[Advances in Botanical Research] Plant Responses to Drought and Salinity Stress - Developments in a Post-Genomic Era Volume 57 || Signalling Strategies During Drought and Salinity,

Signalling Strategies During Drought and Salinity, Recent News

TIJEN DEMIRAL*, ISMAIL TURKAN{,1 AND A. HEDIYE SEKMEN{

*Department of Biology, Faculty of Science and Arts,

Harran University, Sanliurfa, Turkey
{Department of Biology, Faculty of Science, Ege University,
Bornova, Izmir, Turkey

stresinvomod

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AdvanCopyr

s signals, and a variety of genes and gene products have been identifiedlve responses to drought and high-salinity stress. In the past decade, a gel plant, Arabidopsis thaliana, has been widely used for unravelling the mol

orresponding author: E-mail: [email protected]

ces in Botanical Research, Vol. 57 0065-2296/1ight 2011, Elsevier Ltd. All rights reserved. DOI: 10.1016/B978-0-12-387692-8

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I. I
ntro duction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 94 II. O smo sensors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 97 III. S igna lling Components Involved During Salt and Drought Stress . . . . . . . . . 2 99
A
. ROS Signalling..... .. ... .. .. .. .. .. .. .. .. ... .. .. .. .. .. .. .. .. .. ... .. .. .. .. .. .. .. .. 3 00 B . ABA and Stress Signalling Through ROS..... .. .. .. .. .. ... .. .. .. .. .. .. .. .. 3 04 C. Antioxidative Signalling ..... .. .. .. .. .. ... .. .. .. .. .. .. .. .. .. ... .. .. .. .. .. .. .. .. 305
IV. Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 306References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 307

ABSTRACT

Agricultural production has been adversely affected worldwide by environmentalrestraints, especially by drought and salinity because of their high scale of impactand wide distribution. Conventional breeding programmes seeking improvement ofstress tolerance are a long-term endeavour as the trait is multigenic, and geneticvariability among crop plants is scarce. Many effective protection systems exist inplants that allow them to perceive, respond to and appropriately adapt to a range of

thateticular

35.00008-4

294 T. DEMIRAL ET AL.

basis of stress tolerance. The availability of knockout mutants and its suitability toallow genetic transformation proved the vital importance of Arabidopsis for assessingfunctions for individual stress-associated genes. In this review, the responses of plantsto salt and water stress are described, the regulatory circuits, which allow plants tocope with stress, are presented and how the present knowledge can be applied toobtain tolerant plants is discussed.

I. INTRODUCTION

Salinity and drought are responsible for much of the yield decline in agricul-

tural lands throughout the world. Moreover, persistent salinization of arable

land is becoming more widespread because of poor local irrigation practices,

thus decreasing the yield from formerly productive land (Kaya et al., 2010).

Not only anthropogenic factors but also some natural sources, such as parent

material, entrance of seawater along the coast, salt-laden sands blown by sea

winds, shallow groundwater and capillary rise, decay and release of salts,

absence of natural drainage, result in accumulation of salts in soil. Approxi-

mately 6% of the world’s land and 30% of the world’s irrigated areas are

already estimated to suffer from salinity problems (Unesco Water Portal,

2007). Further, the rapid change in global climate which is more than

estimated (Intergovernmental Panel on Climate Change, 2007) seems to

increase dryness for the semiarid regions of the world (Bates et al., 2008;

Lehner et al., 2005). Therefore, drought in concert with overpopulation will

lead to an overexploitation of water resources for agriculture purposes,

increase restraints to plant growth and survival and thus reduce crop

yield potential (Chaves et al., 2002, 2003; Passioura, 2007) as much as

salinity does.

The basic physiological responses developed against salinity stress and

drought stress overlie with each other as both these stresses eventually lead

to dehydration of the cell and osmotic imbalance. However, recent molecu-

lar, genomic and transcriptome analyses have shown that many genes and

various signalling factors with diverse functions are induced by drought and

high-salinity stresses (Seki et al., 2007). Although there has been a remark-

able progress in revealing the molecular mechanisms of stress tolerance and

responses of higher plants through the development of microarray-based

expression profiling methods, together with the availability of genomic and/

or cDNA sequence data, and gene-knockout mutants (Alonso et al., 2003;

Cheong et al., 2002; Chinnusamy et al., 2004; Edgar et al., 2002; Seki et al.,

2007; Shinozaki and Yamaguchi-Shinozaki, 2007), the understanding how to

employ this knowledge to engineer plants with improved stress tolerance is

still in the developmental stages.

