2012_very good review_drought salt temp stress induced metabolic rearragements[1]

Journal of Experimental Botany, of 16doi:10.1093/jxb/err460

REVIEW PAPER

Drought, salt, and temperature stress-induced metabolicrearrangements and regulatory networks

Julia Krasensky and Claudia Jonak*

GMI–Gregor Mendel Institute of Molecular Plant Biology, Austrian Academy of Sciences, Dr. Bohr-Gasse 3, 1030 Vienna, Austria

* To whom correspondence should be addressed. E-mail: [email protected]

Received 7 October 2011; Revised 21 December 2011; Accepted 22 December 2011

Abstract

Plants regularly face adverse growth conditions, such as drought, salinity, chilling, freezing, and high temperatures.

These stresses can delay growth and development, reduce productivity, and, in extreme cases, cause plant death.

Plant stress responses are dynamic and involve complex cross-talk between different regulatory levels, including

adjustment of metabolism and gene expression for physiological and morphological adaptation. In this review, infor-

mation about metabolic regulation in response to drought, extreme temperature, and salinity stress is summarized and

the signalling events involved in mediating stress-induced metabolic changes are presented.

Key words: Abiotic stress, metabolism, protein kinase, signal transduction, transcription factor.

Plants in adverse environments

Plants frequently encounter unfavourable growth conditions.Climatic factors, such as extreme temperatures (heat, cold,

freezing), drought (deficient precipitation, drying winds), and

contamination of soils by high salt concentration, are major

abiotic environmental stressors that limit plant growth and

development, and thus agronomical yield, and play a major

role in determining the geographic distribution of plant

species. These different adverse but not necessarily lethal

conditions are generally known as stress.Environmental stress can disrupt cellular structures and

impair key physiological functions (Larcher, 2003). Drought,

salinity, and low temperature stress impose an osmotic stress

that can lead to turgor loss. Membranes may become dis-

organized, proteins may undergo loss of activity or be de-

natured, and often excess levels of reactive oxygen species

(ROS) are produced leading to oxidative damage. As a con-

sequence, inhibition of photosynthesis, metabolic dysfunc-tion, and damage of cellular structures contribute to growth

perturbances, reduced fertility, and premature senescence.

Different plant species are highly variable with respect to

their optimum environments, and a harsh environmental

condition, which is harmful for one plant species, might not

be stressful for another (Larcher, 2003; Munns and Tester,

2008). This is also reflected in the multitude of different

stress-response mechanisms. Two major strategies can bedistinguished: stress avoidance and stress tolerance (Levitt,

1980). Stress avoidance includes a variety of protective

mechanisms that delay or prevent the negative impact of a

stress factor on a plant. For example, cacti have constitu-

tively adapted their morphology, physiology, and metabo-

lism to hot and arid climates. Adaptation is stable and

inherited. On the other hand, stress tolerance is the potential

of a plant to acclimate to a stressful condition. For example,in summer, trees and herbaceous plants in northern latitudes

cannot withstand freezing. Exposure to chilling temperatures,

however, induces hardening and acclimated plants survive

winter temperatures far below freezing. Plants can increase

their resistance to various stresses including heat, saline, and

drought conditions in response to a period of gradual

exposure to these constraints. Acclimation is plastic and

reversible. The physiological modifications induced duringacclimation are diverse and are usually lost when the adverse

environmental condition does not persist.

Responses to environmental stresses occur at all levels of

organization. Cellular responses to stress include adjustments

of the membrane system, modifications of the cell wall

architecture, and changes in cell cycle and cell division. In

addition, plants alter metabolism in various ways, including

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production of compatible solutes (e.g. proline, raffinose, and

glycine betaine) that are able to stabilize proteins and cellular

structures and/or to maintain cell turgor by osmotic adjust-

ment, and redox metabolism to remove excess levels of ROS

and re-establish the cellular redox balance (Bartels and

Sunkar, 2005; Valliyodan and Nguyen, 2006; Munns and

Tester, 2008; Janska et al.; 2010). At the molecular level, gene

expression is modified upon stress (Chinnusamy et al., 2007;Shinozaki and Yamaguchi-Shinozaki, 2007) and epigenetic

regulation plays an important role in the regulation of gene

expression in response to environmental stress (Hauser et al.,

2011; Khraiwesh et al., 2011). Stress-inducible genes comprise

genes involved in direct protection from stress, including the

synthesis of osmoprotectants, detoxifying enzymes, and tran-

sporters, as well as genes that encode regulatory proteins such

as transcription factors, protein kinases, and phosphatases.

In this review, the focus is on metabolic adjustments in

response to high salt stress, drought, and extreme temper-

atures and our current knowledge of signal transduction

components that regulate metabolite levels under thesestress conditions will be summarized. Figures 1 and 2 give

an overview of the biosynthesis and degradation pathways

of important metabolites connected with stress tolerance

and will guide you through the next paragraphs.

