JXB Advance Access originally published online on August 8, 2003
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Journal of Experimental Botany, Vol. 54, No. 391, pp. 2231-2237,
October 1, 2003
© 2003 Oxford University Press
Salt tolerance-related protein STO binds to a Myb transcription factor homologue and confers salt tolerance in Arabidopsis
Received 3 March 2003; Accepted 13 June 2003
Asian Natural Environmental Science Center (ANESC), The University of Tokyo, University Farm, 1-1-1 Midori-cho, Nishitokyo-shi, Tokyo 188-0002, Japan
* To whom correspondence should be addressed. Fax: +81 424 63 1618. E-mail: takano{at}ims.u-tokyo.ac.jp
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Abstract |
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Regulating the intracellular Na+/K+ ratio is an essential process for salinity tolerance. The yeast mutant, can, which is deficient in calcineurin, can not grow on medium containing Na+ because it is unable to regulate the intracellular Na+/K+ ratio. Expression of the STO gene of Arabidopsis thaliana in the can mutant complements the salt-sensitive phenotype. A protein of Arabidopsis, an H-protein promoter binding factor (HPPBF-1), that binds to STO protein was isolated. HPPBF-1 cDNA has a sequence encoding a Myb DNA binding-motif and its gene expression is induced by salt stress. Furthermore, HPPBF-1 protein is localized in the nucleus. Although, the expression level of STO is not induced under salt-stress conditions, overexpression of STO in a transgenic Arabidopsis plant gave it a higher salt tolerance than was observed in the wild type. When STO transgenic plants and wild-type plants were subjected to salt stress, root growth was increased by 33–70% in the transgenic plants under salt stress. These results suggest that STO is involved in salt-stress responses in Arabidopsis.
Key words: Arabidopsis thaliana, HPPBF-1, Myb, salt tolerance, STO, stress, transgenic plants.
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Introduction |
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When plants are exposed to excessive salinity, ions from the external environment accumulate in the cytosol and have many negative effects on metabolism. Plants express a number of genes to adapt to high salinity stress. Analysis of the expression of genes that are induced by salt and dehydration stress in A. thaliana have indicated that there are several independent signal pathways (Shinozaki and Yamaguchi-Shinozaki, 1997), and genes related to signal transduction pathways must have critical roles in these mechanisms. In addition, Ca2+ is an essential element in the transduction of stress signals. The cytoplasmic Ca2+ content has been shown to increase immediately after stress stimuli (Poovaiah and Reddy, 1993; Sanders et al., 1999). The expression of calcium-dependent protein kinases increases after plants are exposed to salt or drought stress. This suggests that Ca2+ plays an important role in an early step of the transduction pathway of the stress signal. In yeast, calcineurin (CaN), a Ca2+- and calmodulin-dependent protein phosphatase is an integral intermediate in the transduction pathway of the salt-stress signal. This pathway affects Na+ tolerance through the regulation of Na+ influx and efflux. The yeast can mutant lacking CaN can not grow on a medium containing Na+ because it has lost the ability to control the influx and efflux of intracellular Na+. The can mutant of yeast accumulates an abnormally high level of Li+ (Mendoza et al., 1994; Nakamura et al., 1993). This is partly due to a reduced expression of ENA1/PMR2, which encodes a P-type ATPase involved in Na+ and Li+ efflux in yeast, and partly due to a failure of the K+ uptake system encoded by TRK to convert to the high affinity state of K+ transport. The transport processes that regulate ion fluxes, particularly those involved in the control of Na+ influx, are of critical importance in the adaptation of plants to high salinity. In plants, a CaN-like protein, SOS3, has a role in the adaptation to salt stress. Under salt stress, a mutant Arabidopsis that lacks SOS3 was found to accumulate more Na+ and retain less K+ than the wild type (Liu and Zhu, 1997, 1998), which indicates that SOS3 functions in Arabidopsis in the same way that CaN functions in yeast. The expression of activated CaN improved NaCl tolerance in transgenic plants (Pardo et al., 1998). Furthermore, the gain-of-function of a vacuolar Na+/H+ antiporter gene (NHX1) improved salt tolerance (Apse et al., 1999), whereas the loss-of-function of a putative plasma membrane Na+/H+ antiporter gene (SOS1) decreased salt tolerance (Shi et al., 2000). These results demonstrate the importance of compartmentalization of Na+ in the vacuoles and the efflux of Na+ from the plant cell. The expressions of NHX1 and SOS1 are induced by salt stress. Many genes are up-regulated by salt stress, and salt-stress signalling in plants occurs via pathways that are both dependent and independent of abscisic acid, and many transcription factors are related to both pathways (Shinozaki and Yamaguchi-Shinozaki, 2000).
