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Apr 20, 2012 - maximize cold tolerance by adjusting their metabolism. The regulation of ... exposure to stress causes plant necrosis or death. To overcome ...
Planta (2012) 235:1091–1105 DOI 10.1007/s00425-012-1641-y

REVIEW

Physiological and molecular changes in plants grown at low temperatures Andreas Theocharis • Christophe Cle´ment Essaı¨d Ait Barka



Received: 30 November 2011 / Accepted: 13 March 2012 / Published online: 20 April 2012 Ó Springer-Verlag 2012

Abstract Apart from water availability, low temperature is the most important environmental factor limiting the productivity and geographical distribution of plants across the world. To cope with cold stress, plant species have evolved several physiological and molecular adaptations to maximize cold tolerance by adjusting their metabolism. The regulation of some gene products represents an additional mechanism of cold tolerance. A consequence of these mechanisms is that plants are able to survive exposure to low temperature via a process known as cold acclimation. In this review, we briefly summarize recent progress in research and hypotheses on how sensitive plants perceive cold. We also explore how this perception is translated into changes within plants following exposure to low temperatures. Particular emphasis is placed on physiological parameters as well as transcriptional, posttranscriptional and post-translational regulation of coldinduced gene products that occur after exposure to low temperatures, leading to cold acclimation. Keywords C-repeat binding factor  Low temperatures  Plant acclimation  Signal perception Abbreviations ABA Abscisic acid CBF C-repeat binding factor COR Cold-responsive genes CRT C-repeat elements

A. Theocharis  C. Cle´ment  E. A. Barka (&) Laboratoire de Stress, De´fense et Reproduction des Plantes, URVVC, UPRES EA 2069, Universite´ de Reims Champagne-Ardenne, BP 1039, 51687 Reims Cedex 2, France e-mail: [email protected]

DRE DREB ICE LT

Dehydration-responsive elements Dehydration-responsive element binding Inducer of CBF expression Low temperature

Introduction Among various environmental stresses, low temperature (LT) is one of the most important factors limiting the productivity and distribution of plants. Low temperatures, defined as low but not freezing temperatures (0–15 °C), are common in nature and can damage many plant species. In order to cope with such conditions, several plant species have the ability to increase their degree of freezing tolerance in response to low, non-freezing temperatures, a phenomenon known as cold acclimation. It is well established that some of the molecular and physiological changes that occur during cold acclimation are important for plant cold tolerance (Hsieh et al. 2004; Zhu et al. 2007). Accordingly, it has been concluded that cold tolerance that develops in initially insensitive plants is not entirely constitutive and at least some of it is developed during exposure to low temperatures. This review addresses plant adaptive responses to cold stress, with a special emphasis on understanding (i) the key elements involved in cold signal perception and transduction, (ii) the major physiological and biochemical changes that occur following cold exposure, (iii) cold-inducible gene products that help the plant to accomplish a synergistic response to cold, and finally (iv) products that may play major roles in cold acclimation and tolerance.

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Mechanisms of acclimation to low non-freezing temperatures

How do plants perceive cold? As a result of exposure to low temperatures, many physiological and biochemical cell functions have been correlated with visible symptoms (wilting, chlorosis, or necrosis) (Ruelland and Zachowski 2010). Often, these adverse effects are accompanied by changes in cell membrane structure and lipid composition (Uemura and Steponkus 1999; Matteucci et al. 2011), cellular leakage of electrolytes and amino acids, a diversion of electron flow to alternate pathways (Seo et al. 2010), alterations in protoplasmic streaming and redistribution of intracellular calcium ions (Knight et al. 1998) (Fig. 1). They also involve changes in protein content and enzyme activities (Ruelland and Zachowski 2010) as well as ultrastructural changes in a wide range of cell components, including plastids, thylakoid membranes and the phosphorylation of thylakoid proteins, and mitochondria (Zhang et al. 2011). Brief exposures to low temperatures may only cause transitory changes, and plants generally survive. However, prolonged exposure to stress causes plant necrosis or death. To overcome stresses generated by exposure to low non-freezing temperatures, plants can trigger a cascade of events that cause changes in gene expression and thus induce biochemical and physiological modifications that enhance their tolerance (Smallwood and Bowles 2002; Zhu et al. 2007). This phenomenon is known as chilling or cold acclimation.

Fig. 1 A model to explain symptoms of chilling injury in chilling-sensitive plants. Membranes are the primary site of cold-induced injury, leading to a cascade of cellular processes with adverse effects on the plant. When exposure to low temperature is brief, the effects may be transitory and plants survive. However, the plant will exhibit necrosis or die if exposure is maintained (Lyons 1973; Raison and Lyons 1986)

The primary mechanisms involved in cold acclimation are related to a number of processes discussed below. These include molecular and physiological modifications occurring in plant membranes, the accumulation of cytosolic Ca2?, increased levels of ROS and the activation of ROS scavenger systems, changes in the expression of coldrelated genes and transcription factors, alterations in protein and sugar synthesis, proline accumulation, and biochemical changes that affect photosynthesis (Fig. 2). Modifications to plant cell membranes Membranes are a primary site of cold-induced injury (Fig. 1). Several studies have demonstrated that membrane rigidification, coupled with cytoskeletal rearrangements, calcium influxes, and the activation of MAPK cascades, triggers LT responses (Uemura and Steponkus 1999; Orvar et al. 2000; Xin and Browse 2000; Sangwan et al. 2002). The lipid composition of the plasma membrane and chloroplast envelopes in acclimated plants changes such that the threshold temperature for membrane damage is lowered relative to that for non-acclimated plants (Uemura and Steponkus 1999). This is achieved by increasing the coldadapted membranes’ unsaturated fatty acid content, which makes them more fluid (Vogg et al. 1998). The process of

