Journal of Experimental Botany, Vol. 53, No. 369, pp. 727-735,
April 1, 2002
© 2002 Oxford University Press
Original Papers |
IDI7, a new iron-regulated ABC transporter from barley roots, localizes to the tonoplast
1 Laboratory of Plant Molecular Physiology, Department of Applied Biological Chemistry, The University of Tokyo, 1-1 Yayoi, Bunkyo-ku, 113-8657 Tokyo, Japan
2 Laboratory of Plant Biotechnology, Department of Global Agricultural Sciences, The University of Tokyo, 1-1 Yayoi, Bunkyo-ku, 113-8657 Tokyo, Japan
3 Core Research for Evolutional Science and Technology, Japan Science and Technology Corporation, 4-1-8 Honcho, Kawaguchi-shi, 332-0012, Saitama, Japan
Received 8 May 2001; Accepted 6 November 2001
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Abstract |
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A new Fe-deficiency-induced cDNA, IDI7, was isolated from the roots of Fe-deficient barley (Hordeum vulgare L. cv. Ehimehadaka no. 1). The transcript levels of IDI7 in roots strongly correlated with iron nutritional status, and induction by Fe-deficiency was restricted to roots. Excess treatment with heavy metal ions, such as copper, manganese, and zinc, did not cause obvious IDI7 induction in either leaves or roots. IDI7 encodes a 644 amino acid protein, and has features typical of ATP-binding cassette (ABC) transporters. Phylogenetic analysis revealed that IDI7 is closely related to the half-type ABC protein subfamily, which includes mammalian transporters associated with antigen processing (TAPs). A transiently expressed fusion protein of IDI7 to green fluorescent protein (GFP) was localized to tonoplasts in suspension-cultured tobacco (Nicotiana tabacum L.) cells. IDI7 and its orthologues are thought to comprise a new class of ABC transporters, located in the tonoplasts of higher plants. A possible Fe-deficiency adaptation role for IDI7 in barley root cells, involving transport across the tonoplast, is proposed.
Key words: ABC transporter, barley, iron, tonoplast, vacuole.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The ATP-binding cassette (ABC) superfamily is one of the largest protein families; it is widely distributed in both prokaryotes and eukaryotes (Higgins, 1992
). Most of the ABC proteins are engaged in the ATP hydrolysis-coupled transport of a wide variety of substrates, including inorganic ions, organic compounds, amino acids, peptides, and proteins. A complete ABC transporter molecule consists of two transmembrane domains (TMD) and two nucleotide-binding domains (NBD), which are encoded as either a single polypeptide or as separate polypeptides. A TMD is usually predicted to contain 5–10 membrane-spanning helices, and an NBD contains the highly conserved Walker A and B motifs and the ABC signature motif. In Arabidopsis thaliana, 129 open reading frames are capable of encoding ABC proteins, and 103 of these proteins are thought to be functional ABC transporters with TMD (Sánchez-Fernández et al., 2001). However, only a few have been functionally characterized (Rea et al., 1998; Theodoulou, 2000).
The vacuole is a multifunctional organelle in higher plant cells (Wink, 1993), which serves as a storage compartment, a lytic compartment, and a pool for metabolic intermediates such as organic acids; it is also involved in the regulation of turgor pressure, space filling, and the maintenance of cytosolic pH (Raven, 1985; Wink, 1993; Martinoia and Rentsch, 1994; Martinoia and Ratajczak, 1997). In addition, the vacuole plays a role in tolerance to various environmental stresses, including exposure to chemicals (Blake-Kalff and Coleman, 1996; Wink, 1997; Rea et al., 1998), heavy metals (Steffens, 1990; Vögeli-Lange and Wagner, 1990), damage inflicted by herbivores and fungi (Wink, 1997), and salt stress (Serrano et al., 1999). All of these functions are based on its ability to accumulate or exchange solutes, such as glutathione and its conjugates, defence compounds, phytochelatin, or organic and inorganic ions, across the tonoplast.
Some of these transport processes have been shown to be dependent on 
pH potential generated by tonoplast H+-ATPases and/or H+-pyrophosphatases (Wink, 1993; Martinoia and Ratajczak, 1997; Maeshima, 2000; Ratajczak, 2000). However, evidence has accumulated that some of the transport processes into isolated vacuoles or tonoplast vesicles are dependent on ATP hydrolysis and independent of pH (Rea et al., 1998). Only a few ABC transporter proteins have been postulated to be responsible for these transport processes. AtMRP1, AtMRP2, and AtMRP3 are plant homologues of multidrug-resistance-associated proteins (MRPs) that were isolated from Arabidopsis thaliana. It has been shown that they transport glutathione conjugates into vacuoles when expressed in yeast cells (Lu et al., 1997, 1998; Tommasini et al., 1998). These ABC transporters are hypothesized to be involved in the transport of a wide variety of substrates into the vacuoles in higher plants (Rea et al., 1998; Rea, 1999). Recently, the involvement of AtMRP5 in root development and stomatal movement was demonstrated in an experiment using a mutant of Arabidopsis with a T-DNA insertion (Gaedeke et al., 2001). The involvement of ABC transport proteins in transport across the tonoplast is just beginning to be understood.
