AOBPreview originally published online on July 26, 2004
Annals of Botany 2004 94(3):345-351; doi:10.1093/aob/mch150
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Annals of Botany 94/3, © Annals of Botany Company 2004; all rights reserved
Effect of Drought Stress on Lipid Metabolism in the Leaves of Arabidopsis thaliana (Ecotype Columbia)
Laboratoire d'Ecophysiologie Moléculaire, UMR-IRD 137, Université Paris XII Val de Marne, 94010 Créteil Cedex, France
* For correspondence. E-mail phamthi{at}univ-paris12.fr
Received: 3 March 2004 Returned for revision: 19 April 2004 Accepted: 6 May 2004 Published electronically: 26 July 2004
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ABSTRACT |
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• Background and Aims Cell membranes are major targets of environmental stresses. Lipids are important membrane components, and changes in their composition may help to maintain membrane integrity and preserve cell compartmentation under water stress conditions. The aim of this work was to investigate the effects of water stress on membrane lipid composition and other aspects of lipid metabolism in the leaves of the model plant, Arabidopsis thaliana.
• Methods Arabidopsis thaliana (ecotype Columbia) plants were submitted to progressive drought stress by withholding irrigation. Studies were carried out in plants with hydration levels ranging from slight to very severe water deficit. Enzymatic activities hydrolysing MGDG, DGDG and PC were measured. Expression of several genes essential to lipid metabolism, such as genes coding for enzymes involved in lipid biosynthesis (MGDG synthase, DGDG synthase) and degradation (phospholipases D, lipoxygenase, patatin-like lipolytic-acylhydrolase), was studied.
• Key Results In response to drought, total leaf lipid contents decreased progressively. However, for leaf relative water content as low as 47·5 %, total fatty acids still represented 61 % of control contents. Lipid content of extremely dehydrated leaves rapidly increased after rehydration. The time-course of the decrease in leaf lipid contents correlated well with the increase in lipolytic activities of leaf extracts and with the expression of genes involved in lipid degradation. Despite a decrease in total lipid content, lipid class distribution remained relatively stable until the stress became very severe.
• Conclusions Arabidopsis leaf membranes appeared to be very resistant to water deficit, as shown by their capacity to maintain their polar lipid contents and the stability of their lipid composition under severe water loss conditions. Moreover, arabidopsis displayed several characteristics indicative of a so far unknown adaptation capacity to drought-stress at the cellular level, such as an increase in the DGDG : MGDG ratio and fatty acid unsaturation.
Key words: Drought, membrane lipids, MGDG, DGDG, phospholipase, galactolipase, gene expression, Arabidopsis thaliana
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INTRODUCTION |
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TOPFOOTNOTESABSTRACTINTRODUCTIONMaterials and methodsRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Plant tolerance to drought results from both morphological adaptation and responses at the biochemical and genetic levels (Levitt, 1980
). Among the various mechanisms developed by plants to resist drought, tolerance at the cellular level is essential since it allows tolerant plants to maintain cellular homeostasis. In contrast, sensitive plants suffer rapid irreversible cell damage essentially due to degradation of their membranes (Vieira da Silva et al., 1974). Membranes are main targets of degradative processes induced by drought and it has been shown that, under water stress, a decrease in membrane lipid content (Pham Thi et al., 1985; Monteiro de Paula et al., 1990) is correlated to an inhibition of lipid biosynthesis (Pham Thi et al., 1987; Monteiro de Paula et al., 1993) and a stimulation of lipolytic and peroxidative activities (Ferrari-Iliou et al., 1994; Sahsah et al., 1998; El Maarouf et al., 1999; Matos et al., 2001). Recently, the model plant Arabidopsis thaliana has been used to study changes in gene expression in response to water deficit, using large-scale screening methods, such as DNA microarrays (Seki et al., 2002). However, no data have been collected regarding variations in the lipid composition of arabidopsis leaf cell membranes, in response to drought stress. In most studies on molecular responses to water deficits, water stress treatments consisted in rapid dehydration of detached leaves or uprooted plants. The metabolic changes occurring over the course of a controlled water stress have rarely been studied, although it has been established that plants respond differently when subjected to a rapid or to a gradual drought treatment (Leone et al., 1994; El Maarouf et al., 1999). The study reported here was on the changes in polar lipids and in lipolytic activities in the leaves of arabidopsis plants at four hydration levels ranging from slight to extremely severe dehydration. In addition, the expression of several genes involved in lipid metabolism was investigated, taking advantage of the Arabidopsis Genome sequencing programme. Taken together, the results showed that the cell membranes of Arabidopsis thaliana (ecotype Columbia) leaves are remarkably tolerant of water deficit, as indicated by the stability of their leaf polar lipid content. The most striking changes in lipid composition were an increase in fatty acid unsaturation and variations in the balance between the two galactolipid classes [monogalactosyl-diacylglycerol (MGDG) and digalactosyl-diacylglycerol (DGDG)]. The potential impact of such lipid modifications in relation to chloroplast membrane properties, and Arabidopsis tolerance to drought was discussed.
