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First published online March 31, 2006; 10.1104/pp.106.076786 Plant Physiology 141:135-146 (2006) © 2006 American Society of Plant Biologists Functional Characterization of Ice Plant SKD1, an AAA-Type ATPase Associated with the Endoplasmic Reticulum-Golgi Network, and Its Role in Adaptation to Salt Stress1,[W]Department of Life Sciences, National Chung Hsing University, Taichung, Taiwan 40227 (Y.J., C.P.C., H.E.Y.); and Institute of Plant and Microbial Biology, Academia Sinica, Nankang, Taipei, Taiwan 11529 (G.Y.J.)
A salt-induced gene mcSKD1 (suppressor of K+ transport growth defect) able to facilitate K+ uptake has previously been identified from the halophyte ice plant (Mesembryanthemum crystallinum). The sequence of mcSKD1 is homologous to vacuolar protein sorting 4, an ATPase associated with a variety of cellular activities-type ATPase that participates in the sorting of vacuolar proteins into multivesicular bodies in yeast (Saccharomyces cerevisiae). Recombinant mcSKD1 exhibited ATP hydrolytic activities in vitro with a half-maximal rate at an ATP concentration of 1.25 mM. Point mutations on active site residues abolished its ATPase activity. ADP is both a product and a strong inhibitor of the reaction. ADP-binding form of mcSDK1 greatly reduced its catalytic activity. The mcSKD1 protein accumulated ubiquitously in both vegetative and reproductive parts of plants. Highest accumulation was observed in cells actively engaging in the secretory processes, such as bladder cells of leaf epidermis. Membrane fractionation and double-labeling immunofluorescence showed the predominant localization of mcSKD1 in the endoplasmic reticulum-Golgi network. Immunoelectron microscopy identified the formation of mcSKD1 proteins into small aggregates in the cytosol and associated with membrane continuum within the endomembrane compartments. These results indicated that this ATPase participates in the endoplasmic reticulum-Golgi mediated protein sorting machinery for both housekeeping function and compartmentalization of excess Na+ under high salinity.
Ice plant (Mesembryanthemum crystallinum) is an inducible halophyte and Crassulacean acid metabolism (CAM) plant. The induction of CAM at a late juvenile stage is an adaptation to drought and salinity (for review, see Cushman, 2001  ). The day/night fluctuation of malate content is the main characteristic of the CAM cycle. Malate is synthesized by nocturnal CO2 fixation and is transported into the vacuole via malate transporters (Hafke et al., 2003). In addition to CAM induction, ice plants are able to sequester excess Na+ into the vacuole. Epidermal bladder cells (BCs) are the major sites to compartmentalize salt within their huge central vacuoles. This process is initiated by high salinity conditions and enabled by a salt-induced Na+/H+ antiporter located in the tonoplast (Barkla et al., 2002). The energy required for this active transport is mainly provided by vacuolar (V)-type ATPase and the expression of certain salt-induced V-ATPase subunits has been reported (Golldack and Dietz, 2001; Kluge et al., 2003). Under salt stress, an increase in the diameter of tonoplast-derived vesicles resulted largely from an increase in V-type ATPase (Rockel et al., 1994). Recently, Epimashko et al. (2004) discovered two types of functionally distinct vacuoles in salt-treated ice plant mesophyll cells: salt storing and malate cycling. The development of functionally distinct vacuoles is achieved presumably by precise and efficient protein sorting machinery, i.e. targeting Na+/H+ antiporter to the Na+ storage vacuole and malate transporter to the malate storage vacuole. The mechanism of vacuolar protein trafficking in ice plants remains largely unknown.
SNAREs, a complex vesicle-mediated transport system, are responsible for the delivery of proteins and lipids to different subcellular organelles. Fusion between vesicles and target membranes is driven by protein-protein interactions between vesicle (v)-SNARE and target (t)-SNARE (for review, see Pratelli et al., 2004
SKD (suppressor of K+ transport growth defect) were first identified by screening mouse cDNA library for the heterologous suppression of the K+-uptake-defect yeast (Saccharomyces cerevisiae) phenotype (Périer et al., 1994
A salt-induced cDNA mcSKD1 was isolated from salt-treated ice plants by suppression subtractive hybridization (Yen et al., 2000 In this report, we first characterized the enzymatic properties of mcSKD1 and then analyzed the accumulation of mcSKD1 at cellular and subcellular levels. This report demonstrated ATPase activity and possible regulation in this group of AAA proteins in plants. Evidence for tissue-specific accumulation and subcellular location of SKD1 is also provided in this study.