The Arabidopsis thaliana STO gene complements the salt-sensitive phenotype of the yeast can mutant (Lippuner et al., 1996), which suggests that STO, like SOS3, is involved in regulating of the internal Na+/K+ ratio. STO is similar to the Arabidopsis CONSTNS protein in regions that may be zinc fingers (Lippuner et al., 1996). In this paper, a protein of Arabidopsis, an H-protein promoter binding factor-1 (HPPBF-1) which binds to STO protein was isolated. Salt stress increased the expression of the HPPBF-1 gene and the HPPBF-1 protein is localized in the nucleus. Overexpression of the STO gene improved the tolerance for NaCl stress. These findings suggest that STO and HPPBF-1 function as transcription factors that induce the expression of genes that respond to salt stress.
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Materials and methods |
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Plant material and growth conditions
Plant seeds (Arabidopsis thaliana ecotype Columbia) were surface-sterilized and placed on agar plates containing MS salts, B5 vitamins and 1% sucrose. The plates were kept in the dark at 4 °C for stratification for 3 d and then transferred to a 16/8 h light/dark cycle at 22 °C.
Plasmid construction and plant transformation
The full-length cDNA of STO of Arabidopsis (accession number X95572
[GenBank]
) was amplified by the polymerase chain reaction (PCR) using a forward primer (5'-CGTCTAGATTTTGGTTTCTTGTA TCCGG) and a reverse primer (5'-CAGTGTCGACACTCCACA CATGCAGATAGG) containing XbaI and SalI sites, respectively. cDNA prepared from mRNA extracted from Arabidopsis was used as a template. The amplified cDNA was cloned into the XbaI and SalI sites of the pBI221 (Clontech, USA) and digested with XbaI and EcoRI. The digested fragment containing STO cDNA and a NOS terminator was put under the control of the cauliflower mosaic virus 35S promoter (CaMV 35S) in a transformation vector (pBI121, Clontech, USA). Agrobacterium-mediated transformation was performed via vacuum infiltration of flowering Arabidopsis (Bechtold and Pelletier, 1998). Transgenic plants were selected by placing seeds of the infected plants on plates containing MS salts, B5 vitamins, 1% sucrose and 50 mg l–1 kanamycin. Plants were subsequently selected with kanamycin for two generations to identify transgenic plants homozygous for the transgene. Wild-type plants and homozygous plants over-expressing STO were used to assay salt-stress tolerance.
Yeast two-hybrid screening
The vectors and yeast strains for the screening of the library are described by James et al. (1996), and were kindly provided by Dr P James (University of Wisconsin Medical School). The full-length cDNA of STO was amplified by PCR using a forward primer (5'-CGGAATTCTATTTTGGTTTCTTGTATCC) and a reverse primer (5'-CGGGATCCACTCCACACATGCAGATAGG) containing EcoRI and BamHI sites, respectively. The PCR product was digested with EcoRI and BamHI, and was subcloned in-frame with the GAL4 DNA-binding domain of pGBDC1 to create the bait plasmid pGBD-STO. Yeast was first transformed with plasmid pGBD-STO and then with the Arabidopsis cDNA library which was made from the vegetative tissues of 3-week-old plants by a modification of the method of Gubler and Hoffman (1983). S. cerevisiae strain PJ69-4A (MATa, trp1-901, leu2-3, 112, ura3-52, his3-200, gal4
, gal180, GAL2-ADE2, LYS::GAL1-HIS3, mtt2::GAL7-lacZ) was transformed using the lithium acetate method as described previously (Soni et al., 1993). The transformation mixture was plated on yeast drop-out selection medium lacking tryptophan, leucine and histidine and supplemented with 3-amino-1, 2, 4-triazole (3-AT). The transformants, which recovered during a 3–4 d period, were checked for growth in the presence of 50 mM 3-AT.