SIGNALLING STRATEGIES DURING DROUGHT AND SALINITY 295

In recent years, several hundred genes have been identified that are induced

or repressed at the transcriptional level when plants or plant parts are

subjected to drought and salinity (Mahajan and Tuteja, 2005; Miller et al.,

2010; Saibo et al., 2009; Shinozaki and Yamaguchi-Shinozaki, 2000, 2007;

Xiong et al., 2002; Zhu, 2002). The mechanism in which genes are regulated

during the stress conditions brings out an important question as well. After

the perception of the stress factor by the receptors, the signal is transduced

downstream, which induces the generation of second messengers such as

calcium, reactive oxygen species (ROS) and inositol phosphates (Mahajan

and Tuteja, 2005) to switch on the stress-responsive genes for mediating

stress tolerance. One such signal is the plant hormone abscisic acid (ABA)

that plays a critical role in response to drought/salinity stresses. ABA treat-

ment imitates the effects of a stress condition, and the concentration of ABA

shows increment during stress. Therefore, the expression pattern of stress-

related genes after cold, drought, salinity stresses and ABA application

overlaps, suggesting that diverse stress signals and ABA share common

aspects in their signalling pathways and these common elements cross-talk

with each other, to be able to maintain cellular homeostasis (Finkelstein

et al., 2002; Leung and Giraudat, 1998; Shinozaki and Yamaguchi-

Shinozaki, 2000).

The introduction of many stress-inducible genes through gene transfer

significantly improved stress tolerance of transgenic plants (Chen et al.,

2009; Hasegawa et al., 2000; Shinozaki and Yamaguchi-Shinozaki, 2000;

Zhang, 2003). However, recent molecular and genetic analyses have unra-

velled that newly identified small RNAs as stress modulators, in addition to

small RNAs, RNA processing and chromatin regulation, are also involved in

the drought and salinity stress responses (Phillips et al., 2007; Seki et al.,

2007; Sunkar and Zhu, 2004) besides the regulation of stress-induced gene

expression at both transcriptional and posttranscriptional level by various

types of molecules. Regulation by small RNA can cause both transcriptional

and posttranscriptional suppression of gene expression (Phillips et al., 2007).

Further, in a recent work, the key role of epigenetic regulation in ABA-

mediated plant mechanisms has been highlighted (Chinnusamy et al., 2008).

Chromatin regulators, such as histone deacetylase and linker histone gene,

have been shown to be involved in abiotic stress responses of higher plants,

and ABA has been shown to induce chromatin remodelling which regulates

stress-responsive genes and stress tolerance (Meyer, 2001, Seki et al., 2007).

Therefore, it is apparent that for the success of the transgenic plants to exert

increased resistance to salt/drought stress, the regulatory role of transcriptomic

factors needs to be considered (Chinnusamy et al., 2007).


Drought and salinity entail oxidative stress accompanied by the forma-

tion of ROS due to stomatal closure that restricts CO2 influx through the

leaves. ROS such as superoxide (O2.�), hydroxyl (OH.) radical, hydrogen

peroxide (H2O2) and alkoxyl radical (RO) are produced by enhanced

leakage of electrons to molecular oxygen. Chloroplasts, mitochondria and

peroxisomes are the major sources of ROS in plant cells (Asada, 1999).

Toxic concentrations of ROS disturb normal metabolism through peroxi-

dation of lipid membranes and consequently lead to membrane injury,

protein degradation, enzyme inactivation, pigment bleaching and disrup-

tion of DNA strands (Fridovich, 1986; McCord, 2000). Nonetheless, oxi-

dative damage in the plant tissue is alleviated by a concerted action of both

enzymatic and non-enzymatic antioxidant mechanisms. These mechanisms

include carotenoids, �-tocopherol, ascorbate, glutathione and enzymes

including superoxide dismutase (SOD), catalase (CAT), peroxidase

(POX), ascorbate peroxidase (APX) and glutathione reductase (GR)

(Miller et al., 2010; Mittler et al., 2004; Smirnoff, 1993). There are many

reports in the literature that emphasize the close relationship between

enhanced or constitutive antioxidant enzyme activities and increased resis-

tance to drought or salinity stress (Acar et al., 2001; Bor et al., 2003;

Demiral and Turkan, 2005; Koca et al., 2007; Ozkur et al., 2009; Seckin

et al., 2009, 2010; Sekmen et al., 2007; Turkan et al., 2005; Yazici et al.,

2007). Although ROS have the potential to cause oxidative damage to cells

during environmental stresses, recent studies have shown that ROS play a

key role in plants as signal transduction molecules involved in mediating

responses to environmental stresses, pathogen infection, programmed cell

death and different developmental stimulus (Mittler et al., 2004; Torres and

Dangl, 2005; Verslues et al., 2007). The rapid increase in ROS production,

referred to as ‘‘the oxidative burst,’’ has been shown to be crucial for many

of these processes. Genetic studies have shown that respiratory burst

oxidase homolog (Rboh) genes, encoding plasma membrane-associated

NADPH oxidases, are the key producers of signal transduction-associated

ROS in cells during these processes (Kwak et al., 2003; Mittler et al., 2004;

Torres and Dangl, 2005).