Fig. 1. Schematic overview of amino acid, polyamine, and glycine betaine metabolism. Plants with enhanced or reduced activity of the

indicated enzymes show altered tolerance to abiotic stress. ApGSMT, Aphanothece halophytica glycine sarcosine methyl transferase (EC

2.1.1.156); ApDMT, Aphanothece halophytica dimethylglycine methyltransferase (EC 2.1.1.157); codA, choline oxidase (EC 1.1.3.17);

betA, choline dehydrogenase (EC 1.1.99.1); betB, betaine aldehyde dehydrogenase (EC 1.2.1.8); GAD, glutamate decarboxylase (EC

4.1.1.15); GABA-T, 4-aminobutyrate aminotransferase (EC 2.6.1.19); SSADH, succinic semialdehyde dehydrogenase (EC 1.2.1.16);

P5CS, 1-pyrroline-5-carboxylate synthetase (EC 2.7.2.11 and EC 1.2.1.41); P5CR, pyrroline-5-carboxylate reductase (EC 1.5.1.2);

ProDH, proline dehydrogenase (EC 1.5.99.8), P5CDH, 1-pyrroline-5-carboxylate dehydrogenase (EC 1.5.1.12); d-OAT, ornithine

d-aminotransferase (EC 2.6.1.13); ADC, arginine decarboxylase (EC 4.1.1.19); ODC, ornithine decarboxylase (EC 4.1.1.17); SPDS,

spermidine synthase (EC 2.5.1.16); SPMS, spermine synthase (EC 2.1.5.22); PAO, polyamine oxidase (EC 1.5.3.11); DAO, diamine

oxidase (EC 1.4.3.22).

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Amino acids

Accumulation of amino acids has been observed in many

studies on plants exposed to abiotic stress (Barnett and

Naylor, 1966; Draper, 1972; Handa et al., 1983; Rhodes

et al., 1986; Fougere et al., 1991; Kaplan et al., 2004;

Brosche et al., 2005; Zuther et al., 2007; Kempa et al.,

2008; Sanchez et al., 2008; Usadel et al., 2008; Luganet al., 2010). This increase might stem from amino acid

production and/or from enhanced stress-induced protein

breakdown. While the overall accumulation of amino

acids upon stress might indicate cell damage in some

species (Widodo et al., 2009), increased levels of specific

amino acids have a beneficial effect during stress acclima-

tion.

Proline

For many years, the capacity to accumulate proline has

been correlated with stress tolerance (Barnett and Naylor,

1966; Singh et al., 1972; Stewart and Lee, 1974). Proline is

considered to act as an osmolyte, a ROS scavenger, and

a molecular chaperone stabilizing the structure of proteins,

thereby protecting cells from damage caused by stress (Hare

and Cress, 1997; Rhodes et al., 1986; Verbruggen and

Hermans, 2008; Szabados and Savoure, 2010). Proline

accumulates in many plant species in response to different

environmental stresses including drought, high salinity, and

heavy metals. Interestingly, heat stress did not lead to

proline accumulation in tobacco and Arabidopsis plants

and induced proline accumulation rendered plants more

Fig. 2. Schematic overview of starch, fructan, sugar, and polyol metabolism. Plants with enhanced or reduced activity of the indicated

enzymes show altered tolerance to abiotic stress. SEX1, a-glucan water dikinase (EC 2.7.9.4); St. phos, starch phosphorylase (2.4.1.1);

BMY, b-amylase (EC 3.2.1.2); DPE2, glucanotransferase (EC 2.4.1.25); 1-SST, sucrose:sucrose 1-fructosyltransferase (EC 2.4.1.99); 6-

SFT, sucrose:fructan 6-fructosyltransferase (EC 2.4.1.10); FBF, fructan beta-fructosidase (EC 3.2.1.80); mtlD, mannitol-1-phosphate

dehydrogenase (EC 1.1.1.17); S6PDH, sorbitol-6-phosphate dehydrogenase (EC 1.1.1.200); SDH, sorbitol dehydrogenase (EC

1.1.1.14); Pase, unspecific phosphatase; MIPS, inositol-1-phosphate synthase (EC 5.5.1.4); IMP, inositol-1-phosphate phosphatase (EC

3.1.3.25); IMT, inositol methyltransferase (EC 2.1.1.40); GolS, galactinol synthase (EC 2.4.1.123); RS, raffinose synthase (EC 2.4.1.82),

StS, stachyose synthase (EC 2.4.1.67); TPS, trehalose-6-phosphate synthase (EC 2.4.1.15); TPP, trehalose-6-phosphate phosphatase

(EC 3.1.3.12).

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sensitive to heat (Rizhsky et al., 2004; Dobra et al., 2010;

Lv et al., 2011). Proline levels are determined by the

balance between biosynthesis and catabolism (Szabados

and Savoure, 2010). Proline is produced in the cytosol or

chloroplasts from glutamate, which is reduced to gluta-

mate-semialdehyde (GSA) by D-1-pyrroline-5-carboxylatesynthetase (P5CS). GSA can spontaneously convert to

pyrroline-5-carboxylate (P5C), which is then further re-duced by P5C reductase (P5CR) to proline. Proline is

degraded in mitochondria by proline dehydrogenase

(ProDH) and P5C dehydrogenase (P5CDH) to glutamate.

Stress conditions stimulate proline synthesis while proline

catabolism is enhanced during recovery from stress. Over-

expression of P5CS in tobacco and petunia led to increased

proline accumulation and enhanced salt and drought

tolerance (Kishor et al., 1995; Hong et al., 2000; Yamadaet al., 2005), whereas Arabidopsis P5CS1 knock-out plants

were impaired in stress-induced proline synthesis and were

hypersensitive to salinity (Szekely et al., 2008). Consis-

tently, ProDH antisense Arabidopsis accumulated more

proline and showed enhanced tolerance to freezing and

high salinity (Nanjo et al., 1999). It is discussed that, in an

alternative pathway, mitochondrial P5C can be produced

by d-ornithine aminotransferase (d-OAT) from ornithine(Miller et al., 2009). Over-expression of Arabidopsis d-OAT

has been shown to enhance proline levels and to increase

the stress tolerance of rice and tobacco (Roosens et al.,

2002; Qu et al., 2005) even though Arabidopsis plants

deficient in d-OAT accumulated proline in response to

stress and showed a salt stress tolerance similar to the wild

type (Funck et al., 2008).

