You are on page 1of 16

Journal of Experimental Botany Advance Access published January 30, 2012

Journal of Experimental Botany, Page 1 of 16 doi:10.1093/jxb/err460

REVIEW PAPER

Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks
Julia Krasensky and Claudia Jonak*
GMIGregor 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: claudia.jonak@gmi.oeaw.ac.at
Received 7 October 2011; Revised 21 December 2011; Accepted 22 December 2011
Downloaded from http://jxb.oxfordjournals.org/ at Max Perutz Library on February 13, 2012

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, information 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 (decient 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 disorganized, proteins may undergo loss of activity or be denatured, and often excess levels of reactive oxygen species (ROS) are produced leading to oxidative damage. As a consequence, inhibition of photosynthesis, metabolic dysfunction, 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 reected in the multitude of different stress-response mechanisms. Two major strategies can be distinguished: 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 constitutively adapted their morphology, physiology, and metabolism 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 modications induced during acclimation 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, modications of the cell wall architecture, and changes in cell cycle and cell division. In addition, plants alter metabolism in various ways, including

The Author [2012]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com

2 of 16 | Krasensky and Jonak


production of compatible solutes (e.g. proline, rafnose, and glycine betaine) that are able to stabilize proteins and cellular structures and/or to maintain cell turgor by osmotic adjustment, 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 modied 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 transporters, 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 temperatures and our current knowledge of signal transduction components that regulate metabolite levels under these stress 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.

Downloaded from http://jxb.oxfordjournals.org/ at Max Perutz Library on February 13, 2012

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).

Metabolic adjustment and signalling in response to stress | 3 of 16

Downloaded from http://jxb.oxfordjournals.org/ at Max Perutz Library on February 13, 2012

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); 6SFT, 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, unspecic 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, rafnose 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).

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; Lugan et 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 specic amino acids have a benecial effect during stress acclimation.

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

4 of 16 | Krasensky and Jonak


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 glutamate-semialdehyde (GSA) by D-1-pyrroline-5-carboxylate synthetase (P5CS). GSA can spontaneously convert to pyrroline-5-carboxylate (P5C), which is then further reduced 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. Overexpression 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; Yamada et al., 2005), whereas Arabidopsis P5CS1 knock-out plants were impaired in stress-induced proline synthesis and were hypersensitive to salinity (Szekely et al., 2008). Consistently, 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 decient in d-OAT accumulated proline in response to stress and showed a salt stress tolerance similar to the wild type (Funck et al., 2008).

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 common 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 specic function in stress tolerance is not well understood. Analyses of transgenic plants and of mutants involved in PA metabolism clearly showed a positive role of PAs in stress tolerance. Plants decient in ADC1 or ADC2 had reduced putrescine 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 putrescine 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 decient in SPMS were unable to synthesize spermine and are hypersensitive 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).

Downloaded from http://jxb.oxfordjournals.org/ at Max Perutz Library on February 13, 2012

GABA
The non-protein amino acid c-aminobutyric acid (GABA) rapidly accumulates to high levels under different adverse environmental 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 into the TCA-cycle (Shelp et al., 1999; Fait et al., 2008). GABA metabolism has been associated with carbonnitrogen 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 showed increased 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 dwarsm and hypersensitivity to UV-B and heat stress (Bouche et al., 2003).

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 ability to tolerate abiotic stress conditions (Hayashi et al., 1997; Alia et al., 1998; Sakamoto et al., 1998, 2000; Holmstrom et al., 2000; Park et al., 2004; Waditee et al., 2005; Bansal et al., 2011), pointing to the benecial 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

Metabolic adjustment and signalling in response to stress | 5 of 16


can also accumulate to osmotically signicant levels (Rhodes and Hanson, 1993). It has been suggested that GB protects photosystem II, stabilizes membranes, and mitigates oxidative damage (Chen and Murata, 2011). Hydrolysis of starch by the b-amolytic pathway represents 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 briey pre-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 decient in plastidial a-glucan phosphorylase showed enhanced formation of lesions surrounded by cells with high starch levels after exposure to low air humidity or salt stress.

Carbohydrates
Fructans
Plants accumulate carbohydrates such as starch and fructans 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, accumulate fructans (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 membranes (Valluru and Van den Ende, 2008) and might indirectly contribute to osmotic adjustment upon freezing and dehydration by the release of hexose sugars (Spollen and Nelson, 1994; Olien and Clark, 1995). Fructans are branched fructose polymers that are synthesized 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 fructosyltransferases to fructan non-accumulating tobacco and rice plants stimulated fructan production associated with enhanced tolerance to low-temperature stress and drought (Pilonsmits et al., 1995; Li et al., 2007; Kawakami et al., 2008).

Downloaded from http://jxb.oxfordjournals.org/ at Max Perutz Library on February 13, 2012

Trehalose
The non-reducing disaccharide trehalose accumulates to high amounts in some desiccation-tolerant plants, for example, Myrothamnus abellifolius (Bianchi et al., 1993; Drennan et al., 1993). At sufcient 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 increase in 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).

Starch, mono- and disaccharides


Starch is composed of glucose polymers arranged into osmotically inert granules. It serves as the main carbohydrate 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 uctuations 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). Sugars that 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 pyrophosphorylase (AGPase), starch synthases, branching enzymes, and debranching enzymes. Phosphorylation of starch granules by 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).

6 of 16 | Krasensky and Jonak


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 stress remains to be further elucidated. 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 dehydrogenase (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 of tobacco (Sheveleva et al., 1997; Majee et al., 2004; Patra et al., 2010).

Rafnose family oligosaccharides


Rafnose family oligosaccharides (RFO) such as rafnose, 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). Sequential addition of galactose units, provided by galactinol, to sucrose leads to the formation of rafnose and higher order RFO (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 rafnose and were more tolerant to drought and salinity stress (Taji et al., 2002; Nishizawa et al., 2008). Similarly, constitutive and stressinducible expression of GolS1 from the resurrection plant Boea hygrometrica in tobacco conferred enhanced drought tolerance (Wang et al., 2009). By contrast, increased rafnose content in Arabidopsis plants constitutively expressing cucumber GolS did not enhance freezing tolerance (Zuther et al., 2004) and neither gols1 knock-out plants nor knockout mutants in the rafnose synthase gene, that were both impaired in rafnose accumulation, showed any obvious increase in sensitivity to heat or freezing stress, respectively (Panikulangara et al., 2004; Zuther et al., 2004).