In this review, the most recent advances in revealing ROS-mediated

signalling under salinity and drought stresses were focused, and the regu-

latory circuits that allow plants to cope with stress are presented. Some

examples were also cited of how osmotic change is sensed and relayed, and

the role of some signalling components covering of ROS and ABA has

been discussed.


II. OSMOSENSORS

Despite remarkable advances in revealing signalling components during

osmotic stress, how plants sense osmotic stress is still an open question. As

no plant molecule has actually been identified as an osmosensor so far, the

studies were focused on how yeast and microorganisms sense osmotic stress

instead. Cellular adaptation to hyperosmotic stress in yeast is mediated by

HOG (high osmolarity glycerol) response pathway (Hohmann, 2009). Phos-

phorylation and hence activity of the MAP kinase Hog1, the yeast ortholo-

gue of mammalian p38, are controlled by two branches, the Sln1 (synthetic

lethal of N-end rule1) branch and the Sho1 (SH3 domain osmosensor1)

branch, which congregate on the MAP kinase kinase (MAPKK) Pbs2.

Sho1 branch has been suggested to play a role to direct signalling between

the HOG and other MAPK pathways. (SLN1), a two-component histidine

kinase, is more sensitive to osmotic changes around and activates full path-

way even in the absence of Sho1 branch (O’Rourke and Herskowitz, 2004).

Hyperosmotic stress stimulates loss of turgor that leads concurrently to

shrinkage of cell volume and an increase in the space between plasma

membrane and cell wall. SLN1 possibly senses the change in turgor pressure

(Reiser et al., 2003).

The two-component regulatory system consists of a phosphorelay among

three proteins, Sln1, Ypd1 and Ssk1. Although SLN1 is active under optimal

conditions, it is inactivated upon hyperosmotic shock. Active Sln1 is a dimer

that autophosphorylates a histidine residue in the N-terminal sensor domain

and then transfers the phosphate group to an aspartate residue in the

C-terminal-located response regulator domain. The phosphate is then trans-

ferred to receiver domain in YPD1, and eventually to the receiver domain in

Ssk1. The inactive form of Ssk1, phosphor-Ssk1, is dephosphorylated upon

hyperosmotic shock and thus increased concentration of unphosphorylated

Ssk1 binds to the regulatory domain of the Ssk2 and Ssk22 MAPKKKs

(Posas and Saito, 1998), which allows Ssk2 and Ssk22 to autophosphorylate

and stimulate themselves. Active Ssk2 and Ssk22 then phosphorylate and

activate Pbs2, which in turn phosphorylates (on Thr174 and Tyr176) and

activates Hog1 (Hohmann 2002, 2009). Consequently, activation of HOG

pathway up-regulates osmolyte (glycerol) accumulation that play a role in

osmoregulation and redox balancing (Hohmann, 2009; Posas et al., 1996;

Wurgler-Murphy and Saito, 1997). Hog1 has been suggested to control

glycerol accumulation by four ways (Hohmann, 2009): (i) by partly

up-regulating the expression of the biosynthetic genes including glycerol-3-

phosphate dehydrogenase (Gpd1) and glycerol-3-phosphatases (Gpp1 and

Gpp2) (Remize et al., 2001; Rep et al., 2000), (ii) enhancing the expression of


the Stl1 active glycerol uptake system (Rep et al., 2000), which allows

glycerol uptake from the surrounding medium (Ferreira et al., 2005); (iii)

increasing the activity of phosphofructo-2-kinase to increase the rate of

glycerol production and (iv) by controlling the activity of the glycerol export

channel Fps1 (Thorsen et al., 2006).

Yeast osmoregulating HOG pathway seems very suitable model to study

system-level properties of signalling pathways in higher plants. Regarding

this, an SLN1 homologue, AtHK1, was identified in Arabidopsis, which also

complements SLN1-deficient yeast mutants (Urao et al., 1999). Osmosensing

role of AtHK1 has further been shown in transgenic lines of Lycium bar-

barum plants (Chen et al., 2009). Transgenic L. barbarum plants ectopically

expressing AtHK1 exhibited improved tolerance against drought and salinity

and faster recovery with subsequent rewatering in comparison to wild-type

plants. Further, AtHK1 remarkably prevented oxidative damage caused by

ROS through enhancing the activities of antioxidative enzymes such as SOD,

CAT and POX (Chen et al., 2009).