GABA

The non-protein amino acid c-aminobutyric acid (GABA)

rapidly accumulates to high levels under different adverseenvironmental conditions (Shelp et al., 1999; Rhodes et al.,

1986; Kinnersley and Turano, 2000; Kaplan and Guy, 2004;

Kempa et al., 2008; Renault et al., 2010).

GABA is mainly synthesized from glutamate in the

cytosol by glutamate decarboxylase (GAD) and then

transported to the mitochondria. GABA transaminase

(GABA-T) and succinic semialdehyde dehydrogenase

(SSADH) convert GABA into succinate that feeds intothe TCA-cycle (Shelp et al., 1999; Fait et al., 2008). GABA

metabolism has been associated with carbon–nitrogen

balance and ROS scavenging (Bouche and Fromm, 2004;

Song et al., 2010; Liu et al., 2011). A functional GABA

shunt is important for stress tolerance. Salt stress enhances

the activity of enzymes involved in GABA metabolism

(Renault et al., 2010). Arabidopsis mutants defective in

GABA-T were hypersensitive to ionic stress and showedincreased levels of amino acid (including GABA), while

carbohydrate levels were decreased (Renault et al., 2010).

Disruption of the SSADH gene led to the accumulation of

ROS associated with dwarfism and hypersensitivity to UV-B

and heat stress (Bouche et al., 2003).

Amines

Polyamines

Polyamines (PA) are small aliphatic molecules positively

charged at cellular pH. Various stresses, such as drought,

salinity and cold, modulate PA levels, and high PA levels

have been positively correlated with stress tolerance (Yang

et al., 2007; Cuevas et al., 2008; Groppa and Benavides,

2008; Usadel et al., 2008; Kovacs et al., 2010; Quinet et al.,2010; Alcazar et al., 2011).

Putrescine, spermidine, and spermine are the most com-

mon PAs in higher plants. Putrescine is produced from either

ornithine or arginine by ornithine decarboxylase (ODC) and

arginine decarboxylase (ADC), respectively. Putrescine is

converted to spermidine by spermidine synthase (SPDS) and

then to spermine by spermine synthase (SPMS). Spermidine

and spermine are substrates of polyamine-oxidases (PAOs),which catalyse the back-conversion to putrescine.

PAs have been implicated in protecting membranes and

alleviating oxidative stress (Groppa and Benavides, 2008;

Alcazar et al., 2011; Hussain et al., 2011) but their specific

function in stress tolerance is not well understood. Analyses

of transgenic plants and of mutants involved in PA meta-

bolism clearly showed a positive role of PAs in stress

tolerance. Plants deficient in ADC1 or ADC2 had reducedputrescine levels and were hypersensitive to stress (Urano

et al., 2004; Cuevas et al., 2008), whereas constitutive or

stress-induced over-expression of ADC led to higher putres-

cine levels and enhanced drought and freezing tolerance

(Capell et al., 2004; Alcazar et al., 2010; Alet et al., 2011).

Arabidopsis plants over-expressing SPDS produced higher

amounts spermidine and were more resistant to drought, salt,

and cold stress (Kasukabe et al., 2004). Plants deficient inSPMS were unable to synthesize spermine and are hypersen-

sitive to salinity (Yamaguchi et al., 2006). Furthermore, the

introduction of ornithine decarboxylase (ODC) from mouse

enhanced polyamine levels and the tolerance of tobacco to

salt stress (Kumriaa and Rajam, 2002).

Glycine betaine

Glycine betaine (GB) is a quaternary ammonium compound

that occurs in a wide variety of plants, but its distribution

among plants is sporadic (Cromwell and Rennie, 1953).

Arabidopsis and many crop species do not accumulate GB.In plants that produce GB naturally, abiotic stress, such as

cold, drought, and salt stress, enhances GB accumulation

(Rhodes and Hanson, 1993; Chen and Murata, 2011).

GB can be synthesized from choline and glycine (Chen

and Murata, 2011). Introduction of the GB biosynthesis

pathway genes into non-accumulators improved their abil-

ity to tolerate abiotic stress conditions (Hayashi et al., 1997;

Alia et al., 1998; Sakamoto et al., 1998, 2000; Holmstromet al., 2000; Park et al., 2004; Waditee et al., 2005; Bansal

et al., 2011), pointing to the beneficial role of GB in stress

tolerance. Targeting GB production to the chloroplasts led

to a higher tolerance of plants against stress than in the

cytosol (Park et al., 2007). In salt-tolerant plant species, GB




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can also accumulate to osmotically significant levels (Rhodes

and Hanson, 1993). It has been suggested that GB protects

photosystem II, stabilizes membranes, and mitigates oxida-

tive damage (Chen and Murata, 2011).

Carbohydrates

Fructans

Plants accumulate carbohydrates such as starch and fruc-

tans as storage substances that can be mobilized during

periods of limited energy supply or enhanced energetic

demands. While most plant species use starch as their main

storage carbohydrate, several angiosperms, mainly from

regions with seasonal cold and dry periods, accumulatefructans (Hendry, 1993). Accumulation of fructans might

be advantageous, due to their high water solubility, their

resistance to crystallization at freezing temperatures, and

the fact that fructan synthesis functions normally under

low temperatures (Vijn and Smeekens, 1999; Livingston

et al., 2009). Furthermore, fructans can stabilize mem-

branes (Valluru and Van den Ende, 2008) and might

indirectly contribute to osmotic adjustment upon freezingand dehydration by the release of hexose sugars (Spollen

and Nelson, 1994; Olien and Clark, 1995).

