Molecular Stress Physiology of Plants || Molecular Physiology of Osmotic Stress in Plants

Molecular Physiology of Osmotic Stressin Plants 7Hrishikesh Upadhyaya, Lingaraj Sahoo, and Sanjib KumarPanda

Abstract

Osmotic stress apparently reduces growth and productivity of crop plants.

When plants are subjected to abiotic stress conditions like drought and

salinity stress, most of the affected cellular processes are common and

some overlap with cold stress. One important response to osmotic stress is

the accumulation of the phytohormone abscisic acid (ABA), which

induces several responses to osmotic stress. Osmotic stress signaling

consists of an ABA-dependent and an ABA-independent pathway.

Osmotic stress also caused increased ROS generation, which in turn elicits

various cellular signaling networks resulting into physiological damage to

plant cell. Osmotic stress signaling activates specific kinases, including

one that belongs to the SNF1-related protein kinase (SnRK) 2 family,

which is a plant-specific protein kinase family with 10 members

(SnRK2.1-2-10) in Arabidopsis. ABA strongly activates SnRK2.2, 2.3,

and 2.6, whereas osmotic stress activate almost all members of SnRK2s.

Previous report revealed that SnRK2.2, 2.3, and 2.6 are core components

of the ABA pathways whereas SnRK2s are essential kinases for osmotic

stress signaling. Though the activation mechanism of SnRK2s in the ABA

pathway is elucidated, regulatory mechanisms of SnRK2s in the ABA-

independent pathway remain obscure. Thus, further analysis of SnRK2s

must be a key study to draw the whole signaling pathways. This chapter is

an insight into the molecular physiology of osmotic stress signaling and

response in plants.

H. Upadhyaya

Department of Botany and Biotechnology, Karimganj

College, Karimganj 788710, Assam, India

e-mail: [email protected]

L. Sahoo

Department of Biotechnology, Indian Institute of

Technology Guwahati, Gauhati 781039, India


S.K. Panda (*)

Plant Molecular Biotechnology Laboratory, Department

of Life Science and Bioinformatics, Assam University,

Silchar 788011, India


G.R. Rout and A.B. Das (eds.), Molecular Stress Physiology of Plants,DOI 10.1007/978-81-322-0807-5_7, # Springer India 2013

179

mailto:[email protected]



Introduction

Plants are often subjected to adverse changes in the

environment which they quickly recognize and

respond with suitable reactions. Drought, heat,

cold, and salinity are among the major abiotic

stresses that adversely affect plant growth and

productivity around the globe. Abiotic stress is

the principal cause of crop yield loss worldwide,

reducing normal yields of crop plant by more than

50% and thereby causing enormous economic loss

as well. Osmotic stress, caused by either drought,

salinity, or cold stress, is one of the important

abiotic factors which had a great impact on plant

evolution. Osmotic stress in its broadest sense

encompasses both drought and salinity stress-

induced lowering of water potential in plant cell

(Hoffmann 2002). Osmotic stress is becoming par-

ticularly widespread in many regions as a conse-

quence of serious salinization of more than 50% of

all arable lands by the year 2050. In general,

osmotic stress often causes a series of morpholog-

ical, physiological, biochemical, and molecular

changes that alters growth, development, and pro-

ductivity of plant. Drought, salinity, and cold

stress-induced oxidative stress are often interre-

lated, and these conditions singularly or in combi-

nation induce various cellular damages. Such

stress stimuli inducing osmotic stress in plants

are complex in nature (Huang et al. 2011). Almost

all the abiotic stresses including osmotic stress

lead to oxidative damage and involve the forma-

tion of reactive oxygen species (ROS) in plant

cells. However, plants have evolved the mechan-

isms to reduce their oxidative damage by the acti-

vation of antioxidant enzymes and the

accumulation of compatible solutes that effectively

scavenge ROS (Upadhyaya and Panda 2004;

Upadhyaya et al. 2008, 2011; Gill and Tuteza

2010). If the production of ROS exceeds the

plant’s ability to detoxify it, adverse reactions

occurs, the typical symptoms being loss of osmotic

responsiveness, wilting, and necrosis. Therefore,

the balance between the production and the

scavenging of ROS is needed, which is critical

for the maintenance of normal growth and metab-

olism of the plant and overall osmotic stress toler-

ance in plants.