Catalytic Properties of mcSKD1 To identify the possible ATPase activity of mcSKD1, the open reading frame of mcSKD1 fused with six His at the C terminus, was cloned into a pET vector, was overexpressed in Escherichia coli, and a 51-kD protein was purified by affinity chromatography (Fig. 1A ). The N-terminal sequence of the first 10 amino acids exactly matched the N-terminal sequence of mcSKD1. The procedures for mcSKD1 purification were described in "Materials and Methods" and the result was shown in Supplemental Figure 1.
The activity of ATPase was measured by incubation of [  -32P]ATP with crude protein extract isolated from isopropyl- -D-thiogalactopyranoside (IPTG)-induced E. coli cells or affinity-purified mcSKD1 and then separation by thin-layer chromatography (TLC; Fig. 1B). A small amount of ATP was autolyzed into ADP, AMP, and free phosphate during 20 min of incubation at 30°C (lane 1). When crude extract was added to the reaction mixture, a large portion of ATP was converted into ADP and AMP (lane 2). When purified mcSKD1 was used, ATP was essentially converted into ADP and did not further convert to AMP (lane 3). Addition of 5 mM N-ethylmaleimide (NEM), a known NSF inhibitor, did not significantly inhibit the enzymatic activity of purified mcSKD1 (lane 4). The failure to observe inhibition by NEM may be due to the presence of trace amounts of impurity with high ATPase activity in the assay. Therefore, two recombinant proteins with single change in active site residue Lys 177 to Ala (Walker A motif) and Glu 231 to Gln (Walker B motif) were used as negative controls. Residue 177 is critical for ATP binding, while residue 231 is essential for ATP hydrolysis. After going through the same purification steps (Fig. 1A, lanes 4 and 5), the ATPase activities were measured in these two mutants along with the wild-type protein. As shown in Figure 1C, the ATPase activity was reduced 70% in K177A mutant, and the mutation on E231 almost abolished mcSKD1's ATPase activity. The result showed that the activity of ATP hydrolysis detected in our assay system was mostly contributed by mcSKD1. The enzyme kinetics of affinity-purified mcSKD1 was measured in the range of 0 to 4 mM ATP as substrate. ADP spots of each treatment that appeared on the phosphorimage plate were directly quantified, and the rate of ATP hydrolysis was calculated (Fig. 1D). ATPase activity increased as the substrate concentration increased and reached maximum activity at 3.0 mM ATP. At the half-maximal rate, the ATP concentration was about 1.25 mM. Furthermore, when the ATP concentration exceeded 3.0 mM, ATPase activity rapidly dropped. The inhibition of ATPase activity may be due to the presence of a high level of substrate or the gradual accumulation of product in the reaction mixture.
To further characterize the enzymatic properties of mcSKD1, a competition assay was performed using different nucleotides or deoxynucleotides as competitors (Fig. 2A
). In addition to 0.02 µM [
We further investigated the hypothesis that ADP binding causes inhibition of ATPase activity (Fig. 2B). The enzyme assay was performed at either noninhibitory (1.8 mM ATP) or inhibitory (4.0 mM ATP) conditions. After 20 min incubation, the reaction was stopped and the reaction mixture was divided into two parts. One part was loaded directly on the TLC plate (control), while the other half was filtrated through a Sephadex G50 column before loading onto the TLC plate (centrifugal gel filtration [CGF]). The purpose of CGF was to remove unbounded free nucleotides from the proteins. Results showed that the Sephadex G50 column effectively removed free nucleotides but showed no change to the ATP/ADP ratio in treatments with different ATP concentrations (compare lane 5 versus lane 7) as well as under noninhibitory condition (compare lane 2 versus lane 6). Under inhibitory condition, 20% more ADP was detected following CGF (compare lane 4 versus lane 8). This is because ADP was bound to mcSKD1 and cofractionated through the Sephadex G50 column under inhibitory conditions. The result clearly indicated that this ATPase is subjected to product inhibition. The significance of this finding will be discussed.