Fructans are branched fructose polymers that are syn-

thesized in the vacuole by fructosyltransferases, including

1-SST and 6-SFT, which transfer fructose from sucrose to

the growing fructan chain (Vijn and Smeekens, 1999;

Livingston et al., 2009). The introduction of fructosyltrans-

ferases to fructan non-accumulating tobacco and rice plantsstimulated fructan production associated with enhanced

tolerance to low-temperature stress and drought (Pilonsmits

et al., 1995; Li et al., 2007; Kawakami et al., 2008).

Starch, mono- and disaccharides

Starch is composed of glucose polymers arranged intoosmotically inert granules. It serves as the main carbohy-

drate store in most plants and can be rapidly mobilized to

provide soluble sugars. Its metabolism is very sensitive to

changes in the environment. In addition to diurnal fluctua-

tions in starch levels, salt and drought stress generally leads

to a depletion of starch content and to the accumulation of

soluble sugars in leaves (Todaka et al., 2000; Kaplan and

Guy, 2004; Basu et al., 2007; Kempa et al., 2008). Sugarsthat accumulate in response to stress can function as

osmolytes to maintain cell turgor and have the ability to

protect membranes and proteins from stress damage

(Madden et al., 1985; Kaplan and Guy, 2004).

Starch is produced in plastids from excess sugars during

photosynthesis and involves ADP-glucose pyrophosphory-

lase (AGPase), starch synthases, branching enzymes, and

debranching enzymes. Phosphorylation of starch granulesby glucan-water dikinase (GWD) and phosphoglucan-water

dikinase (PWD) stimulates starch degradation. b-amylases

produce maltose from glucans. In the cytosol, maltose is

converted to glucose and, subsequently, fructose and sucrose

are formed (Tetlow et al., 2004; Kotting et al., 2010).

Hydrolysis of starch by the b-amolytic pathway repre-

sents the predominant pathway of starch degradation in

leaves under normal growth conditions and may also be

involved in stress-induced starch hydrolysis. Arabidopsis sex1

(starch excess 1) mutants, that are impaired in GWD activity,

were compromised in cold-induced malto-oligosaccharide,

glucose, and fructose accumulation during the early stages

of cold acclimation and sex1 plants that have been brieflypre-exposed to cold showed a reduced freezing tolerance

(Yano et al., 2005). Osmotic stress was shown to enhance

total b-amylase activity and to reduce light-stimulated

starch accumulation in wild-type Arabidopsis but not in

bam1 (bmy7) mutants, which appeared to be hypersensitive

to osmotic stress (Valerio et al., 2011). Similarly, BMY8

(BAM3) antisense plants accumulated high starch levels,

were impaired in cold-induced maltose, glucose, fructose,and sucrose accumulation, and showed a reduced tolerance

of photosystem II to low temperature stress (Kaplan and

Guy, 2005). Data by Zeeman et al. (2004) also suggest a role

of the phosphorolytic starch degradation pathway during

stress. Arabidopsis plants deficient in plastidial a-glucanphosphorylase showed enhanced formation of lesions sur-

rounded by cells with high starch levels after exposure to

low air humidity or salt stress.

Trehalose

The non-reducing disaccharide trehalose accumulates to high

amounts in some desiccation-tolerant plants, for example,Myrothamnus flabellifolius (Bianchi et al., 1993; Drennan

et al., 1993). At sufficient levels, trehalose can function as an

osmolyte and stabilize proteins and membranes (Paul et al.,

2008). In most angiosperms however, trehalose is present in

trace amounts and abiotic stress increases the levels of

trehalose only moderately (Fougere et al., 1991; Garg et al.,

2002; Kaplan et al., 2004; Panikulangara et al., 2004;

Rizhsky et al., 2004; Guy et al., 2008; Kempa et al., 2008).In plants, trehalose is synthesized in a two-step process

(Paul et al., 2008). Trehalose-6-phosphate synthase (TPS)

generates trehalose-6-phosphate (T6P) from UDP-glucose

and glucose-6-phosphate followed by dephosphorylation

to trehalose by trehalose-6-phosphate phosphatase (TPP).

Transgenic expression of trehalose biosynthesis genes showed

that enhanced trehalose metabolism can positively regulate

tolerance to abiotic stress, even though only a limited increasein trehalose content could be observed, excluding a direct

protective role of trehalose in these plants. Heterologous

expression of genes involved in the trehalose pathway from

E. coli or Saccharomyces cerevisiae enhanced tolerance to

drought, salt, and low temperature stress in several plant

species (Iordachescu and Imai, 2008). Over-expression of

different isoforms of TPS from rice conferred enhanced

resistance to salinity, cold, and/or drought (Li et al., 2011).Arabidopsis plants constitutively over-expressing AtTPS1

showed a small increase in trehalose and T6P levels and were

more tolerant to drought (Avonce et al., 2004). Consistently,

loss of TPS5 function, a TPS with a TPP domain, reduced

the basal thermotolerance of Arabidopsis (Suzuki et al., 2008).




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TPP activity and trehalose levels transiently increased in

response to cold stress in rice (Panikulangara et al., 2004) and

over-expression of OsTPP1 rendered rice more tolerant to

salinity and cold even though no increase in the trehalose

content could be observed (Ge et al., 2008). These genetically

engineered plants provide evidence that enhanced trehalose

metabolism can positively regulate stress tolerance, but the

precise role of T6P and trehalose during abiotic stressremains to be further elucidated.