Osmotic stress signaling activates specific

kinases, including one that belongs to the

SNF1-related protein kinase (SnRK) 2 family,

which is a plant-specific protein kinase family

with 10 members (SnRK2.1-2.10) in Arabidop-

sis. ABA strongly activates SnRK2.2, 2.3, and

2.6, whereas osmotic stress activate almost all

members of SnRK2s. Recent study reveals that

SnRK2.2, 2.3, and 2.6 are core components of

the ABA pathways whereas SnRK2s are essen-

tial kinases for osmotic stress signaling (Fujii

et al. 2009, 2011; Fuji and Jhu 2009; Umezawa

et al. 2010). Though the activation mechanism of

SnRK2s in the ABA pathway is elucidated, reg-

ulatory mechanisms of SnRK2s in the ABA-

independent pathway remain obscure. Thus, fur-

ther analysis of SnRK2s must be a key study to

draw the whole signaling pathways. Plant genetic

engineering strategies for osmotic stress toler-

ance have been focused largely on the expression

of genes that are involved in osmolyte biosynthe-

sis (glycine betaine, mannitol, proline, etc.);

genes encoding enzymes for scavenging ROS

(superoxide dismutase (SOD), glutathione S-

transferase, glutathione reductase, glyoxylases,

etc); genes encoding late embryogenesis protein

(LEA) (LEA, HVA1, LE25, dehydrin, etc);

genes encoding transcription factors (DREB1A,

CBF1, Alfin1); engineering of cell membranes;

and proteins involved in ion homeostasis. These

aspects have opened up the avenue to produce

transgenics with improved osmotic stress toler-

ance. To cope with osmotic stress, it is important

to understand plant responses to drought, salin-

ity, cold, etc., stresses that disturb the cellular

homeostasis in order to identify a common mech-

anism for multiple stress tolerance. This book

chapter is an insight into molecular physiological

mechanism of osmotic stress responses in plants.

Osmotic Stress Sensing and Signalingin Plants

As other living organisms, plant cells perceive

and process information with the use of various

receptors exposed on the cell surface (Rodrıguez

et al. 2005). Membrane protein kinases of two

classes—receptor-like Ser/Thr kinases (RLKs)

180 H. Upadhyaya et al.

(Shiu and Bleecker 2001) and receptor Hiski-

nases (HKs) (Urao et al. 2001)—act as receptors

in osmotic stress. In the late 1990s, Arabidopsisthaliana was found to possess AtHK1, which

is homologous to Saccharomyces cerevisiae

SLN1. In yeast cells, SLN1 senses the changes

in osmolarity and triggers a two-component sys-

tem, which activates MAPK (mitogen-activated

protein kinase) pathways. Although direct evi-

dence for the osmosensor role of AtHK1 in A.

thaliana is still lacking, AtHK1 expression is

known to increase in salt stress (250 mM NaCl)

or a decrease in temperature to 4�C (Urao et al.

1999). In the sln1 D sho1 D double mutant

(the two affected proteins act as osmosensors

in yeasts), AtHK1 expression inhibited the salt-

sensitive sln1D sho1D phenotype (Urao et al.

1999). It is important to note that AtHK1 did

not interact with any of the five A. thaliana

response regulators examined (Urao et al.

2001). Yeast SHO1, which acts as an osmosensor

at a high osmolarity, contains four transmem-

brane domains and the SH3 domain exposed

into the cytoplasm and lacks enzymatic activity.

SHO1 initiates a signaling pathway typical of

higher eukaryotic cells (Raitt et al. 2000; Reiser

et al. 2000). At a high osmolarity, HK CRE1,

which acts as a membrane cytokinin receptor in

A. thaliana, substitutes HK SLN1 in sln1D yeast

cells when activated with its ligand zeatin (Inoue

et al. 2001). Such CRE1 activity was also

observed when osmotic stress was simulated

with sorbitol and, consequently, the turgor pres-

sure and cell volume decreased (Reiser et al.

2003). CRE1 and SLN1 are similar in domain

organization but are highly homologous only in

the cytoplasmic kinase and sensor domains. The

questions arise as to how CRE1 perceives the

changes in turgor pressure and which domains

are indispensable for the osmosensor function of

activated CRE1. Reiser et al. (2003) assumed

that CRE1 mediates a physical contact of the

cell wall with the plasma membrane. The osmo-

sensor function requires a unique combination

of the periplasmatic and transmembrane domains

of CRE1, as well as the integrity of the total

periplasmatic domain. The above property of

CRE1 is of immense importance, suggesting

that plants have an osmosensing system that is

structurally and functionally similar to its yeast

analog. This assumption needs verification with

plant cells. Recent analyses of cultured plant

cells with altered levels of the putative Ca2+-

permeable mechanosensitive channel indicate

that OsMCA1 is involved in regulation of plasma

membrane Ca2+ influx and ROS generation

induced by hypo-osmotic stress in cultured rice

cells (Kurusu et al. 2012). Such findings enlight

our understanding of mechanical osmotic stress

sensing pathways.