To assess mcSKD1's function, antiserum raised against purified mcSKD1 was used to identify the localization of this protein in ice plants. Immunoblot analysis showed this antiserum reacted specifically with a 60-kD protein in both vegetative and reproductive organs of ice plants (Fig. 3B ). The results showed mcSDK1 ubiquitously accumulated in this halophyte. Salt stress treatment slightly increased its accumulation in the leaves (Fig. 3B). As shown in Figure 1A, the open reading frame of mcSKD1 encodes a protein with molecular mass of 51 kD. This result suggests that plant SKD1 protein may have some posttranslational modification.
Tissue-specific and salt-induced accumulation of mcSKD1 was examined using immunostaining. Paraffin sections were first reacted with anti-mcSKD1 antibodies and then detected by fluorescein-isothiocyanate (FITC)-conjugated secondary antibodies under fluorescence microscope (Fig. 4 ). A yellowish fluorescence was detected in all the tissues examined when preimmune antiserum were used as primary antibodies (Fig. 4, A, C, E, and G). This nonspecific autofluorescence was probably caused by phenolic compounds present in the cell wall of mesophyll cells. In salt-treated leaves, mcSKD1 highly accumulated in the epidermal BCs as shown by the emission of green fluorescence (Fig. 4B). Some green fluorescence also emitted from the mesophyll cells but was overlapped with the yellow fluorescence. BCs are major storage sites for excess Na+ in this halophyte, and large numbers of cisternae of endoplasmic reticulum (ER) were presented in these cells (Kramer, 1979 ). The accumulation of mcSKD1 was also found in the phloem and cortex of salt-treated roots (Fig. 4D), outer layer of pollen sacs (Fig. 4F), and seed coats (Fig. 4H). All these cells are actively engaged in the secretory processes, either exclusion out of cells, or compartmentalization into the vacuole.
Although the hydropathy plot showed mcSKD1 to have no apparent transmembrane domains (Jou et al., 2004 ), the mcSKD1 yeast homolog VPS4 associated with the endosomal membrane through protein-protein interactions. Cell fractionation experiment showed mcSKD1 was mainly associated with microsomes but not with soluble fractions (Fig. 5A
). Microsomes were further fractionated by Suc gradient. Preliminary fractionation experiment using a 20% to 45% continuous Suc gradient showed mcSKD1 appeared in the very top of the gradient (data not shown). Therefore, a broad range of 8% to 45% gradient was used to separate the relatively light vesicles. Western-blot analysis showed mcSKD1 distributed in the fraction 1 through 7 (8%–34% Suc), mainly in the top four fractions (less than 20% Suc). The pattern of mcSKD1 distribution matched with microsomal epoxide hydrolase (mEH), an ER marker, and AtTLG2a, a trans-Golgi network (TGN) marker (Fig. 5B). A less amount of mcSKD1 was detected in microsomes derived from the tonoplast and PVC distributed in denser fractions (34%–45% Suc) as indicated by the tonoplast marker V-type ATPase and PVC markers vacuolar sorting receptor (VSR) and BP-80. The results showed that mcSKD1 is mainly present in microsomes derived from the ER-Golgi network.
The density of tonoplast fraction shown in these cultured cells (34%) was heavier than the density observed in the mesophyll cells (22%; Barkla et al., 1995 ). This difference was mainly due to the changes of tonoplast density during vacuole development. According to Herman et al. (1994), the density of tonoplast in mature root cells was enriched in 20% to 22% Suc, while the density of tonoplast was distributed in the heavier fractions in undifferentiated root tip cells, which lack large central vacuoles. The localization of mcSKD1 relative to mEH, AtTLG2a, BP-80, VSR, and V-type ATPase in isolated cultured ice plant cells was further examined by double-labeling immunofluorescence (Fig. 6 ). The magenta fluorescence indicated the distribution of mcSKD1 scattering over the cytoplasm with some concentrated spots (section I). High degrees of colocalization of mcSKD1 with the ER marker mEH and the TGN marker AtTLG2a were observed with 81% and 74%, respectively (section II; green fluorescence). Although the degrees of colocalization were high, there were some distinct spots that appeared only for mcSKD1, as indicated by the magenta arrowheads (section III; merged image). About 40% of colocalization was observed when double labeling with tonoplast marker V-type ATPase. The merged image shows punctuate concentrated magenta spots located next to the tonoplast marker. An even lesser degree of colocalization was observed when double labeling with PVC markers BP-80 or VSR. However, we constantly observed some overlapping area as indicated by the white arrowheads (section III). The result obtained by double labeling was consistent with the membrane fractionation study, whereby the majorities of mcSKD1 shared the same location with mEH and AtTLG2a and suggest that mcSKD1 is predominantly gathered in specific sites of the ER-Golgi network but also occasionally associates with the tonoplast.