Raffinose family oligosaccharides

Raffinose family oligosaccharides (RFO) such as raffinose,

stachyose, and verbascose accumulate in various plant

species during seed desiccation (Peterbauer and Richter,

2001) and in leaves of plants experiencing environmental

stress like cold, heat, drought or high salinity (Castonguay

and Nadeau, 1998; Gilmour et al., 2000; Taji et al., 2002;Cook et al., 2004; Kaplan et al., 2004; Peters et al., 2007;

Kempa et al., 2008; Usadel et al., 2008). RFOs have been

implicated in membrane protection and radical scavenging

(Hincha, 2003; Nishizawa et al., 2008). Biosynthesis of RFO

is initiated by the formation of galactinol from myo-inositol

and UDP-galactose by galactinol synthase (GolS). Sequen-

tial addition of galactose units, provided by galactinol, to

sucrose leads to the formation of raffinose and higher orderRFO (Peterbauer and Richter, 2001).

The role of the RFO pathway in acquiring stress

tolerance is not yet fully understood. Arabidopsis plants

over-expressing Arabidopsis GolS1 or GolS2 accumulated

high levels of galactinol and raffinose and were more

tolerant to drought and salinity stress (Taji et al., 2002;

Nishizawa et al., 2008). Similarly, constitutive and stress-

inducible expression of GolS1 from the resurrection plantBoea hygrometrica in tobacco conferred enhanced drought

tolerance (Wang et al., 2009). By contrast, increased raffinose

content in Arabidopsis plants constitutively expressing cu-

cumber GolS did not enhance freezing tolerance (Zuther

et al., 2004) and neither gols1 knock-out plants nor knock-

out mutants in the raffinose synthase gene, that were both

impaired in raffinose accumulation, showed any obvious

increase in sensitivity to heat or freezing stress, respectively(Panikulangara et al., 2004; Zuther et al., 2004).

Polyols

Polyols are implicated in stabilizing macromolecules and in

scavenging hydroxyl radicals, thereby preventing oxidative

damage of membranes and enzymes (Smirnoff and Cumbes,

1989; Shen et al., 1997). Accumulation of the straight-chain

polyols, mannitol and sorbitol, has been correlated with

stress tolerance in several plants species (Stoop et al., 1996).

Expression of mannitol-1-phosphate dehydrogenase (mtlD)from E. coli, which catalyses the reversible conversion of

fructose-6-phosphate to mannitol-1-phosphate in Arabidopsis,

tobacco, poplar, and wheat induced mannitol accumula-

tion and enhanced tolerance to salinity and/or water deficit

(Tarczynski et al., 1993; Thomas et al., 1995; Abebe et al.,

2003; Chen et al., 2005). Similarly, photosystem II was less

affected by salinity in persimmon trees that accumulated

sorbitol by over-expression of sorbitol-6-phosphate dehy-

drogenase (S6PDH) from apple (Gao et al., 2001).

The cyclic polyols myo-inositol, and its methylated

derivatives D-ononitol and D-pinitol, accumulate upon salt

stress in several halotolerant plant species (Adams et al.,

1992; Vernon and Bohnert, 1992; Ishitani et al., 1996;Sengupta et al., 2008). L-myo-inositol-1-phosphate synthase

(MIPS) forms myo-inositol-1-P from glucose-6-P, which is

dephosphorylated by myo-inositol 1-phosphate phosphatase

(IMP) to form myo-inositol. Inositol O-methyltransferase

(IMT) methylates inositol to form D-ononitol, which is

epimerized to D-pinitol. In line with a stress-protective role,

over-expression of MIPS and IMT from halotolerant plants

increased cyclic polyols levels and salt stress tolerance oftobacco (Sheveleva et al., 1997; Majee et al., 2004; Patra

et al., 2010).

Complexity of the metabolic response

Metabolic adjustments in response to unfavourable con-

ditions are dynamic and multifaceted and not only depend

on the type and strength of the stress, but also on the

cultivar and the plant species. Traditionally, metabolic

studies focused on single metabolites or groups of metabo-

lites. Recent advances in metabolic profiling allow increas-

ingly comprehensive metabolite analyses, illustrating thecomplexity of metabolic adjustments to stress. The meta-

bolic profiles of different plant species, including rice,

poplar, Vitis vinifera, Thellungiella halophila, and Arabidopsis

thaliana, have been analysed after exposure to drought

(Rizhsky et al., 2004; Cramer et al., 2007; Urano et al.,

2009), salinity (Gong et al., 2005; Cramer et al., 2007;

Gagneul et al., 2007; Kempa et al., 2008; Sanchez et al.,

2008; Janz et al., 2010; Lugan et al., 2010), and temperaturestress (Cook et al., 2004; Kaplan et al., 2004, 2007; Rizhsky

et al., 2004; Usadel et al., 2008; Espinoza et al., 2010;

Caldana et al., 2011).

Plants respond to stress by a progressive adjustment of

their metabolism with sustained, transient, early- and late-

responsive metabolic alterations. For example, raffinose and

proline accumulate to high levels over the course of several

days of salt exposure, drought, or cold, whereas centralcarbohydrate metabolism changes rapidly in a complex,

time-dependent manner.

Some metabolic changes are common to salt, drought,

and temperature stress, whereas others are specific. For

example, levels of amino acids, sugars, and sugar alcohols

typically increase in response to different stress conditions.

