Lignins and Abiotic Stresses

Lignins and Abiotic Stresses

MIREILLE CABANE,*,1 DANY AFIF* AND SIMON HAWKINS{

*Nancy-Universite´, INRA, UMR 1137, Ecologie et Ecophysiologie Forestie`res, Boulevard des Aiguillettes, B.P. 70239, Vandœuvre le`s Nancy, France { Universite´ Lille Nord de France, Lille 1 UMR 1281, Villeneuve d’Ascq cedex, France

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Lignins ........................................................................... B. Abiotic Stresses ................................................................. II. Response to Abiotic Stresses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Drought .......................................................................... B. Salinity ........................................................................... C. Heavy Metals.................................................................... D. Wounding........................................................................ E. Low Temperature .............................................................. F. Ozone............................................................................. G. UV-B Radiation ................................................................ H. Light .............................................................................. I. Elevated CO2 .................................................................... J. Nitrogen Stress.................................................................. III. Lignin role in Response to Abiotic Stresses. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV. Regulation of the Response . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V. Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Corresponding author: E-mail: [email protected]

Advances in Botanical Research, Vol. 61 Copyright 2012, Elsevier Ltd. All rights reserved.

0065-2296/12 $35.00 DOI: 10.1016/B978-0-12-416023-1.00007-0

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ABSTRACT Lignins, major components of the vascular plant cell wall, provided the mechanical support that allowed the development of upright plants adapted to a terrestrial habitat. Their biosynthesis through the phenylpropanoid and monolignol pathways has been extensively studied and significant advances have recently been made in understanding the regulation of this process. Lignin deposition is also modified in response to both abiotic and biotic stresses. Here, we present an overview of lignin biosynthesis in response to various abiotic stresses: drought, salinity, heavy metals, wounding, low temperature, ozone, UV-B radiation, light, elevated CO2 and nitrogen stress. Although the stimulation of the phenylpropanoid pathway is a common feature of stress response, the subsequent synthesis of lignin is only demonstrated in some cases. The roles of lignins in different phases of abiotic stress response are discussed as well as the regulation of their synthesis under stress.

I. INTRODUCTION A. LIGNINS

Lignins are complex phenolic polymers that provide strength, rigidity and hydrophobicity to certain plant cell walls (Boerjan et al., 2003; Ralph et al., 2004; Rogers and Campbell, 2004). The presence of lignin in vascular tissues allows plants to stand upright and to withstand the pressure of water transport. The emergence of lignin biosynthesis during evolution is considered to be crucial for the development of land plants (Weng and Chapple, 2010). Due to the high amounts of this compound in tree wood, lignin is the second most abundant biopolymer on Earth after cellulose and represents a significant carbon sink (Boudet et al., 2003). The lignin biosynthesis pathway has been extensively studied over the past two decades and it is relatively well understood even if some gaps remain (Bonawitz and Chapple, 2010). Lignin is synthesized through the oxidative polymerization of the three most abundant lignin monomers or monolignols, namely p-coumaryl alcohol, coniferyl alcohol and sinapyl alcohol (Fig. 1). Upon incorporation in the lignin polymer, these monolignols give rise to p-hydroxyphenyl (H), guaiacyl (G) and syringyl (S) units. The lignin structure varies substantially between cell types and species according to the relative proportion of each unit and the different kinds of interunit bounds (Neutelings, 2011; Ralph et al., 2004). The term lignin therefore refers to a class of biopolymers with considerable diversity and it is probably more accurate to use the plural form lignins. Monolignols are synthesized through a metabolic grid involving 10 different steps and begins with the general phenylpropanoid pathway (Fig. 1). Phenylalanine ammonia-lyase (PAL) catalyses the first step of

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Fig. 1. Phenylpropanoid pathway leading to lignin biosynthesis. The most favoured route in angiosperms is shown. Enzymes involved in the phenylpropanoid and monolignol pathways are phenylalanine ammonia-lyase (PAL), cinnamate-4hydroxylase (C4H), 4-coumarate:CoA ligase (4CL), p-hydroxycinnamoyl-CoA:quinate/shikimate p-hydroxycinnamoyltransferase (HCT), 4-coumarate 3-hydroxylase (C3H), caffeoyl-CoA O-methyltransferase (CCoAOMT), cinnamoyl-CoA reductase (CCR), ferulate (coniferaldehyde)-5-hydroxylase (F5H), caffeic acid/5-hydroxyconiferaldehyde O-methyltransferase (COMT), cinnamyl alcohol dehydrogenase (CAD). The shikimate pathway which provides substrates to the phenylpropanoid pathway is also shown: 3-deoxyarabinoheptulosonate-7-phosphate synthase (DAHPS), shikimate dehydrogenase (SHDH), chorismate synthase (CS).

the phenylpropanoid pathway, the deamination of phenylalanine to cinnamic acid. In the subsequent two steps, cinnamate-4-hydroxylase (C4H) and 4-coumarate:CoA ligase (4CL) give rise to p-coumaroyl-CoA, one of the most important branch points of the phenylpropanoid biosynthesis pathway. From this point, the p-coumaryl alcohol (precursor of H lignin) is synthesized in two steps requiring cinnamoyl-CoA reductase (CCR) and cinnamyl alcohol dehydrogenase (CAD). The production of coniferyl alcohol (precursor of G lignin) and sinapyl alcohol (precursor of S lignin) needs supplementary steps. A decisive step for both monolignols is initiated by

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p-hydroxycinnamoyl-CoA:quinate/shikimate p-hydroxycinnamoyltransferase (HCT) and 4-coumarate 3-hydroxylase (C3H) and involves products from the shikimate pathway. The synthesis of coniferyl alcohol (and G lignin) subsequently requires caffeoyl-CoA O-methyltransferase (CCoAOMT), CCR and CAD and the synthesis of sinapyl alcohol (and S lignin) requires in addition two more enzymes, ferulate (coniferaldehyde)-5-hydroxylase (F5H) and caffeic acid/5-hydroxyconiferaldehyde O-methyltransferase (COMT). It should be underlined that the general phenylpropanoid pathway also generates a huge range of various phenolic compounds including flavonoids, stilbenes, etc. (Vogt, 2010). Monolignols, in addition to forming lignins, may also produce (neo)lignans and oligolignols by dimerization or oligomerization (Davin et al., 2008). Consequently, stress-induced modifications of the phenylpropanoid metabolism do not necessary imply changes in lignin synthesis. The phenylpropanoid pathway itself is supplied with phenylalanine through the shikimate pathway. This pathway drives approximately 20% of carbon fixed by photosynthesis and feeds various pathways (Bentley, 1990; Herrmann and Weaver, 1999). Lignin synthesis therefore requires a good coordination between both shikimate and phenylpropanoid metabolism. In fact, stimulation of the phenylpropanoid pathway may only be effective if substrate availability from the shikimate pathway is sufficient. Moreover, shikimate pathway intermediates are involved in HCT- and C3H-catalysed reactions and can therefore exert metabolic control on monolignol biosynthesis by controlling the channelling of shikimate pathway intermediates. In lignified cells, lignin constitutes a major component of cell walls together with cellulose and hemicellulose with a proportion of approximately 2:1:1 (cellulose, lignin, hemicellulose). The lignin content of cell walls is usually expressed with regards to the relative abundance of other major components. Consequently, a variation in cellulose synthesis will affect not only the cellulose content but also the measured lignin content, even though lignin biosynthesis per se may not have been affected. Therefore, changes in lignin content must be interpreted carefully and analysed together with other parameters such as histological analyses and/or enzymatic activities involved in the lignin biosynthesis pathway and/or cellulose and hemicellulose biosynthesis pathways. Lignins are deposited within the carbohydrate matrix of the cell wall and can form chemical bonds with other cell wall components. The quantification of lignin is difficult because lignins are covalently linked with cell wall carbohydrates, proteins, phenolics, or other compounds. These compounds may interfere with determination of lignins leading to over- or underestimation (Brinkmann et al., 2002; Dence, 1992). Lignins are essential for plant development and the production and deposition of these polymers are highly regulated (Rogers and Campbell, 2004).

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The recent characterization of transcription factors involved in controlling the expression of genes encoding lignin biosynthesis enzymes is enabling a better understanding of the regulation of this complex process (Zhao and Dixon, 2011). Lignins also play an important role in plant defence, by acting as a physical barrier against pathogens. More recent studies also suggest a role for phenylpropanoids in chemical defence mechanisms (Naoumkina et al., 2010). Abiotic stresses are also known to modulate lignification and lignins are supposed to play a role in abiotic stress tolerance. The objective of this review is to provide an overview of our current knowledge about this topic.