Physiochemical Effect of OsmoticStress in Plants

Osmotic stress results into various physiochemical

responses in plants growing at different develop-

mental stages. Accumulation of compatible

solutes, such as proline (Pro) and glycine

betaine (GB), in response to drought and salin-

ity to facilitate water uptake (Ashraf and

Foolad 2007) is common in plants. In addition

to osmotic adjustments, these osmolytes were

suggested to be important for protecting cells

against increased levels of ROS accumulation

under stress conditions. Pro accumulates in the

cytosol and the vacuole during stress (Aubert

et al. 1999; McNeil et al. 1999) and was shown

to protect plant cells against damages caused

by 1O2 or HO· (Matysik et al. 2002). By

quenching 1O2 and directly scavenging HO,

Pro might be able to protect proteins, DNA,

and membranes (Matysik et al. 2002). In addi-

tion to directly scavenging of HO, Pro might

bind to redox-active metal ions and protect

biological tissues against damages caused by

HO· formation (Matysik et al. 2002). Trans-

genic wheat plants that accumulated higher

Pro than wild type exhibited less lipid peroxi-

dation of membranes during osmotic stress,

indicating a role for Pro in reducing ROS

damages during osmotic stress (Vendruscolo

et al. 2007). Arabidopsis mutants deficient in

salt-induced siRNA that suppresses the expres-

sion of pyrroline-5-carboxylate dehydrogenase

(functions in Pro degradation) were impaired

in Pro accumulation, enhanced the accumula-

tion ROS, and consequently enhanced plant

7 Molecular Physiology of Osmotic Stress in Plants 181

sensitivity to salinity stress (Borsani et al.

2005). Pro synthesis from glutamate, previ-

ously documented in the cytosol, was now

shown to occur, at least in part, in the chloro-

plast (Szekely et al. 2008). During Pro synthe-

sis, NADPH is used for the reduction of

glutamate, which increases NADP+ availability,

required for relieving of PSI over-reduction dur-

ing stress, as well as increasing NADP+/NADPH

ratio that prevents perturbation of redox-sensitive

pathways during drought- and salt-induced

osmotic stresses. Accordingly, Pro was shown to

protect photochemical efficiency of PSII and pre-

vent lipid peroxidation during drought-induced

osmotic stress (Molinari et al. 2007). These

results indicate that Pro functions to indirectly

protect PSII as well as directly scavenge ROS

during drought. In contrast to Pro, GB is not

thought to directly scavenge ROS during abiotic

stresses (Smirnoff and Cumbes 1989; Chen and

Murata 2008). However, GB has been shown to

protect cells against oxidative damage during

abiotic stresses (Park et al. 2007; Chen and Mur-

ata 2008). Accumulation of GB is mainly in the

chloroplast and is involved in the maintenance of

PSII efficiency under stress conditions (Genard

et al. 1991; Ashraf and Foolad 2007; Ben Hassine

et al. 2008). A previous study showed that accu-

mulation of GB in the chloroplast is more effec-

tive than that in other cellular compartments in

protecting plants against oxidative stress and

salinity (Park et al. 2007). In addition, exogenous

GB treatment prevents osmotic stress-induced

structural damages to ROS-producing organelles,

such as chloroplasts and mitochondria (Ashraf

and Foolad 2007). These results suggest that GB

acts to prevent excess ROS production by protect-

ing chloroplasts during salinity-induced osmotic

stress. Activation of antioxidant mechanisms by

Pro and GB during salinity has been studied using

tobacco Bright Yellow-2 suspension-cultured

cells (Hoque et al. 2007; Banu et al. 2009). Salin-

ity significantly inhibited the amount of reduced

AsA, reduced GSH, and the activity of AsA–GSH

cycle enzymes, and exogenous application of Pro

or GB increased the activity of these enzymes

(Hoque et al. 2007). These results suggest a role

of Pro and GB in the regulation of antioxidant

enzymes during osmotic stress induced by salin-

ity. Soluble sugars also contribute to the regula-

tion of ROS signaling as well as osmotic

adjustments during abiotic stresses (Vinocur and

Altman 2005; Seki et al. 2007). Soluble sugars are

involved in themetabolism and protection of both

ROS-producing and ROS-scavenging pathways,

such as mitochondrial respiration, photosynthe-

sis, and oxidative-pentose-phosphate pathway

(Couee et al. 2006). A number of studies have

suggested that mannitol can protect against

photooxidative damages to the chloroplastic

apparatus caused especially by HO· during stress.

Transgenic tobacco plants with increased manni-

tol production targeted to the chloroplast showed

increased scavenging capacity of HO· enhancing

their resistance to oxidative stress. Because the

increase in mannitol content was insufficient to

account for osmotic adjustments in transgenic

wheat plants expressing the Escherichia coli

mannitol biosynthetic gene mtlD during drought

and salinity, mannitol function in enhancing

stress tolerance in these plants was mainly attrib-

uted to its potential for scavenging of HO· and

O2� (Abebe et al. 2003). Trehalose, a disaccha-

ride, is known as a signaling molecule that reg-

ulates carbon and ABA metabolism under

osmotic stress conditions (Avonce et al. 2004).

In previous studies, overexpression of trehalose

biosynthetic genes enhanced tolerance of trans-

genic plants to drought and salinity (Garg et al.