Chefdor et al. (2006) presented the first proof of osmotic stress sensing

multi-step phosphorelay system in a woody species, Populus, by showing the

up-regulation of histidine-aspartate kinase (HK1) during osmotic stress and

detecting a specific interaction between HK1 and histidine-containing phos-

photransfer protein2 (HPt2) through yeast two-hybrid system. HK1 shares

the same characteristics as those reported for the yeast (SLN1) and Arabi-

dopsis (ATHK1) osmosensors, which suggest that HK1 in Populus might

have the same function as Arabidopsis AtHK1 during osmotic stress. Simi-

larly, a high-affinity Kþ transporter has been cloned in Eucalyptus camaldu-

lensis (EcHKT) showing some similarities to AtHK1 in sensing osmotic

changes in external medium (Liu et al., 2001). In accordance with this,

Urao et al. (2000) cloned three potential phosphorelay intermediates

(ATHP1-1) and four response regulators (ATRR1-4) that might be involved

in the step after osmosensing. Further, the results of Reiser et al. (2003)

implicated the regulation of plant histidine kinase cytokinin response 1

(Cre1) by changes in turgor pressure, in a similar manner to that of Sln1, in

the presence of cytokinin. Tamura et al. (2003) investigated the responses of

transgenic tobacco seeds overexpressing NtC7 and found out that over-

expression of NtC7 provided osmotic stress tolerance induced by mannitol

but not by NaCl. Therefore, NtC7 might be involved in sensing specifically

osmotic stress (Bartels and Sunkar, 2005).

The interaction of cationic and anionic amphiphilic components with

plasma membranes can change the physical status or protein–lipid interac-

tions of membranes that relay osmosensing, and such a mechanism has been

described in Lactococcus lactis, where activation of the osmoregulated ABC


transporter OpuA was mediated by changes in membrane properties and

protein–lipid interactions (Heide and Poolman, 2000). More importantly, the

activity of major integral membrane proteins involving aquaporins may also

be regulated by the changes in the physical state of membranes (Tyerman

et al., 2002), gene expression of which is affected by water and osmotic

stresses (Kawasaki et al., 2001; Morillon and Chrispeels, 2001). Integrins in

mammalian cells are involved in the perception of mechanical stimuli (Shyy

and Chien, 1997). Concomitant with this, the important role of the interac-

tion between the cell wall and plasma membrane to sense osmotic stress has

recently been highlighted, and the fundamental position of integrin-like

protein to mediate this interaction and thus to induce osmotic stress-induced

ABA biosynthesis has been revealed in Arabidopsis thaliana (Lu et al., 2007a)

and maize (Lu et al., 2007b). The knowledge about the role of integrins in

stress responses of higher plants is limited to few studies (Trewavas and

Knight, 1994; Zhu et al., 1993). Therefore, the indispensable roles of integ-

rin-like proteins in mediating osmotic stress perception and transmission in

higher plants are awaiting further research.

III. SIGNALLING COMPONENTS INVOLVED DURINGSALT AND DROUGHT STRESS

The early responses of plants to stress are the perception and consequent

signal transduction leading to stress-responsive gene expression. As a re-

sponse to osmotic stress induced by water deficit or high salt, the expressions

of a set of genes are altered (Seki et al., 2007). Stress-responsive genes have

been identified inmany plant species includingArabidopsis (Kreps et al., 2002;

Matsui et al., 2008; Seki et al., 2002), Thellungiella halophila (Taji et al., 2004;

Wong et al., 2006), sunflower (Hewezi et al., 2008), barley (Oztur et al., 2002),

maize (Wang et al., 2003; Yu and Setter, 2003), rice (Gorantla et al., 2007;

Kawasaki et al., 2001; Lan et al., 2005; Rabbani et al., 2003), wheat (Gulick

et al., 2005), poplar (Brosche et al., 2005), pine (Watkinson et al., 2003), hot

pepper (Hwang et al., 2005), potato (Rensink et al., 2005) and sorghum

(Buchanan et al., 2005). Although the interaction and exact positions of

transduction components in the intricate signalling network are largely un-

known, various components of the signal transduction have been character-

ized. These signalling pathways include a network of protein–protein

reactions and signalling molecules that generally increase or decrease in a

transient mode (e.g. hormones, ROS, Ca2þ, sugars, etc.). Organisms also

regulate cellular processes in response to environmental cues through revers-

ible phosphorylation of proteins. Consequent systemic signals generated


conduct the management and implementation of plant stress responses with

respect to metabolic and developmental adjustments.