B. ABIOTIC STRESSES

Abiotic stresses are defined as environmental factors that reduce cell activity and plant growth and cause a profound reorganization of plant metabolism (Lichtenthaler et al., 1998). Abiotic stresses include various natural or anthropogenic factors including light, UV, heat, low temperatures, drought, flooding, mineral deficiencies or excess, pollutants, ozone, heavy metals and elevated CO2. Plants respond to stresses through a dynamic process that can be divided into four phases according to the unifying stress concept (Fig. 2; Kosova et al., 2011; Larcher, 2003; Lichtenthaler et al., 1998). Before the stress application, plants are in a physiological standard situation that is optimum in its location. At the beginning of the stress, the plants are in an alarm phase: the plant vitality declines, the tolerance level is minimum and stress-signalling pathways are induced. Acute damage and senescence may occur if the stress is too high and the plant possesses low tolerance mechanisms. If the plant survives, this phase is followed by an acclimation phase that corresponds to a new physiological standard with a maximum resistance to stress. This phase is associated with the activation of protection, detoxification and repair mechanisms and may result in readjustments leading to a maintenance phase if the new physiological standard is stable under stress. Plant metabolism undergoes profound reorganizations due to the reorientation of metabolism to stress acclimation. This phase may be stabilized and maintained under prolonged exposure to stress. If the plant is unable to maintain this phase or the stress intensity is too high, the vitality declines and chronic damage occurs leading to cell death. This is the exhaustion phase. When the stressor is removed before the beginning of the senescence, a regeneration phase may be observed leading to new physiological standards. The sequence of these phases depends on stress duration and intensity and plant tolerance capacity. Specific modifications in cell metabolism may be observed at each stage and different roles can be assigned to alterations in

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Fig. 2. General concept of the different phases occurring during stress response. Plants are in physiological standard conditions when stress is applied. The early phase of stress response (alarm phase) is associated with sensing and signalling pathways followed by an acclimation phase associated with detoxification, repair and protection activation. This phase can be stabilized (maintenance phase) resulting in profound metabolic readjustments. If the plant is not able to maintain this phase and is overtaxed by chronic stress, irreversible damages occur (exhaustion). If the stress is removed before the damages are too high, a recovery phase leads to new physiological standards.

plant factor levels (transcript, protein, metabolite) according to the phase(s) involved, that is, signalling, acclimation, adjustment, or exhaustion.

II. RESPONSE TO ABIOTIC STRESSES A. DROUGHT

Water is a universal requirement for life and is essential for metabolism. The lack of water resulting from drought stress impacts negatively on plant growth and productivity. This situation will become worse because of global climatic change (IPCC, 2007), and it is therefore important to improve our understanding of how plants react to this stress in order to develop efficient breeding programmes to select tolerant varieties. Several reports have shown that stress modifies the expression of cell wall-related genes and modifies cell

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wall structure in both dicot and monocot species (Fan et al., 2006; Kim and Leestadelmann, 1984; Wu and Cosgrove, 2000). Pectin-associated arabinose polymers such as arabinans and/or arabinogalactans, as well as xyloglucans may play an important role in conferring resistance to extreme drought stress in the leaves of desiccation-tolerant plants such as Craterostigma wilmsii and Myrothamnus flabellifolia (Moore et al., 2006). Drought stress also affects plant secondary metabolism and lignification. As with other types of abiotic stress, the effect (stimulation or inhibition) varies depending upon the intensity and stress period, the species, the organ/tissue considered and the moment when the analyses are performed. For example, drought was associated with decreased lignin biosynthesis in maize roots and leaves (Alvarez et al., 2008; Vincent et al., 2005). In contrast to maize, cell growth extensibility and the expression of lignin biosynthesis genes all increased in rice roots under water stress conditions (Yang et al., 2006). Increased lignin biosynthesis but reduced growth was observed in Citrullus lanatus roots associated with drought resistance of this plant (Yoshimura et al., 2008). Further evidence linking drought stress to modifications in lignification was provided by 2D-PAGE of soluble proteins extracted from leaves of two different drought-tolerant maize (Zea mays L.) inbred lines subjected to PEG-induced drought stress (Hu et al., 2009). This study identified 58 protein spots that were differentially accumulated in both lines after 17, 24 and 48 h water stress. Three of these proteins accumulated in both lines at all three time points. Peptide fingerprinting showed that two of the proteins corresponded to the lignin biosynthetic enzymes COMT and CAD and the third spot corresponded to an S-adenosyl-L-methionine synthase (SAMS) protein potentially involved in supplying methyl groups during monolignol biosynthesis. Further analyses by qRT-PCR of three drought-tolerant lines and one drought-sensitive line showed that both CAD and COMT expression decreased in all four lines at 17 h compared to 0 h, but subsequently increased in the three tolerant lines, but not the sensitive line. In a subsequent experiment, chemical analyses revealed that leaf lignin content increased significantly in highly drought-tolerant maize lines under severe and moderate stress, but not in drought-sensitive lines. The authors suggest that increased lignification in maize leaves might represent a strategy to increase mechanical strength and/or water impermeability. Increased lignification also appears to be associated with drought-stress resistance in the Mediterranean shrub Cistus albidus (Jubany-Mari et al., 2009). In this study, the levels and sub-cellular localization of hydrogen peroxide together with the oxidative stress status and lignin content were all followed in this plant during a 1-year period that allowed the authors to investigate the effects of summer-related drought stress. During the summer

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months (June–August), leaf relative water content decreased while abscissic acid (ABA) and H2O2 levels increased. Sub-cellular localization by CsCl3 precipitation indicated that H2O2 started to accumulate in leaf mesophyll cells at the start of the summer drought period (June). In July, H2O2 started to accumulate in the cell walls of both xylem vessels and sclerenchyma. Interestingly, high H2O2 levels were also correlated with the de novo formation of sclerenchyma cells in the leaf cortex. Although H2O2 is necessary for peroxidase-mediated monolignol polymerization, an observed augmentation in H2O2 levels should not be automatically linked to increased lignification. Drought stress, like other abiotic stress, stimulates reactive oxygen species (ROS) production leading to oxidative stress and it is therefore interesting to verify ROS sub-cellular distribution. Analyses showing that levels of the antioxidant ascorbic acid together with the absence of any observable organelle damage also suggested that the high H2O2 content was not associated with intracellular oxidative stress. The observation showing that increases in cell wall localized H2O2 were associated with significant increases (up to 69%) in leaf lignin content suggested that H2O2 was needed for oxidative polymerization. However, the maximum increase in lignin accumulation occurred in May, prior to the peak of H2O2 production that was observed in July, suggesting that ROS production might also be involved in stress-signalling pathways. In trees, drought stress affects both xylem anatomy and lignification. In poplar, drought stress reduced both fibre length and cross-sectional area in early summer but not in late summer (Arend and Fromm, 2007). Similarly, early summer drought stress also reduced vessel cross-sectional area. Overall, total vessel area was not significantly affected because vessel number increased. However, no cell wall analyses were performed and it is therefore difficult to know whether the observed reduction in xylem cell expansion was associated with modifications in the quantity and/or chemical composition of different cell wall polymers including lignin. In Pinus radiata logs, frequent drought stress has been shown to induce concentric shelling (Donaldson, 2002). Microscopic examination revealed the presence of numerous false growth rings alternating with bands of poorly lignified tracheids. A closer study of individual cells showed that both the middle lamella and outer S1 layer of the secondary cell wall were poorly lignified and most likely the cause of the observed poor cohesion between individual cells. In certain cases, wall lignification was extremely reduced and collapsed cells were observed. The presence of collapsed, deformed cells is reminiscent of the irregular xylem phenotype observed in the Arabidopsis irx4 mutant characterized by extremely reduced cell wall lignin content due to a mutation in the CCR gene (Jones et al., 2001). In contrast to the less lignified status of the S1 layer, the S3 layer of drought-stressed tracheids was often more heavily lignified

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than in control xylem, suggesting that the stressed cell modifies its pattern of lignin deposition when confronted to drought stress. B. SALINITY

Salt stress is caused by the presence of high concentrations of salt ions— mainly sodium and chloride. Analysing the effects of this stress on plants is difficult since the high salt ion concentrations provoke not only a chemical (ionic) imbalance in plant cells, but also induce a drought stress by increasing the water potential (C) of the soil. Major resistance mechanisms to salt stress are associated with transporter-mediated export/sequestration of Naþ ions across the plasma membrane and tonoplast, respectively (Zhu, 2003). Although a number of studies have generated experimental results suggesting that lignification might play a role in salt tolerance, direct evidence linking salt stress to modifications in the lignification process is difficult to find in the literature. For example, metabolic profiling of Arabidopsis cell cultures suggested that the methylation cycle (supplying methyl groups), the phenylpropanoid pathway and glycinebetain biosynthesis were all synergistically induced as a short-term response to salt stress (Kim et al., 2007). However, phenylpropanoids are not just destined to lignin biosynthesis and the observation of increased carbon flow in this metabolic pathway is not definite proof of an effect on lignification. In another study (Quiroga et al., 2000), the effect of salt stress (100 mM NaCl) on the expression of a tomato peroxidase gene (TPX1) was investigated. Under non-stress conditions, this gene is specifically expressed in root tissues and Northern blot analyses indicated that the gene was upregulated by salt stress. The same gene is also activated in aerial tissues following wounding and its overexpression in tomato leaves is associated with increased lignification. In situ hybridization of roots from non-stressed tomato plants showed that TPX1 transcripts accumulated in the endodermis and protoxylem in the apical zone (first 0.5 cm), in the endodermis and hypodermis of the medium zone (8–10 cm from root tip) and in the endodermis and exodermis of the basal zone (13–15 cm from root tip). Since these tissues are lignified and/or suberized, the observed expression pattern of the TPX1 gene is coherent with a role in root lignification/suberization. Salt stress modified TPX1 expression in tomato roots; the TPX1 gene was repressed in the apical root zone, stimulated in the medium zone and decreased in the exodermis, but not the endodermis of basal root samples. Unfortunately, lignin/suberin levels were not evaluated in the roots of salt-stressed plants, and it is therefore not possible to know whether alterations in TPX1 expression were associated with modified lignification.