Northern blot analysis
Arabidopsis was grown on agar plates containing MS salts, B5 vitamins and 1% sucrose for 2 weeks and then transferred to 200 mM NaCl solution. RNA was extracted from Arabidopsis with an RNeasy Miniprep kit according to the manufacturer’s instructions (QIAGEN, USA). Ten micrograms of total RNA was electrophoresed on a morpholino propane sulphonic acid (MOPS)-formaldehyde-1% agarose gel. The RNA was blotted onto a Hybond N plus membrane (Amersham, UK). The STO mRNA was detected by chemiluminescence by using a DIG RNA Labeling kit according to the manufacturer’s instructions (Roche, Switzerland). Actin2 mRNA of Arabidopsis was used as the internal control. The final wash was performed with 0.1x SSC and 0.1% SDS for 15 min. The intensity of the bands was determined using a Lumino-image analyser (LAS-1000 plus, Fuji Film, Japan) and analysed with Image Gauge software. The intensity of the bands for HPPBF-1 and actin2 (internal control) at time 0 was considered as 100, and the relative intensity of the other bands was calculated.
Transient expression of the fusion gene and its localization
The full length coding-region of the HPPBF-1 cDNA was amplified by PCR using a forward primer (5'-AGGGTCGACCATGGTCAA AAGGAAGTT) and a reverse primer (5'-CATGTCATGAACAT GGACGAACCTGCTTC) containing SalI and BspHI sites, respectively. The full length coding-region of the STO was amplified by PCR using a forward primer (5'-GGGTCGACATGAAGATACA GTGTGATGT) and a reverse primer (5'-GTTCATGAAGCCAA GATCAGGGACAATG) containing SalI and BspHI sites, respectively. cDNA prepared from mRNA extracted from Arabidopsis was used as a template. HPPBF-1 and STO were fused in-frame to green fluorescent protein (GFP) in the sGFP (S65T) plasmid at SalI and NcoI sites under the CaMV 35S promoter. The fusion constructs were introduced into onion epidermal cells with a Biolistic PDS-1000/He particle bombardment system (Bio-Rad, USA) at a bombardment pressure of 1100 psi. All other basic adjustments were set according to the manufacturer’s recommendations. After incubation overnight, the bombarded samples were examined with a Bio-Rad confocal laser scanning microscope (Micro-Radiance MR/AG-2: Bio-Rad). The samples were illuminated with an argon ion laser using 488 nm light for GFP.
NaCl tolerance assay
Arabidopsis seeds were surface-sterilized and sown on agar medium containing MS salts, B5 vitamins and 1% sucrose with or without 120 mM NaCl. Seedlings were grown for 8 d at 22 °C, under 16/8 h light/dark conditions. For a root growth assay, 4-d-old seedlings were transferred to fresh medium that was supplemented with 0, 50, 100, and 200 mM NaCl. Root length was measured 10 d after NaCl treatments.
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Results |
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Isolation of Arabidopsis STO-related cDNA clone
A construct fusing the full-length STO gene to the GAL4 DNA-binding domain was generated and used as a bait to look for cDNAs encoding proteins that interact with STO. The cDNA library of Arabidopsis was screened for clones that signalled an interaction with this bait. Several positive clones were identified by the screening and were sequenced. One of the positive clones was found to be a part of a cDNA for the H-protein promoter binding factor-1 (HPPBF-1, accession number AF072536 [GenBank] ) which consists of 640 amino acids. The positive clone comprised amino acid residues 249 to 423 of HPPBF-1.