Downloaded from http://jxb.oxfordjournals.org/ at Max Perutz Library on February 13, 2012

Complexity of the metabolic response


Metabolic adjustments in response to unfavourable conditions 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 metabolites. Recent advances in metabolic proling allow increasingly comprehensive metabolite analyses, illustrating the complexity of metabolic adjustments to stress. The metabolic proles 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 temperature stress (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 lateresponsive metabolic alterations. For example, rafnose and proline accumulate to high levels over the course of several days of salt exposure, drought, or cold, whereas central carbohydrate metabolism changes rapidly in a complex, time-dependent manner. Some metabolic changes are common to salt, drought, and temperature stress, whereas others are specic. 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 (Kaplan et 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

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 accumulation and enhanced tolerance to salinity and/or water decit (Tarczynski et al., 1993; Thomas et al., 1995; Abebe et al.,

Metabolic adjustment and signalling in response to stress | 7 of 16


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 prole of Arabidopsis thaliana acclimated to either low or high temperatures showed a signicant overlap, but also major differences in metabolic adjustments (Kaplan and Guy, 2004). A greater number of metabolite levels changed specically in response to cold than to heat, pointing towards a strong impact of cold on plant metabolism. Similarly, metabolic rearrangements after drought were more profound than after heat stress and the metabolic prole of Arabidopsis plants exposed to a combination 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 metabolic responses highlighting the complexity of metabolic adjustments in natural environments (Rizhsky et al., 2004). Comparison of the metabolome of stress-tolerant accessions, 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, stress tolerant plants have higher levels of stress-related metabolites under normal growth conditions and/or accumulate larger amounts of protective metabolites, such as proline and soluble sugars, under unfavourable conditions, indicating that their metabolism is prepared for adverse growth conditions. For example, analyses of the metabolic prole of Arabidopsis accessions with different freezing tolerances point to a crucial role of compatible solutes, including proline and rafnose, in freezing tolerance (Hannah et al., 2006; Korn et al., 2010). Similarly, comparison of the metabolome of cultivars or species with different salt tolerance indicates a benecial role of compatible solutes under salinity conditions (Gong et al., 2005; Zuther et al., 2007; Janz et al., 2010; Lugan et al., 2010). Interestingly, metabolism of salt-tolerant plants appeared to be pre-adapted to saline environments by constitutively high levels of some protective metabolites such as proline and rafnose. Consistent 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. trehalose, proline, glycine betaine) and there is no absolute requirement for the accumulation of a specic metabolite for acclimation to stress. In some cases, the ux through a metabolic pathway, rather than the accumulation of a specic 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 ower 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, ower, and gametophyte 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 inorescence development (Eastmond et al., 2002; van Dijken et al., 2004; Satoh-Nagasawa et al., 2006).

Signal transduction and transcriptional control involved in stress-induced metabolic changes


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 metabolites are altered, and thus might be directly or indirectly involved in metabolic adjustment upon stress. However, due to post-transcriptional and post-translational modications, compartmentalization, metabolite stability, substrate availability, 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 the metabolite response upon drought, salt, and temperature stress conditions including targeted analyses of metabolites and metabolic proling of mutants in signalling components.

Downloaded from http://jxb.oxfordjournals.org/ at Max Perutz Library on February 13, 2012

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 environmental stress conditions and ABA-decient 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 prole of Arabidopsis plants treated with ABA, or exposed to high soil salinity, revealed ABA-induced and ABA-independent steps of salt stressinduced 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 ux appears to be differentially regulated. While

8 of 16 | Krasensky and Jonak


glucose-6-phosphate and fructose-6-phosphate levels, and the glucose/fructose ratio, decreased under salt stress conditions, 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 rafnose accumulation (Kempa et al., 2008). In support of an ABA-independent induction of these sugars, Arabidopsis mutants decient in stress-induced ABA accumulation were able to induce galactinol and rafnose under drought conditions (Urano et al., 2009). Similarly, stress-induced accumulation 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). inuence 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 stress tolerance and proline content in Arabidopsis, suggesting a central role for intracellular calcium signals in proline metabolism. MAPK (mitogen activated protein kinase) cascades regulate 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 proline accumulation (Kong et al., 2011; Zhang et al., 2011a). While ABA and several stress-related protein kinases can stimulate proline accumulation, a maize protein phosphatase type 2C negatively regulated stress-induced proline accumulation 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).

Downloaded from http://jxb.oxfordjournals.org/ at Max Perutz Library on February 13, 2012

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 accumulation (Fig. 3). SNF-related protein kinases 2 (SnRK2s) are activated 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 stressand 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 CBL interacting kinases (CIPKs), are also involved in modulating proline levels. In rice, over-expression of OsCIPK03 and OsCIPK12 enhanced tolerance to cold and drought, respectively, and increased the levels of proline under stress conditions. However, over-expression of the closely related OsCIPK15 enhanced salt tolerance without any signicant

Protein kinases involved in stress-induced changes in carbon 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 signalling and carbon metabolism (Kempa et al., 2007). The Medicago sativa MsK4 is a positive regulator of salt stress tolerance. Plants over-expressing MsK4 have elevated levels of sugars including rafnose and galactinol, increased amounts of putrescine and amino acids under normal growth conditions. Remarkably, MsK4 associates with starch granules 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 also interesting from an evolutionary point of view as GSK-3 was originally identied 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 accumulation. 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 overexpressing these protein kinases and/or knock-outs of these kinases have altered proline and/or sugar levels. (This gure is available in colour at JXB online.)

Metabolic adjustment and signalling in response to stress | 9 of 16


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). thermo tolerance (Prandl et al., 1998) and rafnose levels under normal and heat stress conditions (Panikulangara et al., 2004). The NAC domain family of plant-specic transcriptional 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 stressinduced 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 elevated under 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).