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In addition to peroxidases, laccases have also been implicated in the oxidation of monolignols during lignin formation. In one study (Liang et al., 2006), salt treatment was associated with reduced root elongation and apical swelling in maize roots, together with a significant increase in ZmLAC1 expression. The authors initially hypothesized that the reduction in root elongation was associated with increased lignification and/or crosslinking of cell wall phenolics mediated by the ZmLAC1 protein. However, subsequent experiments showed that other treatments causing similar inhibition of root elongation did not modify ZmLAC1 gene expression. This latter observation would argue against a role of lignification in the inhibition of root elongation; however, since neither lignin biosynthesis nor phenolic metabolism were investigated in this study, it is difficult to come to any firm conclusions. Interestingly, salt stress, as well as drought stress, cold stress and ABA treatment have all been shown to stimulate the production of the microRNA miR393, miR397b and miR402 in Arabidopsis (Martin et al., 2010). The miR397b is predicted to target a laccase gene previously shown to reduce root growth under dehydration in a knock-out mutant (Cai et al., 2006). More recently, miR397a/b have been predicted to target the Arabidopsis laccase genes AtLAC4 and AtLAC17 that play a role in the lignification of interfascicular fibres (Berthet et al., 2011). Taken together, these observations demonstrate that salt stress, like other abiotic stress, affects the expression of both peroxidase and laccase genes with a likely concomitant affect on lignification. Another link between salt stress and lignification was revealed by a study on the roots of tomato plants (Sanchez-Aguayo et al., 2004). In this work, the expression of three SAM genes (encoding SAMS) was compared in the roots and leaves of tomato plants after 6 days salt stress (5 g L 1). Salt stress stimulated SAM1 gene expression in both roots and leaves, but had no effect on the expression of SAM2 and SAM3. SAM1 was also more highly expressed in root tissues under non-stress conditions. Western blot analyses confirmed the increase of SAMS proteins in stressed plants. S-Adenosyl-L-methionine is the main methyl group donor for numerous transmethylation reactions in plants and lignin biosynthesis (involving successive methylation to form coniferyl and sinapyl alcohol) is believed to impose the largest demand for methyl groups in plants (Hanson et al., 1994). The authors suggest that the observed increase in SAM1 gene expression and accumulation of SAMS proteins is potentially related to an increase in lignification. Subsequent immunolocalization indicated that SAMS proteins accumulated in all cell types of roots, leaves and stems in both control and non-stressed plants, but that some cell types appeared to accumulate SAMS proteins to a greater extent. SAMS proteins were

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observed to be particularly abundant in xylem cells in all three organs, as well as in stem collenchyma cells and root epidermal cells. Histochemical staining revealed that salt stress induced a significant increase in the quantity of lignified xylem tissue in stems (11 ) and roots (2 ), but did not appear to stimulate lignin production in individual cells. The authors suggest that the increased lignification of vascular tissue is necessary to impart greater selectivity and to compensate for diminished bulk flow along the apoplastic pathway.

C. HEAVY METALS

Metal pollutants (Zn, Pb, Cd, Cu, As, etc.) enter the biosphere mainly as a result of anthropomorphic activities (industry, mining, agriculture, etc.) where they represent a danger for plant, animal and human well-being (Sharma and Dietz, 2009). Metal toxicity in plants can be assigned to three main actions: (i) direct interaction with proteins by targeting of structural and catalytic sites, (ii) stimulation of ROS production and associated oxidative stress and (iii) displacement of cations from specific binding sites resulting in the disruption of physiological processes (Sharma and Dietz, 2009). Metals can be classified as heavy metals, toxic metals and metalloids; however, since no clear agreement exists on exactly what metals belong to which group it is better to consider each element separately. 1. Copper Copper (Cu) is known to be essential for lignin biosynthesis and sub-/supraoptimal levels are often associated with modifications in lignin production (Moura et al., 2010). In one study (Lin et al., 2005), Cu treatment of soybean seedlings was associated with a significant reduction (18–56% depending upon the concentration) in root growth. Copper also provoked a rapid increase, then decrease in whole root H2O2 levels, together with an increase in both laccase and peroxidase activity and a global increase in lignin (thioglycolic acid assay). Activities of both anionic and cationic peroxidases increased and semi-quantitative RT-PCR showed that the expression of two (out of three tested) peroxidase genes increased following Cu treatment. Copper ions form part of the catalytic site of laccase enzymes and it is possible that Cu-induced lignification is associated with increased laccase activity and gene expression (see Chapter 5). Interestingly, copper also plays a central role in regulating the expression of different laccase genes in Arabidopsis through a post-transcriptional mechanism implicating different microRNAs (miRNAs; Abdel-Ghany and Pilon, 2008).

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2. Cadmium Cadmium (Cd) is another metal pollutant impacting directly or indirectly on different plant physiological processes and plants have evolved a wide range of different mechanisms to increase their tolerance to this metal (Xiong et al., 2009). Studies (Wang et al., 2008) showed that up to 60% of total cadmium taken up by plants is located in the cell wall of Ramie and affects the structure of primary cell wall polysaccharides in flax hypocotyls (Douchiche et al., 2010). A recent study (Finger-Teixeira et al., 2010) showed that cadmium treatment of soybean plants was associated with reduced root elongation and fresh-/dry-weight production, as well as an increase in PAL activity, H2O2 levels and both soluble- and cell wall-bound peroxidase activity. Determination of lignin levels (thioglycolic acid assay) revealed a dramatic increase (16.1–131%) in cell wall residue (CWR) lignin content. In agreement with these results, subsequent nitrobenzene oxidation indicated an increase in total (H þ G þ S) monomer yield when expressed on a CWR basis. When total monomer yield was based on lignin content it was decreased, suggesting that the lignin structure was modified (increased condensation). In agreement with this observation, the percentage of H units increased. 3. Zinc The metal zinc (Zn) serves as a cofactor for more than 300 enzymes and is therefore an essential micronutrient for both plants and animals (Guerinot and Eide, 1999). In a global transcriptomic approach (van de Mortel et al., 2006), the differential expression of Arabidopsis thaliana—a non-zinc accumulator and Thlaspi caerulescens a zinc hyperaccumulator—under different zinc concentrations revealed that more than 2000 genes were significantly differentially expressed ( 5-fold) between the two species. In addition to genes known to be involved in metal homeostasis (Zn transporters, defensins), 24 genes with a potential function in lignification (Ehlting et al., 2005)—including transcripts corresponding to F5H, CAD, COMT, 4CL and laccase genes—as well as 13 genes involved in suberin synthesis (Costaglioli et al., 2005) were more highly expressed in T. caerulescens as compared to A. thaliana. Subsequent microscopic examination by autofluorescence revealed higher autofluorescence of the root endodermis (and occasional presence of a second cell layer) in T. caerulescens suggesting a higher degree of lignin/suberin biosynthesis. Autofluorescent cell wall thickenings are deposed in a U-shape in radial walls and inner tangential walls. Similar thickenings have been observed in the salt-adapted crucifer Thellungiella halophila (Inan et al., 2004). The authors observed that the U-shaped deposits occurred mainly in the cell walls of the older non-absorbing root region and hypothesized that increased lignin/suberin deposition was mainly linked

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with preventing excess metal efflux from the vascular cylinder rather than controlling metal influx. 4. Aluminium Aluminium (Al) limits plant growth and productivity in acidic soils. Al toxicity is associated with ROS production and lipid peroxidation, and is also characterized by the inhibition of root elongation that is believed to contribute greatly to reduced plant productivity (Kochian, 1995). Another study (Ma et al., 2011) showed that Al treatment of rice seedlings inhibited root elongation to a greater extent in the Al-sensitive variety IR64 when compared to the Al-tolerant variety azucena. Al treatment also significantly increased lignin content as determined by the acetyl bromide method in the Al-sensitive, but not the Al-tolerant variety. Increased lignin accumulation was also associated with a significant increase in H2O2 production, as well as in the quantity of cell wall-associated peroxidase activity. The authors suggest that Al stimulates lignification in the roots of Al-sensitive varieties by increasing H2O2 production. A similar analysis (You et al., 2011) compared global expressions in root apices of an Al-tolerant genotype of soybean after 4 h in the presence and absence of 30 mmol L 1 AlCl3. Aluminium treatment upregulated a number of cell wall-related genes including lignin genes and the authors hypothesize that the expression of these genes might be related to Al-induced root growth inhibition. D. WOUNDING