Higher plants respond to an Fe-deficient environment with different iron acquisition strategies, including rhizosphere acidification by proton extrusion, ferrous iron uptake following reduction of ferric chelates to ferrous iron by plasma membrane-bound ferric chelate reductase in dicots (Strategy I), and an efficient monocot strategy for acquiring iron from soils mediated by phytosiderophores (Strategy II) (Takagi, 1976; Römheld, 1987). In addition, the efficient regulation of metabolic activity and the transport of metabolites and inorganic solutes between organs or intracellular compartments should be of great importance in adaptation to an environment with low iron availability. The involvement of the plant vacuole in these adaptation mechanisms is poorly understood. It should have an important role in metabolic changes in the cytosol, the intracellular compartmentalization of metabolites, and the maintenance of cytosolic pH and the cation–anion balance, which are both altered by Fe-deficiency responses.
To elucidate the molecular mechanisms of Fe-deficiency adaptation, a search was made for cDNA clones whose transcripts increased in barley roots in response to Fe-deficiency. An Fe-deficiency-induced cDNA clone, IDI7, which encodes a protein with features typical of ABC transporter proteins was isolated. IDI7 mRNA levels in roots is strongly correlated with iron nutritional status, and a fusion protein of IDI7 to green fluorescence protein (GFP) was shown to be localized to the tonoplasts of cultured tobacco cells. In this report, a possible role for IDI7 in substrate transport across the tonoplast in Fe-deficient barley root cells is proposed. A potential role for the vacuole in the Fe-deficiency adaptation mechanisms of higher plants is also proposed.
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Materials and methods |
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Plant materials
Barley seeds (Hordeum vulgare L. var. Ehimehadaka no. 1) were germinated and seedlings were grown hydroponically as previously described (Mori and Nishizawa, 1987
). For Fe-deficiency treatment, the plants were transferred to a culture solution without iron when the third leaf emerged (17-d-old). The plants were harvested after the indicated period. For excess copper, manganese and zinc treatments, 4-week-old plants were transferred to a culture solution with a 100-times higher concentration of the respective heavy metal ion (20 µM CuSO4, 50 µM MnSO4, 50 µM ZnSO4). The plants were harvested after 3 d of treatment. The tobacco BY-2 cell suspension culture used for transient expression of the chimeric construct was grown as previously described (Nagata et al., 1992).
Isolation of an IDI7 cDNA clone
Total RNA was isolated from plant material by the guanidine thiocyanate/caesium chloride method. Poly(A)+ RNA was purified using the PolyATtract mRNA Isolation System (Promega, Madison, WI). A cDNA library was constructed with poly(A)+ RNA from Fe-deficient barley roots, according to the instruction manual (SUPERSCRIPT Plasmid System for cDNA Synthesis and Plasmid Cloning, Gibco-BRL, Rockville, MD). The cDNA MACRO array technique was performed as follows. Two thousand independent Escherichia coli colonies from the cDNA library were inoculated and grown in 3 ml of LB media with 50 µg ml-1 ampicillin at 37 °C overnight. Plasmids were prepared by the alkaline/SDS method. One µg of plasmid DNA was cleaved with EcoRI and BamHI, releasing the cDNA insert. The reaction mixtures were separated by 0.8% (w/v) TAE (40 mM TRIS-acetate pH 8.0, 1 mM EDTA) agarose gel electrophoresis. Twenty-four reaction mixtures were loaded on one agarose gel. Agarose gels were blotted to nylon membranes by capillary blotting using alkaline blotting buffer (0.5 M NaOH, 1.5 M NaCl). The membranes were washed with 2xSSPE (0.2 M NaH2PO4 pH 7.4, 3 M NaCl, and 20 mM NaCl), dried on paper towels, and fixed with a UV transilluminator. Two identical membranes were made for subsequent hybridization with cDNA probes. 32P-labelled cDNA probes were synthesized using 5 µg of poly(A)+ RNA from both Fe-deficient and Fe-sufficient barley roots. Two identical membranes were hybridized with these probes in separate hybridization tubes. Positive clones whose hybridization signals were stronger with the Fe-deficient probe than with the Fe-sufficient probe were selected. Positive clones were checked further for their induction with Fe-deficiency by Northern hybridization.