2002; Penna 2003; Miranda et al. 2007), suggest-

ing the involvement of trehalose in the response

of plants to these stresses. Transgenic rice plants

that express E. coli trehalose biosynthetic genes

showed less photooxidative damage to PSII dur-

ing drought and salinity compared with wild-type

plants (Garg et al. 2002). Drought stress-induced

osmotic stress is known to reduce protein synthe-

sis, photosynthetic efficiency, nutrient accumula-

tion, antioxidant metabolism and increased ROS

level, lipid peroxidation, and oxidative metabo-

lism in plant cell (Upadhyaya and Panda 2004;

Bartels and Sunkar 2005; Shinozaki and


Yamaguchi-Shinozaki 2007; Upadhyaya et al.

2008, 2011) (Fig. 7.1).

SOS Signaling Pathway and OsmoticStress

Cellular ion homeostasis during salinity-induced

osmotic stress is achieved by the following stra-

tegies: (1) exclusion of Na+ from the cell by

plasma membrane-bound Na+/H+ antiporters or

by limiting the Na+ entry, (2) utilization of Na+

for osmotic adjustment by compartmentation of

Na+ into the vacuole through tonoplast Na+/H+

antiporters, and (3) Na+ secretion. Thus, regula-

tion of ion transport systems is fundamental to

plant salt tolerance. Genetic analysis of salt

overly sensitive (sos) mutants of Arabidopsisled to the identification of the SOS pathway,

which regulates cellular ion homeostasis and

Drought stress

Stress perception

Osmoticstress

Signal TransductionMachinary

Protein kinases, MAPK, Ca+,IP3, etc.

Salt stress

Cold stress

Cytoplasmicproteins synthesis

Transcriptionalfactors

Transcriptionalprocessings

OSRF

OSRG

OSREmRNAStress

mRNA

OSP

Cytoplasmicproteins synthesis

BiochemicalResponses

CellularResponse

Osmotic stress Response and Tolerance

promoters

Fig. 7.1 Schematic model depicting the generalized

molecular mechanism of osmotic stress response in

plants. OSRF osmotic stress responsive factors, OSRE

osmotic stress responsive elements, OSRG osmotic stress

responsive genes, OSP osmotic stress proteins


salt tolerance (Zhu 2002). The Arabidopsis sos3mutant is hypersensitive to salt stress. Molecular

cloning revealed that the SOS3 encodes a Ca2+-

binding protein homologous to the regulatory

subunit of yeast calcineurin and animal neuronal

calcium sensors. It has an N-myristoylation motif

and three calcium-binding EF hands. SOS3

senses salt stress-induced increases in cytosolic

Ca2+ concentration in plants (Liu and Zhu 1998;

Ishitani et al. 2000). Myristoylated SOS3 is

recruited to the plasma membrane (Quintero

et al. 2002). Mutations that disrupt either myris-

toylation (G2A) or calcium binding (sos3-1)

cause salt stress hypersensitivity to Arabidopsis

plants. Since myristoylation of SOS3 is essential

for salt tolerance, it is likely that membrane

recruitment of SOS3 is essential for its function.

Membrane localization of SOS3 may help in

the regulation of its target ion transporters

(Ishitani et al. 2000). Identification of additional

SOS loci (SOS2 and SOS1) revealed that the

SOS pathway regulates cellular ion homeostasis

under salt stress. Arabidopsis sos1 and sos2

mutants are also hypersensitive to salt stress

and sos1, sos2, and sos3 mutations do not show

an additive effect, implying that they are in

the same pathway of salt stress response. SOS2

is a ser/thr protein kinase with an N-terminal

kinase catalytic domain and a C-terminal regu-

latory domain. The SOS2 C-terminal regulatory

domain consists of the SOS3-binding, autoinhi-

bitory FISL motif (Liu et al. 2000). Binding of

SOS3 activates the SOS2 protein kinase (Halfter

et al. 2000). Deletion of the FISL motif from

SOS2 leads to constitutive activation of the

kinase. Molecular genetic analysis of the sos1mutant led to the identification of a target for

the SOS3–SOS2 kinase complex. SOS1 encodes

a plasma membrane Na+/H+ antiporter. The

sos1 mutant accumulates high levels of Na+ in

tissues under salt stress, and isolated plasma

membrane vesicles from sos1 mutants showed

significantly less Na+/H+ exchange activity

than the wild type, suggesting that the SOS1

Na+/H+ antiporter is located on the plasma

membrane (Qiu et al. 2002). The sos3 and sos2

mutants accumulate higher levels of Na+ than

wild-type plants. Isolated plasma membrane

vesicles from these mutants also showed signifi-

cantly less Na+/H+ exchange activity, and this

could be restored to the wild-type levels by the

addition of activated SOS2. The SOS3–SOS2

kinase complex activates SOS1 by phosphoryla-

tion (Quintero et al. 2002). SOS1 complemented

yeast mutants defective in Na+ transporters.