After the first sensing of osmotic changes during osmotic stress conditions

by osmosensors, signal transduction cascade is transduced by protein phos-

phorylation and dephosphorylation events through various protein kinases

and phosphatases, the genes of which have already been shown to be

up-regulated by initial perception of dehydration (Lee et al., 1999; Luan,

1998; Zhang et al., 2006). Osmotic stress imposed by drought or high salt is

transmitted through at least two pathways; one is ABA-dependent and

the other is ABA independent (Mahajan and Tuteja, 2005; Shinozaki

and Yamaguchi-Shinozaki, 1996). As the components involved in ABA-

dependent and ABA-independent pathways often cross-talk or even con-

verge on the signalling pathway, there is no clear-cut discrepancy between

two pathways (Kizis et al., 2001; Knight and Knight, 2001; Xiong and Zhu,

2001). Calcium also serves as a second messenger under various stress con-

ditions and mediates cross-talk. Numerous studies have shown that ABA,

drought and high salt rapidly increase calcium levels in plant cells (Pardo,

2010; Sanders et al., 1999). The resulting signalling pathway activates various

genes that play crucial role to maintain cellular homeostasis.

A. ROS SIGNALLING

ROS such as hydrogen peroxide (H2O2), superoxide (O2.�), hydroxyl (OH.)

radicals and the singlet oxygen (1O2) are produced inevitably as by-products

of aerobic metabolism in a cell. Abiotic stresses including drought and

salinity result in the enhanced formation of these toxic species by disturbing

the metabolic balance of the cells. These compounds indeed have long been

considered toxic to the organisms. Recently, however, increasing number of

evidence suggests that they play significant role in stress signal transduction

(Foyer and Noctor, 2003; Hong-bo et al., 2008; Jaspers and Kangasjarvi,

2010; Kacperska, 2004; Miller et al., 2008, 2010; Pardo, 2010). Hence, ROS

play a dual role both as toxic compounds and key regulators of biological

processes such as growth, cell cycle, programmed cell death, hormone signal-

ling, biotic and abiotic cell responses and development (Foyer and Noctor,

2005; Fujita et al., 2006; Miller et al., 2008).

During their long evolutionary history, plants have developed an elaborate

and efficient network of ROS-scavenging mechanisms composed of enzy-

matic and non-enzymatic molecules. Antioxidative enzymes such as SOD,

CAT, POX, GR and APX are produced in subcellular organelles with a

highly oxidizing metabolic activity such as chloroplasts, mitochondria, per-

oxisomes or microbodies to overcome ROS toxicity (Bailey-Serres and


Mittler, 2006; Foyer and Noctor, 2003; Miller et al., 2008). Chloroplast and

peroxisomes are considered the two major contributors to the oxidative load

in plant cells during abiotic stresses (Miller et al., 2008). It has been shown

that ABA accumulation induced by drought triggers the increased genera-

tion of ROS, which, in turn, leads to the up-regulation of the antioxidant

defence system in plants (Hu et al., 2005; Jiang and Zhang, 2002a,b). ABA

has been reported to induce the expression of antioxidant genes encoding

SOD, CAT and APX (Guan and Scandalios, 1998; Guan et al., 2000; Park

et al., 2004) and enhance the activities of these antioxidant enzymes in plant

tissues (Bellaire et al., 2000; Bueno et al., 1998; Jiang and Zhang, 2001, 2002a,

b, 2003). A rapid increase in the production of H2O2, OH. and O2.� was

observed in Arabidopsis guard cells after they were induced to close by ABA

(Pei et al., 2000), and the effect was concentration dependent. These results

bear a question about the source of ROS in the cell induced by ABA. Among

potential sources of ROS in the cell, chloroplasts, mitochondria and peroxi-

somes, plasma membrane NADPH oxidases (Rbohs for respiratory burst

oxidase homologues), cell wall POX, apoplastic oxalate oxidases and amine

oxidases are remarkable (Ming-Yi and Jian-Hua, 2004; Mittler, 2002; Neill

et al., 2002).