Often associated with insect or herbivore activities, mechanical wounding exposes plant tissues to dehydration and opportunist pathogen attack by fungi, bacteria and viruses. It is therefore vitally important that plants rapidly protect the exposed tissues. Both lignification and suberization of plant cell walls play an important role in this process and they are often associated with the formation of a wound (necrophylactic) periderm (Biggs, 1986; Vance et al., 1980). Autofluorescence and histochemical staining of wounded eucalyptus seedlings (Hawkins and Boudet, 1996) showed that both lignin and suberin could be detected after 24 h in the xylem wound zone and after 72 h in the cortex. Histochemical staining suggested that the lignin formed during these early defence responses were relatively poor in S units as previously observed (Biggs, 1986). Wounding has been shown to induce large-scale changes in gene expression profiles (Cheong et al., 2002) including genes encoding enzymes in the phenylpropanoid pathway (Dixon and Paiva, 1995). In one particularly detailed study, semi-quantitative RT-PCR and promoter-GUS fusions were

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used to characterize the developmental- and wound-induced expression profiles of the four 4CL genes (At4CL1–At4CL4) in Arabidopsis (Soltani et al., 2006). The semi-quantitative RT-PCR revealed that the four genes responded differently to wounding of leaves of 3–4-week-old plants. At4CL1 and At4CL2 expression increased 2.5 h post-wounding before falling to basal levels at 12 h and then increasing again to a maximum between 48 and 72 h. At4CL4 expression also increased at 2.5 h post-wounding and remained elevated for 12 h before declining. Finally, At4CL3 decreased following wounding before returning to basal levels at 4 h post-wounding and then gradually increasing to 72 h. The genes At4CL1 and At4CL2 are believed to be the 4CL genes associated with lignification, while At4CL3 is more likely associated with flavonoid biosynthesis. At4CL4 is expressed throughout seedling roots. Promoter-GUS histochemical staining showed that the At4CL4 promoter is rapidly activated (within minutes) following wounding whereas At4CL3 is not activated. At4CL1 and At4CL2 are activated, but only after 72 h postwounding. Taken together, these results suggest that At4CL4 is involved in the early wound response in Arabidopsis leaves. Promoter deletions indicated the presence of both positive and negative regulatory elements as well as suggesting the existence of an intron regulatory element. However, although this work provided detailed information on the expression profiles of the 4CL gene family in Arabidopsis, it did not examine whether wounding induced lignification and it is possible that 4CL gene expression might be associated with the production of secondary metabolites. In support of this hypothesis, a recent study (Deflorio et al., 2011) of the effect of wounding on phenylpropanoid gene expression in Sitka spruce indicated differences in the response of bark and sapwood to wounding. Trees were wounded by drilling, and samples from both the wound zone and at 1 cm distant from the wound zone were analysed 3 days post-wounding. Quantitative RT-PCR indicated that, in bark tissues, the expression of PAL, CCR, HCT and PX3 (peroxidase) increased. In contrast, CAD gene expression decreased. In sapwood samples, the expressions of PAL, CCR, HCT and CAD either decreased or did not change. The expression of the PX3 gene increased. Analyses of lignin content (thioglycolic acid assay) showed that wounding did not induce a significant increase in lignin content in either bark or sapwood samples 3 days after wounding. In contrast, HPLC analyses showed that combined wounding and fungal inoculation (wounding alone was not tested) induced a significant increase in the amounts of certain phenolics (coniferin, astringin, taxifolin, piceid, isorhapontin) in the cell wall-bound fraction (but not the soluble fraction) in bark samples, but not sapwood samples. These results suggest that the modifications in phenylpropanoid gene expression levels are associated with the production of a wide

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range of secondary metabolites, rather than lignin. However, it is also likely that 3 days is too early to detect any significant increase in lignin synthesis and deposition. It would obviously be of interest to combine molecular studies with chemical and microscopic analyses over a longer experimental time period. In contrast to leaves and other tissues of non-woody plants such as Arabidopsis, the wound response in trees can be highly variable depending upon the depth of the wound (just bark, or bark and cambium/xylem), the season and the general physiology of the tree. A detailed study (Frankenstein et al., 2006) using TEM and UV microspectroscopy of the transition zone formed between xylem laid down prior to wounding and the tissue formed after wounding in 25-year-old poplar trees indicated clear modifications in structure. In this study, samples were harvested between 2 and 95 weeks postwounding. The transition zone was characterized by the development of fibres with significantly thicker secondary cell walls. UV microspectroscopy indicated that the quantity and distribution of cell corner lignin was largely unaffected in contrast to the compound middle lamella and secondary cell wall where increasing absorbance values indicated an increase in lignin content. Modifications of the absorbance peak wavelength also suggested that the relative proportion of G-lignin units increased together with a reduction in H unit content. E. LOW TEMPERATURE

Like other environmental factors, temperature influences plant development and vital functions such as growth rate and patterning, bud break, flowering time and seed germination (Penfield, 2008). Plants facing extreme temperatures (low or high) respond with a complex array of biochemical and molecular processes. Low temperature is responsible for cold stress and reduces plant growth, photosynthesis and induces an inhibition of water uptake leading to cellular dehydration. Nevertheless, plants are able to acclimate to low temperatures. Chilling temperatures (0–15 8C) appear to be necessary for most plants to acquire tolerance to freezing temperatures (sub-zero). However, some plants cannot tolerate ice formation and are unable to tolerate freezing temperatures even after an acclimation period and are considered as chilling sensitive. Plasma membrane rigidification, ABA, ROS and Ca2 þ are involved in the cold signalling process (Chinnusamy et al., 2007). Cold stress induces modifications in plant metabolism including the production of soluble sugars, amino acids and organic acids to reduce cellular dehydration, to stabilize enzymes and membranes and to neutralize toxic molecules (Guy et al., 2008).

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The phenylpropanoid pathway is stimulated by low temperatures; however, variations are observed according to the genes/enzymes and organs/tissues analysed. In maize seedlings transferred to low temperature (10 8C) for 48 h, PAL gene expression was constant during the first 12 h and then increased during the next 12 h. 4CL gene expression was induced rapidly within 6 h and remained unchanged for the following 36 h. When plants were returned to ambient temperature (25 8C) for 48 h, PAL and 4CL gene expression returned to their initial expression levels (Christie et al., 1994). In the stem of Arabidopsis plants exposed to light and subjected to low temperature, PAL1 gene expression was observed in cortical cells in addition to the normal expression pattern in protoxylem (Leyva et al., 1995). Cold acclimated soybeans also showed a stimulation of PAL activity and accumulation of hydroxycinnamic acid esters in root cells (Janas et al., 2000). In leaves of winter oilseed rape plants (Brassica napus) subjected to cold acclimation and freezing, PAL activity was enhanced in mesophyll cells accompanied by an accumulation of hydroxycinnamic acids. The content of ferulic acid was increased in mesophyll cell walls subjected to freezing following the period of cold acclimation. It was hypothesized that these changes were associated with an increase in cell wall rigidity to prevent mechanical stress caused by water freezing. Inhibition of PAL activity abrogated the cold-promoted accumulation of hydroxycinnamic acids (Solecka and Kacperska, 2003). Analysis of lignin gene expression in winter barley exposed for 21 days to a chilling temperature of 3 8C and followed by 1 day at freezing temperature of  3 8C showed that PAL, HCT, CCR1, CAD were upregulated in leaves after 1 day of acclimation and that high expression levels were maintained under freezing. In contrast, however, most of the lignin genes were downregulated in the crown after 1 day of acclimation (Janska et al., 2011). The authors suggested that monolignols, rather than lignin polymers, were synthesized in acclimated leaves since peroxidase genes involved in polymerization were downregulated. This hypothesis could not be validated, as measurements of lignin content were not performed in this study. A study of oak (Quercus suber) exposed for 53 days to two temperature treatments (10 and 28 8C) showed that PAL and CHS (chalcone synthase, gene encoding a flavonoid pathway enzyme) transcript levels were increased at low temperature compared to high temperature. Conversely, CAD and CS (chorismate synthase, gene encoding a shikimate pathway enzyme) genes were more highly expressed under high temperature (Chaves et al., 2011). The authors suggested that the coordinated expression of PAL and CHS at 10 8C could favour the synthesis of flavonoids, while high temperature would promote lignin synthesis. However, lignin levels were not evaluated in this study.