A BLAST search revealed that HPPBF-1 has a unique motif of a Myb DNA binding domain. It also shares sequence similarity with Catharanthus roseus BPF-1 (CrBPF-1, accession number AJ251686 [GenBank] ), which has recently been shown to be a pathogen-induced DNA-binding protein involved in the defence response (van der Fits et al., 2000), and with an Arabidopsis telomere-binding protein homologue (Salanoubat et al., 2000, accession number NC003074). Figure 1 shows an alignment of amino acid sequences of the Arabidopsis HPPBF-1 protein, Petroselinum BPF-1 protein (PcBPF-1, da Costa e Silva et al., 1993, accession number X62653 [GenBank] ), Catharanthus BPF-1 protein, and Arabidopsis telomere binding protein. Petroselinum BPF-1, Catharanthus BPF-1 and telomere binding protein share 44, 47 and 43% identity in amino acid sequences with HPPBF-1 protein, respectively. Although the homology occurs throughout the length of the proteins, some regions have higher levels of homology. Amino acid residues that are important for the Myb DNA binding domain are highly conserved in these proteins, including HPPBF-1 protein. In particular, HPPBF-1 protein has three expected tryptophan residues which are thought to comprise a Myb DNA binding domain. However, in contrast to most known plant Myb proteins in plants which have two DNA binding domains, the HPPBF-1 sequence has only one such domain (Kirik and Baumlein, 1996).
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HPPBF-1 expression level is up-regulated by salt stress
As an additional test to determine whether HPPBF-1 is related to the response to salt stress, the expression level of the HPPBF-1 in the presence of NaCl was examined. The transcription level of HPPBF-1 was increased within 1 h after transferring the seedlings to NaCl solution and reached a maximum at 2 h (Fig. 2). The transcription levels then began to decrease, and after 24 h,; Returned to the basal level, even though the stress condition was maintained.
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Nuclear localization of HPPBF-1 and STO
Because HPPBF-1 has a unique motif in the form of the Myb DNA binding domain, it was considered that HPPBF-1 works as a transcription factor in the nucleus. Furthermore, STO is also thought to be putative transcription factor. To determine the subcellular localization of HPPBF-1 and STO, the coding region of HPPBF-1 and STO was fused in-frame to the synthetic green fluorescent protein gene, sGFP (S65T). The fused gene was driven by a constitutively expressed CaMV 35S promoter. A construct without the additional coding region served as a control. The three constructs were delivered into an onion epidermal cell layer by particle bombardment, and after an overnight induction, the cells were inspected by confocal microscopy. The control plasmid gave rise to a uniform distribution of the GFP within the cell (Fig. 3), whereas the plasmids with GFP fused to HPPBF-1 and STO resulted in a localization of the GFP fusion protein strictly in the nucleus (Fig. 3). This demonstrates the presence of a functional nuclear localization signal within the HPPBF-1 and STO sequence. STO is similar to the Arabidopsis CONSTNS protein in regions that may be zinc fingers. These results indicate that STO is localized in the nucleus and that it may be a transcriptional factor. They also indicate that HPPBF-1 co-exists with STO in the nucleus and that HPPBF-1:STO complex has a DNA binding region.
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Salinity tolerance of STO transgenic plants
In order to investigate the biological role of STO in salinity tolerance, transgenic Arabidopsis plants overexpressing the STO gene was generated by introducing the STO gene under the control of the CaMV 35S promoter. Six kanamycin-resistant T1 transgenic plants harbouring the 35S:STO transgene were obtained. One T2 transgenic plant from each T1 transgenic line was selected and compared with the wild-type plants in salt tolerance tests. An RNA blot analysis showed that STO was not induced by the salt stress and the transgenic plants had higher levels of STO transcript than wild-type plants with or without salt stress (Fig. 4). When the medium contained NaCl, plants that constitutively overexpressed the STO gene grew faster than the wild-type plants. In particular, the roots of STO transgenic plants grew faster than those of the wild type under the stress condition. Wild-type and STO transgenic plants were germinated and grown vertically on minimal media agar plates which were supplemented with varying concentrations of NaCl. When grown on growth medium without NaCl, STO transgenic seedlings were indistinguishable from wild-type seedlings. Under NaCl treatment, root growth in STO transgenic plants was greater than that in wild-type plants (Fig. 5A). When plants were grown on medium containing 50 mM NaCl and 100 mM NaCl, the root growth of wild-type plants was about 75% and 58%, respectively, of that in the STO transgenic plants (Fig. 5B).