To determine the punctuate pattern of mcSKD1, the subcellular localization of mcSKD1 was performed using immunogold labeling (Fig. 7 ). Ultrathin sections prepared from salt-treated leaves (Fig. 7, A and B), roots (C and D), and cultured cells (E and F) were reacted with preimmune serum or anti-SKD1 antiserum and detected by gold-conjugated anti-rabbit antibodies. In all the tissues examined, mcSKD1 was located in the cytosol in both free form and formation of small aggregates. Under higher magnification, the aggregation of mcSKD1 was found to associate with the cisternal-like membranous structure resembling the ER-Golgi network (Fig. 7B, inset).
Efficient Protein Trafficking Is a Salt-Tolerant Determinant
The possible involvement of intracellular vesicle trafficking in maintaining ion homeostasis includes: (1) the delivery of tonoplastic- or plasma membrane-bound transporters, channels, and ATP-driving pumps that directly participate in the ion transport process (Zhu, 2001
There is an increasing amount of evidence for the importance of the machinery of intracellular vesicle trafficking in adaptation to salt stress. For vesicle targeting and docking, small GTPases of the Rab family have been known to be important (for review, see Zerial and McBride, 2001
The vesicle fusion process requires the specific pairing of SNAREs (for review, see Pratelli et al., 2004
Based on the yeast complementation result, the role of mcSKD1 was proposed as a facilitator of K+ uptake and promoter of Na+ sequestering to maintain a high cytoplasmic K+/Na+ ratio (Jou et al., 2004
A critical point of mcSKD1's function is to understand its role in the trafficking route. Membrane fractionation experiments showed mcSKD1 occurred mainly in the light-density fractions that cofractionated with smooth ER (SER) and TGN markers (Fig. 5). The distribution of mcSKD1 was confirmed by double-labeling immunofluorescence (Fig. 6). Another line of evidence came from Figure 4 where mcSKD1 was highly accumulated in BCs. These specialized cells have been known to contain very high amounts of ER in the cytoplasm (Kramer, 1979
The colocalization with the SER marker shed light on the possible involvement of mcSKD1 in the first sorting event occurring in the ER. Most vesicles that leave the ER are trafficked to the Golgi complex, yet there are additional transport pathways. Some vesicles, such as precursor-accumulating vesicles, bud from the SER bypassing the Golgi on their way to vacuoles (Hara-Nishimura et al., 1998
In yeast, the SKD1 homolog VPS4 mediates protein sorting from endosome to the multivesicular body (MVB; Babst et al., 2002
Evidence provided by this study suggests that mcSKD1 is localized in the cytoplasmic endomembrane system, primarily in the ER-Golgi network. Although the majority of mcSKD1 did not overlap with V-ATPase in the membrane cofractionation experiments (Fig. 5), it showed 40% overlapping localization with V-ATPase by confocal fluorescent microscopy (Fig. 6). V-ATPase is a marker for the tonoplast, but it is also associated with the ER and PVC. The association of V-ATPase with the endomembrane system is most prominent in the undifferentiated cells (Herman et al., 1994
The molecular mechanism of plant SKD1 in intracellular vesicular trafficking remains unsolved. In yeast, the involvement of VPS4 in sorting endosomal proteins has been studied in depth (Babst et al., 2002
Babst et al. (1998)
ADP is a strong competitor for ATP and it inhibits the activity of ATP hydrolysis by binding to mcSKD1 (Fig. 2). The physiological role of ADP-bound inhibition remains unclear. The release of ADP may be a rate-limiting step, and therefore, a regulatory step for mcSKD1 ATP turnover. Recall the nucleotide exchange between GTP- and GDP-bound states of Rab GTPase (Zhu et al., 2004 In summary, findings of this study demonstrate the kinetic properties and cellular localization of plant SKD1 protein. Besides the ability to hydrolyze ATP, plant SKD1 has diverged from that of its yeast equivalent in many aspects. The plant SKD1 appears to associate mainly with the ER-Golgi network, and ATPase activity is regulated by ADP binding. SKD1 protein accumulated mostly in cells actively engaging in the secretory pathway in halophyte ice plants. Exposure to high salinity environments requires the efficient and coordinated operation of all stages of intracellular vesicular trafficking in maintaining ion homeostasis and in salt stress signaling.