Saline soils are often recognized by the presence of white salt encrustation

on the surface and have predominance of chloride and sulphate of sodium,

calcium and magnesium in quantities sufficient to interfere with growth of

most crop plants. Regulation of NaCl responses are controlled by ROS

involvement. Rapid increase in cytosolic calcium induced by Naþ within

seconds is sensed by calcineurin B-like (CBL) protein CBL4/SOS3 and its

interacting protein kinase CIPK24/SOS2 (Luan, 2009; Munns and Tester,

2008; Zhu et al., 2007). The resulting SOS3/SOS2 complex phosphorylates

and activates SOS1, a plasma membrane Naþ/Hþ antiporter. Naþ/Hþ anti-

port activity of SOS1 promotes efflux of excess Naþ ions and hence con-

tributes to Naþ ion homeostasis (Fig. 1; reviewed comprehensively in Munns

and Tester, 2008; Turkan and Demiral, 2009). Recent evidence has indicated

that Naþ-induced stability of SOS1 transcripts upon exposure to NaCl stress

is mediated by ROS generated by NADPH oxidase (Chung et al., 2008). The

ROS generated by NADPH oxidase were then suggested to stabilize SOS1

mRNA, thus greatly increasing its activity and consequently NADPH oxi-

dase activity (Chung et al., 2008). NaCl-induced Ca2þ spikes and consequent

SOS1 activation cause apoplastic alkalization, which consequently activate

Rboh (Chung et al., 2008). These results indicate the potential role of SOS1

at early signalling step of a signal transduction pathway that is common to

several abiotic stresses including drought and salinity.

Regulation ofgene expression

PLP

HKT1

ABl2

ABl1

NHX1CAX1

H-ATPaseSOS1SOS5

Maintenance ofcell expansion

Rboh

AKT1 SOS1

SOS3H2O

ABA

[Na+]

?

Na+

Na+

K+

H+Cytoplasm

Apoplast

O-linked carbohydrate chains

PM

H+ H+

H+ Ca2+Na+

Ca2+ Ca2+ Na+ H+

H+

ADP+Pi ATPCytoplasm

Apoplast

PM

O2

[Self-amplifying loop]

H2O2O2

.–

V-ATPasePPase

Vacuole

ATP

NADPH NADP++H+

ADP+Pi

(e.g. SOS1, SOS4)

(e.g. NHX1)

Nucleus

H+

[Ca2+]

Saltsensor

Osmotic stress

Saltstress

SOS2

P

P

P

SOS5??

PL Kinase

Fig. 1. SOS signalling pathway for salt stress adaptation in higher plants. The interaction among SOS1, SOS2 and SOS3was explained inthe text. SOS4 gene encodes a pyridoxal (PL) kinase that play a role in the biosynthesis of PL-5-phosphate (PLP), which contributes Naþ and


SOS2 kinase also plays a special role in signalling process through its

interaction with triphosphate kinase 2 (NDP kinase2), CAT2 and CAT3

(Verslues et al., 2007). Moon et al. (2003) revealed previously uncharacter-

ized regulatory role of NDP kinase2 in ROS signalling by showing its

involvement in H2O2-induced activation of MPK3 and MPK6. Further,

mutants lacking AtNDPKinase2 had increased sensitivity to salinity stress

(Moon et al., 2003), and sos2-2 ndpkinase2 double mutants further

deteriorated the sensitivity of sos2 mutants to salinity (Verslues et al., 2007).

A sos2-2 ndpkinase2 double mutant did not accumulate H2O2 in response to

salt stress, suggesting that it is a change in signalling rather thanH2O2 toxicity

alone that is responsible for the increased salt sensitivity of the sos2-2 ndpki-

nase2 double mutant in comparison to single mutants.

Very recently, an additional sosmutantSOS6, encoding a cellulose synthase-

like protein, AtCSLD5, has been identified by Zhu et al. (2010). sos6-1mutant

plants have been shown to accumulate higher levels of ROS after exposure to

osmotic stress than the wild-type plants and are hypersensitive to the oxidative

stress reagent methyl viologen (MV). These results suggested that SOS6

and SOS6-dependent cell wall components might control osmotic stress toler-

ance partly by regulating and maintaining stress-induced ROS levels in plant

cells (Zhu et al., 2010). High accumulation of ROS in sos6-1 mutant upon

exposure to osmotic stress might imply its specific role in osmotic sensing

as well.

Plasma membrane NADPH oxidase, which transfers electrons from cyto-

plasmic NADPH to O2 to form O2.�, has been shown one of the major

sources of ROS generation induced by ABA and drought stress (Zhu et al.,

2006). Jiang and Zhang (2002a), using two-phase fractionated plasma mem-

brane extracts and several widely used NADPH oxidase inhibitors, such as

DPI, imidazole and pyridine, have demonstrated that NADPH oxidase is

involved in ABA and drought stress-induced ROS production, and drought

stress-induced ABA accumulation plays important role in the regulation of

Kþ homeostasis by regulating ion channels and transporters. SOS5 is involved in themaintenance of cell expansion. Dashed arrow shows SOS3-independent and SOS2-dependent pathway. Formation of self-amplifying loop through the activity of plasmamembrane NADPH oxidase (Rboh) is modulated by ABA-induced activation of Ca2þ

channels. Ca2þ is involved in Rboh activation as well as serving as a target for the Rbohproduct (ROS) (Jaspers and Kangasjarvi, 2010; Mittler et al., 2004; Sagi and Fluhr,2006). (The figure wasmodified fromChinnusamy et al., 2005; Jaspers andKangasjarvi,2010; Mahajan and Tuteja, 2005; Mahajan et al., 2008; Shi and Zhu, 2002; Turkan andDemiral, 2008, 2009; Zhang et al., 2004; Zhu, 2003).