Notably, proline accumulates upon drought, salt, and low

temperature but not upon high temperature stress (Kaplanet al., 2004; Rizhsky et al., 2004; Gong et al., 2005; Cramer

et al., 2007; Gagneul et al., 2007; Kempa et al., 2008;

Sanchez et al., 2008; Usadel et al., 2008; Urano et al., 2009;

Lugan et al., 2010;). In most studies, organic acids and

TCA-cycle intermediates decreased in glycophytes after salt




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stress (Gong et al., 2005; Gagneul et al., 2007; Zuther et al.,

2007; Sanchez et al., 2008), but increased in response to

temperature or drought stress (Kaplan et al., 2004; Usadel

et al., 2008; Urano et al., 2009). A direct comparison of the

metabolic profile of Arabidopsis thaliana acclimated to

either low or high temperatures showed a significant over-

lap, but also major differences in metabolic adjustments

(Kaplan and Guy, 2004). A greater number of metabolitelevels changed specifically in response to cold than to heat,

pointing towards a strong impact of cold on plant metabo-

lism. Similarly, metabolic rearrangements after drought

were more profound than after heat stress and the

metabolic profile of Arabidopsis plants exposed to a combi-

nation of drought and heat was more similar to that of

drought-stressed than heat-stressed plants. Exposure of

drought-stressed plants to heat also induced unique meta-bolic responses highlighting the complexity of metabolic

adjustments in natural environments (Rizhsky et al., 2004).

Comparison of the metabolome of stress-tolerant acces-

sions, cultivars, or species, with that of stress-sensitive ones,

further show that, the role of metabolism in natural stress

tolerance is multifaceted and diverse (Gong et al., 2005;

Hannah et al., 2006; Zuther et al., 2007; Janz et al., 2010;

Korn et al., 2010; Lugan et al., 2010). Generally, stresstolerant plants have higher levels of stress-related metabo-

lites under normal growth conditions and/or accumulate

larger amounts of protective metabolites, such as proline

and soluble sugars, under unfavourable conditions, indicat-

ing that their metabolism is prepared for adverse growth

conditions. For example, analyses of the metabolic profile

of Arabidopsis accessions with different freezing tolerances

point to a crucial role of compatible solutes, including pro-line and raffinose, in freezing tolerance (Hannah et al.,

2006; Korn et al., 2010). Similarly, comparison of the meta-

bolome of cultivars or species with different salt tolerance

indicates a beneficial role of compatible solutes under

salinity conditions (Gong et al., 2005; Zuther et al., 2007;

Janz et al., 2010; Lugan et al., 2010). Interestingly, meta-

bolism of salt-tolerant plants appeared to be pre-adapted to

saline environments by constitutively high levels of someprotective metabolites such as proline and raffinose. Con-

sistent with classical studies, these recent metabolomic

analyses illustrate that plants have developed a whole range

of strategies to adapt their metabolism to unfavourable

growth conditions and that enhanced stress resistance is not

restricted to a single compound or mechanism. Different

plant species accumulate different metabolites (e.g. treha-

lose, proline, glycine betaine) and there is no absolute req-uirement for the accumulation of a specific metabolite for

acclimation to stress. In some cases, the flux through a meta-

bolic pathway, rather than the accumulation of a specific

metabolite per se, might contribute to stress tolerance.

Several metabolites/metabolic pathways that contribute

to stress acclimation also play a role in development.

Appropriate proline levels have been shown to be important

for embryo and flower development (Nanjo et al., 1999;Samach et al., 2000; Mattioli et al., 2008, 2009; Szekely

et al., 2008). GABA regulates pollen tube growth and

guidance (Wilhelmi and Preuss, 1996; Palanivelu et al.,

2003). Polyamines regulate several developmental processes

including embryogenesis, meristem, flower, and gameto-

phyte development (Hanzawa et al., 2000; Imai et al., 2004;

Alcazar et al., 2005; Gupta and Kaur, 2005; Deeb et al.,

2010; Zhang et al., 2011b). Trehalose metabolism is essential

for proper embryo maturation as well as for vegetative and

inflorescence development (Eastmond et al., 2002; vanDijken et al., 2004; Satoh-Nagasawa et al., 2006).

Signal transduction and transcriptionalcontrol involved in stress-induced metabolicchanges

Acclimation of plants to changes in their environment

requires a new state of cellular homeostasis achieved by a

delicate balance between multiple pathways. Hormones,secondary messengers, phosphatases, and protein kinases

are crucial components within the stress-induced signalling

network that regulates a multitude of biochemical and

physiological processes (Hirayama and Shinozaki, 2010).

As highlighted in the previous paragraphs, metabolic

adjustments to stress are vital for acquiring stress tolerance.

Transcriptional analyses of stress signalling mutants showed

that, in numerous mutants with altered stress tolerance,genes involved in the synthesis of stress-associated metabo-

lites are altered, and thus might be directly or indirectly

involved in metabolic adjustment upon stress. However, due

to post-transcriptional and post-translational modifications,

compartmentalization, metabolite stability, substrate avail-

ability, etc. changes in the abundance of transcripts are

not necessarily translated into changes in metabolite levels.

A start has been made to link signal transduction with themetabolite response upon drought, salt, and temperature

stress conditions including targeted analyses of metabolites

and metabolic profiling of mutants in signalling compo-

nents.

ABA and metabolic adjustments

Abscisic acid (ABA) is an integral regulator of abiotic stress

signalling (Cutler et al., 2010; Hubbard et al., 2010;

Raghavendra et al., 2010; Umezawa et al., 2010). ABA

quickly accumulates in response to different environmentalstress conditions and ABA-deficient plants have an altered

stress response. ABA promotes stomatal closure, inhibits

stomatal opening to reduce water loss by transpiration,

induces the expression of numerous stress-related genes, and

recent studies indicate a role in regulation of stress-induced

metabolic adjustments.

Comparison of the metabolic profile of Arabidopsis plants

treated with ABA, or exposed to high soil salinity, revealedABA-induced and ABA-independent steps of salt stress-

induced metabolic rearrangements (Kempa et al., 2008).