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Materials and methods |
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Plant material and drought treatment
Plants of Arabidopsis thaliana (ecotype Columbia) were grown under controlled conditions: 22/20 °C, 10 h/14 h day/night, 250 µmol s–1 m–2 light energy supplied by OSRAM-HQIE lamps, 60 % relative air humidity. Seeds were sown directly in 1-L pots containing a mixture of sand and clay. Three seedlings, as morphologically identical as possible, were left to grow in each pot. They were watered daily with a nutritive solution (N : P : K 4 : 5 : 7, Bo 0·01 %, Cu 0·002 %, Fe 0·02 %, Mn 0·01 %, Mo 0·001 %, Zn 0·002 %).
Drought treatment was applied to 3-week-old plants, at vegetative stage, by withholding watering. The drought treatment lasted 14 d. Thereafter, plants were re-watered, and analysis performed 24 h later. Relative water content (RWC) of leaves was calculated as follows: 100(FW – DW)/(FW – SW), where FW = fresh weight, DW = dry weight (24 h of desiccation at 90 °C), SW = saturated weight (24 h water saturation at 8 °C in darkness). Leaves from plants at five hydration levels were harvested for analysis: control (C, RWC = 85·5 ± 2·4 %); slight water stress (S1, RWC = 82·0 ± 1·8 %) attained 5 d after water suspension; moderate stress (S2, RWC = 73·2 ± 1·6 %) 9 d after the beginning of drought treatment; severe stress (S3, RWC = 47·5 ± 1·5 %) 12 d after; very severe stress (S4, RWC = 17·0 ± 2·3 %) 14 d after. Rehydrated S4 plants attained leaf RWC of 77·6 ± 4·6 % 24 h later. In each pot, one of the three plants was used to measure relative water content, one was immediately frozen in liquid nitrogen for RNA extraction and enzymatic activities measurements, and the third one was used for lipid extraction. In all cases, samples consisted in fully expanded leaves. The senescing leaves, the immature leaves and the floral spikes were discarded.
Lipid and fatty acid analysis
Leaves were plunged for 2 min in boiling water to stop lipolytic activities, and lipophilic compounds were extracted in chloroform : methanol : water 1 : 1 : 1 (Bligh and Dyer, 1959). Lipid classes were analysed by thin layer chromatography (TLC) and fatty acids were quantified by gas liquid chromatography, as previously described (Monteiro de Paula et al., 1990). The lipid classes were separated on silica gel plates (G-60, Merck, VWR, Fontenay-sous-bois, France) with the solvent system developed by Lepage (1967). After visualization with primuline (0·01 % in 80 % acetone), lipid bands were scraped off, saponified and fatty acids methylated with boron trifluoride. Heptadecanoic acid (C17:0) was used as an internal standard for gas chromatography analysis. The DBI (double bond index) was calculated as follows: (1 x % monodienoic acids) + (2 x % dienoic acids) + (3 x % trienoic acids).