Plant Growth Conditions and Callus Culture Ice plants (Mesembryanthemum crystallinum) were grown in mixed soil (humus to vermiculite to sand, 3:1:1, v/v) in a growth chamber with a 16-h-light (800 µmol quanta m–2 s–1)/8-h-dark period at 30°C/18°C. For salt treatment, 6-week-old plants were treated with 400 mM NaCl for 7 d. Samples from salt-treated plants and 10-week-old nonstressed flowers and developing seeds were collected for immunoblotting and immunolocalization.
Callus of ice plant initiated from hypocotyls of seedlings was maintained in a modified Linsmaier-Bedner and Skoog solid medium as described by Treichel (1986)
The bacterial strains used in this work were Escherichia coli DH5
To construct the overexpression system of mcSKD1, an mcSKD1 coding sequence was PCR amplified using plasmid pGEM-MCSKD1 as a template and oligonucleotide primers 5'-CGGCCGCGGGAATTCGATTCATATGTACAG-3' (forward) and 5'-GGATCCATCGAAATTATGCAGCCTT-3' (reverse) tailed with NdeI and BamHI restriction sites, respectively. The NdeI-BamHI fragment was inserted into the corresponding sites of pET32a to give pMCSKD32. The pMCSKD32 was used as a template for generation of point mutations K177A and E231Q using a site-directed mutagenesis kit (Stratagene). The sequences of all constructs were confirmed by DNA sequencing.
An overnight culture of BL21 (DE3) cells harboring pMCSKD32 was diluted 100-fold in 1 L Luria-Bertani medium containing 100 mg L–1 ampicillin and incubated at 37°C with shaking. When A600 of the culture reached 0.6, IPTG was added to a final concentration of 0.5 mM. After 2 h, the induced cells were harvested by centrifugation and used for purification of the mcSKD1 protein. All purification steps were carried out at 4°C. IPTG-induced cells were resuspended in 50 mL of equilibration/wash buffer (50 mM sodium phosphate, pH 7.0, 500 mM NaCl, and 5% glycerol) containing 1 mM phenylmethyl sulfonyl fluoride and disrupted by sonication. Cell extract was centrifuged at 13,000g for 30 min. The supernatant was applied to a Co2+ affinity column (BD TALON, BD Bio Science). After washing the column with equilibration/wash buffer containing 10 mM imidazole, bound proteins were eluted with equilibration/wash buffer containing continuant 20 to 100 mM imidazole (Supplemental Fig. 1). Fractions containing 40 mM imidazole had the highest amount of mcSKD1 protein. At 70 mM imidazole, the eluent contained mostly mcSKD1. Therefore, fractions containing 70 to 100 mM imidazole were collected and concentrated by an Amicon Ultra PL-30 (Millpore) column. The identity of purified mcSKD1 protein was confirmed by N-terminal sequencing. Protein samples collected from 70 to 100 mM imidazole were directly spotted on a polyvinylidene difluoride membrane and subjected to Edman degradation. The N-terminal sequencing was performed by an ABI 492 automatic protein sequencer (Perkin-Elmer).
ATPase activity of purified mcSKD1 protein was assayed by TLC described by Babst et al. (1998)
For detection of substrate affinity, ATPase activity was assayed with 0.02 µM [
SDS-PAGE purified mcSKD1 protein was emulsified with Freund's complete adjuvant and injected intramuscularly into rabbits or mice. After 2 weeks, the animals were boosted with purified mcSKD1 protein emulsified with Freund's incomplete adjuvant. Four boosters were given in this manner at 2-week intervals. The titer of the serum was estimated by western blotting.