Chilling stress

Cell membranes Liquid-Crystalline Survival

Return to normal metabolism

Brief exposure and return to 20 °C

‘’FLUID’’

Solid gel Transition phase

‘’SOLID’’

Cessation of protoplasmic streaming

Increased activation of energy-bound enzymes

Enhanced permeability

Reduced ATP supply

Imbalance in metabolism

Solute leakage and disrupted ion balance

Accumulation of toxic metabolites Prolonged exposure

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Injury and death of cells and tissues

Planta (2012) 235:1091–1105 Fig. 2 Different cellular processes induced as a consequence of plant acclimation to cold

1093 Accumulation of cryoprotectants sugars, proline, ...

Accumulation of ROS and activation of scavenge system

Cold Acclimation

Accumulation of [Ca2+cyt]

Photosynthetic acclimation

Changes in gene expression and protein synthesis

Modification in plant membranes

Change in lipid composition Reduction of lower threshold temperature in acclimated plants

cold acclimation promotes the stabilization of membranes, which prevents damage leading to cell death. The acclimation process also activates mechanisms that protect membrane fluidity by ensuring the optimal activity of associated enzymes (Matteucci et al. 2011). Photosynthesis and photosynthesis-related pigments At the physiological level, photosynthesis is strongly affected by exposure to cold. The cessation of growth resulting from cold stress reduces the capacity for energy utilization, causing feedback inhibition of photosynthesis (Ruelland and Zachowski 2010). In cold-acclimated winter annuals, photosynthetic activity is maintained by increases in the abundance and activity of several Calvin cycle enzymes (Goulas et al. 2006). This recovery is associated with elevated levels of thylakoid plastoquinone A and a concomitant rise in the apparent size of the intersystem electron donor pool to PSI (Baena-Gonzalez et al. 2001). Consequently, non-photochemical quenching increases in cold-stressed leaves in parallel with increased zeaxanthin levels to compensate for the reduced electron consumption by photosynthesis. Zeaxanthin protects the PSII reaction centres from over-excitation (Krol et al. 1999). Nevertheless, Ruelland and Zachowski (2010) reported that energy dissipation via nonphotochemical quenching (NPQ) and electron transport was not only enhanced following cold acclimation but also contributed to protection from oxidative damage. Xanthophylls Although they are not considered photosynthetic pigments per se, the xanthophylls (notably, violaxanthin, antheraxanthin, and zeaxanthin) help in protecting the photosystems

Increase in desaturated fatty acids Increased fluidity of membranes

and their abundance increases at low temperatures (Ivanov et al. 2006). Xanthophylls have structural roles and act as natural antioxidants, quenching triplet Chl and singlet oxygen, which are potentially harmful to the chloroplast (Passarini et al. 2009; Han et al. 2010). It has also been postulated that unbound zeaxanthin and other carotenoids may also stabilize thylakoid membranes against putative peroxidative damage and heat stress (Laugier et al. 2010). Flavonoids These accumulate in leaves and stems in response to low temperatures. They are synthesized via the phenylpropanoid pathway, which is controlled by key enzymes, including phenylalanine ammonia-lyase and chalcone synthase (Sharma et al. 2007). Recently, it has been reported that cold stress induces transcriptomic modifications that increase flavonoid biosynthesis, including reactions involved in anthocyanin biosynthesis and the metabolic pathways that supply it (Crifo et al. 2011). Calcium and cold temperatures Calcium acts as a mediator of stimulus–response coupling in the regulation of plant growth, development, and responses to environmental stimuli (Sanders et al. 2002; Du and Poovaiah 2005). Cold stress-induced rigidification of plasma membrane microdomains can cause actin cytoskeletal rearrangement. This may be followed by the activation of Ca2? channels and increased cytosolic Ca2? levels (Fig. 3), which may be involved in the cold acclimation process (Sangwan et al. 2001; Catala et al. 2003). The Ca2? released from internal cellular reserves, mediated by inositol triphosphate, is upstream of the expression of

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1094 Fig. 3 Ca2? and reactive oxygen species (ROS) responses to chilling in sensitive plants. ROS are not simply toxic by-products of metabolism; they also act as signalling molecules by modulating the expression of various genes, including those encoding antioxidant enzymes and modulators of H2O2 production. Changes to the plasma membrane can cause actin cytoskeletal rearrangements that may be followed by the activation of Ca2? channels and increased cytosolic Ca2? concentrations, triggering a series of reactions such as the expression of cold-regulated genes

Planta (2012) 235:1091–1105

Chilling stress Inactivation of enzymes Plasma membranes

Lipid peroxidation

ROS Protein degradation

PS I, II

Damage to DNA

[Ca2+cyt] Cessation of cytoplasm streaming

Changes in cytoplasm viscosity

Inhibition of ethylene biosynthesis

Inhibition of photosynthesis

Activation or repression of phosphatase activity

Induction of cold related genes (COR )