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In another study, acclimation to chilling induced nine peroxidase isozymes in maize mesocotyls. Two of them were localized in the cell wall and lignin content was enhanced in acclimated mesocotyls (Anderson et al., 1995). Lignin could be involved in the chilling tolerance process by increasing the rigidity of the mesocotyl. Cold acclimation of winter wheat (Triticum aestivum) was associated with accumulation of phenolic compounds in leaves, and increased lignin content in tillering nodes and roots (Olenichenko and Zagoskina, 2005; Zagoskina et al., 2005). Increased lignin deposition was also observed in poplar plants (Populus tremula  tremuloides) obtained from cuttings and exposed for 14 days to a chilling temperature (10 8C). Lignin content started to increase within 2 days of treatment and continued until the end of chilling exposure (Hausman et al., 2000). Taken together, these different observations suggest that chilling/freezing induces lignin synthesis and deposition, which could lead to a reinforcement of the cell wall, potentially to combat mechanical stress and/or cell dehydration. Results supporting a role for cold-induced lignification in cell wall stability were recently provided by a study of the EARLI1 (early Arabidopsis aluminium-induced gene1) gene in Arabidopsis. This gene is induced by low temperature and the corresponding protein was localized in the cell wall where it is believed to maintain the stability between the plasma membrane and the cell wall through binding with other proteins. EARLI1 RNAi plants showed a lower lignin content than wild type and downregulation of the CCR1 gene (Shi et al., 2011). These findings suggest that induction of EARLI1 under cold stress could modulate lignin deposition, although more analyses are necessary. F. OZONE

Tropospheric ozone is one of the main pollutants known to have a detrimental effect on plants (Booker et al., 2009; Karnosky et al., 2007). Since the beginning of the industrial era, tropospheric ozone concentration has been increasing and is predicted to keep increasing in the future (IPCC, 2007). Plants exposed to ozone displayed reduced photosynthesis resulting in decreased growth and yield (Booker et al., 2009; Wittig et al., 2007, 2009). In addition, ozone has been shown to cause visible damages to leaves. This gas enters the leaf through the stomata and reacts with the apoplast constituents generating ROS. It has also been suggested that ozone may function as an abiotic elicitor of plant defence reactions such as programmed cell death (Sandermann et al., 1998). In addition to inducing a diverse range of defence responses, ozone has been shown to stimulate phenylpropanoid metabolism in leaves of many species and under different fumigation protocols involving both acute and

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chronic exposure. In the different studies described below, ozone varied between ambient levels (30–50 ppb) to high levels (600 ppb) and exposure times ranged from 3 h to several years. In addition, plant age varied between 3 weeks and 4 years. Ozone increased PAL enzyme activity in Pinus sylvestris (Rosemann et al., 1991), parsley (Petroselinum crispum; Eckey-Kaltenbach et al., 1994), soybean (Glycine max; Booker and Miller, 1998), grape (Vitis vinifera; Sgarbi et al., 2003), poplar (Populus spp.; Cabane´ et al., 2004; Di Baccio et al., 2008) and Centaurea jacea (Francini et al., 2008). 4CL activity was also increased in soybean (Booker and Miller, 1998) and CAD activity increased in response to ozone in Picea abies (Galliano et al., 1993a; Heller et al., 1990), parsley (Eckey-Kaltenbach et al., 1994), soybean (Booker and Miller, 1998), P. sylvestris (Zinser et al., 1998) and poplar (Cabane´ et al., 2004; Di Baccio et al., 2008). Transcript abundance of genes encoding phenylpropanoid pathway enzymes responded in the same way suggesting that ozone-induced lignification involved transcriptional regulation. For example, PAL transcript levels were more abundant following ozone treatment in parsley (Eckey-Kaltenbach et al., 1994), A. thaliana (Sharma and Davis, 1994), birch (Betula pendula; Pa¨a¨kko¨nen et al., 1998; Tuomainen et al., 1996), poplar (Koch et al., 1998; Wustman et al., 2001) and C. jacea (Francini et al., 2008). Increased transcript levels were also observed for 4CL in parsley (Eckey-Kaltenbach et al., 1994) and for COMT in poplar (Koch et al., 1998) and beech (Fagus sylvatica; Jehnes et al., 2007; Olbrich et al., 2005). CAD transcripts increased in P. abies (Galliano et al., 1993b), P. sylvestris (Zinser et al., 1998) and poplar (Cabane´ et al., 2004). Transcriptomic studies indicated that PAL, 4CL, C3H, CCoAOMT and CCR responded to ozone treatment in rice (Oryza sativa; Frei et al., 2011), COMT in beech and Arabidopsis (Olbrich et al., 2005, 2009; Tosti et al., 2006) and CCR in birch (Kontunen-Soppela et al., 2010). The responses of the phenylpropanoid metabolism can be both fast (Koch et al., 1998; Sharma and Davis, 1994) and substantial (Cabane´ et al., 2004). Within an experiment, induction levels were correlated with ozone concentrations (Cabane´ et al., 2004; Galliano et al., 1993a; Rosemann et al., 1991). Stimulation of the phenylpropanoid pathway was often maintained during the whole period of ozone exposure (Cabane´ et al., 2004; Galliano et al., 1993b) and could even continue after the end of the treatment (Tuomainen et al., 1996). Interestingly, the shikimate pathway, which supplies substrates to the phenylpropanoid pathway, was also found to be upregulated by ozone treatment (Betz et al., 2009a,b; Cabane´ et al., 2004; Guidi et al., 2005; Janzik et al., 2005). This observation suggests a strong coordination between primary and secondary metabolism to provide substrates to the phenylpropanoid pathway. Most of the above results were obtained from plants cultivated in controlled or open

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top chambers and the same trend was also observed in more natural conditions such as free air ozone fumigation facilities (Betz et al., 2009a; Wustman et al., 2001). All these results unambiguously demonstrate that the phenylpropanoid pathway is upregulated in leaves under ozone exposure and is therefore probably involved in defence and acclimation mechanisms. However, the effects of ozone fumigation on lignin content in leaves were not so clear. No modifications of lignin content were recorded in Pinus ponderosa (Tingey et al., 1976), black cherry (Prunus serotina) and yellow poplar (Liriodendron tulipifera; Boerner and Rebbeck, 1995), Pinus taeda (Booker et al., 1996), soybean (Booker and Miller, 1998), cotton (Gossypium hirsutum; Booker, 2000), birch (Oksanen et al., 2005), barley (Hordeum vulgare; Plessl et al., 2005) and Quercus ilex (Baldantoni et al., 2011). Lignin content was increased after ozone treatments in sugar maple (Acer saccharum; Boerner and Rebbeck, 1995), bahiagrass (Paspalum notatum; Muntifering et al., 2000), poplar (Cabane´ et al., 2004), Trifolium spp. (Muntifering et al., 2006; Sanz et al., 2005), beech (Betz et al., 2009a; Jehnes et al., 2007; Olbrich et al., 2010), Echinacea purpurea (Szantoi et al., 2007), rice (Frei et al., 2010, 2011) and Briza maxima (Sanz et al., 2011). These varying results may be explained by species-specific differences in response to ozone treatment. For example, conifers never showed increased lignin content. Stimulation of the phenylpropanoid pathway could in such cases be associated with a modification of the pool of soluble phenolic and not necessarily lead to increased lignification (Booker and Miller, 1998; Tingey et al., 1976). Another source of potential error could be due to the different techniques (Klason, LTGA, etc.) used to determine lignin content as well as their relative (in)sensitivity (Dence, 1992), especially in the case of weak variations between control and experimental samples. Nevertheless, the structure of newly synthesized lignin (following ozone treatment) has been determined in poplar and beech and both species displayed comparable changes in lignin structure (Betz et al., 2009a; Cabane´ et al., 2004). Lignins were enriched in carbon–carbon interunit bonds and in H units indicating the production of a more condensed lignin than usual. Moreover, lignified cells were observed in the mesophyll or epidermis near the necrotic lesions in the leaf (Cabane´ et al., 2004). These results support the idea that stress lignins are synthesized in response to and in defence against ozone or ROS excess. Comparable studies on other species are needed in order to identify a general trend. The response to ozone has been extensively studied in leaves. This is understandable since it is mainly this organ that shows clear ozone-induced damage. Few studies have analysed the ozone response of stems, especially in trees. An increase in lignin content was observed in poplar and birch fumigated for 3 years in a free air fumigation experiment (Kaakinen et al., 2004),

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but this observation was not maintained after 5 years (Kostiainen et al., 2008). In one study, ozone was observed to repress the phenylpropanoid pathway in poplar wood (Richet et al., 2011), probably as a result of reduced cambial growth. However, the relative cell wall lignin content increased due to ozone-induced reductions in cellulose biosynthesis, thereby modifying the cellulose to lignin ratio. The stem response seems to correspond to a metabolic adjustment due to the reorientation of the metabolism to stress acclimation in leaves, rather than to a specific defence mechanism. It was hypothesized that the modification of the cellulose to lignin ratio in the stem could allow the tree to maintain (radial and height) growth while minimizing carbon cost. More detailed analyses are needed to draw definite conclusions. G. UV-B RADIATION