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 transcription factors have been shown to induce changes in stress-associated metabolite levels. The CBF/DREB1 proteins (C-repeat binding factor or dehydration responsive element binding proteins) are members 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 overexpressing plants accumulated higher levels of proline and soluble sugars (glucose, fructose, sucrose, and rafnose) 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 prole 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 protein 2A) is activated by osmotic stress and over-expression of a constitutively active version of DREB2A, lacking the inhibitory domain, improved tolerance to dehydration but only slightly to freezing temperatures (Sakuma et al., 2006a). In line with this tolerance pattern, the metabolite prole 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 prole of plants over-expressing the constitutively active DREB2A resembled that of stressed plants, levels of galactinol, rafnose, and proline were not increased. Proline accumulates 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 expression patterns and functions (von Koskull-Doring et al., 2007). Over expression of HsFA2 led to the constitutive accumulation of galactinol and rafnose and improved the tolerance of Arabidopsis plants to different environmental stresses (Nishizawa et al., 2006, 2008; Ogawa et al., 2007). Similarly, over-expression of HSF3/HsfA1b enhanced

Downloaded from http://jxb.oxfordjournals.org/ at Max Perutz Library on February 13, 2012

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 metabolic 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 metabolism changes during development. Thus, it will be interesting to analyze how the developmental stage inuences the metabolic adjustment to stress conditions. Metabolic networks are highly dynamic. Metabolites can move between different cellular compartments. Since metabolic proling only reveals the steady-state level of metabolites, detailed kinetics and ux analyses will be instrumental for a better understanding of metabolic uctuations in response to stress. Metabolic analysis at the subcellular level in specic 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 environments are just starting to emerge. Better understanding of how environmental changes are communicated via cellular signal transduction to induce a co-ordinated metabolic response, and how the function of metabolic enzymes are adjusted by transcriptional and post-translational modications, are of basic scientic interest and will contribute to meet the goal of increased plant stress tolerance and productivity in an ever-changing environment.

10 of 16 | Krasensky and Jonak

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.

Basu PS, Ali M, Chaturvedi SK. 2007. Osmotic adjustment increases water uptake, remobilization of assimilates and maintains photosynthesis in chickpea under drought. Indian Journal of Experimental Biology 45, 261267. Bianchi G, Gamba A, Limiroli R, Pozzi N, Elster R, Salamini F, Bartels D. 1993. The unusual sugar composition in leaves of the resurrection plant Myrothamnus abellifolia. Physiologia Plantarum 87, 223226. Bouche N, Fait A, Bouchez D, Moller SG, Fromm H. 2003. Mitochondrial succinic-semialdehyde dehydrogenase of the gammaaminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants. Proceedings of the National Academy of Sciences, USA 100, 68436848. Bouche N, Fromm H. 2004. GABA in plants: just a metabolite? Trends in Plant Science 9, 110115. Boudsocq M, Barbier-Brygoo H, Lauriere C. 2004. Identication of nine sucrose nonfermenting 1-related protein kinases 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. Journal of Biological Chemistry 279, 4175841766. Brosche M, Vinocur B, Alatalo ER, et al. 2005. Gene expression and metabolite proling of Populus euphratica growing in the Negev desert. Genome Biology 6, R101. Caldana C, Degenkolbe T, Cuadros-Inostroza A, Klie S, Sulpice R, Leisse A, Steinhauser D, Fernie AR, Willmitzer L, Hannah MA. 2011. High-density kinetic analysis of the metabolomic and transcriptomic response of Arabidopsis to eight environmental conditions. The Plant Journal 67, 869884. Capell T, Bassie L, Christou P. 2004. Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proceedings of the National Academy of Sciences, USA 101, 99099914. Castonguay Y, Nadeau P. 1998. Enzymatic control of soluble carbohydrate accumulation in cold-acclimated crowns of alfalfa. Crop Science 38, 11831189. Chen TH, Murata N. 2011. Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant, Cell and Environment 34, 120. Chen XM, Hu L, Lu H, Liu QL, Jiang XN. 2005. Overexpression of mtlD gene in transgenic Populus tomentosa improves salt tolerance through accumulation of mannitol. Tree Physiology 25, 12731281. Chinnusamy V, Zhu J, Zhu JK. 2007. Cold stress regulation of gene expression in plants. Trends in Plant Science 12, 444451. Cook D, Fowler S, Fiehn O, Thomashow MF. 2004. A prominent role for the CBF cold response pathway in conguring the lowtemperature metabolome of Arabidopsis. Proceedings of the National Academy of Sciences, USA 101, 1524315248. Cramer GR, Ergul A, Grimplet J, et al. 2007. Water and salinity stress in grapevines: early and late changes in transcript and metabolite proles. Functional and Integrative Genomics 7, 111134. Cromwell BT, Rennie SD. 1953. The biosynthesis and metabolism of betaines in plants. 1. The estimation and distribution of glycinebetaine (betaine) in Beta vulgaris L. and other plants. Biochemical Journal 55, 189192.
Downloaded from http://jxb.oxfordjournals.org/ at Max Perutz Library on February 13, 2012

References
Abebe T, Guenzi AC, Martin B, Cushman JC. 2003. Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity. Plant Physiology 131, 17481755. Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P. 2008. The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growthrepressing DELLA proteins via its effect on gibberellin metabolism. The Plant Cell 20, 21172129. Adams P, Thomas JC, Vernon DM, Bohnert HJ, Jensen RG. 1992. Distinct cellular and organismic responses to salt stress. Plant and Cell Physiology 33, 12151223. Alcazar R, Cuevas JC, Planas J, Zarza X, Bortolotti C, Carrasco P, Salinas J, Tiburcio AF, Altabella T. 2011. Integration of polyamines in the cold acclimation response. Plant Science 180, 3138. Alcazar R, Garcia-Martinez JL, Cuevas JC, Tiburcio AF, Altabella T. 2005. Overexpression of ADC2 in Arabidopsis induces dwarsm and late-owering through GA deciency. The Plant Journal 43, 425436. Alcazar R, Planas J, Saxena T, Zarza X, Bortolotti C, Cuevas J, Bitrian M, Tiburcio AF, Altabella T. 2010. Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants overexpressing the homologous arginine decarboxylase 2 gene. Plant Physiology and Biochemistry 48, 547552. Alet AI, Sanchez DH, Cuevas JC, et al. 2011. Putrescine accumulation in Arabidopsis thaliana transgenic lines enhances tolerance to dehydration and freezing stress. Plant Signaling and Behavior 6, 278286. Alia, Hayashi H, Sakamoto A, Murata N. 1998. Enhancement of the tolerance of Arabidopsis to high temperatures by genetic engineering of the synthesis of glycinebetaine. The Plant Journal 16, 155161. Avonce N, Leyman B, Mascorro-Gallardo JO, Van Dijck P, Thevelein JM, Iturriaga G. 2004. The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiology 136, 36493659. Bansal KC, Goel D, Singh AK, Yadav V, Babbar SB, Murata N. 2011. Transformation of tomato with a bacterial codA gene enhances tolerance to salt and water stresses. Journal of Plant Physiology 168, 12861294. Barnett NM, Naylor AW. 1966. Amino acid and protein metabolism in Bermuda grass during water stress. Plant Physiology 41, 12221230. Bartels D, Sunkar R. 2005. Drought and salt tolerance in plants. Critical Reviews in Plant Sciences 24, 2358.