Elevation of proline and total soluble sugars contents

CBFs (C-repeat binding factors) and COR (cold responsive) genes in the cold-signalling pathway(s) (Chinnusamy et al. 2007, 2010). Recently, Doherty et al. (2009) provided more evidence for a link between calcium signalling and cold induction of the CBF pathway, showing that calmodulin binding transcription activator (CAMTA) factors bind to a regulatory element in the CBF2 gene promoter. As the CAMTA proteins are calmodulin binding transcription factors, they may act directly in the transduction of LT-induced cytosolic calcium signals into downstream regulation of gene expression (Doherty et al. 2009). Similarly, CRLK1, a novel calcium/calmodulin-regulated receptor-like kinase, was reported to be crucial for cold tolerance in plants (Yang et al. 2010). Role of reactive oxygen species in acclimation to low temperatures The role of ROS in abiotic stress management has become a subject of considerable research interest, particularly since ROS have been reported to be involved in processes leading to plant stress acclimation (Suzuki et al. 2011). This finding indicates that ROS are not simply toxic by-products of metabolism, but act as signalling molecules that modulate the expression of various genes, including those encoding antioxidant enzymes and modulators of H2O2 production (Neill et al. 2002; Gechev et al. 2003; Suzuki et al. 2011) (Fig. 3). In addition, LT stress has been reported to cause significant increases in the levels of the soluble non-enzymatic antioxidants ascorbate and glutathione, as well as the activity of the main NADPH-generating dehydrogenases (Airaki et al. 2011).

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Cold-mediated transcription regulation Plant acclimation to LT depends on changes in the expression of specific genes encoding products that confer increased cold tolerance (Gilmour et al. 1998; Doherty et al. 2009) (Fig. 4). The process involves modifying preexisting proteins and up- or down-regulating gene expression and protein synthesis. Several studies have suggested that activity of cold/chilling-induced genes may facilitate the metabolic changes that confer LT tolerance (Gilmour et al. 1998; Doherty et al. 2009). They may also be involved in the signal transduction of the stress-response (Ingram and Bartels 1996; Thomashow 2010). HOS15, one of 237 predicted WD40-repeat proteins in Arabidopsis, functions as a repressor that modifies chromatin and thereby controls the expression of genes involved in cold tolerance (Zhu et al. 2008). In addition, HOS1 is a RINGtype ubiquitin E3 ligase that mediates the ubiquitination and proteosomal degradation of ICE1 and thus negatively regulates CBF regulons. The constitutive HOS9 and HOS10 regulons have a role in the negative regulation of CBF-target genes (Fig. 4). The CRT/DREB1 regulatory pathway A wide variety of COR genes have been isolated from coldacclimated plants (Svensson et al. 2006). The cloned genes’ products can be classified as (i) proteins that protect cells against environmental cold/chilling stress, and (ii) proteins that regulate gene expression during the adaptation response (Fowler and Thomashow 2002). Further classification divides the gene products into (i) mediators of

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biochemical and physiological changes required for growth and development at low temperatures and (ii) gene products with a direct role in chilling and freezing tolerance (Thomashow 2010). A transcriptome analysis of resistant Arabidopsis treated at 13 °C indicated that 20 % of about 8,000 genes were affected by treatment, particularly those involved in protein biosynthesis (Provart et al. 2003; Chinnusamy et al. 2010). The mRNA profiles for the chilling-lethal mutants were very similar and included extensive chilling-induced and mutant-specific alterations in gene expression. The expression pattern of the mutants upon chilling suggests that the normal function of the mutated loci is to prevent a wide-ranging damaging effect of LT on transcriptional regulation (Provart et al. 2003). Role of CBF transcription factors in cold acclimation The signal transduction pathways that control COR expression incorporate a regulatory network (Fig. 4) in which a few regulatory genes control those involved in the cold response (Fowler and Thomashow 2002; YamaguchiShinozaki and Shinozaki 2006; Chinnusamy et al. 2010; Thomashow 2010). Attempts to isolate the regulatory elements responsible for the initiation of the COR gene transcription under LT have primarily focused on Arabidopsis. The ability to express all of the COR genes in concert at warm temperatures was described following the discovery of the CBF family of transcriptional activators (Gilmour et al. 2004; Skinner et al. 2005; Chinnusamy et al. 2010), which are also known as DREs (drought responsive elements) or LTREs (low temperature responsive elements) (Shinwari et al. 1998; Shinozaki and Yamaguchi-Shinozaki 2000; Yamaguchi-Shinozaki and Shinozaki 2006). The CBF1, CBF2, and CBF3 genes follow one-another in sequence on Arabidopsis chromosome 4 (Shinwari et al. 1998; Gilmour et al. 2004). DRE/LTREs stimulate gene expression in response to cold, high salinity and drought, but not in response to exogenously applied abscisic acid (Shinozaki and Yamaguchi-Shinozaki 2000). Using the yeast one-hybrid system, the DRE/CRT elements have been used as bait to isolate DRE/CRT-binding proteins. The five different DRE binding proteins isolated to date have been classified into two groups, DREB1 and DREB2 (Liu et al. 1998), which bind specifically to the DRE/CRT elements and transcriptionally activate the expression of COR genes. The promoters of CBF/DREB-regulated COR genes contain a cold- and dehydration-responsive DNA regulatory element known as CBF/DRE (Shinozaki and Yamaguchi-Shinozaki 2000). Overexpression of CBF1 in Arabidopsis has been shown to activate the expression of the entire battery of known CBF/DREB-regulated COR genes and to enhance whole plant freezing survival without a low temperature stimulus