UV-B radiation (280–320 nm) is currently reaching the Earth’s surface in larger proportions because of the depletion of stratospheric ozone (Caldwell et al., 2003; Frohnmeyer and Staiger, 2003). Elevated UV-B radiation causes multitude effects on plants such as reduced growth, leaf thickening, decreased photosynthesis and DNA damage (Frohnmeyer and Staiger, 2003). Among other physiological responses, UV-B exposure induces the accumulation of UV-B-absorbing compounds such as phenolics in a large number of plant species (Caldwell et al., 2003). Phenylpropanoids such as hydroxycinnamic acids and their derivatives (sinapate esters) as well as flavonoids play complementary roles in UV-B protection. The first group are constitutive (present at leaf emergence), whereas the second group are important for the adjustment of epidermal screening during leaf development (Burchard et al., 2000). The absorption of UV-B by epidermal localized aromatic phenolics prevents radiation-induced damage to photosystem II and chlorophyll degradation. Ambient UV-B radiation reduced leaf elongation in Antarctic grass (Deschampsia antarctica) when compared with plants exposed to reduced UV-B (Ruhland and Day, 2000). This reduction could be explained partly by the accumulation of insoluble hydroxycinnamic acids (p-coumaric, caffeic and ferulic acids) cross-linking the polysaccharide network of the cell wall limiting the expansion of epidermal cells and leaf elongation (Ruhland et al., 2005). UV-B radiation probably also affects cell wall reticulation and cell expansion in grapevine (V. vinifera) leaves. The lignin pathway genes PAL, C4H, 4CL and CCoAOMT were all upregulated in response to UV-B radiation while genes associated with cell wall loosening were downregulated (Pontin et al., 2010). Evidence for lignin deposition in response to UV-B was provided by a study of leaves of the dune grassland species (Calamagrostis epigeios). During one growing season, enhanced

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UV-B radiation induced an increase in lignin content (56%) in comparison with plants exposed to ambient UV-B (Rozema et al., 1997). This lignin accumulation limits the microbial degradability in leaf litter. Similarly, cucumber (Cucumis sativus) seedlings exposed to continuous UV-B radiation for 15 days showed an accumulation of phenolic compounds in epidermal cells and sharp-headed trichomes of cotyledons. In addition, lignin was deposited in cotyledon sharp-headed trichomes over a short period from day 9 to day 15 (Yamasaki et al., 2007). It was suggested that sharp-headed trichomes may play an important role in sensing and transmitting signals during defence mechanism induction. Detailed information on the effects of UV-B radiation on phenylpropanoid metabolism has come from studies of different cell culture systems. UV-B radiation induced the expression of the gene encoding DAHPS (3-deoxyarabinoheptulosonate-7-phosphate synthase), an enzyme of the shikimate pathway providing substrates for the phenylpropanoid pathway in parsley cultures. DAHPS was induced immediately after applying UV-B radiation followed by PAL gene induction 2 h later (Logemann et al., 2000). Similarly, transcript levels of the gene encoding chorismate mutase, the enzyme providing phenylalanine and tyrosine, were increased in maize plants irradiated with UV-B (Casati and Walbot, 2003). UV-B radiation applied to suspensioncultured cells of carrot (Daucus carota) immediately induced the expression of the DcMYB1 gene followed by the expression of DcPAL1. DcMYB1 encodes an MYB transcription factor and is similar to the AtMYB15 gene that is induced by wounding and controls the expression of genes in the shikimate pathway (Maeda et al., 2005). In this study, the stimulation of the shikimate pathway was necessary to provide sufficient precursors for the production of cell wall and phenolic UV-B-absorbing compounds. In another study, increased production of UV-B-absorbing compounds (sinapate esters) was shown to coincide with enhanced expression of the C4H gene. Jin et al. (2000) characterized an Arabidopsis mutant for the R2R3 MYB gene AtMYB4. The mutant is tolerant to UV-B radiation, accumulates high transcript levels of C4H and contains high levels of sinapate ester. Analyses indicated that UV-B radiation repressed AtMYB4 expression in Arabidopsis wild-type plants associated with C4H gene induction and phenolic accumulation. In this case, the AtMYB4 acts as a repressor of the C4H gene (Jin et al., 2000). Another Arabidopsis lignin mutant is similarly compromised in its UV-B tolerance. The fah-1 mutant is unable to synthesize the F5H enzyme resulting in the absence of sinapic acid and its ester sinapoyl malate (Chapple et al., 1992). Although the mutant is still able to produce flavonoids, it is more sensitive to UV-B radiation than WT plants and UV-B exposure leads to an

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acceleration in the degradation of photosystem II D1, D2 proteins (BooijJames et al., 2000). UV-B radiation can also affect lignin gene expression in organs not directly exposed to this stress. In one recent study, it was shown that PAL, CCR, CAD, genes were upregulated in light-shielded organs of maize plants where only the canopy leaves were exposed to radiation. The authors suggest that this might be part of a general acclimation response to UV-B radiation (Casati et al., 2011). The phenylpropanoid and lignin pathways seem to be necessary for both acclimation and defence responses to UV-B light in both short- or long-term exposure situations. Carbon partitioning into and within these pathways also appears to play a central role in privileging one or the other response. H. LIGHT

Light is one of the most important environmental factors for plant development and the energy source for photosynthesis. The photosynthetically active radiation (400–700 nm) regulates a number of different physiological processes and metabolic pathways. Phenylpropanoid and lignin biosynthetic pathways are regulated by the photoperiod. In Arabidopsis, the genes involved in monolignol biosynthesis (PAL1, C4H1, CCR1 and CAD6) display a diurnal cycle of expression with two peaks—one of them just before dawn and the other one between 0.5 and 4 h after the beginning of the photoperiod (Rogers et al., 2005). Some of these genes and others of the monolignol pathway (C4H1, COMT, CCoAOMT1, CCR1 and CAD6) show a circadian oscillation in their transcript abundance. Similar results were obtained from developing xylem of Eucalyptus trees (Solomon et al., 2010). One peak of expression levels occurred in mid-afternoon and may be associated with producing phenolic compounds for oxidative stress protection, and the other one occurred just before dawn possibly for the reinforcement of new cell walls. The phenylpropanoid pathway is also controlled by light quality, as well as by light quantity. Roots of Arabidopsis plants lacking phytochrome B (PHYB) contained less monolignol glucosides than wild-type plants (Hemm et al., 2004). Such an observation could suggest that the photoreceptor for red light, PHYB, is important for phenylpropanoid pathway activity. The photoreceptor for blue-light cryptochrome (CRY2), acting in concert with PHYB, is also required for the accumulation of phenylpropanoids. Members of the PAL gene family are differentially regulated according to the duration of light treatment or wavelength and flux rate. The PAL3 gene was significantly upregulated in roots of Arabidopsis plants exposed for 1 h to red light but

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not in roots from seedlings grown in continuous white light. In contrast, PAL1 and PAL2 were upregulated in the hypocotyl and root of seedlings exposed to white light for 5 h (Molas et al., 2006). Changes in light conditions have been shown to be associated with an increase in lignin content in a number of different developmental processes. For example, 2 days of continuous light induced a reduction in the length of mungbean (Phaseolus radiatus) hypocotyls. This reduction was correlated to an increase in lignin content and linked to significant increases in peroxidase and laccase activities (Chen et al., 2002). Callus cultures of P. radiata grown with a 16 h photoperiod showed an enhanced rate of tracheary element differentiation as well as increased PAL and CAD enzyme activities and lignin content in comparison with those of dark-grown conditions (Mo¨ller et al., 2006). The observed alteration in leaf morphology in response to changing light conditions/gradient could be the consequence of modifications to the structural components of the leaf. The lignin content in leaves has been positively linked to irradiation (Niinemets, 1999) and the sun leaves of coffee plants have been shown to exhibit an increase of bulk modulus elasticity that could be explained by the higher content of lignin when compared with shade leaves. The decrease in tissue elasticity could also affect water uptake (Cavatte et al., 2011). The comparison of two Mediterranean Quercus species showed that leaves of Q. ilex had a lower specific leaf area and higher lignin content per leaf area than Q. suber leaves (Vaz et al., 2011). Such structural differences might contribute to reducing leaf transpiration under drought conditions. Light intensity has also been shown to exert an effect on the activity of enzymes involved in shikimate, phenylpropanoid and lignin pathways. Analyses of orchid (Phalaenopsis) plants exposed to different light intensities (60, 160 and 300 mmol m 2 s 1) after transfer from in vitro to soil plantation revealed that SKDH, PAL and CAD enzyme activities were induced in leaves (Ali et al., 2006). It is important that precursors of the phenylpropanoid pathway are available in sufficient (non-limiting) quantity to supply this pathway whatever the light intensity. Moreover, a positive correlation between PAL, CAD activity and lignin concentration was observed. The authors conclude that lignin synthesis probably induces defence against radiation stress. In certain situations, the amount of light energy exceeds the photosynthetic capacity of the plant and induces an oxidative stress. The induction of the phenylpropanoid pathway, as well as activation of different antioxidant systems can help to limit cell damage. In one study, the transfer of 10-day-old Arabidopsis seedlings developed under low light conditions to high light conditions for 3 h was associated with the induction of PAL, 4CL, CCoAOMT, CCR and CAD gene expression. Stimulation of phenylpropanoid

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gene expression was also correlated with increased lignin content and this increase was dependant on exposure duration (Kimura et al., 2003). I. ELEVATED CO2