Both ABA and salt stress led to a depletion of starch

and the accumulation of maltose. However, subsequent

carbon flux appears to be differentially regulated. While




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glucose-6-phosphate and fructose-6-phosphate levels, and

the glucose/fructose ratio, decreased under salt stress con-

ditions, glucose-6-phosphate and fructose-6-phosphate levels

and the glucose/fructose ratio increased in response to ABA

treatment. Interestingly, ABA did not induce galactinol and

raffinose accumulation (Kempa et al., 2008). In support of

an ABA-independent induction of these sugars, Arabidopsis

mutants deficient in stress-induced ABA accumulation wereable to induce galactinol and raffinose under drought con-

ditions (Urano et al., 2009). Similarly, stress-induced accu-

mulation of citrate, malate, succinate (TCA cycle), and

GABA is ABA-independent (Kempa et al., 2008; Urano

et al., 2009). In contrast, accumulation of many osmotic

stress-induced proteinogenic amino acids, including proline,

were induced and depended on ABA (Kempa et al., 2008;

Urano et al., 2009).

Signalling towards proline accumulation

Proline plays a mulifunctional role in stress defence. Several

protein kinases important for salt, drought, and/or cold

tolerance, have been shown to regulate proline accumula-

tion (Fig. 3). SNF-related protein kinases 2 (SnRK2s) areactivated by osmotic stress (Boudsocq et al., 2004). Analyses

of Arabidopsis mutants revealed that the ABA-responsive

SnRKs 2.2, 2.3, and 2.6 are important for osmotic stress-

and ABA-induced proline accumulation, whereas SnRK2.9

appears to play a negative role in ABA-induced proline

accumulation (Fujii et al., 2011).

SnRK3s, which interact with calcineurin B-like (CBL)

calcium binding proteins, and are thus also known as CBLinteracting kinases (CIPKs), are also involved in modulat-

ing proline levels. In rice, over-expression of OsCIPK03 and

OsCIPK12 enhanced tolerance to cold and drought, re-

spectively, and increased the levels of proline under stress

conditions. However, over-expression of the closely related

OsCIPK15 enhanced salt tolerance without any significant

influence on stress-induced proline content indicating that

only a subset of SnRK3s are involved in signalling towards

proline accumulation in response to stress (Xiang et al.,

2007).

In addition to the above-mentioned calcium-responsive

protein kinases, Arabidopsis calcium-dependent protein

kinase 6 (CDPK6) (Xu et al., 2010) and soybean calmodulin

GmCAM4 (Yoo et al., 2005) positively regulate stresstolerance and proline content in Arabidopsis, suggesting

a central role for intracellular calcium signals in proline

metabolism.

MAPK (mitogen activated protein kinase) cascades regu-

late numerous processes including abiotic stress responses.

Several MAPKs are activated by cold, salt, and drought in

monocot and dicot plants (Jonak et al., 1996; Hoyos and

Zhang, 2000; Ichimura et al., 2000; Xiong and Yang, 2003)and genetic manipulation of MAPK signalling alters plant

tolerance to these stresses (Xiong and Yang, 2003; Shou

et al., 2004a, b; Teige et al., 2004). Recent data indicate a

positive role for MAPK-based signalling in stress-induced pro-

line accumulation (Kong et al., 2011; Zhang et al., 2011a).

While ABA and several stress-related protein kinases can

stimulate proline accumulation, a maize protein phospha-

tase type 2C negatively regulated stress-induced prolineaccumulation and tolerance to hyperosmotic stress (Liu

et al., 2009). PP2C type phosphatases PP2Cs are involved in

regulating diverse processes including development and

responses to environmental stress and have been shown to

regulate stress-induced MAPK and SnRK2 protein kinases

negatively (Schweighofer et al., 2004; Cutler et al., 2010;

Hubbard et al., 2010; Raghavendra et al., 2010; Umezawa

et al., 2010).Phospholipid metabolism is involved in mediating

hyperosmotic-stress responses (Testerink and Munnik, 2011).

Based on a pharmacological approach PLC-based signalling

has been implicated in salt-induced proline accumulation

(Parre et al., 2007).

Protein kinases involved in stress-induced changes incarbon metabolism

Carbohydrate metabolism is quickly modulated in response

to adverse environments. Plant glycogen synthase kinase 3

(GSK-3)/shaggy-like kinases appear to connect stress signal-

ling and carbon metabolism (Kempa et al., 2007). TheMedicago sativa MsK4 is a positive regulator of salt stress

tolerance. Plants over-expressing MsK4 have elevated levels

of sugars including raffinose and galactinol, increased

amounts of putrescine and amino acids under normal growth

conditions. Remarkably, MsK4 associates with starch gran-

ules and over-expression of MsK4 in Arabidopsis increased

the levels of starch and of several soluble sugars under salt

stress conditions (Kempa et al., 2007). These data are alsointeresting from an evolutionary point of view as GSK-3 was

originally identified as a regulator of the animal storage

carbohydrate glycogen (Woodgett and Cohen, 1984).

OsCIPK03, OsCIPK12, and the MAPK kinase ZmMKK4,

which promote proline accumulation under stress conditions,

Fig. 3. Stress-related protein kinases mediating solute accumula-

tion. AtSnRK2.3, AtSnRK2.4, AtSnRK2.6, CDPK6, OsCIPK03,

OsCIPK12, GhMPK6, ZmMKK4, and MsK4 positively regulate

tolerance to high salinity, drought, and/or cold stress. Plants over-

expressing these protein kinases and/or knock-outs of these

kinases have altered proline and/or sugar levels. (This figure is

available in colour at JXB online.)




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also stimulated stress-induced increase in soluble sugar

content (Xiang et al., 2007; Kong et al., 2011).