Measurement of lipolytic activities
Leaf material was fixed in liquid nitrogen and homogenized in ice-cold 0·1 M Tris–HCl pH 7·0 containing 10 mM DTT, 0·2 mM AEBSF, 0·5 mM benzamidin, 1 µM pepstatin A, 5 mM CaCl2, and 1 % Triton X-100 to solubilize the membrane-bound proteins. The homogenate was centrifuged at 30 000 g for 30 min, at 4 °C, and the supernatant was used for enzymatic activity measurements. [14C]MGDG and [14C]DGDG, used as substrates, were prepared as described previously (Sahsah et al., 1998). [14C]PC (1-palmitoyl-2[1-14C]linoleoyl PC, 2·04 GBq mmol–1) was purchased from Amersham Pharmacia Biotech, Orsay, France. Non-radioactive palmitoyl-linoleoyl PC (Sigma, St Quentin Fallavier, France) was added to obtain a 100 µM solution used for enzymatic assays. Measurements of lipolytic activities were as described by Sahsah et al. (1998). Briefly, lipid substrates were sonicated in the presence of Triton X-100 to obtain mixed micelles, reactions were performed at 25 °C, for 20 min with PC and 1 h with MGDG and DGDG. Lipids of the reaction mixtures were extracted and separated by TLC on silicagel plates (G-60, Merck). The lipid bands were scraped off, and their radioactivity was counted. Enzymatic degradation of the two galactolipids was measured as the radioactivity of released fatty acids. The degradation of PC led to the formation of PA, phosphatidyl-methanol and free fatty acids. PA resulted from hydrolytic activity of PLD, phosphatidyl-methanol from its transphosphatidylation activity. Free fatty acids would come from activities of phospholipases A and/or non-specific lipolytic acylhydrolase (LAH) activities of the leaf extracts. Enzymatic degradation of PC was measured as the radioactivity of the degraded substrate.
Proteins were determined following the method of Bradford (1976) using the Bio-Rad protein assay reagent and BSA as a standard.
RNA extraction and RT-PCR
Leaf total RNA was extracted using a commercial kit (Qiagen, total RNA extraction kit), following the recommendations of the manufacturer. One hundred nanograms total RNA was used in RT-PCR reactions (one-step RT-PCR kit, Qiagen, Courtaboeuf, France) with primers specific to the following genes: PLD
(Genbank accession U36381), PLD
(AF32228), patatin-like acyl hydrolase (AC0014504), chloroplastic lipoxygenase LOX-2 (L23968), MGDG synthase MGD1 (AB047399), DGDG synthase DGD1 (AAF02140). The RT-PCR conditions were adapted to each gene. S19, a gene coding for a ribosomal protein, with near constitutive expression during the drought treatment was used as control in the PCR reactions.
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RESULTS |
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Relative water content of arabidopsis leaves during the drought treatment
Following water withholding, RWC of arabidopsis leaves remained relatively stable for 5 d (Fig. 1). Afterwards, it slowly declined from 82·0 ± 1·8 % to 67·5 ± 1·5 % and abruptly reached values corresponding to a very severe water deficit at day 14 (RWC = 17·0 ± 2·3 %). The plants were then rehydrated, and the RWC of leaves returned to nearly normal values 24 h after. At day 15, well-watered plants displayed RWC values equivalent to those measured at day 1.
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Lipid and fatty acid composition of arabidopsis leaves
Because of the duration of the drought treatment, well-watered plants were compared at the beginning (C, day 1) and the end of the experiment (C15, day 15). As shown in Fig. 2, leaves contained fewer lipids at day 15 than at day 1, on a dry weight basis. However, the distribution of lipid classes and their fatty acid composition were not significantly affected by plant age (Table 1). Therefore, comparisons could be made between drought-stressed plants and control at day 1.
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When expressed on a dry weight basis (Fig. 2), total leaf fatty acid content of Arabidopsis thaliana (ecotype Columbia) decreased progressively from moderate (S2, RWC = 78·2 %) to severe (S3, RWC = 47·5 %) drought stress. In S3 plants, leaf fatty acid content was 61 % of the control. Extremely dehydrated plants (S4, RWC = 17 %) had lost 77·5 % of their leaf lipid content. Twenty-four hours after rehydration, leaf fatty acid content amounted to 76 % of the control.
As indicated by lipid class distribution (Fig. 3), the proportions of PC and PG, the main phospholipid classes of leaf cell membranes remained unchanged in S1, S2 and S3 plants. In S4 plants, there was only a slight decrease in PG percentage. The most important changes concerned the two galactolipids. MGDG percentage decreased from 34·9 % (control plants, C) to 19 % (S4 plants). On the other hand, DGDG percentages increased, from 16·20 % (C) to 20·7 % (S4). This resulted in an increase in the DGDG : MGDG ratio from 0·46 (C) to 1·09 (S4). In rehydrated leaves, the main polar lipid distribution did not change compared with S4 leaves; however, an increase in the percentage of neutral lipids and free fatty acids, together with the previously shown increase in total lipids (Fig. 2), indicated a recovery in lipid biosynthetic activities.