Metabolic adjustment and signalling in response to stress | 11 of 16


Cuevas JC, Lopez-Cobollo R, Alcazar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A. 2008. Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiology 148, 10941105. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR. 2010. Abscisic acid: emergence of a core signaling network. Annual Review of Plant Biology 61, 651679. Deeb F, van der Weele CM, Wolniak SM. 2010. Spermidine is a morphogenetic determinant for cell fate specication in the male gametophyte of the water fern Marsilea vestita. The Plant Cell 22, 36783691. Dobra J, Motyka V, Dobrev P, Malbeck J, Prasil IT, Haisel D, Gaudinova A, Havlova M, Gubis J, Vankova R. 2010. Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. Journal of Plant Physiology 167, 13601370. Draper SR. 1972. Amino-acid changes associated with lowtemperature treatment of Lolium-perenne. Phytochemistry 11, 639641. Drennan PM, Smith MT, Goldsworthy D, van Staden J. 1993. The occurence of trehalose in the leaves of the desiccation-tolerant angiosperm Myrothamnus abellifolius Welw. Journal of Plant Physiology 142, 493496. Eastmond PJ, van Dijken AJ, Spielman M, Kerr A, Tissier AF, Dickinson HG, Jones JD, Smeekens SC, Graham IA. 2002. Trehalose-6-phosphate synthase 1, which catalyses the rst step in trehalose synthesis, is essential for Arabidopsis embryo maturation. The Plant Journal 29, 225235. Espinoza C, Degenkolbe T, Caldana C, Zuther E, Leisse A, Willmitzer L, Hincha DK, Hannah MA. 2010. Interaction with diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in Arabidopsis. PLoS One 5, e14101. Fait A, Fromm H, Walter D, Galili G, Fernie AR. 2008. Highway or byway: the metabolic role of the GABA shunt in plants. Trends in Plant Science 13, 1419. Fougere F, Le Rudulier D, Streeter JG. 1991. Effects of salt stress on amino acid, organic acid, and carbohydrate composition of roots, bacteroids, and cytosol of alfalfa (Medicago sativa L.). Plant Physiology 96, 12281236. Fujii H, Verslues PE, Zhu JK. 2011. Arabidopsis decuple mutant reveals the importance of SnRK2 kinases in osmotic stress responses in vivo. Proceedings of the National Academy of Sciences, USA 108, 17171722. Funck D, Stadelhofer B, Koch W. 2008. Ornithinedelta-aminotransferase is essential for arginine catabolism but not for proline biosynthesis. BMC Plant Biology 8, 40. Gagneul D, Ainouche A, Duhaze C, Lugan R, Larher FR, Bouchereau A. 2007. A reassessment of the function of the so-called compatible solutes in the halophytic Plumbaginaceae Limonium latifolium. Plant Physiology 144, 15981611. Gao M, Tao R, Miura K, Dandekar AM, Sugiura A. 2001. Transformation of Japanese persimmon (Diospyros kaki Thunb.) with apple cDNA encoding NADP-dependent sorbitol-6-phosphate dehydrogenase. Plant Science 160, 837845. Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ. 2002. Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proceedings of the National Academy of Sciences, USA 99, 1589815903. Ge LF, Chao DY, Shi M, Zhu MZ, Gao JP, Lin HX. 2008. Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta 228, 191201. Gilmour SJ, Fowler SG, Thomashow MF. 2004. Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Molecular Biology 54, 767781. Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF. 2000. Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiology 124, 18541865. Gong Q, Li P, Ma S, Indu Rupassara S, Bohnert HJ. 2005. Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. The Plant Journal 44, 826839. Groppa MD, Benavides MP. 2008. Polyamines and abiotic stress: recent advances. Amino Acids 34, 3545. Gupta AK, Kaur N. 2005. Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. Journal of Biosciences 30, 761776. Guy C, Kaplan F, Kopka J, Selbig J, Hincha DK. 2008. Metabolomics of temperature stress. Physiologia Plantarum 132, 220235. Handa S, Bressan RA, Handa AK, Carpita NC, Hasegawa PM. 1983. Solutes contributing to osmotic adjustment in cultured plantcells adapted to water-stress. Plant Physiology 73, 834843. Hannah MA, Wiese D, Freund S, Fiehn O, Heyer AG, Hincha DK. 2006. Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiology 142, 98112. Hanzawa Y, Takahashi T, Michael AJ, Burtin D, Long D, Pineiro M, Coupland G, Komeda Y. 2000. ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO Journal 19, 42484256. Hare PD, Cress WA. 1997. Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regulation 21, 79102. Hauser MT, Aufsatz W, Jonak C, Luschnig C. 2011. Transgenerational epigenetic inheritance in plants. Biochimica et Biophysica Acta 1809, 459468. Hayashi H, Alia, Mustardy L, Deshnium P, Ida M, Murata N. 1997. Transformation of Arabidopsis thaliana with the codA gene for choline oxidase; accumulation of glycinebetaine and enhanced tolerance to salt and cold stress. The Plant Journal 12, 133142. Hendry GAF. 1993. Evolutionary origins and natural functions of fructans: a climatological, biogeography and mechanistic appraisal. New Phytologist 123, 314. Hincha DK. 2003. Effects of calcium-induced aggregation on the physical stability of liposomes containing plant glycolipids. Biochimica et Biophysica Acta 1611, 180186.