RNA and DNA procedures
Plasmid purification, subcloning, electrophoresis, blotting, and hybridization were carried out according to standard protocols (Sambrook et al., 1989). For genomic Southern analysis, genomic DNA was prepared from barley leaves by the cetyltrimethylammonium bromide method (Murray and Thompson, 1980). 32P-labelled full-length IDI7 cDNA was used as the probe for both the Northern and genomic Southern analyses.
Molecular phylogenetic analysis of the ABC protein superfamily
A molecular phylogenetic tree of the ABC transport proteins including IDI7 was constructed using the program CLUSTAL W Version 1.8. The tree was plotted using TreeView for Macintosh (68K) Version 1.5.
IDI7::GFP plasmid construction
pYH61, a binary vector carrying the chimeric IDI7::sGFP(S65T) gene in the T-DNA region, was constructed as follows. The 1.7 kb XhoI/MscI IDI7 cDNA fragment, which lacks the two C-terminal amino acid residues, was subcloned into pblue-sGFP(S65T)-NOS SK in-frame with sGFP(S65T). pblue-sGFP(S65T)-NOS SK harbours a synthetic gene for the improved green fluorescent protein sGFP(S65T), hereafter referred to simply as GFP, followed by the nopaline synthase (tNOS) terminator sequence (Chiu et al., 1996). The IDI7::GFP::tNOS fragment was excised from this plasmid and ligated into pBI121 (Clontech, Palo Alto, CA), replacing uidA::tNOS to give pYH61. pYH61 was used for the transient expression studies. The fusion protein was expressed under control of the cauliflower mosaic virus 35S promoter in suspension-cultured tobacco cells.
Transient expression of IDI7::GFP in suspension-cultured BY-2 tobacco cells by particle bombardment
pYH61 carrying the IDI7::GFP chimeric construct was introduced into suspension-cultured tobacco BY-2 cells using a particle gun (Biolistic PDS-1000/He Particle Delivery System, Bio-Rad, Hercules, CA) according to the manufacturer's recommendations. Gold particles with a diameter of 1.0 µm were coated with plasmid DNA. The cell suspensions were plated on filter paper placed on BY-2 media (Nagata et al., 1992) containing 0.2% (w/v) gellan gum, and bombarded. The conditions of bombardment were: vacuum of 28 inches of Hg, helium pressure of 1550 psi, and a 6 cm target distance. After bombardment, tissues were incubated at 26 °C for 24 h.
Microscopic observations
For confocal images, the cells were visualized using a laser-scanning microscope LSM510 (Carl Zeiss, Jena, Germany) with the 488 nm excitation line of an Ar laser. Green fluorescence signals from the fusion protein were detected with barrier filters for FITC (BP 505–550 nm). Sequential images from different focus planes were recorded automatically.
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Results |
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Isolation of IDI7 cDNA
A new screening strategy, the cDNA MACRO array technique, was employed to isolate cDNA clones whose transcripts increase in barley roots during Fe-deficiency (Yamaguchi et al., 2000
). This technique is an improved differential screening method with low background and high detection sensitivity. cDNA probes are hybridized with membranes to which digested cDNA is fixed by Southern blotting, instead of to replica membranes of colonies or plaques. Two thousand independent cDNA clones were examined using this method in order to determine whether they were induced by Fe-deficient conditions in barley roots. Known Fe-deficiency-inducible cDNA clones, such as nas (Higuchi et al., 1999), naat (Takahashi et al., 1999), Ids1 (Okumura et al., 1992), Ids2 (Okumura et al., 1994), Ids3 (Nakanishi et al., 1993), and FDH (Suzuki et al., 1998), IDI2 (Yamaguchi et al., 2000), and several new cDNA clones, were successfully isolated. This report characterizes one of the new clones, designated IDI7 (iron-deficiency induced gene 7).
Induction of the IDI7 gene by Fe-deficiency
Induction of IDI7 in roots and leaves was examined after various periods of Fe-deficiency. As shown in Fig. 1, IDI7 mRNA was rare in both leaves and roots under Fe-sufficient conditions. After 6 d of Fe-deficient treatment, IDI7 transcripts had begun to accumulate in the roots, and the amount increased with the duration of the Fe-deficient treatment. The transcripts rapidly disappeared within 3 d of supplying iron to the growth media. In leaves, however, there was no apparent induction of IDI7 gene expression in response to Fe-deficiency.