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The major change in the fatty acid composition of polar lipid classes (Table 2) was a 13 % increase in DGDG 18:3 in S3 plants compared with the control. To a lesser extent, a similar trend was observed for 18:3 in PC. This increase in lipid desaturation raised the DBI. In S4 plants, however, the percentage of triunsaturated fatty acids (16:3 and 18:3) declined in all lipid classes.
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Lipolytic activities of leaf extracts
In vitro enzymatic degradation of MGDG, DGDG and PC remained stable until day 7 after withholding water (Fig. 4). On day 7 (MGDG and PC), and on day 10 (DGDG), degradation increased and was maximum in S3 leaves (day 12) for the two galactolipids. In severely stressed plants (S4, day 14), galactolipase activity slowed down, whereas enzymatic degradation of PC was still high.
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Gene expression
Using RT-PCR, expression of the following genes related to lipid metabolism was investigated during drought-stress: patatin-like gene (AC0014504) coding for a lipolytic acylhydrolase (Matos et al., 2001
); phospholipase D alpha (PLD, U36381) and phospholipase D delta (PLD, AF32228), involved in phospholipid degradation in response to drought (El Maarouf et al., 1999; Katagiri et al., 2001; Sang et al., 2001); chloroplastic lipoxygenase (LOX-2, L23968); MGDG synthase (MGD1, AB047399) and DGDG synthase (DGD1, AAF02140). In response to drought stress (Fig. 5), transcripts corresponding to the two PLD isoforms and to the DGDG synthase accumulated progressively. On the other hand, water stress inhibited expression of MGDG synthase gene, particularly in S3 and S4 plants. Lipoxygenase gene expression was stimulated at slight and moderate water deficits and decreased sharply at more severe stresses. Patatin-like transcript levels were highest at the onset of stress (S1) and at very severe stress (S4) (Fig. 5).
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DISCUSSION |
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TOPFOOTNOTESABSTRACTINTRODUCTIONMaterials and methodsRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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To study stress-induced leaf lipid modifications in Arabidopsis thaliana ecotype Columbia, whole plants were subjected to progressive drought characterized by RWC % values ranging from 82·0 % (slight stress, S1) to 17·4 % (extremely severe stress, S4). In response to drought, total leaf lipid contents decreased progressively (Fig. 2). Beyond S2 conditions, lipid degradation processes prevailed over biosynthesis, as indicated by the general reduction in polar lipid content. This suggested that cell homeostasis could not be maintained for RWC values lower than 73·2 %. However, for RWC% as low as 47·5 % (S3), total fatty acids still represented 61 % of control contents, and 24 h after rewatering, lipid content in leaves rapidly increased, showing the capacity of arabidopsis plants to withstand and recover from drought stress. The time-course of the decrease in leaf lipid contents correlated well with the increase in lipolytic activities of leaf extracts (Fig. 4). Enzymatic measurements indicated that the main products of galactolipids and PC hydrolysis were FFA and PA (see Materials and Methods), compounds that are toxic for the cell. However, they did not accumulate in the leaves of drought-stressed arabidopsis plants (results not shown), suggesting the existence of efficient detoxification processes in this plant species.
Until RWC reached values as low as 47·5 %, lipid class distribution remained relatively stable despite a decrease in total lipid content (Fig. 3). At more severe water deficits, changes in membrane lipid composition may lead to conformational changes in membrane proteins (Navari-Izzo et al., 2000) and to alterations of the cell ultrastructure (Vieira da Silva et al., 1974).