The concentration of CO2 has increased from 280 mL L 1 before the industrial era to 380 mL L 1 at the present time and is predicted to double in 2100 according to IPCC scenarios (IPCC, 2007). The effects of elevated CO2 on plants have been extensively studied. In particular, ‘Free-Air CO2 Enrichment’ (FACE) systems involving long-term exposures under natural open-air conditions have provided us with plausible hypotheses of how plants will respond to higher CO2 concentrations. Elevated carbon dioxide constitutes a stress in that it causes profound reorganizations of plant physiology. In general, high CO2 reduces stomatal conductance but increases growth, biomass and yield (Ainsworth and Long, 2005). Stimulation of growth and biomass is often linked with higher carbon assimilation (Ainsworth and Rogers, 2007) although the response depends on the species considered. Trees were more responsive than herbaceous species whereas high CO2 had little effect on C4 species. Nitrogen (N) availability was shown to modulate the response with the CO2-induced stimulation of photosynthesis increasing under high N conditions. Elevated CO2 is predicted to increase the concentration of secondary or structural compounds according to the ‘source-sink balance hypothesis’ (Penuelas and Estiarte, 1998). Factors such as elevated CO2 or nutrient stress induce a relative increase in carbon availability and consequently lead to the accumulation of carbon-based secondary or structural compounds in source leaves. Although different results showed a general trend towards increasing levels of secondary compounds, their chemical nature varies depending upon the plant species or genotype (Bidart-Bouzat and Imeh-Nathaniel, 2008). Lignin content increased under elevated CO2 in tree leaves (Couteaux et al., 1999; Norby et al., 2001; Porteaus et al., 2009; Staudt et al., 2001) and in tobacco (Nicotiana tabacum; Matros et al., 2006), although other results, from long-term FACE studies, have shown no such effects (Finzi and Schlesinger, 2002; Liu et al., 2009; Oksanen et al., 2005; Parsons et al., 2008). However, the effect was shown to be highly dependent on N supply in F. sylvatica (Blaschke et al., 2002). In N-limited plants, leaf lignin content increased under elevated CO2 whereas in plants grown with high nutrient supply, the lignin content was unaffected or decreased by elevated CO2. Transcriptomic analyses of plants grown under elevated CO2 revealed a stimulation of the phenylpropanoid pathway. For example, phenylpropanoid pathway transcripts accumulated during the month of August in birch

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trees cultivated for 6 years under elevated CO2 concentrations. The authors suggested that this stimulation would give rise to phenolic compounds rather than lignins (Kontunen-Soppela et al., 2010). Arabidopsis growing under elevated CO2 also showed increased phenylpropanoid pathway gene expression. PAL1 and LAC4 were upregulated as were other cell wall-related genes. Metabolite profiling indicated that levels of most amino acids decreased under elevated CO2 except histidine, tryptophan and phenylalanine which is consistent with an increased flux towards secondary metabolism (Li et al., 2008). Soybean grown for 40 days under elevated CO2 also displayed increased expression in genes involved in secondary metabolism, particularly phenylpropanoid pathway. COMT and CCR were upregulated in leaves and the overall gene expression profile suggested an increased flux to secondary metabolism. Nevertheless, the response may differ according to the genotype as showed by Cseke et al. (2009). In this study, leaf transcription profiles, physiology and biochemistry were compared between CO2-responsive and unresponsive clones of P. tremuloides grown in long-term FACE experiments. The physiological responses of these clones were similar (photosynthesis, stomatal conductance and leaf area index) except for radial growth. Comparison of transcriptomic profiles from these two genotypes suggested that they used different partitioning strategies under elevated CO2. The CO2-responsive clone partitions carbon into pathways associated with active defence and stress responses, carbohydrate synthesis and subsequent growth, whereas the CO2unresponsive clone partitions carbon into pathways associated with passive defence (phenylpropanoid) and cell wall thickening. However, precise determinations of phenolic and lignin content in leaves from both genotypes would be necessary in order to confirm or infirm these hypotheses. Most studies concerning the effect of elevated CO2 on plants have been focused on source organs, that is, leaves. Modifications in leaf physiology and biochemistry could also impact on sink organs, for example, stems— especially in trees. Gene expression profiles of leaves and stems were compared in P. tremuloides grown for 3 years under elevated CO2 and high N supply (Druart et al., 2006). CO2-responsive genes were more abundant in stems compared to leaves suggesting a higher readjustment to elevated CO2 levels in stems. Genes involved in shikimate and flavanol synthesis were upregulated in leaves whereas genes related to phenylpropanoid and lignin synthesis (C3H, COMT and CAD) were stimulated in stems. Although it was suggested that lignification was enhanced by elevated CO2 in stems, no data were available on lignin content. The effect of elevated CO2 on wood lignin content has been assessed and it appears that responses depend on the species, the season and N supply. Lignin content was increased in the wood from coppices of both

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Populus  euramericana and Populus nigra in a FACE experiment (Luo and Polle, 2009; Luo et al., 2008) as well as in birch (Mattson et al., 2005). However, different responses were observed in other experiments. Lignin content was reduced in beech (Blaschke et al., 2002) whereas no modification was reported in birch, maple, or aspen clones in a FACE experiment (Kaakinen et al., 2004; Kostiainen et al., 2008). J. NITROGEN STRESS

Plants require mineral nutrients from the soil for their growth. Among these, nitrogen (N) is the most important inorganic nutrient in plants and it is generally considered to be the most limiting nutrient for tree growth (Finzi et al., 2007) and agricultural productivity (Tonitto et al., 2006). Nitrogen is a major constituent of proteins, nucleic acids, many cofactors and secondary metabolites (Maathuis, 2009). Therefore, strong variations in nutrient supply, both deficiency and excess, induce important changes in plant metabolism with a subsequent impact on biomass, yield and nutritional or wood quality (Amtmann and Armengaud, 2009). As with elevated CO2 levels, nitrogen deficiency alters the C/N balance. Plants growing on low N displayed a shift in shoot/root ratio to roots, a decrease in amino acids, proteins and chlorophyll and an increase in starch (Larcher, 2003). Nitrogen deficiency typically led to the accumulation of secondary metabolites including phenylpropanoids. Increased lignin content has been demonstrated in tobacco stems (Fritz et al., 2006) and in chamomile (Matricaria chamomilla) roots together with a stimulation of PAL activity (Kovacik et al., 2011). Further information on the interactions between nitrogen levels and phenylpropanoid metabolism was provided by a study on tobacco (Fritz et al., 2006). Wild-type tobacco was grown on low or high nitrate supply and compared with a nitrate reductasedeficient mutant growing on high nitrate supply. Low-N wild-type plants were highly lignified compared to high-N wild-type plants. The nitrate reductase-deficient mutant accumulated large amounts of nitrate and resembled high-N wild-type plants with respect to phenylpropanoid and lignin levels, but to low-N wild-type concerning amino acids. PAL, 4CL and HCT transcripts were induced in low-N wild-type plants but not in the nitrate reductase-deficient mutant. It was concluded that nitrogen deficiency leads to a marked shift of metabolism towards phenylpropanoids and that stimulation of phenylpropanoid metabolism is triggered by changes of nitrate levels, rather than downstream nitrogen metabolites. In Arabidopsis, nitrate deficiency led to a coordinated induction of phenylpropanoid and shikimate pathways (Scheible et al., 2004).

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Since nitrogen availability is considered to be a limiting factor in plant productivity, N fertilization has been used to improve harvest yields and biomass production. At the same time, human activities are increasing N levels in the environment, including forest ecosystems (Tilman et al., 2001). N fertilization or luxuriant supply induces dramatic changes in whole-plant architecture, biomass accumulation and plant metabolism (Cooke et al., 2005). The impact of nitrogen fertilization on lignification has been documented in forage grasses in relation to their nutritional value and contrasting responses have been observed. N fertilization had no effect on the forage lignin content in Trifolium subterraneum and rice (Nori et al., 2006; Sanz et al., 2005) but resulted in increased lignin content in tall fescue (Festuca arundinacea; Wolf and von Boberfeld, 2003). However, the developmental stage of the plant at the time of N application may also modulate the response. For instance, late-season N application to tall fescue maintained the forage in a physiologically younger stage and led to accumulation of lower amounts of lignin. The impact of N supply on lignification has also been studied in woody species. The effects depend on the species, developmental stage and mode of N application. N fertilization reduced the lignin content in roots but had no effect on needles and stems of 1-year-old longleaf pine seedlings (Entry et al., 1998). Wood lignin content was not affected in coppices of P. nigra fertilized with N (Luo et al., 2008) nor in young spruce by a 3-year N fertilization (Ha¨ttenschwiller et al., 1996) whereas, a long-term nutrient fertilization (N, P, K, Mg) led to increased lignin content in wood of 41-year-old Norway spruces (Kostiainen et al., 2004). A detailed analysis on poplar grown under controlled conditions showed that the lignin structure may be altered in the wood of trees under N fertilization (Pitre et al., 2007). Short-term (28-day) N fertilization induced modifications in wood anatomy, especially thicker cell walls. Lignin content in the newly formed wood decreased and its structure was similar to that of tension wood lignin, with a reduced S/G ratio as well as a reduced frequency of b-O-4 bonds. In a comparison between high-N wood and tension wood, transcriptomic analyses suggest that high nitrogen fertilization and tension wood formation induce largely distinct molecular pathways albeit with partial overlap (Pitre et al., 2010). Consistent with reduced lignification and S/G ratio, F5H and COMT were downregulated in high N wood and tension wood compared to low-N normal wood. Interestingly, in a phenotypic analysis of 396 genotypes from an interspecific pseudo-backcross pedigree of Populus, N fertilization significantly decreased lignin content in wood together with S/G ratio (Novaes et al., 2009). Quantitative trait loci corresponding to lignin content and S/G ratio were specific for one of the two nitrogen treatments demonstrating a significant nitrogen-dependent genetic control.