NADPH oxidase activity in maize leaves. Similarly, Hu et al. (2005) pointed

out the importance of apoplastic H2O2 accumulation induced by ABA to

induce the cytosolic antioxidant enzyme activities. These results suggest that

NADPH oxidase contributes to early ABA signalling.

NaCl stress comprising both ionic and osmotic stresses has recently been

shown to induce formation of endosomes containing high concentrations

of H2O2 in Arabidopsis cells (Leshem et al., 2006, 2007). Phosphatidylinositol

3-kinase (PI3K)-dependent plasma membrane internalization and ROS pro-

duction have been triggered within endosomes of Arabidopsis root cells

(Leshem et al., 2007). Endosomal membrane in root cells has rolled up

ROS which is possibly the product of NADPH oxidase in response to salinity

stress. pi3k mutants exhibited reduced oxidative stress but enhanced salt

sensitivity due to suppression of the salt-specific induction of NADPH

oxidase-mediated ROS production within endosomes (Leshem et al., 2007).

Further, level of ROS in endosomes of root hair cells was reduced after

treatment with a PI3K-specific inhibitor LY294002, suggesting that PI3K is

essential for ROS generation inside endosomes and thus for the final stage of

endocytosis in tip-growing root hair cells (Lee et al., 2008). These results

suggest new vital regulatory roles of ROS in intracellular trafficking trough

vesicles for developmental control of organelle biogenesis in addition to their

role in retrograde stress signalling (Miller et al., 2010).

B. ABA AND STRESS SIGNALLING THROUGH ROS

ABA can be produced both in shoots and roots as a response to salinity and

drought stresses. ABA produced in the roots is transported to the shoots,

thus causing stomatal closure and eventually restricts cellular growth

(Wilkinson and Davies, 2002). Xylem/apoplastic pH has been shown to

affect ABA compartmentation and accordingly the amount of ABA arriving

at the stomata. Drought, high light and salinity conditions might lead to a

higher xylem sap pH (Jia and Davies, 2007) facilitating the modulation of

stomatal aperture in response to a variety of environmental variables. The

resulting more alkaline pH in xylem/apoplast decreases the removal of ABA

from xylem and leaf apoplast to the symplast thus allowing more ABA to

reach the guard cells. Control of stomatal aperture is strongly regulated by

ROS–ABA signalling as ABA has been shown to enhance the expression of

the genes encoding CAT1, APX1, GR1 and their activities (Cho et al., 2009)

and also the activities of cytosolic Cu/ZnSOD, APX and GR in leaves of

maize plants (Hu et al., 2005). ABA-induced stomatal closure is partially

dependant on NADPH oxidase activity (Kwak et al., 2003; Pei et al., 2000;

Torres and Dangl, 2005). ABA and drought stress induced the activities of


cytosolic aldehyde oxidase (AO) and xanthine dehyrogenase (XDH) that

produce, respectively, H2O2 and O2.� (Guan and Scandalios, 2000; Hu

et al., 2005; Yesbergenova et al., 2005; Zhang et al., 2001), which suggested

that drought can enhance ROS accumulation through XDH and AO in an

ABA-dependent manner (Yesbergenova et al., 2005). Confirming this, ABA-

deficient mutants of Arabidopsis, tomato and tobacco plants did not show

AO and XDH activities (Leydecker et al., 1995; Sagi et al., 1999; Schwartz

et al., 1997). Further, stomatal conductance is regulated by the signal trans-

duction initiated by photorespiratory glycolate oxidase reaction in peroxi-

somes under certain stresses including drought, osmotic stress and salinity,

highlighting the importance of redox homeostasis as suggested by Foyer and

Noctor (2005). However, stomatal closure by ABA is also controlled through

ion channels such as SLAC1 and KAT1 which are activated by phosphory-

lation via an ABA-activated protein kinase OST1 (open stomata1) and Ca2þ

(Mustilli et al., 2002; Siegel et al., 2009). One of the targets of OST1 is

NADPH oxidase that generates H2O2 (Pei et al., 2000; Sirichandra et al.,

2009). Enhanced production of H2O2 intercedes stomatal closure by inacti-

vating ABI1 and ABI2, which were shown to be very sensitive to H2O2 and

oxidation (Meinhard and Grill, 2001; Meinhard et al., 2002). OST1-dependent

H2O2 production could start release of further active OST1 by PP2C inactiva-

tion in a positive feedback loop (Raghavendra et al., 2010).