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(Jaglo-Ottosen et al. 1998). In Arabidopsis, overexpression of CBF1 and CBF3 activates COR gene expression and enhances freezing tolerance (Liu et al. 1998; Maruyama et al. 2004). Additionally, when overexpressed in transgenic Arabidopsis plants, the homolog of the CBF/DREB1 protein CBF4 activates a C-repeat/dehydration-responsive element containing downstream genes that are involved in cold acclimation (Haake et al. 2002). The three CBF genes are cold-induced. Indeed, CBF transcript levels start to increase within 15 min of exposing plants to low temperatures, and transcripts from the targeted CBF/DRE-regulated COR genes start to accumulate within approximately 2 h (Mantyla et al. 1995). The precise mechanism whereby the CBF genes are activated by LT does not involve autoregulation (Gilmour et al. 1998, 2004) but is controlled by a set of redundant interacting transcription factors (Vogel et al. 2005; Chinnusamy et al. 2007, 2010). Many of these genes are also induced by abscisic acid (Knight et al. 2004) or by dehydration (Shinozaki and Yamaguchi-Shinozaki 2000), which is consistent with the fact that both of these factors can increase freezing tolerance in transgenic plants (Jaglo-Ottosen et al. 1998; Liu et al. 1998). However, the existence of CBF-parallel pathways involved in cold acclimation has been supported by transcription profiling of plants overexpressing the three members of the CBF family (Fowler and Thomashow 2002). On the other hand, the Arabidopsis mutant eskimo1 displays freezing tolerance in the absence of cold treatment, without changes in expression of the components of the CBF pathway, but with a high level of proline accumulation. This suggests that distinct signalling pathways activate different aspects of cold acclimation. The activation of one pathway can result in considerable freezing tolerance without activation of other pathways (Xin and Browse 2000). Subsequent to their discovery in Arabidopsis, many CBF homologues have been found in both monocotyledonous and dicotyledonous species capable of cold acclimation, but they are also found in species that are not (Ruelland et al. 2009). For instance, grapevines have five CBF/DREB1-like genes (CBFs), CBF1 to CBF4 (Xiao et al. 2006, 2008) and one undefined CBF-like transcription factor, CBFL (XM_002270601). CBF expression was reported to be induced within a few hours of exposure to low temperatures, particularly CBF4 (Xiao et al. 2008). More recently, Takuhara et al. (2011) have demonstrated that LT enhanced the expression of VvCBF2, VvCBF4, and VvCBFL within 3 h, but not VvCBF1 or VvCBF3 expression. CBF1, 2 and 3 transcripts also accumulated in response to drought and treatment with exogenous abscisic acid (ABA), indicating that grapevines contain unique CBF genes. The expression of the endogenous Vitis CBF4 genes

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LOW TEMPERATURES

METABOLISM UNKNOWN SENSORS ROS Ca2+ influx HOS1

ICE1

ICE1

Kinase/ Phosphatase

ICE1

Proteolysis

MYB15

LOS2

STZ ZAT12

ICE1 like

CBF

HOS1 RAV1

MYB/MADS/NAC/ others

MYBRS

ICE1 box

Unknown ciselements

Target

SFR6

HOS9 HOS10

ZAT10

EP2

CBF1

CBF2

CBF3

RAP 2.6

?

CRT/DRE

ABRE

Rd29a Cor15a

Rd29a Rd29b

COR/KIN/RD/LT

?

MYCR/MYBR Rd22 AtADH1

PROTECTIVE PROTEINS and METABOLITES

U P S

COLD ACCLIMATION/ TOLERANCE

was low at ambient temperature but increased on exposure to LT (4 °C). This expression was maintained for several days, which is uncommon for CBF genes. Further, in contrast to the previously described Vitis CBF1-3, vCBF4 was expressed in both young and mature tissue. Altogether, these results suggest that CBF4 represents a second type of CBF in grape that might be more important for the overwintering of grapevine plants. This raises the question as to whether the CBF transcription factors are limited to activating the expression of COR genes encoding cryoprotective polypeptides, or

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alternatively have a role in activating multiple components of the cold acclimation response. When both CBF1 and CBF3 are shut down, the cold induction of all CBF targets is lower, suggesting that a basal level of CBF proteins would be needed for the induction of all CBF targets and for the activation of cold acclimation in Arabidopsis. This level would be reached only when the CBF1, CBF2, and CBF3 genes are properly induced in a co-ordinated fashion (Novillo et al. 2007). On the other hand, overexpression of CBF3 in Arabidopsis results in multiple biochemical changes that ultimately increase the concentration of

Planta (2012) 235:1091–1105 b Fig. 4 Schematic diagram of the regulatory network involved in low

temperature responses. Plants sense low temperatures and activate a calcium signal mediated via protein kinases, and other species that activate multiple transcriptional cascades, one of which involves ICE1 and CBFs. The CBF genes play important roles in cold acclimation and are regulated by multiple pathways. They activate the transcription of CBFs and repress MYB15. ICE1, a constitutively expressed gene, is activated by cold stress via sumoylation and phosphorylation. HOS1 is a RING-type ubiquitin E3 ligase that negatively regulates cold-induced DREB1/CBF expression. The constitutive HOS9 and HOS10 regulons have a role in the negative regulation of CBF-target genes. CBFs regulate the expression of COR genes that confer freezing tolerance. The expression of CBFs is negatively regulated by MYB15 and ZAT12. HOS1 mediates the ubiquitination and proteosomal degradation of ICE1 and, thus, negatively regulates CBF regulons. Transcription of CBFs might be cross-regulated. Transcription factor binding sites are represented at the bottom of the diagram, with the representative promoters listed below. Yellow arrows indicate post-translational regulation; solid arrows indicate activation, whereas broken lines show negative regulation; small circles indicate post-transcriptional modification, such as phosphorylation; question marks indicates unknown ciselements. ABRE ABA responsive element, CBF C-repeat binding factor (an AP2-type transcription factor); COR cold-responsive genes, CRT C-repeat elements, DRE dehydration-responsive elements, HOS1 high expression of osmotically responsive genes1, HOS9 and HOS10, ICE1 inducer of CBF expression 1, KIN cold-induced genes, LOS2 low expression of osmotically responsive genes 2 (a bifunctional enolase with transcriptional repression activity), LTI low temperature-induced genes, MYB myeloblastosis, MYBRS MYB recognition sequence, MYCRS MYC recognition sequence, RD responsive to dehydration) genes, ROS reactive oxygen species, SIZ1 SAP and MiZ1 (a SUMO E3 ligase), P phosphorylation, S SUMO (small ubiquitin-related modifier), U ubiquitin