Six-week-old leaves were treated with 400 mM NaCl, and 10-week-old flowers and developing seeds were collected and ground in an extraction buffer (100 mM Tris, pH 7.6, 5 mM MgCl2, 1 mM EDTA, 100 mM NaCl, 1 mM phenylmethyl sulfonyl fluoride, and 2 mM leupeptin) using a mortar and pestle. Protein crude extracts were separated on 12% SDS-PAGE and detected mcSKD1 protein by anti-SKD1 antiserum according to standard procedures.
The ice plant paraffin sections of pot-grown 7-week-old leaves and roots were salt treated for 1 week, and 10-week-old floral organs were prepared as described by Jou et al. (2004)
Two-week-old callus was ground in THM buffer (50 mM Tris, pH 7.5, 10 mM KCl, 1 mM EDTA, and 0.1 mM MgCl2) containing 8% Suc and centrifuged at 30,000g for 1 h to isolate microsomes. Microsomes were fractionated using an 8% to 45% continuous Suc gradient and separated into nine fractions. Membrane proteins in each fraction were separated by SDS-PAGE and immunoblotting against anti-mcSKD1, an ER marker anti-mEH (Galteau et al., 1985
The cultured ice plant cells were fixed in 3.7% paraformaldehyde in 50 mM sodium phosphate buffer, pH 7.0, and 5 mM EGTA. To disperse single cells, the cells were treated with 3% cellulase for 20 min to partially digest cell walls. The plasma membrane was permeabilized with 0.5% Triton X-100 in 50 mM sodium phosphate buffer, pH 7.0, and 5 mM EGTA for 5 min. The cells were incubated in blocking buffer (phosphate-buffered saline containing 0.25% bovine serum albumin, 0.25% gelatin, 0.05% Nonidet P-40, and 0.02% sodium azide) at room temperature. The primary antibodies including affinity-purified polyclonal antibodies (mcSKD1, mEH, AtTLG2a, VSR, BP-80, and V-type ATPase B1) were used at a dilution of one-tenth in blocking buffer and incubated for 1 h. After washing with blocking buffer three times for 30 min, the cells were incubated with secondary antibodies anti-mouse IgG conjugated to rhodamine and anti-rabbit IgG conjugated to FITC (Jackson ImmunoResearch) at a dilution of 1/100. A Zeiss LSM 510 laser scanning confocal microscope equipped with a water objective was used to examine the labeled cells. The confocal scanner used excitation argon laser and the beam splitter HFT UV/488/543/633. Filters BP500-530IR and LP560 collected the emitted fluorescence. Fifteen to twenty-five cells were scanned for each treatment. The images were collected sequentially from the same optical section, analyzed by Zeiss LSM Browers, and quantified by Adobe Photoshop 7.0 software. The magenta (M) and white (W) pixel areas in single sections were measured and the percent of mcSKD1 colocalized with various membrane markers was defined as W/M.
Ultrathin sections (70 nm) were obtained from salt-treated ice plant leaves, roots, and callus and were collected on formvar-coated nickel grids according to Chung et al. (2002) Sequence data from this article can be found in the EMBL/GenBank data libraries under accession number AF165422.
We thank Dr. Kuan-Chih Chow, Institute of Biomedical Science, National Chung Hsing University, Taiwan, for kindly providing anti-mEH antiserum and Dr. Liwen Jiang, Department of Biology, Chinese University of Hong Kong, China, for generously providing affinity-purified anti-VSR and anti-BP80. We are grateful to Dr. Mei-Chu Chung, Institute of Botany and Microbiology, Academic Sinica, Taiwan, for assistance in electron and confocal microscopy and Dr. Hui-Chih Hung, Department of Life Sciences, National Chung Hsing University, Taiwan, for helpful discussion of enzyme kinetics. Received January 7, 2006; returned for revision March 22, 2006; accepted March 22, 2006.
1 This work was supported by the National Science Council of Taiwan (grant no. NSC 92–2311–B005–006 to H.E.Y.). 
2 These authors contributed equally to the paper. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Hungchen E. Yen (heyen{at}dragon.nchu.edu.tw).
[W] The online version of this article contains Web-only data. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.106.076786. * Corresponding author; e-mail heyen{at}dragon.nchu.edu.tw; fax 886–4–22874740.
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–pyrroline-5-carboxylate reductase in proline-accumulating cell suspension cultures of Mesembryanthemum nodiflorum and other halophytes. Physiol Plant 67: 173–181