C. ANTIOXIDATIVE SIGNALLING

ROS-scavenging enzymes have been shown to be involved in signalling as well

as their more customary role in protection from oxidative stress in recent

years (Chen et al., 2005; Miller et al., 2010). Although overproduction of

antioxidant enzymes in transgenic plants has been resulted in enhanced

tolerance to drought and salinity stresses (Eltayeb et al., 2007; Lu et al.,

2007; Tseng et al., 2007; Yan et al., 2003), in some cases their reduced

expression unexpectedly resulted in tolerant plants. For example, tobacco

was engineered to repress APX and CAT expression levels, individually and

together by Rizhsky et al. (2002). Double antisense plants exhibited more

tolerance than in plants that lacked only APX or CAT against oxidative

damage by suppressing photosynthetic activity, up-regulating the pentose

phosphate pathway, enhancing monodehydroascorbate reductase activity

and inducing a chloroplast homologue of the mitochondrial alternative oxi-

dase (AOX) (Rizhsky et al., 2002). Likewise, each of antisense APX1 and

antisense CAT1 tobacco plants was constantly subjected to oxidative dam-

age, but the double antisense lines exerted more tolerance (Rizhsky et al.,

2002). Consistent with this, double mutant Arabidopsis plants apx1/tylapx


showed enhanced sensitivity to sorbitol treatment while sustaining salinity

tolerance (Miller et al., 2007). Even though apx1 plants show increased

sensitivity to photo-oxidative as well as paraquat-induced oxidative stress

(Davletova et al., 2005; Miller et al., 2007), they grew better than wild-type

plants under hyperosmotic or salinity condition (Ciftci-Yilmaz et al., 2007;

Miller et al., 2007). Similarly, reduced expression of tylAPX inArabidopsis led

to increased tolerance to both osmotic and salt stresses but did not affect

growth under oxidative stress conditions.Arabidopsis plants lacking cytosolic

APX1 had constitutively higher levels of H2O2 than wild-type plants and

induced the expression of many stress-responsive genes when exposed to a

modest level of light stress (Davletova et al., 2005). Likewise, antisense

repression of AOX also leads to considerably higher ROS production, where-

as AOX overexpression has the opposite effect (Maxwell et al., 1999; Parsons

et al., 1999). Moreover, mutant Arabidopsis plants aox1a, deficient in mito-

chondrial AOX1a, showed higher sensitivity to a combination of drought and

moderate light stress (Giraud et al., 2008). It appears that integrated signal-

ling networks are responsible for the activation of acclimation pathways.

Moreover, while some changes in ROSmetabolism cause enhanced tolerance

to stress, other changes cause enhanced sensitivity (Miller et al., 2010).

IV. CONCLUDING REMARKS

Numerous types of plant stress conditions enhance the production of ROS

along with ABA accumulation, which has been suggested to be key consti-

tuents of ‘cross tolerance’ to multiple types of stresses. Previously, the

oxidative stress was used to be considered as a harmful event to be avoided

or alleviated but is now viewed as an advantage for the plant to appropriately

respond and induce adequate acclimation mechanisms. Increasing body of

evidence suggests the vital importance of ROS in signal transduction. Links

between ROS and hormone signalling have already been suggested (Cho

et al., 2009; Guan et al., 2000; Kwak et al., 2003; Raghavendra et al., 2010;

Zhu et al., 2006). Further, one of the emerging issues that must be kept up

with the twenty-first century is to increase water use efficiency (WUE) of

cultivated plants facing an environment with increasing CO2 concentrations

and global temperature. With regard to this, getting the hang of stomatal

response to osmotic stress is rather vital, and recently considerable progress

has been made in this respect by researchers. Therefore, understanding the

perception and transmission of osmotic stress signal from plasma membrane

to the nucleus and then regulation of gene expression to give a better

response is crucial to enhance WUE in plants. Thus, future issues to be


addressed concern the questions of how ROS are incorporated into the

general signalling network of a cell, in which metabolic processes are the

source of ROS and could lead to the breakthrough of new signalling func-

tions for well-known metabolic enzymes, and what factors determine the

specificity of the biological activities of ROS. Filling these gaps in our

knowledge is an urgent need to avert a looming crisis of global warming

and its side effects on plants.

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[Advances in Botanical Research] Plant Responses to Drought and Salinity Stress - Developments in a Post-Genomic Era Volume 57 || Signalling Strategies During Drought and Salinity,