Coexpression of SOS2 and SOS3 significantly

increased SOS1-dependent Na+ tolerance of the

yeast mutant (Quintero et al. 2002). These results

show that SOS1 is a Na+/H+ antiporter involved

in Na+ efflux, which is activated by the SOS3–-

SOS2 kinase complex ( Qiu et al. 2002; Quintero

et al. 2002). Constitutive expression of a CaMV

35S promoter-driven active form of SOS2 could

rescue sos2 and sos3 mutants under salt stress

(Xiong et al. 2002). The expression of SOS1 is

stronger in cells bordering the xylem. Under salt

stress (100 mM NaCl), a higher concentration of

Na+ accumulates in shoots of sos1 mutants than

in those of the wild type. These results suggest

that SOS1 might retrieve Na+ from the xylem,

thereby preventing excess Na+ accumulation

in the shoot (Shi et al. 2002). Transgenic Arabi-

dopsis plants overexpressing SOS1 showed

improved salt tolerance and accumulated less

Na+ in the xylem transpirational stream as well

as in the shoot compared to the wild-type plants.

This demonstrated that Na+ efflux from the root

cells and long-distance Na+ transport within the

plant under salt stress are regulated by SOS1 (Shi

et al. 2003), which in turn is regulated by the

SOS3–SOS2 kinase complex. In addition to the

activation of Na+/H+ antiporter activity of SOS1,

SOS3–SOS2 kinase complex also is involved in

salt stress-induced upregulation of SOS1 expres-

sion (Shi et al. 2000). In the sos3 mutant, salt

stress could not induce SOS1 expression, while

the sos2 mutant is impaired in SOS1 expression

only in roots, but not in shoots. Interestingly,

SOS1 overexpressing transgenic Arabidopsis

showed a significantly higher steady-state level

of SOS1 mRNA under salt stress than that grown

under normal conditions. Since SOS1 was


overexpressed under the control of the CaMV

35S promoter, its higher mRNA abundance

under salt stress might be due to an increase in

SOS1 transcript stability (Shi et al. 2003). In

addition to positive control of Na+ exclusion

from the cytosol, the SOS pathway may also

negatively regulate Na+ influx systems. Expres-

sion of plant high-affinity K+ transporters,

AtHKT1, EcHKT1, and EcHKT2, in Xenopuslaevis oocytes showed that they could mediate

Na+ uptake. Transgenic wheat plants expressing

the wheat HKT1 in antisense orientation under

control of a ubiquitin promoter showed signifi-

cant downregulation of the native HKT1 tran-

script. These lines showed significantly less

22Na uptake and enhanced growth under salinity

when compared with the control (Laurie et al.

2002). These results suggest that HKT1 mediates

sodium uptake under salinity and salt tolerance

can be improved by downregulation of HKT1

expression. Consistent with this observation, a

suppressor genetic screen for the sos3 mutation

revealed that functional disruption of AtHKT1

could suppress the salt-sensitive phenotype of

sos3. In addition, the athkt1 mutation alleviates

the K+-deficient phenotype of the sos3 mutant

(Rus et al. 2001), which suggests that the K+-

deficient phenotype of the sos3 mutant might be

due to an excess of cytoplasmic Na+, as sos3

impairs the Na+ efflux mediated by SOS1.

These results suggest that ATHKT1 might func-

tion as low-affinity Na+ transporter that is

involved in Na+ influx under salinity. Significant

amounts of Na+ enter plant roots through

voltage-independent channels, which are proba-

bly regulated by Ca2+ concentrations. It is not

known whether activity of these channels and

their gene expression are also regulated by the

calcium-dependent SOS3–SOS2 kinase com-

plex. Thus, the SOS3–SOS2 kinase complex pos-

itively regulates Na+ efflux by activating SOS1

and upregulating the SOS1 transcript level and

may negatively regulate Na+ influx by downre-

gulating low-affinity Na+ transporter (HKT1)

genes to restore cellular ion homeostasis under

salt stress in plants (Fig. 7.2; Zhu 2002).

Hormonal Regulation of OsmoticStress in Plant

The plant hormones play a pivotal role in a vari-

ety of developmental processes and adaptive

stress responses to environmental stimuli in

plants. Cellular dehydration during the seed mat-

uration and vegetative growth stages induces an

increase in endogenous ABA levels, which con-

trol many dehydration-responsive genes. In

Arabidopsis plants, ABA regulates nearly 10%

of the protein-coding genes, a much higher

percentage than other plant hormones. Expres-

sion of the genes is mainly regulated by two

different families of bZIP transcription factors

(TFs), ABI5 in the seeds and AREB/ABFs in

the vegetative stage, in an ABA-responsive-

element (ABRE)-dependent manner (Fig. 7.2).