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III. LIGNIN ROLE IN RESPONSE TO ABIOTIC STRESSES Phenylpropanoid metabolism is clearly stimulated by abiotic stresses such as drought, salinity, ozone and heavy metals. However, experiments clearly demonstrating a subsequent increase in lignin synthesis are not so abundant. In fact, this latter parameter was not assessed in many studies. In other investigations, stress-induced phenylpropanoid metabolism was clearly associated with the synthesis of secondary phenolic compounds and not lignin. Nevertheless, certain studies have clearly demonstrated that lignin content increases in response to abiotic stresses. Such observations raise questions about the biological role(s) of lignin synthesized in response to abiotic stresses. Lignin could be involved in the first alarm phase during stress response (Fig. 2). Most abiotic stresses result in the production of ROS that can damage the cell when produced in excess but can also act as stress sensor and signal transduction molecules (Foyer and Noctor, 2005). Moreover, ROS generated in the apoplast may react with cell wall aromatic compounds such as lignin to generate signalling molecules. Interestingly, ozone has been shown to cause oxidative modification of the cell wall and the release of wallbound phenolics in tomato plants and cell wall extracts from tomato leaves. These molecules were proposed to act as signalling molecules to trigger defence reactions (Wiese and Pell, 2003). The hypothesis of ozone perception by the cell wall is consistent with the rapid increase of cytosolic-free calcium observed in A. thaliana exposed to ozone (Evans et al., 2005). However, the direct involvement of lignins in this signalling process still needs to be demonstrated. The most plausible role for lignins is probably in the defence mechanisms utilized during the acclimation phase of the stress response (Fig. 2). The rapid stimulation of the phenylpropanoid pathway in response to various stresses (Koch et al., 1998) is in favour of such a role, even though associated lignin synthesis still needs to be demonstrated in many cases. Further proof for a role in defence is that the lignin increase in response to abiotic stresses is related to stress intensity and damages (Betz et al., 2009a; Cabane´ et al., 2004; Frei et al., 2011). Finally, it is interesting to note that—when analysed—the structure of newly synthesized, stress-induced lignins are different from those of constitutive lignins (Betz et al., 2009a; Cabane´ et al., 2004; Finger-Teixeira et al., 2010; Frankenstein et al., 2006; Pitre et al., 2007). These findings could suggest that the newly synthesized lignins possess different properties from constitutive lignins that allow them to play a more efficient role in defence. If stress-induced lignins do indeed play a role in the acclimation phase defence mechanisms, then questions still remain as to their biological

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function(s). ROS produced by many abiotic stresses may be in excess and therefore likely to cause irreversible damages to the cell. Due to its scavenging properties, lignin may act as an antioxidant (Blokhina et al., 2003; Dizhbite et al., 2004). In ozone-exposed leaves of poplar, mesophyll cells with newly synthesized lignins were located near the necrotic lesion (Cabane´ et al., 2004). ROS (H2O2) were also shown to be accumulated near the necrotic spots in birch, tobacco and tomato (Pellinen et al., 2002; Wohlgemuth et al., 2002). Although the authors suggested that H2O2 might act as a signal molecule for triggering programmed cell death, it is also possible that lignin could contribute to maintaining the delicate ROS equilibrium between signalling and toxicity. Consistent with this hypothesis, ozone-induced H2O2 production was restricted to the apoplast in ozonetolerant poplar, whereas H2O2 accumulation occurred in the cell wall, the plasma membrane, cytosol and chloroplasts in sensitive plants (Oksanen et al., 2004). Lignins may contribute, together with other antioxidants, to limit ROS production to the apoplast. Lignins are also likely to play a role in acclimation phase defence mechanisms by strengthening the cell wall. Both drought and cold stress can lead to wilting and increased lignification would contribute to improved mechanical support of the plant aerial structure as well as water transport. Lignification could also help to reduce cell expansion and plant growth during this phase, thereby favouring reallocation of carbon resources to other defence mechanisms. Lignin may also waterproof plant cell walls and limit the apoplastic transport, thereby allowing a higher degree of ion selectivity as observed in the case of salt stress. In this case, lignification (and/or suberization) occurs in the root endodermis. Finally, as a major component of the cell wall, lignin may play a role in metabolic readjustment during the maintenance phase of the stress response (Fig. 2). For example, the late lignification response of poplar stems to ozone was typically an adjustment response (Richet et al., 2011). In this case, most of the leaf metabolism was devoted to the acclimation process, thereby reducing carbon availability to stem and provoking a readjustment of stem metabolism.

IV. REGULATION OF THE RESPONSE Because lignin biosynthesis is a metabolically costly process (Amthor, 2003) and its carbon investment is not reversible, the activation of this pathway in response to abiotic stresses must be tightly regulated. However, few data are available in the literature.

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The phenylpropanoid pathway is supplied with substrates derived from the shikimate pathway. Under stress, the phenylpropanoid pathway could be stimulated by rerouting of substrates to this pathway or by increasing carbon supply via the shikimate pathway. Observations showing a coordinated activation of the shikimate and phenylpropanoid pathways under abiotic stress support this idea (Betz et al., 2009a,b; Cabane´ et al., 2004; Scheible et al., 2004). The response of the phenylpropanoid pathway also appears to be regulated at the transcriptional level. As shown above a number of stresses induce significant differences in the accumulation of different phenylpropanoid gene transcript levels. Although transcription factors specifically involved in the regulation of the phenylpropanoid response to stress have not yet been functionally characterized, recent analyses have suggested that a battery of different transcription factors are involved in abiotic stress responses (Ahuja et al., 2010; Saibo et al., 2009; Shin, 2011). It also seems possible that transcription factors involved in developmental lignin biosynthesis may also be regulated by abiotic stresses. A recent review of lignin transcriptional regulation networks (Zhao and Dixon, 2011) highlighted the fact that the repressor MYB factor AtMYB4 responds to wounding and UV (Jin et al., 2000). Interestingly, another study revealed a significant upregulation of a NAC domain transcription factor in poplar leaves in response to elevated CO2 (Cseke et al., 2009). NAC domain transcription factors have been implicated as transcriptional switches that regulate secondary wall synthesis including lignin synthesis and may then control carbon deposition into secondary cell wall thickening in the poplar leaves (Zhao and Dixon, 2011). A better understanding of the regulation of stress lignin biosynthesis is also complicated by the fact that most enzymes of the phenylpropanoid pathway are encoded by multigene families. Only certain family members are involved in the synthesis of constitutive lignins whereas others may be specifically induced in response to both abiotic stresses (Molas et al., 2006; Soltani et al., 2006) and biotic stresses (Bi et al., 2011). These observations suggest that lignin synthesis in response to abiotic stresses is regulated differentially from constitutive lignin synthesis. Finally, lignin is only one of the major components of the secondary cell wall, together with cellulose and hemicellulose. Lignin biosynthesis must then be coordinated with cellulose and hemicellulose synthesis. Consistent with this, some transcription factors which regulate developmental lignin biosynthesis are also activators of the entire process of secondary wall formation (Zhao and Dixon, 2011). It is likely that lignification in response to abiotic stresses is also coordinated with the synthesis and deposition of other cell wall polymers.

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V. CONCLUDING REMARKS The results of many studies clearly show that abiotic stresses modulate both the phenylpropanoid and lignin pathways. However, conclusive proof of lignin synthesis is less often reported and in many cases is absent. Moreover, the tissue and cellular localization/characterization of lignified cells is almost inexistent even though such knowledge could greatly contribute to a better understanding of the role that lignin plays in tolerance to abiotic stresses. Examples of increased lignin synthesis were found for almost all abiotic stresses without being able to confirm whether it is a general feature or whether it is highly species dependent. Indeed, stress-induced lignification also appears to vary depending upon the organ/tissue examined. Although it is likely that stress-induced lignins play different role such as signalling, defence and adjustment during the stress response, direct evidence of these roles are still necessary. The regulation of the stress response should be investigated in order to assess whether it overlaps with the better characterized regulation pathways for constitutive lignin and whether different abiotic stresses share common regulation mechanisms. This knowledge is essential in a perspective of lignin manipulation for industrial purposes without compromising the plant’s ability to respond to stress.

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