proline and total soluble sugars, including sucrose, raffinose, glucose and fructose (Gilmour et al. 2000). Nevertheless, transcriptome analysis of transgenic Arabidopsis overexpressing CBF revealed that only about 12 % of the cold-responsive genes are components of the CBF regulon (Fowler and Thomashow 2002), suggesting that other transcriptional activators/repressors also play a significant role in cold acclimation. Inducer of CBF expression (ICE), a regulator of cold acclimation Since CBF genes are cold-induced, it may be that an upstream transcription factor present in the cell at normal growth temperatures is activated by cold stress and, in turn, induces the expression of CBFs. A constitutive transcription factor, inducer of CBF expression 1 (ICE1), which acts upstream of the CBFs in the cold-response pathway, has been identified (Chinnusamy et al. 2003). ICE1 binds to the CBF3 promoter and may activate CBF3 expression upon cold treatment (Figs. 3, 4). The dominant ice1 mutation blocks the cold induction of CBF3, but not CBF1 or CBF2, and decreases the expression of many CBF-target genes (Chinnusamy et al. 2003, 2004). The serine 403

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residue of ICE1 is involved in regulating the transactivation and stability of the ICE1 protein. Interestingly, the substitution of serine 403 by alanine was reported to enhance the transactivational activity of ICE1 in Arabidopsis protoplasts (Miura et al. 2011). These authors also reported that overexpression of ICE1(S403A) conferred more freezing tolerance than ICE1(WT) in Arabidopsis, and the expression of cold-regulated genes such as CBF3/ DREB1A, COR47 and KIN1 (cold-induced gene) was enhanced in plants overexpressing ICE1(S403A). Whereas ICE1 primarily affects CBF3/DREB1A expression (Chinnusamy et al. 2003), the protein encoded by ICE2 (a homolog of ICE1; At1g12860) primarily influences the expression of CBF1/DREB1B but has little effect on CBF3/ DREB1A (Fursova et al. 2009). Therefore, ICE1 and ICE2 play pivotal roles in the transcriptional regulation of the CBF/DREB1 genes (Miura et al. 2011). The MYB transcription factor and the ABA-independent cold acclimation pathway ABA-dependent gene expression is regulated by transcription factors that belong to the bZIP (ABRE binding factors—or AREBs), MYC and MYB families. In A. thaliana, the MYB family transcription factor PAP2 regulates the flavonoid biosynthesis pathway, which is reported to be involved in cold tolerance (see above). OsMYB4, a member of the MYB family of transcription factors, has also been shown to be inducible by cold, but not by ABA in rice (Park et al. 2010). Surprisingly, Su et al. (2010) reported that MYBS3 repressed the DREB1/CBF-dependent coldsignalling pathway in rice at the transcriptional level. Further, DREB1 responded quickly and transiently, whereas MYBS3 responded slowly to cold stress, suggesting distinct pathways acting sequentially to acclimate rice to cold stress. In A. thaliana the abundance of MYBC1 transcripts was not affected by overexpression of CBF1, CBF2, and CBF3, suggesting that MYBC1 is not downregulated by these CBF family members (Zhai et al. 2010). Abscisic acid (ABA)-dependent cold signal pathway and other phytohormones (a) Abscisic acid: ABA serves as a secondary signal that plays at least some role in the transduction of cold signals via second messengers, such as H2O2 and Ca2?. This is demonstrated by the los5 (low expression of osmotically responsive genes) mutant, which exhibits significantly decreased cold- and salt/drought-induced expression of COR. ABA enhanced antioxidant defence and slowed down the accumulation of ROS caused by low temperatures (Liu et al. 2011). ABA can also induce the expression

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of the CBF1, CBF2, and CBF3 genes, but to a significantly lower level than that caused by cold (Knight et al. 2004). (b) Polyamines: There are relatively few reports regarding the involvement of polyamines in LT stress (Alcazar et al. 2010; Gill and Tuteja 2010). Putrescine accumulation under cold stress is essential for proper cold acclimation and survival at freezing temperatures (Cuevas et al. 2008). Indeed, Arabidopsis mutants defective in putrescine biosynthesis (adc1, adc2) exhibit reduced freezing tolerance compared to wild-type plants, suggesting that the detrimental consequences of putrescine depletion during cold stress are at least partially due to changes in the concentration of ABA. On the other hand, the accumulation of putrescine in the early stages of mango fruit ripening promoted by LT stress did not prevent chilling injury (Nair and Singh 2004). During treatment, the spermidine content of leaves increased substantially in cold-tolerant cucumber cultivars but not in sensitive ones, while the concentrations of putrescine and spermine did not change (Shen et al. 2000). The depletion of endogenous spermidine and spermine in response to chilling and the reduced severity of chilling injuries in mango fruits that had been treated with these polyamines prior to storage both suggest that polyamine biosynthesis influences cold sensitivity. Polyamines have also been reported to have a role in alleviating oxidative stress: inhibiting polyamine synthesis causes increased oxidative damage in cold-treated plants (Groppa and Benavides 2008). (c) Other regulators affecting cold acclimation: A number of genes involved in the biosynthesis or signalling of plant hormones, such as gibberellic acid and auxin, may be also regulated by cold stress. The regulation of these genes might be important in co-ordinating cold tolerance with growth and development. A role for cytokinin in mediating plant growth rates at LT was recently reported (Xia et al. 2009). Mutants with elevated cytokinin levels (amp1) displayed enhanced cell division at 4 °C. Moreover, no changes in CBF expression were recorded in amp1 or NahG plants at LT, suggesting that the effects of cytokinin and salicylic acid (SA) on temperature-regulated growth are independent of the CBF regulon. In addition to its role in plant pathogen defences, SA is also involved in suppressing plant growth during chilling and accumulates at LT (Scott et al. 2004). However, SA is not required for thermotolerance (Clarke et al. 2004). Post-transcriptional regulation Transcriptomic analyses of gene expression at the mRNA level have contributed greatly to our understanding of cold responses in Arabidopsis (Kreps et al. 2002; Zhou et al. 2008, 2011). However, the abundance of individual mRNAs does not always correlate well with that of the