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Discussion |
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Although neither STO nor SOS3 is induced by NaCl stress, both genes are thought to have important functions in the response to NaCl stress (Lippuner et al., 1996; Piao et al., 2001). Transgenic plants overexpressing the STO gene display enhanced tolerance to NaCl stress (Fig. 5). Because STO was identified by its ability to complement the phenotype of calcineurin-deficient mutant yeast, STO is thought to be involved in regulating the intracellular Na+/K+ ratio in plant cells as calcineurin does in yeast cells. This function seems to be enhanced in the STO transgenic plants, which could explain their increased tolerance to NaCl stress. Recently, AtHKT1 of Arabidopsis was found to be a determinant of salt tolerance that controlled Na+ entry into plant cells (Uozumi et al., 2000; Rus et al., 2001). In the preliminary experiment, it was found that the intracellular Na+/K+ ratio was maintained better in STO transgenic plants than in wild-type plants under NaCl treatment (S Nagaoka, T Takano, unpublished data). STO might be involved in the Na+ influx into plant cells via AtHKT1. Until now, a plant P-type ATPase that, like ENA1/PMR2 of yeast, is involved in Na+ efflux from cells, has not been found. Another possibility is that STO might be involved in some other mechanism of Na+ efflux in plants that has not yet been described.
A cDNA clone, HPPBF-1, encoding a protein that belongs to the family of Myb transcription factors was isolated using STO as bait in a yeast two-hybrid screen. The expression of Myb transcription factors are involved in a drought stress signal pathway in plants (Urao et al., 1993; Abe et al., 1997). Plants also respond to pathogen attack by the induction of various defence responses. In Catharanthus roseus, the elicitor-induced expression of the strictosidine synthase gene (Str) is mediated via the binding of CrBPF-1. CrBPF-1 is a single Myb DNA binding factor of Catharanthus roseus, and it binds to the promoter region of Str (van der Fits et al., 2000). PcMYB1 of Petroselinum crispum, also has a single Myb-type DNA binding domain which is responsible for DNA binding (Feldbugge et al., 1997). HPPBF-1 has a single Myb-type DNA binding domain that is highly conserved among plant species. These results therefore suggest that HPPBF-1 also specifically binds to the promoter region of salt-stress-related genes (Fig. 1).
The RNA gel blot analysis showed that HPPBF-1 mRNA accumulated upon salt treatment and that the HPPBF-1 protein is localized in the nucleus (Figs 2, 3). These results indicate that HPPBF-1 is related to the signal transduction pathway of the salt-stress response. Myb recognition elements have been identified in promoters of salt- and drought-related genes (Abe et al., 1997). Therefore, it is considered that HPPBF-1, which has a single Myb DNA binding domain, acts as a transcription factor. However, the expression level of HPPBF-1 reached a maximum within 2 h after plants were challenged to NaCl stress and then decreased. This suggests that HPPBF-1 is involved in the early steps in the responses to NaCl stress.
Yeast calcineurin regulates the nuclear localization of the Crz1p transcription factor through dephosphorylation (Stathopoulos-Gerontides et al., 1999), and has also been implicated in the control of ion transport (Matheos et al., 1997). STO may have the same function in plant cells. The STO protein might participate in salt-stress responses by regulating the nuclear localization of many proteins including HPPBF-1 through dephosphorylation.
It is possible that STO also affects the regulation of other genes that are involved in salt-stress response mechanisms. Many genes have been reported to respond to salt and drought stress, and proteins that are encoded by these genes are thought to have a role in protecting against these stresses. These results indicate that the STO protein functions as a transcription factor in the salt-stress response.
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Acknowledgements |
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We thank Dr Y Niwa of Shizuoka University for the generous gift of the enhanced GFP expression vector and Dr P James of Wisconsin University Medical School for providing vectors and yeast strains for the yeast two-hybrid screening. We thank Dr S Arimura of Tokyo University for excellent technical assistance with the confocal microscope.
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