Downloaded from http://jxb.oxfordjournals.org/ at Max Perutz Library on February 13, 2012

12 of 16 | Krasensky and Jonak


Hirayama T, Shinozaki K. 2010. Research on plant abiotic stress responses in the post-genome era: past, present and future. The Plant Journal 61, 10411052. Holmstrom KO, Somersalo S, Mandal A, Palva TE, Welin B. 2000. Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine. Journal of Experimental Botany 51, 177185. Hong Z, Lakkineni K, Zhang Z, Verma DP. 2000. Removal of feedback inhibition of delta(1)-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiology 122, 11291136. Hoyos ME, Zhang S. 2000. Calcium-independent activation of salicylic acid-induced protein kinase and a 40-kilodalton protein kinase by hyperosmotic stress. Plant Physiology 122, 13551363. Hubbard KE, Nishimura N, Hitomi K, Getzoff ED, Schroeder JI. 2010. Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genesand Development 24, 16951708. Hussain SS, Ali M, Ahmad M, Siddique KH. 2011. Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnology Advances 29, 300311. Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K. 2000. Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. The Plant Journal 24, 655665. Imai A, Matsuyama T, Hanzawa Y, et al. 2004. Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiology 135, 15651573. Iordachescu M, Imai R. 2008. Trehalose biosynthesis in response to abiotic stresses. Journal of Integrative Plant Biology 50, 12231229. Ishitani M, Majumder AL, Bornhouser A, Michalowski CB, Jensen RG, Bohnert HJ. 1996. Coordinate transcriptional induction of myo-inositol metabolism during environmental stress. The Plant Journal 9, 537548. Janska A, Marsik P, Zelenkova S, Ovesna J. 2010. Cold stress and acclimation: what is important for metabolic adjustment? Plant Biology 12, 395405. Janz D, Behnke K, Schnitzler JP, Kanawati B, SchmittKopplin P, Polle A. 2010. Pathway analysis of the transcriptome and metabolome of salt sensitive and tolerant poplar species reveals evolutionary adaption of stress tolerance mechanisms. BMC Plant Bioogy 10, 150. Jonak C, Kiegerl S, Ligterink W, Barker PJ, Huskisson NS, Hirt H. 1996. Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proceedings of the National Academy of Sciences, USA 93, 1127411279. Kaplan F, Guy CL. 2004. beta-Amylase induction and the protective role of maltose during temperature shock. Plant Physiology 135, 16741684. Kaplan F, Guy CL. 2005. RNA interference of Arabidopsis betaamylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efciency to freezing stress. The Plant Journal 44, 730743. Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL. 2004. Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiology 136, 41594168. Kaplan F, Kopka J, Sung DY, Zhao W, Popp M, Porat R, Guy CL. 2007. Transcript and metabolite proling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modications in metabolite content. The Plant Journal 50, 967981. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K. 1999. Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nature Biotechnology 17, 287291. Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S. 2004. Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant and Cell Physiology 45, 712722. Kawakami A, Sato Y, Yoshida M. 2008. Genetic engineering of rice capable of synthesizing fructans and enhancing chilling tolerance. Journal of Experimental Botany 59, 793802. Kempa S, Krasensky J, Dal Santo S, Kopka J, Jonak C. 2008. A central role of abscisic acid in stress-regulated carbohydrate metabolism. PLoS One 3, e3935. Kempa S, Rozhon W, Samaj J, et al. 2007. A plastid-localized glycogen synthase kinase 3 modulates stress tolerance and carbohydrate metabolism. The Plant Journal 49, 10761090. Khraiwesh B, Zhu JK, Zhu J. 2011. Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochimica et Biophysica Acta http://dx.doi.org/10.1016/j.bbagrm.2011.05.001. Kinnersley AM, Turano FJ. 2000. Gamma aminobutyric acid (GABA) and plant responses to stress. Critical Reviews in Plant Sciences 19, 479509. Kishor P, Hong Z, Miao GH, Hu C, Verma D. 1995. Overexpression of [delta]-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiology 108, 13871394. Kong X, Pan J, Zhang M, Xing X, Zhou Y, Liu Y, Li D. 2011. ZmMKK4, a novel group C mitogen-activated protein kinase kinase in maize (Zea mays), confers salt and cold tolerance in transgenic Arabidopsis. Plant, Cell and Environment 34, 12911303. Korn M, Gartner T, Erban A, Kopka J, Selbig J, Hincha DK. 2010. Predicting Arabidopsis freezing tolerance and heterosis in freezing tolerance from metabolite composition. Molecular Plant 3, 224235. Kotting O, Kossmann J, Zeeman SC, Lloyd JR. 2010. Regulation of starch metabolism: the age of enlightenment? Current Opinion in Plant Biology 13, 321329. Kovacs Z, Simon-Sarkadi L, Szucs A, Kocsy G. 2010. Differential effects of cold, osmotic stress and abscisic acid on polyamine accumulation in wheat. Amino Acids 38, 623631. Kumriaa R, Rajam MV. 2002. Ornithine decarboxylase transgene in tobacco affects polyamines, in vitro-morphogenesis and response to salt stress. Journal of Plant Physiology 159, 933990. Larcher W. 2003. Physiological plant ecology, 4th edn. Springer. Levitt J, (ed). 1980. Responses of plants to environmental stresses. New York: Academic Press. Li HJ, Yang AF, Zhang XC, Gao F, Zhang JR. 2007. Improving freezing tolerance of transgenic tobacco expressing sucrose: sucrose

Downloaded from http://jxb.oxfordjournals.org/ at Max Perutz Library on February 13, 2012