Among the polar lipid classes, MGDG was mostly sensitive to degradation. Similar results were obtained from lipid analysis in the leaves of water-stressed cotton (Ferrari-Iliou et al., 1984; Pham Thi et al., 1985), coconut tree (Repellin et al., 1997), the resurrection plants Ramonda serbica and Ramonda nathaliae (Stevanovic et al., 1992), rape (Benhassaine-Kesri et al., 2002) and cowpea plants (Monteiro de Paula et al., 1993). In the latter, enhanced galactolipase activity was also detected (El Hafid et al., 1989; Sahsah et al., 1998). To determine the origin of MGDG disappearance in arabidopsis, expression of genes involved in MGDG metabolism was analysed in water-stressed plants. Our results (Fig. 5) showed that expresssion of a patatin-like gene was stimulated in response to water deficit, particularly in S4 plants. The corresponding protein was shown recently to have galactolipase activity (Matos et al., 2001). Additionally, our RT-PCR results indicated that the expression of AtMGD1, the gene responsible for 75 % of the bulk MGDG synthesis (Jarvis et al., 2000), decreased under drought stress. An increase in the degradation and a decrease in the biosynthesis therefore led to the observed decrease in MGDG content of arabidopsis leaves. It could be noted that patatin gene expression was stimulated in response to slight drought stress (S1). This is also the case for the chloroplastic lipoxygenase (LOX-2) (Fig. 5). Enhanced lipolytic activity most probably leads to losses in cell compartmentation and membrane protein function. However, it has been shown recently that lipid molecules produced by lipid degrading enzymes in response to environmental stresses can act as secondary messengers of stress-response signal transduction pathways (Munnik et al., 1998), such as the phytooxylipin pathway (Blée, 2002; Howe and Schilmiller, 2002). In light of these results, early stimulation of patatin and lipoxygenase gene expression in S1 plants could correspond to an adaptive response to drought-stress.
While MGDG content decreased regularly over the course of the drought treatment, DGDG content increased in S1–S3 plants, leading to an increase in the DGDG : MGDG ratio. Furthermore, expression of AtDGD1, a DGDG synthase gene was stimulated in response to drought while that of MGDG synthase decreased (Fig. 5). Härtel et al. (2000, 2001) showed that under phosphate-limiting conditions, DGDG accumulated in extraplastidial membranes of arabidopsis plants, where it replaced the phospholipids missing under such growth conditions. Under conditions of soil water deficits, since absorption by the roots stops, phosphate also becomes limiting. This leads to a decrease in phospholipid biosynthesis (Monteiro de Paula et al., 1993), in addition to an overall lipid degradation. As a result, DGDG could compensate for the lack of phospholipids in extraplastidial membranes.
In pure lipid–water mixtures, MGDG molecules tend to form hexagonal phase structures (HexII) due to their conical shape, whereas cylindrical DGDG forms lamellar phases (Williams and Quinn, 1987; Web and Green, 1991). The proportion between MGDG and DGDG is therefore very important for the stability of the chloroplast membrane (Dörmann and Benning, 2002). Under stress conditions, an increase in the DGDG : MGDG ratio could help to maintain the membrane in a bilayer conformation necessary for the biological functions of chloroplastic membranes, such as protein transport (Bruce, 1998; Chen and Li, 1998) and photosystem activities (Dörmann and Benning, 2002).
In S1–S3 plants, a slight increase in 18:3 percentages was observed in DGDG and in PC to a lesser extent. Such an increase could result from the activation of desaturase activities as well as from a better protection against lipid peroxidation. Previous comparative studies between plants of the same species with different capacities to tolerate water deficit showed that the unsaturation level of polar lipids decreased in sensitive plants, whereas it remained unchanged or even increased in resistant cultivars under drought stress conditions (Monteiro de Paula et al., 1990; Repellin et al., 1997). Although no clear relationship between the unsaturation level of membrane lipids and drought tolerance has yet been established, our results obtained on cowpea plants (Monteiro de Paula et al., 1990), coconut tree (Repellin et al., 1997), and in the present study, on arabidopsis, allow us to suggest a relationship between the capacity of a plant to maintain (or increase) its polyunsaturated fatty acids contents and its resistance to drought stress. A similar relationship has already been established in the case of low temperature (Kodama et al., 1994; Moon et al., 1995; Routaboul et al., 2000) and salinity (Allakhverdiev et al., 2001) stresses.
Together, our results show that Arabidopsis thaliana (ecotype Columbia) plants display a strong capacity to tolerate water deficits at the cell level. Indications for this are: (a) leaf membrane lipid composition and expression of several genes important in lipid metabolism remained relatively stable until RWC as low as 67·5 % (between S2 and S3); (b) membrane repair processes after rehydration are extremely efficient; (c) DGDG : MGDG ratio and fatty acid unsaturation levels increase, suggesting a so far unknown capacity for adaptation to drought stress.
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ACKNOWLEDGEMENTS |
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The authors thank Dr Anne Repellin for language correction and constructive comments on this manuscript.
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FOOTNOTES |
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Present address: Laboratoire de Physiologie Cellulaire et Moléculaire des Plantes, UMR 7632 CNRS, tour 53, Université Pierre et Marie Curie, 4 Place Jussieu, 75252 Paris Cedex 05, France 
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LITERATURE CITED |
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