Further to the protein kinases mentioned, the negative

regulator of drought tolerance, SAL1, has been associated

with sugar and starch metabolism (Wilson et al., 2009).

Transcription factors regulating metabolite levels

Salinity, drought, and temperature stress have a strong

impact on gene expression. Many genes coding for enzymes

involved in cellular metabolism are differentially expressed

upon stress, and modulation of some stress-related tran-

scription factors have been shown to induce changes instress-associated metabolite levels.

The CBF/DREB1 proteins (C-repeat binding factor or

dehydration responsive element binding proteins) are mem-

bers of the AP2/EREBP (Apetala2/ethylene-responsive

element binding protein) family of transcription factors.

CBF1/DREB1B, CBF2/DREB1C, and CBF3/DREB1A

play an important role in the transcriptional response to

osmotic stress (Shinozaki and Yamaguchi-Shinozaki, 2007;Thomashow, 2010). Over-expression of these transcription

factors in Arabidopsis improved tolerance to freezing,

drought, and/or salt stress (Liu et al., 1998; Kasuga et al.,

1999; Gilmour et al., 2000, 2004) and CBF/DREB1 over-

expressing plants accumulated higher levels of proline and

soluble sugars (glucose, fructose, sucrose, and raffinose)

when grown under normal growth conditions and during

cold acclimation (Gilmour et al., 2000, 2004; Cook et al.,2004; Achard et al., 2008). The overall metabolic profile of

CBF3/DREB1A over-expressers grown at normal growth

temperatures resembled that of cold-exposed plants (Cook

et al., 2004; Maruyama et al., 2009).

DREB2A (dehydration responsive element binding pro-

tein 2A) is activated by osmotic stress and over-expression

of a constitutively active version of DREB2A, lacking the

inhibitory domain, improved tolerance to dehydration butonly slightly to freezing temperatures (Sakuma et al., 2006a).

In line with this tolerance pattern, the metabolite profile of

plants over-expressing constitutively active DREB2A was

more similar to that of dehydration-exposed than that of

cold-treated plants (Maruyama et al., 2009). While the global

metabolic profile of plants over-expressing the constitutively

active DREB2A resembled that of stressed plants, levels of

galactinol, raffinose, and proline were not increased. Prolineaccumulates in response to drought, but not to heat or

a combination of drought and heat (Rizhsky et al., 2004).

Interestingly, DREB2A has also been shown to promote heat

stress tolerance (Sakuma et al., 2006b).

Heat shock transcription factors (HSF) are central

regulators of heat stress responsive genes. In plants, HSFs

are encoded by a large gene family with different expres-

sion patterns and functions (von Koskull-Doring et al.,2007). Over expression of HsFA2 led to the constitutive

accumulation of galactinol and raffinose and improved

the tolerance of Arabidopsis plants to different environ-

mental stresses (Nishizawa et al., 2006, 2008; Ogawa et al.,

2007). Similarly, over-expression of HSF3/HsfA1b enhanced

thermo tolerance (Prandl et al., 1998) and raffinose levels

under normal and heat stress conditions (Panikulangara

et al., 2004).

The NAC domain family of plant-specific transcrip-

tional regulators are involved in developmental processes,

as well as in hormonal control and stress defence (Olsen

et al., 2005). OsNAC5 is induced by osmotic stress and

ABA. Over-expression of OsNAC5 enhanced stress-induced proline and soluble sugar levels and tolerance to

cold, salt, and drought stress (Takasaki et al., 2010; Song

et al., 2011) whereas knock-down lines were impaired

in proline and soluble sugar accumulation upon stress

exposure and were more sensitive to stress (Song et al.,

2011).

Levels of soluble sugars (glucose, fructose, and sucrose)

and proline, as well as glycine betaine, were also elevatedunder normal and stress conditions in Arabidopsis plants

over-expressing the rice Myb transcription factor, OsMyb4.

Accumulation of these metabolites was concomitant with

enhanced drought and freezing tolerance (Mattana et al.,

2005).

Conclusion

During the last decade, our knowledge on the importance of

metabolic adjustments to unfavourable growth conditions

has increased considerably. Natural stress tolerance is a very

complex process involving numerous metabolites and meta-bolic pathways. Analyses of metabolic adjustments of

plants with different levels of stress tolerance and transgenic

approaches provide important complementing evidence for

better understanding the role of different metabolites in

adjusting to harsh environments. Despite these substantial

gains, several questions remain to be addressed. For example,

the developmental stage of a plant is important for its

potential to tolerate an adverse condition and cellular meta-bolism changes during development. Thus, it will be in-

teresting to analyze how the developmental stage influences

the metabolic adjustment to stress conditions.

Metabolic networks are highly dynamic. Metabolites can

move between different cellular compartments. Since meta-

bolic profiling only reveals the steady-state level of metabo-

lites, detailed kinetics and flux analyses will be instrumental

for a better understanding of metabolic fluctuations inresponse to stress. Metabolic analysis at the subcellular level

in specific tissues is a further challenge.

Stress-induced signalling networks are well studied.

However, the signalling processes required for homeostasis

of basic cellular and metabolic processes in adverse environ-

ments are just starting to emerge. Better understanding of

how environmental changes are communicated via cellular

signal transduction to induce a co-ordinated metabolic res-ponse, and how the function of metabolic enzymes are

adjusted by transcriptional and post-translational modifica-

tions, are of basic scientific interest and will contribute to

meet the goal of increased plant stress tolerance and

productivity in an ever-changing environment.




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Acknowledgements

Work in our laboratory is supported by grants from the

Austrian Science Fund P 20375-B03 and the EU FP7-ITN

‘COSI’. We apologize to authors whose papers have not

been included due to space limitation in this review.

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