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corresponding proteins, which are the crucial agents in the cell (MacKay et al. 2004; Tian et al. 2004). Consequently, it is not sufficient to simply predict protein expression levels from quantitative mRNA data, mainly due to the effects of post-transcriptional regulation mechanisms (Pradet-Balade et al. 2001). The involvement of post-transcriptional cold-induced regulation on the abundance of specific mRNAs has been reported in several species, including Arabidopsis and alfalfa. Maize plants exposed to cooler temperatures respond by phosphorylating a minor chlorophyll a/b protein rather than synthesizing a new protein from a coldregulated gene (Bergantino et al. 1995). Although plant cell membranes exhibit significantly higher levels of unsaturation at lower temperatures, there is no apparent increase in rate of transcription or stability of fatty acid desaturase mRNA at lower temperature. The exception is the Arabidopsis fatty acid desaturase gene FAD8 (Matsuda et al. 2005), which suggests that plant fatty acid desaturases are regulated at the post-transcriptional level. Expression of homology to pathogenesis-related (PR) genes and synthesis of antifreeze proteins (AFPS) Studies in different plant species have shown that several cold-induced genes encode cryoprotective proteins (Hincha 2002). In the last few decades, research has focused on specific proteins with antifreeze activity that accumulate in the apoplast during cold acclimation, thereby offering plant resistance against freezing (Griffith and Yaish 2004; Griffith et al. 2005; Yaish et al. 2006) (Fig. 5). These proteins have been found in many overwintering vascular plants (Griffith and Yaish 2004; Venketesh and Dayananda 2008), but antifreeze activity is present only after their exposure to LT and only in plants that tolerate the presence of ice in their tissues (Griffith and Yaish 2004; Yaish et al. 2006). These proteins were identified as b-1,3-glucanaselike proteins, chitinase-like proteins, thaumatin-like proteins and as polygalacturonase inhibitor proteins (Wang et al. 2006; Yaish et al. 2006). Although they were present in non-acclimated plants, they were found in different locations and did not exhibit antifreeze activity, which suggests that different isoforms of pathogenesis-related proteins are produced under LT conditions (Antikainen et al. 1996; Wang et al. 2006). Until now, no plant has been reported to have constitutive antifreeze activity. Rather, all studies have shown that transcripts and translation products of AFP genes accumulate during cold acclimation (Yeh et al. 2000; Huang and Duman 2002; Wang et al. 2006). Recent studies have shown that many PR genes are induced and disease resistance is enhanced after exposure to LT, linking cold signals with pathogenesis in plants (Seo et al. 2010).

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Chilling stress

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Pathogen attack

Salicylic acid Abscisic acid Ethylene Jasmonic acid

Cold acclimation Expression of genes Encoding for PR proteins Accumulation of transcripts homology to PR genes

Accumulation of antifreeze proteins (AFPs)

Cold acclimation

Accumulation of PR proteins

Resistance to pathogens

Most of these proteins have therefore been named COR (cold responsive), LTI (low temperature induced), RAB (responsive to abscisic acid), KIN (cold induced) or ERD (early responsive to dehydration). These proteins include the dehydrins, which belong to group II of the late embryogenesis abundant (LEA) proteins (Bies-Etheve et al. 2008). The accumulation of one particular dehydrin (WCO R410) is correlated with the capacity to develop freezing tolerance in wheat. However, the overexpression of single dehydrins does not necessarily lead to enhanced freezing tolerance. For instance, the overexpression of RAB18, a cold-induced dehydrin, has no effect on freezing tolerance in Arabidopsis (Lang and Palva 1992). This suggests that to fully play their role, dehydrins may need to be activated by a cold-induced mechanism such as protein phosphorylation. One of the roles that have been also attributed to dehydrins is the prevention of membrane destabilization during dehydration. In addition to this postulated function, it has been proposed that dehydrins possess cryoprotective (Bravo et al. 2003) or antifreeze (Puhakainen et al. 2004) activities. Cold-induced osmolites/osmoprotectants

By accumulating PR proteins during cold acclimation, overwintering grasses and cereals acquire a systemic, nonspecific, pre-emptive defence against pathogens and thus exhibit greater disease resistance.

In response to cold and other osmotic stresses, plants accumulate a range of compatible solutes including cererosides, free sterols, sterol glucosides and acylatedsterols, glucosides, raffinose, arbinoxylans, and other soluble sugars. In addition, plants accumulate other solutes such as glutamic acid, amino acids (alanine, glycine, proline, and serine), polyamines and betaines (Hekneby et al. 2006; Patton et al. 2007; Ruelland and Zachowski 2010). These different molecules, which are often degraded once the stress has passed, are referred to as osmolytes, osmoprotectants or compatible solutes.