The SnRK2-AREB/ABF pathway governs the

majority of ABA-mediated ABRE-dependent

gene expression in response to osmotic stress

during the vegetative stage. In addition to

osmotic stress, the circadian clock and light

conditions also appear to participate in the regu-

lation of ABA-mediated gene expression, likely

conferring versatile tolerance and repressing

growth under stress conditions. Moreover, vari-

ous other TFs belonging to several classes,

including AP2/ERF, MYB, NAC, and HD-ZF,

have been reported to engage in ABA-mediated

gene expression. It was proposed that in roots

auxin and abscisic acid decrease resistance to

water flow. Therefore, an adaptation of plants to

osmotic stress may be an increase in root auxin

concentration and a decrease in leaf auxin con-

centration, or auxin signaling, to minimize water

loss. Indeed, Albacete et al. (2008) found an

increase in root auxin content, whereas leaf

auxin content of tomato stressed with 100 mM

NaCl decreased. A decrease in auxin content

has been shown in plants exposed to osmotic

stress. This has been reported for herbaceous

plants, for example, Anastatica hierochuntica

and Helianthus annuus, but also in the develop-

ing xylem of poplar (Junghans et al. 2006).


Changes in auxin response can be achieved by

regulation of auxin biosynthesis and auxin con-

jugation or by modulation of auxin signaling. In

addition, local auxin concentration and auxin

distribution may be regulated under stress by

changes in auxin transport. It was reported that

osmotic stress caused by increased salinity or

drought has an impact on polar auxin transport,

but response of the auxin transport machinery

seems to be plant and tissue specific. In Avena

mesocotyls, osmotic stress induced a drastic

increase in auxin transport (Sheldrake 1979),

while in Pisum hypocotyls a significant reduction

was observed (Kaldewey et al. 1974). In the

petioles of water-stressed cotton, the basipetal

auxin transport capacity was reduced to 30% of

that in control plants, but these authors did not

investigate whether the reduced capacity was

caused by decreased auxin transport or dimin-

ished auxin synthesis in the leaf blade.

IAA amidoconjugate synthases are encoded

by members of the GH3 gene family (Staswick

et al. 2002, 2005). Park et al. (2007) reported that

environmental stresses, including high salinity

and osmotic stress, induced expression of the

AtGH3.5 gene. Plants overexpressing AtGH3.5

exhibited growth reduction and enhanced stress

resistance, and thus, it suggests that GH3 auxin

conjugate synthases are involved in adjustment

of the hormonal balance in response to stress.

Recent literature showed that transcriptional

responses of rice to high NaCl concentrations

Salt Drought Cold

Osmotic stressIonic stress

Gene expression

Stress response &Tolerance

SOS3/CaBP

SOS2/PKS

SOS1

Ionichomeostasis

ABA Dependent

Proteinsynthesis

MYCRS, MYBRS(rd22)

bZIP

ABRE(rd29B)

DRE (rd 29A)

CBF4DREBS

CBF/DREB1

ABA independent

Ca+2

Fig. 7.2 Osmotic stress signaling and cross talk involved

in cold, drought, and salinity stress gene expression.

Osmotic stress signaling generated via cold, salinity, and

drought stress seems to be mediated by transcription

factors such as DREB2A, DREB2B, bZIP, and MYC

and MYB transcription activators, which interacts with

CRT/DRE, ABRE, or MYCRE/MYBRE elements in the

promoter of stress genes. Two different DRE/CRT-

binding proteins, DREB1/CBF and DREB2, distinguish

two different signal transduction pathways in response to

cold and drought stresses, respectively. Salinity mainly

works through SOS pathway reinstating cellular ionic

equilibrium


provide evidence that auxin signaling is affected

by salt stress. Jain and Khurana (2009) investi-

gated auxin-induced gene expression in rice and

found that 154 auxin-induced and 50 auxin-

repressed genes also responded to abiotic stress

such as drought, increased salinity, and cold.

A total of 51 of the auxin-responsive genes were

differentially expressed under all three of the above

stress conditions. Song et al. (2009) observed that,

out of the 31 predicted AuxIAA genes in rice, 15

were induced by drought while three showed

decreased expression. Under salt stress, eight Aux-

IAA genes were induced and eight repressed, and

seven of these genes showed the same tendency

under salt and drought stress, while three showed

the opposite regulation pattern.

Auxin and ABA are both involved in regula-

tion of plant water status, with opposite functions

in the shoot and complementary roles in the root.

To adapt root conductivity for water and allow

fine-tuning of stomatal aperture, signals for plant

water status have to be integrated. As a prerequi-

site, auxin and ABA signaling chains cannot just

exist in a linear manner but must form a network

that communicates by cross talk (Fig. 7.2).