Metabolic adjustment and signalling in response to stress | 13 of 16


1-fructosyltransferase gene from Lactuca sativa. Cell Tisssue and Organ Culture 89, 3748. Li HW, Zang BS, Deng XW, Wang XP. 2011. Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 234, 10071018. Liu C, Zhao L, Yu G. 2011. The dominant glutamic acid metabolic ux to produce gamma-amino butyric acid over proline in Nicotiana tabacum leaves under water stress relates to its signicant role in antioxidant activity. Journal of Integrative Plant Biology 53, 608618. Liu L, Hu X, Song J, Zong X, Li D. 2009. Over-expression of a Zea mays L. protein phosphatase 2C gene (ZmPP2C) in Arabidopsis thaliana decreases tolerance to salt and drought. Journal of Plant Physiology 166, 531542. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, YamaguchiShinozaki K, Shinozaki K. 1998. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and lowtemperature-responsive gene expression, respectively, in Arabidopsis. The Plant Cell 10, 13911406. Livingston DP, Hincha DK, Heyer AG. 2009. Fructan and its relationship to abiotic stress tolerance in plants. Cellular and Molecular Life Sciences 66, 20072023. Lugan R, Niogret MF, Leport L, Guegan JP, Larher FR, Savoure A, Kopka J, Bouchereau A. 2010. Metabolome and water homeostasis analysis of Thellungiella salsuginea suggests that dehydration tolerance is a key response to osmotic stress in this halophyte. The Plant Journal 64, 215229. Lv WT, Lin B, Zhang M, Hua XJ. 2011. Proline accumulation is inhibitory to Arabidopsis seedlings during heat stress. Plant Physiology 156, 19211933. Madden TD, Bally MB, Hope MJ, Cullis PR, Schieren HP, Janoff AS. 1985. Protection of large unilamellar vesicles by trehalose during dehydration: retention of vesicle contents. Biochimica et Biophysica Acta 817, 6774. Majee M, Maitra S, Dastidar KG, Pattnaik S, Chatterjee A, Hait NC, Das KP, Majumder AL. 2004. A novel salt-tolerant L-myo-inositol-1-phosphate synthase from Porteresia coarctata (Roxb.) Tateoka, a halophytic wild rice: molecular cloning, bacterial overexpression, characterization, and functional introgression into tobacco-conferring salt tolerance phenotype. Journal of Biological Chemistry 279, 2853928552. Maruyama K, Takeda M, Kidokoro S, et al. 2009. Metabolic pathways involved in cold acclimation identied by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiology 150, 19721980. Mattana M, Biazzi E, Consonni R, Locatelli F, Vannini C, Provera S, Coraggio I. 2005. Overexpression of Osmyb4 enhances compatible solute accumulation and increases stress tolerance of Arabidopsis thaliana. Physiologica Plantarum 125, 212223. Mattioli R, Falasca G, Sabatini S, Altamura MM, Costantino P, Trovato M. 2009. The proline biosynthetic genes P5CS1 and P5CS2 play overlapping roles in Arabidopsis ower transition but not in embryo development. Physiologia Plantarum 137, 7285. Mattioli R, Marchese D, DAngeli S, Altamura MM, Costantino P, Trovato M. 2008. Modulation of intracellular proline levels affects owering time and inorescence architecture in Arabidopsis. Plant Molecular Biology 66, 277288. Miller G, Honig A, Stein H, Suzuki N, Mittler R, Zilberstein A. 2009. Unraveling delta1-pyrroline-5-carboxylate-proline cycle in plants by uncoupled expression of proline oxidation enzymes. Journal of Biological Chemistry 284, 2648226492. Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651681. Nanjo T, Kobayashi M, Yoshiba Y, Sanada Y, Wada K, Tsukaya H, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K. 1999. Biological functions of proline in morphogenesis and osmotolerance revealed in antisense transgenic Arabidopsis thaliana. The Plant Journal 18, 185193. Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S. 2006. Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. The Plant Journal 48, 535547. Nishizawa A, Yabuta Y, Shigeoka S. 2008. Galactinol and rafnose constitute a novel function to protect plants from oxidative damage. Plant Physiology 147, 12511263. Ogawa D, Yamaguchi K, Nishiuchi T. 2007. High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth. Journal of Experimental Botany 58, 33733383. Olien CR, Clark JL. 1995. Freeze-induced changes in carbohydrates associated with hardiness of barley and rye. Crop Science 35, 496502. Olsen AN, Ernst HA, Leggio LL, Skriver K. 2005. NAC transcription factors: structurally distinct, functionally diverse. Trends in Plant Science 10, 7987. Palanivelu R, Brass L, Edlund AF, Preuss D. 2003. Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114, 4759. Panikulangara TJ, Eggers-Schumacher G, Wunderlich M, Stransky H, Schof F. 2004. Galactinol synthase1. A novel heat shock factor target gene responsible for heat-induced synthesis of rafnose family oligosaccharides in Arabidopsis. Plant Physiology 136, 31483158. Park EJ, Jeknic Z, Sakamoto A, DeNoma J, Yuwansiri R, Murata N, Chen TH. 2004. Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and owers from chilling damage. The Plant Journal 40, 474487. Park EJ, Jeknic Z, Chen TH, Murata N. 2007. The codA transgene for glycinebetaine synthesis increases the size of owers and fruits in tomato. Plant Biotechnology Journal 5, 422430. Parre E, Ghars MA, Leprince AS, Thiery L, Lefebvre D, Bordenave M, Richard L, Mazars C, Abdelly C, Savoure A. 2007. Calcium signaling via phospholipase C is essential for proline accumulation upon ionic but not nonionic hyperosmotic stresses in Arabidopsis. Plant Physiology 144, 503512. Patra B, Ray S, Richter A, Majumder AL. 2010. Enhanced salt tolerance of transgenic tobacco plants by co-expression of PcINO1
Downloaded from http://jxb.oxfordjournals.org/ at Max Perutz Library on February 13, 2012