Cold shock proteins and RNA binding proteins

Carbohydrate changes

Cold shock domain proteins (CSDPs) play important roles in development and stress adaptation in a variety of organisms, ranging from bacteria to mammals (Chaikam and Karlson 2010). In higher plants, cold shock domain proteins are involved in the cold response (Nakaminami et al. 2006; Sasaki et al. 2007). Recently, it was demonstrated that CSP Arabidopsis 3 (AtCSP3), which shares a cold shock domain with the CSDPs, is involved in the acquisition of freezing tolerance in plants (Kim et al. 2009).

Carbohydrate metabolism has been reported to have greater instantaneous low temperature sensitivity than other components of photosynthesis (Fernandez et al. 2012). Although the precise function of soluble sugars remains to be determined, their accumulation in cold-acclimated plants suggests roles as osmoregulators, cryoprotectants or signalling molecules (Welling and Palva 2006). Sugars play multiple roles in low temperature tolerance. As typical compatible osmolytes, they contribute to the preservation of water within plant cells, thereby reducing water availability for ice nucleation in the apoplast (Uemura and Steponkus 1999; Ruelland et al. 2009). Sugars might protect plant cell membranes during cold-induced dehydration, replacing water molecules in establishing hydrogen bonds with lipid molecules (Uemura et al. 2003; Ruelland et al. 2009). Moreover, carbohydrates may also act as scavengers of reactive oxygen

Fig. 5 Accumulation of antifreeze proteins (AFPs) in cold-acclimated plants with antifungal activity (adapted from Yeh et al. 2000; Huang and Duman 2002; Griffith and Yaish 2004; Yaish et al. 2006). By accumulating PR proteins during cold acclimation, overwintering plants may acquire a systemic, non-specific, pre-emptive defence against pathogens and exhibit greater disease resistance

COR/LEA and dehydrins The accumulation of hydrophilic proteins predicted to form an amphipathic a-helix is one of the best documented responses of plants to cold treatment (Eriksson et al. 2011).

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species and contribute to increased membrane stabilization (Bohnert and Sheveleva 1998). Sugar signalling is also closely associated with hormone signalling, the control of growth and development, and stress responses in plants (Zeng et al. 2011). Depending on the plant species, various forms of soluble sugars are involved in physiological reactions to cold stress. For example, treatment of rice seedlings with fructose or glucose prior to LT treatment increases their resistance to cold. Cotton cotyledon discs floating on a sucrose solution in the dark were less injured by cold than those on non-sugar solutions (Couee et al. 2006). On the other hand, King et al. (1988) reported that cold tolerance in tomato seedlings decreased following pronounced reductions in their starch and sugar levels during a dark period. The soluble carbohydrate content of grasses can undergo a tenfold increase within 8 h of transfer from a warm to a cold environment (Pollock and Lloyd 1987). The oligosaccharides raffinose and stachyose are especially associated with cold hardiness, low temperature and dormancy (Aı¨t Barka and Audran 1996; Couee et al. 2006). Moreover, the concentration of sucrose, the most easily detectable sugar in cold-tolerant species, increases several fold during exposure to LT (Bohnert and Sheveleva 1998; Tabaei-Aghdaei et al. 2003). The accumulation of sucrose in cane sugar exposed to salt stress or to LT stress supports the role of this sugar as an osmoprotectant that stabilizes cellular membranes and maintains turgor (Jouve et al. 2004). In addition, high sucrose levels correlate with the priming of defence responses in rice that overexpresses the PRms gene from maize, which encodes a PR-1 type protein (Casacuberta et al. 1991). Trehalose is a non-reducing disaccharide of glucose that is found in a variety of organisms including bacteria, yeast, fungi, insects and invertebrates, where it serves as a stress protectant and/or a reserve carbohydrate (Penna 2003; Fernandez et al. 2010). Although increased levels of trehalose are associated with abiotic stress tolerance in transgenic plants expressing heterologous microbial genes, the function of endogenous trehalose in higher plants remains unclear. This sugar possesses the unique capacity for reversible water absorption and appears to be superior to other sugars in protecting biological molecules from desiccation-induced damage (Fernandez et al. 2010). Further, transgenic A. thaliana plants that accumulated trehalose displayed significantly enhanced freezing tolerance (Miranda et al. 2007). Increases in trehalose concentration may also be involved in starch accumulation (Fernandez et al. 2010). During exposure to LT, starch content typically declines following hydrolysis, and there is a corresponding increase in the concentration of free saccharides (Pollock and Lloyd

