAT12 regulate the responses to EL and drought
2009; de Lorenzo et al., 2009; Osakabe et al., 2010a; Yang et al., stresses, which are mediated by ROS (Davletova et al., 2005;
2010; Tanaka et al., 2012), indicating that different environmen- Mittler et al., 2006), suggesting their potential roles in pro-
tal stimuli may activate RLK-mediated signaling pathways and tecting photosynthesis from the injury during water stress
convey the osmotic conditions outside of the cells. RLKs that (Figure 2).
bind to cell-walls, such as cell wall-associated kinases (WAKs), Plants can monitor chloroplast status by plastid-to-nucleus
the proline-rich extensin-like receptor kinase (PERKs; Osakabe signals, as plastid-to-nucleus retrograde signaling. This signal-
et al., 2013b), and the CrRLKs (Catharanthus roseus RLK1-like ing system can regulate the expression of genes that function in
family; Schulze-Muth et al., 1996) have recently been predicted to the chloroplast. The retrograde signaling plays an important role
be involved in the perception of turgor pressure (Steinwand and in regulating the chloroplastic processes and also in the adaptive
Kieber, 2010; Christmann et al., 2013). A potential link between responses to environmental stresses (Chan et al., 2010). Chloro-
the RLKs in cell-wall binding, ABA biosynthesis and water stress phyll intermediates, such as Mg-protoporphyrin IX (Mg-Proto),
response could be determined by analyzing their roles in signal- control the expression of nuclear genes in plants exposed to EL
ing systems associated with specific mechanosensing pathways conditions, acting as a retrograde signal. The genomes uncou-
activated in response to water stress. This would shed light on pled (gun) mutants, gun4 and gun5, exhibit impaired generation
the early signaling system controlling water stress tolerance and of Mg-Proto that has been shown to act as a signal to repress
growth adjustment. LHCB gene expression in Arabidopsis (Mochizuki et al., 2001;
Strand et al., 2003; Pontier et al., 2007). LHCB expression is also
PROTECTING PHOTOSYNTHESIS DURING WATER STRESS controlled by GUN1 and ABI4 (ABSCISIC ACID-INSENSITIVE
Water stress directly affects rates of photosynthesis due to the 4) that encodes a TF involved in ABA signaling (Koussevitzky
decreased CO2 availability resulted from stomatal closure (Flexas et al., 2007). Collectively, these factors are thought to be involved
et al., 2006; Chaves et al., 2009), and/or from changes in pho- in multiple retrograde signaling pathways. Moulin et al. (2008)
tosynthetic metabolism (Lawlor, 2002). EL has a negative effect re-examined the proposed role of Mg-Proto and other chloro-
on photosynthesis when the rates of photosynthesis are reduced phyll intermediates as signaling molecules and reported that none
by water stress (Li et al., 2009; Osakabe and Osakabe, 2012). A of the intermediates could be detected in ROS-induced plants
strong interconnection between the responses to EL and drought under conditions where nuclear gene expression was repressed.
stresses has been suggested, and around 70% genes induced The authors hypothesized that Mg-Proto (which accumulates in a
by EL are also induced by drought (Kimura et al., 2002; Chan light-dependent manner) is extremely short-lived and may gener-
et al., 2010; Estavillo et al., 2011). EL also stimulates the pro- ate 1 O2 under EL conditions; however, a much more complex ROS
duction of ROS, such as H2 O2 , superoxide (O2 − ) and singlet signal may be generated during chloroplast degradation. There is
oxygen (1 O2 ), by specific photochemical and biochemical pro- increasing evidence for the regulation of nuclear gene expression
cesses, which also exerts deleterious effects on photosynthesis by 1 O2 (op den Camp et al., 2003) and H2 O2 (Kimura et al., 2003).
(Li et al., 2009). H2 O2 induces the up-regulation of a vari- However, a clear role for these ROS molecules, either individually
ety of genes that overlap with genes up-regulated by various or in combination, requires further investigation.
chemical and environmental stresses, such as methyl viologen, Recently, several novel retrograde signaling pathways have
heat, cold, and drought (Vandenabeele et al., 2004; Vander- been identified, including the 3 -phosphoadenosine 5 -phosphate
auwera et al., 2005). The transcription of cytosolic ascorbate (PAP) pathway, which is regulated by SAL1/ALX8/FRY1, and the
peroxidase encoding genes (APXs), which have important roles methylerythritol cyclodiphosphate (MEcPP) pathway (Estavillo
in the scavenging of cytosolic H2 O2 , responds positively to et al., 2011; Xiao et al., 2012). PAP has been described as a chloro-
EL stress and the redox state of plastoquinone (PQ; Karpin- plast to nuclear mobile signal that regulates gene expression.
ski et al., 1997). APX loss-of-function mutants exhibited an ALX8 encodes a phosphatase that converts PAP to AMP and
accumulation of degraded chloroplast proteins, indicating that regulates PAP levels (Wilson et al., 2009; Estavillo et al., 2011).
APXs play a protective role as ROS scavengers for chloroplast alx8 mutant exhibited drought-tolerant phenotypes and consti-
proteins under EL conditions (Davletova et al., 2005; Li et al., tutive upregulation of approximately 25% of the EL-regulated
2009). AtAPX2 was also induced by drought stress and ABA transcriptome, suggesting that SAL1/ALX8/FRY1 can act as a
(Rossel et al., 2006), suggesting that APX mediates ROS scaveng- component of both EL and drought signaling networks, and
ing in response to both EL and water stress. A gain-of-function that the SAL1-PAP retrograde pathway can alter nuclear gene
mutant, altered apx2 expression 8 (alx8), which has consti- expression during EL and drought (Rossel et al., 2006; Wilson
tutively higher levels of APX2 expression, exhibited improved et al., 2009; Estavillo et al., 2011; Figure 2). MEcPP is a precur-
WUE and drought tolerance (Rossel et al., 2006; Wilson et al., sor of isoprenoids generated by the methylerythritol phosphate
2009; Estavillo et al., 2011). In Arabidopsis, the zinc-finger TFs, (MEP) pathway, and can induce expression of nuclear encoded
ZAT10 and ZAT12, are induced in plants acclimated to EL or stress-responsive genes (Xiao et al., 2012). MEcPP is induced by
ROS treatment. The overexpression of ZAT10 and ZAT12 highly various abiotic stresses, such as high light and wounding, and
induced expression of various stress-related genes, including has been proposed to act as a retrograde signal in response to

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Osakabe et al. Plant water stress response

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This work was supported by the Programme for Promotion 3054.2006.00621.x
of Basic and Applied Researches for Innovations in the Bio- Geiger, D., Scherzer, S., Mumm, P., Marten, I., Ache, P., Matschi, S., et al. (2010).
Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with
Oriented Industry of Japan (Yuriko Osakabe and Kazuo Shi-
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nozaki). Research in Lam-Son P. Tran’s lab was supported by 10.1073/pnas.0912030107
the Grant (No. AP24-1-0076) from RIKEN Strategic Research Geiger, D., Scherzer, S., Mumm, P., Stange, A., Marten, I., Bauer, H., et al.
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Zhang, F., Maeder, M. L., Unger-Wallace, E., Hoshaw, J. P., Reyon, D., Christian, Citation: Osakabe Y, Osakabe K, Shinozaki K and Tran L-SP (2014) Response of plants
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10.1073/pnas.0914991107 Plant Science.
Copyright © 2014 Osakabe, Osakabe, Shinozaki and Tran. This is an open-access article
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