14 of 16 | Krasensky and Jonak


and McIMT1 is accompanied by increased level of myo-inositol and methylated inositol. Protoplasma 245, 143152. Paul MJ, Primavesi LF, Jhurreea D, Zhang YH. 2008. Trehalose metabolism and signaling. Annual Review of Plant Biology 59, 417441. Peterbauer T, Richter A. 2001. Biochemistry and physiology of rafnose family oligosaccharides and galactosyl cyclitols in seeds. Seed Scence Research 11, 185197. Peters S, Mundree SG, Thomson JA, Farrant JM, Keller F. 2007. Protection mechanisms in the resurrection plant Xerophyta viscosa (Baker): both sucrose and rafnose family oligosaccharides (RFOs) accumulate in leaves in response to water decit. Journal of Experimental Botany 58, 19471956. Pilonsmits EAH, Ebskamp MJM, Paul MJ, Jeuken MJW, Weisbeek PJ, Smeekens SCM. 1995. Improved performance of transgenic fructan-accumulating tobacco under drought stress. Plant Physiology 107, 125130. Prandl R, Hinderhofer K, Eggers-Schumacher G, Schof F. 1998. HSF3, a new heat shock factor from Arabidopsis thaliana, derepresses the heat shock response and confers thermotolerance when overexpressed in transgenic plants. Molecular and General Genetics 258, 269278. Qu LJ, Wu LQ, Fan ZM, Guo L, Li YQ, Chen ZL. 2005. Overexpression of the bacterial nhaA gene in rice enhances salt and drought tolerance. Plant Science 168, 297302. Quinet M, Ndayiragije A, Lefevre I, Lambillotte B, DupontGillain CC, Lutts S. 2010. Putrescine differently inuences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance. Journal of Experimental Botany 61, 27192733. Raghavendra AS, Gonugunta VK, Christmann A, Grill E. 2010. ABA perception and signalling. Trends in Plant Science 15, 395401. Renault H, Roussel V, El Amrani A, Arzel M, Renault D, Bouchereau A, Deleu C. 2010. The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biology 10, 20. Rhodes D, Handa S, Bressan RA. 1986. Metabolic changes associated with adaptation of plant-cells to water-stress. Plant Physiology 82, 890903. Rhodes D, Hanson AD. 1993. quaternary ammonium and tertiary sulfonium compounds in higher-plants. Annual Review of Plant Physiology and Plant Molecular Biology 44, 357384. Rizhsky L, Liang HJ, Shuman J, Shulaev V, Davletova S, Mittler R. 2004. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiology 134, 16831696. Roosens NH, Al Bitar F, Loenders K, Angenon G, Jacobs M. 2002. Overexpression of ornithine-delta-aminotransferase increases proline biosynthesis and confers osmotolerance in transgenic plants. Molecular Breeding 9, 7380. Sakamoto A, Alia, Murata N. 1998. Metabolic engineering of rice leading to biosynthesis of glycinebetaine and tolerance to salt and cold. Plant Molecular Biology 38, 10111019. Sakamoto A, Valverde R, Alia, Chen TH, Murata N. 2000. Transformation of Arabidopsis with the codA gene for choline oxidase enhances freezing tolerance of plants. The Plant Journal 22, 449453. Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. 2006a. Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in droughtresponsive gene expression. The Plant Cell 18, 12921309. Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K. 2006b. Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heatstress-responsive gene expression. Proceedings of the National Academy of Sciences, USA 103, 1882218827. Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G. 2000. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288, 16131616. Sanchez DH, Siahpoosh MR, Roessner U, Udvardi M, Kopka J. 2008. Plant metabolomics reveals conserved and divergent metabolic responses to salinity. Physiologia Plantarum 132, 209219. Satoh-Nagasawa N, Nagasawa N, Malcomber S, Sakai H, Jackson D. 2006. A trehalose metabolic enzyme controls inorescence architecture in maize. Nature 441, 227230. Schweighofer A, Hirt H, Meskiene I. 2004. Plant PP2C phosphatases: emerging functions in stress signaling. Trends in Plant Science 9, 236243. Sengupta S, Patra B, Ray S, Majumder AL. 2008. Inositol methyl tranferase from a halophytic wild rice, Porteresia coarctata Roxb. (Tateoka): regulation of pinitol synthesis under abiotic stress. Plant, Cell and Environment 31, 14421459. Shelp BJ, Bown AW, McLean MD. 1999. Metabolism and functions of gamma-aminobutyric acid. Trends in Plant Science 4, 446452. Shen B, Jensen RG, Bohnert HJ. 1997. Increased resistance to oxidative stress in transgenic plants by targeting mannitol biosynthesis to chloroplasts. Plant Physiology 113, 11771183. Sheveleva E, Chmara W, Bohnert HJ, Jensen RG. 1997. Increased salt and drought tolerance by D-ononitol production in transgenic Nicotiana tabacum L. Plant Physiology 115, 12111219. Shinozaki K, Yamaguchi-Shinozaki K. 2007. Gene networks involved in drought stress response and tolerance. Journal of Experimental Botany 58, 221227. Shou H, Bordallo P, Fan JB, Yeakley JM, Bibikova M, Sheen J, Wang K. 2004a. Expression of an active tobacco mitogen-activated protein kinase kinase kinase enhances freezing tolerance in transgenic maize. Proceedings of the National Academy of Sciences, USA 101, 32983303. Shou H, Bordallo P, Wang K. 2004b. Expression of the Nicotiana protein kinase (NPK1) enhanced drought tolerance in transgenic maize. Journal of Experimental Botany 55, 10131019. Singh TN, Aspinal D, Paleg LG. 1972. Proline accumulation and varietal adaptability to drought in barley: potential metabolic measure of drought resistance. Nature New Biology 236, 188190. Smirnoff N, Cumbes QJ. 1989. Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28, 10571060. Song HM, Xu XB, Wang H, Wang HZ, Tao YZ. 2010. Exogenous gamma-aminobutyric acid alleviates oxidative damage caused by
Downloaded from http://jxb.oxfordjournals.org/ at Max Perutz Library on February 13, 2012