Knowledge on cross talk has come from studies

of mutants impaired in ABA or auxin perception

and transgenic plants overexpressing signaling

components. Some of these mutants or trans-

genic lines showed pleiotropic effects that indi-

cated that ABA and auxin signal transduction are

both affected by the mutated gene or overex-

pressed protein. One pathway of ABA signal

transduction is through a mitogen-activated pro-

tein kinase (MAPK) cascade leading to activa-

tion of transcription factors (Fig. 7.1). Possible

targets are ABI3 (abscisic acid-insensitive 3) and

ABI5 (Fedoroff 2002). ABA perception activates

the MAP kinases AtMPK3 and AtMPK6

(Kovtun et al. 2000). These MAPKs are in a

cascade with the MAP3K ANP1 and possibly

the M2Ks AtMKK3 and AtMKK4. A cross-

point of ABA signaling branching off to auxin

signal transduction is ANP1. Activation of ANP1

interferes with activation of auxin signal trans-

duction (Kovtun et al. 1998). More support for

the hypothesis that an ABA-induced MAPK cas-

cade negatively regulates auxin responses comes

from studies of the hyl1 mutant, in which ANP1

and AtMKK3 are overexpressed. Another junc-

tion from ABA signaling to auxin signal trans-

duction is the transcription factor ABI3, involved

in ABA signal transduction. Suzuki et al. (2001)

investigated VIVIPAROUS1 (VP1), the maize

orthologue of ABI3. They reported that in plants

overexpressing VP1 application of ABA inhibits

auxin-induced lateral root formation. In contrast,

loss-of-function mutants of ABI3 need higher

concentrations of exogenous auxin to induce lat-

eral roots (Brady et al. 2003). The expression of

ABI3 in the root is responsive to both auxin and

ABA. Brady et al. (2003) concluded that ABI3 is

necessary for correct auxin signaling during lat-

eral root formation and speculated that ABI3

may interact with ARFs or AUX IAA proteins.

During osmotic stress signaling, it is interest-

ing to note that the stress-induced hormone level

changes and, therefore, extends the network of

hormonal cross talk during the stress response of

plants. A major part of this cross talk may

be that these hormones influence the biosynthesis

of each other, for example, it has been known for

a long time that auxin increases ethylene biosyn-

thesis by upregulation of 1-aminocyclopropane-

1-carboxylate (ACC) synthase (Abel et al. 1995).

However, inhibition of root growth by ethylene is

mediated by an increase of auxin synthesis in

aerial tissues (Ruzicka et al. 2007). Newly

synthesized auxin is transported to the root tip

and redirected via the auxin efflux carrier PIN2

to the root elongation zone. The resulting

increase of auxin in the root elongation zone

causes a reduction in root growth by inhibition

of root cell elongation (Ruzicka et al. 2007). In

contrast, there are data indicating that ethylene

and ABA negatively influence the biosynthesis

of each other (Cheng et al. 2009). The ABA

biosynthesis mutant aba2 exhibits upregulation

of the ethylene biosynthesis gene ACC oxidase

and produces significantly more ethylene than

wild-type plants. Similarly, the ethylene signal

transduction mutant ein2 hyperaccumulates

ABA (Ghassemian et al. 2000). However, con-

trary to data from analysis of mutants, Cheng

et al. (2002) observed that ABA enhances

ethylene synthesis in water-stressed poplar.


Therefore, data from analysis of mutants have to

be examined critically, since due to pleiotropic

effects, mutants may not reflect the situation in

wild-type plants. It will be interesting to deter-

mine the kinetics of changes in ABA, auxin, and

ethylene after onset of stress. These measure-

ments, combined with analysis of hormone

biosynthesis and perception mutants, will help

to unravel the high complexity of hormonal

cross talk during stress. ABA and IAA both

play important roles in the stress adaptation

of annual, herbaceous, and perennial woody

plants. The basic mechanisms on ABA and

IAA biosynthesis and signaling have been eluci-

dated in Arabidopsis. However, data on ABA

biosynthesis in poplar indicate that trees may

differ from annual plants with respect to locali-

zation of biosynthesis and indicate occurrence of

significant root-to-shoot transport of ABA in

trees. It will be worthwhile to investigate if dif-

ferences in hormone biosynthesis and transport

present adaptive mechanisms that are specific

to trees.

ROS Signaling During Osmotic Stressin Plants

Reactive oxygen species (ROS) are known to

accumulate during abiotic stresses in different

cellular compartments. It is now becoming

increasingly evident that even during stress,

ROS production is not necessarily a symptom

of cellular dysfunction but might represent a

necessary signal in adapting the cellular machin-

ery to the stressed conditions. ROS can modulate

many signal transduction pathways, such as

mitogen-activated protein kinase cascades, and

ultimately influence the activity of transcription

factors. However, the picture of ROS-mediated

signaling is still fragmentary and the issues of

ROS perception as well as the signaling specific-

ity remain open. ROS signals originating at dif-

ferent organelles have been shown to induce

large transcriptional changes and cellular repro-

gramming that can either protect the plant cell or

induce programmed cell death ( Davletova et al.

2005; Foyer and Noctor 2005; Gadjev et al.

2006; Rhoads et al. 2006). These types of repro-

gramming suggest the involvement, at least in

part, of organellar retrograde signaling in med-

iating ROS signals in the coordination of the

stress response between ROS generating orga-

nelles to the nucleus and perhaps directly

between the organelles themselves. Retrograde

signaling is largely divided into two phases: (1)

developmental control of organelle biogenesis

and (2) operational control, that is, rapid

adjustments in response to environmental and

developmental constraints (Pogson et al. 2008).