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1987; Bohnert and Sheveleva 1998). However, in several cases, increases in the levels of both soluble sugars and starch have been reported during cold acclimation. For instance, in cabbage seedlings grown at 5 °C, the concentrations of starch and all soluble sugars (myo-inositol aside) in the leaves increased gradually during cold acclimation (Sasaki et al. 1996). However, the induced freezing tolerance was lost after only 1 day of acclimation at control temperatures and this change was associated with a large reduction in sugar content. Carbohydrate accumulation at LT may be explained through the activation of specific enzymes (Bohnert and Sheveleva 1998; Couee et al. 2006). This suggests that although LT inhibits sucrose synthesis and photosynthesis, various biochemical and physiological adaptations to LT counteract these effects. These adaptations include the post-translational activation and enhanced expression of enzymes involved in the sucrose synthesis pathways and those of Calvin cycle—in particular, the cytosolic enzymes fructose-1,6-bisphosphatase, sucrose phosphate synthase and sucrose synthase (Stitt and Hurry 2002). Compatible osmotica other than sugars (a) Proline: The positive correlation between the accumulation of endogenous proline (Pro) and improved cold tolerance has been found mostly in LT-insensitive plants such as barley, rye, winter wheat, grapevine, potato, chickpea and A. thaliana (Verbruggen and Hermans 2008; Szabados and Savoure 2010; Kaur et al. 2011). Proline plays multiple roles in plant stress tolerance, as a mediator of osmotic adjustment, a stabilizer of proteins and membranes, an inducer of osmotic stress-related genes, and as a scavenger of ROS (Verbruggen and Hermans 2008; Szabados and Savoure 2010; Theocharis et al. 2011). The most probable roles of proline are to (a) regulate cytosol acidity, (b) stabilize the NAD?/NADH ratio, (c) increase the photochemical activity of the photosystem II in thylakoid membranes and (d) decrease lipid peroxidation (Kishor et al. 2005). Most chilling-sensitive plants that accumulate Pro under LT conditions do not acquire cold tolerance (Kushad and Yelenosky 1987), unless a high concentration of Pro was applied prior to stress (Xin and Li 1993). It appears therefore that proline possesses the potential to alleviate LT injury in chilling-sensitive plants, but for some reason this system fails under natural conditions. (b) Glycine betaine: The accumulation of glycine betaine (GB) usually correlates with the plant’s level of stress tolerance. Both the genetically engineered biosynthesis of GB in plants that do not naturally accumulate GB and the exogenous application of GB enhance the tolerance of such plants to various abiotic stresses (Chen and Murata 2008).

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Possible roles for GB include stabilization of the transcriptional and translational machinery. GB stabilizes protein complexes and membranes in vitro and may indirectly induce H2O2-mediated signalling pathways. Effect of microorganisms on cold tolerance Deleterious effects Both the aerial parts of the plant and the rhizospheric zone harbour hundreds of species of bacteria, yeast and fungi. Several bacterial and fungal species have the ability to nucleate ice at high sub-freezing temperatures. Bacterial species with ice nucleation activity (Ice? bacteria) such as Pseudomonas syringae contribute to frost injury in many frost-sensitive plant species by reducing their ability to supercool and avoid the formation of membrane damaging ice crystals (Lindow and Leveau 2002). Other ice nucleating bacterial species include P. fluorescens, Erwinia herbicola, and some strains of Xanthomonas campestris, as well as related strains. Some species of Fusarium and related genera of fungi are also active in ice nucleation. Beneficial effects One way to reduce the incidence of LT damage is to use beneficial microorganisms that enhance plant growth and improve their resistance to stress. Alternatively, beneficial bacteria may also be used to eliminate the Ice? bacteria from plant surfaces. Since the ice nucleation temperature increases with the population size of Ice? bacteria, preemptive competitive exclusion of Ice? bacteria by naturally occurring non-ice nucleating active bacteria could be an effective and practical method for managing frost in cold-sensitive plants (Lindow and Leveau 2002). The bacteria could also be genetically altered to not carry the genetic instructions needed to produce the ice nucleating protein. If such new bacteria (INA-) were sprayed onto plants at very high concentrations, naturally occurring bacteria (INA?) would not be able to compete. Recombinant Ice- bacteria, the first engineered microorganisms released into the open environment in field experiments, have been used to illustrate the specificity with which competitive exclusion of Ice? bacteria occurs (Skirvin et al. 2000). Several endophytic bacteria have been reported to induce resistance against biotic stress and tolerance to abiotic stress in several plants. For instance, a plant growth-promoting rhizobacterium (PGPR), Burkholderia phytofirmans strain PsJN, is able to reduce chilling-induced damage (Ait Barka et al. 2006). Similar conclusions were reported during the interaction between Chorispora bungeana and the endophyte Clavibacter sp. strain Enf12

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(Ding et al. 2011). In attempt to explain how some beneficial bacteria may influence cold tolerance, Theocharis et al. (2011) reported that several stress-related gene transcripts (e.g., StSy, PAL, Chit4c, Chit1b, Gluc and LOX) and changes in levels of several stress-related metabolites (e.g., proline, malondialdehyde and other aldehydes known to be lipid peroxidation markers, and hydrogen peroxide) increased earlier, faster, and were more pronounced in chilled-PsJN-bacterized plantlets. This is consistent with the ‘priming’ concept (Theocharis et al. 2011), supporting the establishment of a mutualistic relationship between the bacterium and the grapevine. The endophyte participates in the cold acclimation process via a scavenging system (Ding et al. 2011; Theocharis et al. 2011). The reported increase in the expression of Chit1b, Chit4c and Gluc was not surprising because chitinases and glucanases can be classified as either antifreeze (AFPs, Griffith and Yaish 2004) or PR (Van Loon and Van Strien 1999) proteins; this confirms the link between cold signals and pathogenesis in plants, as shown in Fig. 5. Further, we demonstrated recently that photosynthesis is modulated by the presence of beneficial bacteria in grapevine plantlets, suggesting that the modification of carbohydrate metabolism is one of the major modes by which PGPR reduces chilling-induced damage (Fernandez et al. 2012).

Concluding remarks and future perspectives Plant physiologists and plant molecular biologists have always been interested in mechanisms involved in plant tolerance to cold and how plants may react to withstand damage following stress. The biological and physiological changes that occur following cold exposure have been particularly well-studied. Studies conducted in recent years have analysed the cold signal, the genes that act downstream of it to induce cold acclimation, and the overall cascade of molecular events that occur following cold perception. This has generated a large amount of data that requires collation and interpretation. Thus, there is a real need for a comprehensive model that encapsulates this multi-step process. Acknowledgments The first author (A.T.) was supported by a Grant from the Greek State Scholarship Foundation (I.K.Y.).

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