Metabolic adjustment and signalling in response to stress | 15 of 16


aluminium and proton stresses on barley seedlings. Journal of the Science of Food and Agriculture 90, 14101416. Song SY, Chen Y, Chen J, Dai XY, Zhang WH. 2011. Physiological mechanisms underlying OsNAC5-dependent tolerance of rice plants to abiotic stress. Planta 234, 331345. Spollen WG, Nelson CJ. 1994. Response of fructan to water-decit in growing leaves of tall fescue. Plant Physiology 106, 329336. Stewart GR, Lee JA. 1974. Role of proline accumulation in halophytes. Planta 120, 279289. Stoop JHM, Williamson JD, Pharr DM. 1996. Mannitol metabolism in plants: a method for coping with stress. Trends in Plant Science 1, 139144. Suzuki N, Bajad S, Shuman J, Shulaev V, Mittler R. 2008. The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana. Journal of Biological Chemistry 283, 92699275. Szabados L, Savoure A. 2010. Proline: a multifunctional amino acid. Trends in Plant Science 15, 8997. Szekely G, Abraham E, Cseplo A, et al. 2008. Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. The Plant Journal 53, 1128. Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K. 2002. Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. The Plant Journal 29, 417426. Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K. 2010. The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Molecular Genetics and Genomics 284, 173183. Tarczynski MC, Jensen RG, Bohnert HJ. 1993. Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259, 508510. Teige M, Scheikl E, Eulgem T, Doczi R, Ichimura K, Shinozaki K, Dangl JL, Hirt H. 2004. The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Molecular Cell 15, 141152. Testerink C, Munnik T. 2011. Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. Journal of Experimetnal Botany 62, 23492361. Tetlow IJ, Morell MK, Emes MJ. 2004. Recent developments in understanding the regulation of starch metabolism in higher plants. Journal of Experimental Botany 55, 21312145. Thomas JC, Sepahi M, Arendall B, Bohnert HJ. 1995. Enhancement of seed germination in high salinity by engineering mannitol expression in Arabidopsis thaliana. Plant, Cell and Environment 18, 801806. Thomashow MF. 2010. Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiology 154, 571577. Todaka D, Matsushima H, Morohashi Y. 2000. Water stress enhances beta-amylase activity in cucumber cotyledons. Journal of Experimental Botany 51, 739745. Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K. 2010. Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant and Cell Physiology 51, 18211839. Urano K, Yoshiba Y, Nanjo T, Ito T, Yamaguchi-Shinozaki K, Shinozaki K. 2004. Arabidopsis stress-inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochemical and Biophysical Research Communications 313, 369375. Urano K, Maruyama K, Ogata Y, et al. 2009. Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. The Plant Journal 57, 10651078. Usadel B, Blasing OE, Gibon Y, Poree F, Hohne M, Gunter M, Trethewey R, Kamlage B, Poorter H, Stitt M. 2008. Multilevel genomic analysis of the response of transcripts, enzyme activities and metabolites in Arabidopsis rosettes to a progressive decrease of temperature in the non-freezing range. Plant, Cell and Environment 31, 518547. Valerio C, Costa A, Marri L, Issakidis-Bourguet E, Pupillo P, Trost P, Sparla F. 2011. Thioredoxin-regulated beta-amylase (BAM1) triggers diurnal starch degradation in guard cells, and in mesophyll cells under osmotic stress. Journal of Experimental Botany 62, 545555. Valliyodan B, Nguyen HT. 2006. Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curent Opinion in Plant Biology 9, 189195. Valluru R, Van den Ende W. 2008. Plant fructans in stress environments: emerging concepts and future prospects. Journal of Experimental Botany 59, 29052916. van Dijken AJ, Schluepmann H, Smeekens SC. 2004. Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to owering. Plant Physiology 135, 969977. Verbruggen N, Hermans C. 2008. Proline accumulation in plants: a review. Amino Acids 35, 753759. Vernon DM, Bohnert HJ. 1992. A novel methyl transferase induced by osmotic stress in the facultative halophyte Mesembryanthemum crystallinum. EMBO Journal 11, 20772085. Vijn I, Smeekens S. 1999. Fructan: more than a reserve carbohydrate? Plant Physiology 120, 351359. von Koskull-Doring P, Scharf KD, Nover L. 2007. The diversity of plant heat stress transcription factors. Trends in Plant Science 12, 452457. Waditee R, Bhuiyan MN, Rai V, Aoki K, Tanaka Y, Hibino T, Suzuki S, Takano J, Jagendorf AT, Takabe T. 2005. Genes for direct methylation of glycine provide high levels of glycinebetaine and abiotic-stress tolerance in Synechococcus and Arabidopsis. Proceedings of the National Academy of Sciences, USA 102, 13181323. Wang Z, Zhu Y, Wang L, Liu X, Liu Y, Phillips J, Deng X. 2009. A WRKY transcription factor participates in dehydration tolerance in Boea hygrometrica by binding to the W-box elements of the galactinol synthase (BhGolS1) promoter. Planta 230, 11551166. Widodo, Patterson JH, Newbigin E, Tester M, Bacic A, Roessner U. 2009. Metabolic responses to salt stress of barley

Downloaded from http://jxb.oxfordjournals.org/ at Max Perutz Library on February 13, 2012

16 of 16 | Krasensky and Jonak


(Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. Journal of Experimental Botany 60, 40894103. Wilhelmi LK, Preuss D. 1996. Self-sterility in Arabidopsis due to defective pollen tube guidance. Science 274, 15351537. Wilson PB, Estavillo GM, Field KJ, et al. 2009. The nucleotidase/ phosphatase SAL1 is a negative regulator of drought tolerance in Arabidopsis. The Plant Journal 58, 299317. Woodgett JR, Cohen P. 1984. Multisite phosphorylation of glycogen synthase. Molecular basis for the substrate specicity of glycogen synthase kinase-3 and casein kinase-II (glycogen synthase kinase-5). Biochimica et Biophysica Acta 788, 339347. Xiang Y, Huang Y, Xiong L. 2007. Characterization of stressresponsive CIPK genes in rice for stress tolerance improvement. Plant Physiology 144, 14161428. Xiong L, Yang Y. 2003. Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. The Plant Cell 15, 745759. Xu J, Tian YS, Peng RH, Xiong AS, Zhu B, Jin XF, Gao F, Fu XY, Hou XL, Yao QH. 2010. AtCPK6, a functionally redundant and positive regulator involved in salt/drought stress tolerance in Arabidopsis. Planta 231, 12511260. Yamada M, Morishita H, Urano K, Shiozaki N, YamaguchiShinozaki K, Shinozaki K, Yoshiba Y. 2005. Effects of free proline accumulation in petunias under drought stress. Journal of Experimental Botany 56, 19751981. Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki A, Takahashi T, Michael A, Kusano T. 2006. The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Letters 580, 67836788. Yang J, Zhang J, Liu K, Wang Z, Liu L. 2007. Involvement of polyamines in the drought resistance of rice. Journal of Experimental Botany 58, 15451555. Yano R, Nakamura M, Yoneyama T, Nishida I. 2005. Starchrelated alpha-glucan/water dikinase is involved in the cold-induced development of freezing tolerance in Arabidopsis. Plant Physiology 138, 837846. Yoo JH, Park CY, Kim JC, et al. 2005. Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in arabidopsis. Journal of Biological Chemistry 280, 36973706. Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Weck M, Dunstan H, Haldimann P, Bechtold N, Smith AM, Smith SM. 2004. Plastidial alpha-glucan phosphorylase is not required for starch degradation in Arabidopsis leaves but has a role in the tolerance of abiotic stress. Plant Physiology 135, 849858. Zhang Y, Wu R, Qin G, Chen Z, Gu H, Qu LJ. 2011b. Overexpression of WOX1 leads to defects in meristem development and polyamine homeostasis in Arabidopsis. Journal of Integrative Plant Biology 53, 493506. Zhang L, Xi D, Li S, Gao Z, Zhao S, Shi J, Wu C, Guo X. 2011a. A cotton group C MAP kinase gene, GhMPK2, positively regulates salt and drought tolerance in tobacco. Plant Molecular Biology 77, 1731. Zuther E, Buchel K, Hundertmark M, Stitt M, Hincha DK, Heyer AG. 2004. The role of rafnose in the cold acclimation response of Arabidopsis thaliana. FEBS Letters 576, 169173. Zuther E, Koehl K, Kopka J. 2007. Comparative metabolome analysis of the salt response in breeding cultivars of rice. In: Jenks MA, Hasegawa PM, Jain SM, eds: Advances in molecular breeding toward drought and salt tolerant crops. Netherlands: Springer, 285315.
Downloaded from http://jxb.oxfordjournals.org/ at Max Perutz Library on February 13, 2012