ROS generated in these organelles are consi-

dered to be important signaling molecules that

are involved in retrograde signaling under

abiotic stress conditions (Rhoads and Subbaiah

2007; Pogson et al. 2008; Woodson and Chory

2008). It has been shown that all the chloroplast-

to-nuclei retrograde signaling, including ROS

signaling, converges into a pathway regulated

by GUN1 (genome uncoupled 1) and ABI4

(ABA-insensitive 4) in Arabidopsis seedlings

(Koussevitzky et al. 2007). Mutants of gun1 and

abi4 were shown to be sensitive to heat stress,

suggesting the importance of retrograde signal-

ing to abiotic stress responses (Miller et al.

2007). To understand the role of organelle-to-

nuclei retrograde signaling, as well as intra-

organelle coordination during abiotic stress, the

tolerance and transcriptome reprogramming of

mutants deficient in these key regulators to the

abiotic stress should be tested. ROS signaling is

an integral part of the acclimation response of

plants to abiotic stresses. It is used to sense stress

due to enhanced ROS production caused by met-

abolic imbalances, as well as to actively send

different signals via enhanced production of

ROS at the apoplast by different RBOH (respira-

tory burst oxidase homolog) proteins. ROS sig-

naling during abiotic stress, namely, drought and

salinity, is highly integrated into many of the

other signaling networks that regulate plant

acclimation, including calcium, hormone, and

protein phosphorylation. In light of this view of

the integrated signaling network of plants, which

is responsible for the timely activation of differ-

ent acclimation pathways, it is easy to see why

some changes in ROS metabolism were found to


cause enhanced tolerance to stress, whereas other

changes were found to cause enhanced sensitiv-

ity. It is also difficult to predict how different

changes in ROS metabolism, engineered by dif-

ferent genetic manipulations, will affect crop

tolerance to various abiotic stresses. It is likely

that identifying key regulators which control

stress response activation (Baena-Gonzalez

et al. 2007; Baena-Gonzalez and Sheen 2008)

will provide crucial avenues to enhance crop

tolerance to abiotic stress. The way abiotic

stress-induced alterations would affect ROS

homeostasis and signaling will be an exciting

aspect of these studies. In considering the rela-

tionships between ROS metabolism, signaling,

and plant responses to various abiotic stresses

including drought or salinity, we should also

remember that these stresses almost always

occur in nature or in the field together with other

abiotic stress conditions. Such combinations

could include drought and heat, or drought

and cold, drought and nutrient, drought and

metal, etc., and may even include triple com-

binations such as drought, salinity, and heat and

many others. Such different stress combinations

affecting ROS metabolism and signaling are sub-

ject of active research in recent years (Keles and

Oncel 2002; Rizhsky et al. 2002; Hewezi et al.

2008; Koussevitzky et al. 2008), and it should be

taken into consideration while attempting to engi-

neer crops for abiotic stress tolerant to field

growth conditions (Mittler 2006).

Conclusion and Perspective

An understanding of the plant signaling path-

ways responding to osmotic stress is important

for both basic science and agriculture, because

drought and soil salinity are increasingly impor-

tant problems drastically affecting crop produc-

tivity. Since the mechanisms underlying plants

responses to osmotic stress are complicated,

many questions remain unanswered. Osmotic

stress caused reduction in growth and productiv-

ity of crop plants. Some of the events involved in

the regulation of osmotic stress tolerance by

ABA-dependent and independent pathways are

becoming clearer. However, forward and reverse

genetics approaches will continue to be impera-

tive to dissect complex osmotic stress signaling

pathways. Thorough characterization of mutant

phenotypes will provide an indication whether a

signaling component functions in a specific path-

way or is involved in multiple pathways. Further

proteomic and functional genomic analysis of

expression patterns, combined with biochemical

and molecular characterization of the compo-

nents of signaling complexes and other regu-

latory proteins, will be essential to firmly

establish specificity or cross talk of the signaling

pathways during osmotic stress. DNA sequence

of the AtMPK3 promoter for responses to

osmotic stress has also been identified, which

advances our understanding of the molecular

mechanisms controlling AtMPK3 expression

during osmotic stress in plants. Recent studies

also revealed that SnRK2.2, 2.3, and 2.6 are

core components of the ABA pathways whereas

SnRK2s are essential kinases for osmotic stress

signaling. Though the activation mechanism

of SnRK2s in the ABA pathway is elucidated,

regulatory mechanisms of SnRK2s in the ABA-

independent pathway remain obscure. Thus, fur-

ther analysis of SnRK2s must be a key study to

draw the whole osmotic stress signaling pathways.

Further proteomics, transcriptomics, and metabo-

lite profiling of osmotic stress signaling compo-

nents can bridge the gap in our current knowledge

of osmotic stress signaling networks in plants.

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Molecular Stress Physiology of Plants || Molecular Physiology of Osmotic Stress in Plants