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Nucleotide sequence of IDI7 cDNA and the deduced amino acid sequence of IDI7 protein
The nucleotide sequence of IDI7 cDNA was determined. The IDI7 cDNA is 2216 bp long, and has an open reading frame encoding 644 amino acids (Fig. 2). The deduced IDI7 protein has the typical features of an ABC transporter, including a transmembrane domain (TMD) composed of five putative hydrophobic transmembrane helices (Fig. 3), a nucleotide binding domain (NBD) containing Walker A and B motifs, and an ABC signature sequence. These features suggest that IDI7 is a half-type (TMD-NBD order) ABC transporter protein. Database searches and analysis revealed several ABC transporters from the MDR/TAP family (Bauer et al., 1999; Klein et al., 1999; Saurin et al., 1999) with strong amino acid sequence similarities to IDI7. These proteins included several vertebrate transporters associated with antigen processing (TAPs). Similar proteins include human TAP1 and TAP2 (accession nos L21206 and X66401, amino acid identity 35.3% and 38.2%, respectively) (Trowsdale et al., 1990; Bahram et al., 1991); rat TAP-like ABC transporter (TAPL) (AB027520-1, 39.1%) (Yamaguchi et al., 1999); human mitochondrial ABC transporter M-ABC1 (AF047690-23, 39.6%) (Hogue et al., 1998); MDL1 and MDL2 from Saccharomyces cerevisiae (U17246-23 and Z73626-1, 34.3% and 35.2%, respectively) (Dean et al., 1994); and vertebrate P-glycoproteins or multidrug-resistance proteins (MDRs) (human MDR1, M29447-1, 39.5%) (Chen et al., 1986). In addition, several MDR-like proteins were found in higher plants (AtPGP1 from Arabidopsis thaliana and HvMDR2 from barley, X61370-1 and Y10099-1, 35.1% and 35.5% identity, respectively) (Davies et al., 1997; Dudler and Hertig, 1992). Sta1 from Arabidopsis, which is involved in mitochondrial iron homeostasis, is a half-type transporter (AJ272202) (Kushnir et al., 2001). However, the amino acid identity between IDI7 and Sta1 was relatively low (24.0%).
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The NBD region was strongly conserved between IDI7 and these proteins (more than 50% amino acid identity), while the TMD showed only about 30% amino acid identity. Most of the proteins with homology to IDI7 are half-type (TMD-NBD) ABC transporter proteins with one TMD and one NBD, except for the P-glycoproteins (or MDR proteins) from vertebrates and higher plants, which are full ABC transporters with two TMDs and two NBDs (TMD-NBD-TMD-NBD). Two hypothetical proteins that were deduced from an A. thaliana genomic DNA sequence (AB016892) and a tomato expression sequence tag (AW428933) have the strongest amino acid identity with IDI7. The strong identity (more than 70%) of these two proteins, even in the N-terminus, suggests that these sequences encode IDI7 orthologues. The Arabidopsis sequence was called AtTAP2 (Sánchez-Fernández et al., 2001
). It was reported that a different genomic sequence encoded a half-type transporter, AtTAP1 (AC010796), highly related to TAP1 in Arabidopsis (Sánchez-Fernández et al., 2001). The two sequences may form a heterodimer together to act as a functional transporter.
Molecular phylogeny of IDI7
There are published reports of phylogenetic studies of ABC proteins from yeast (Bauer et al., 1999), humans (Klein et al., 1999), Arabidopsis (Sánchez-Fernández et al., 2001), and several organisms (Saurin et al., 1999). In these reports, the ABC superfamily is subdivided into several families. To estimate the molecular evolutionary position and functional relation of IDI7, the phylogenetic position of IDI7 in the ABC protein superfamily was examined. IDI7 is in the MDR/TAP family, whose members are found in vertebrates, fungi, and higher plants. A molecular phylogenetic tree of the MDR/TAP family, including IDI7, is shown in Fig. 4. In this family, there are full molecule-type MDR-related proteins from vertebrates and higher plants and half-type TAP-related proteins, including TAP proteins from vertebrates, Sta1 from Arabidopsis, M-ABC1 from humans, and MDL proteins from S. cerevisiae, comprise separate subfamilies. IDI7 belongs to this half-type, TAP-related subfamily. Sta1 is a half-type transporter belonging to the MDR/TAP family. However, IDI7 was less closely related to Sta1 than to other proteins.
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IDI7::GFP fusion protein is localized to the tonoplast in suspension-cultured tobacco cells
The chimeric construct encoding the IDI7::GFP protein, in which GFP was fused to the C-terminus of IDI7, was transiently expressed in suspension-cultured tobacco BY-2 cells by particle bombardment. In cells expressing GFP alone, GFP fluorescence was distributed homogeneously in the cytoplasm and nucleus, while it was absent in many of the vacuoles that occupied the majority of the cells (Fig. 5A). On the other hand, in cells expressing the IDI7::GFP fusion protein, the fluorescence was clearly restricted to the tonoplasts and was completely absent in the vacuoles, cytoplasm, nucleus, and plasma membrane (Fig. 5B).
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Induction of IDI7 by excess heavy metal ion treatment
Several lines of evidence suggest that tonoplast ABC transporters are involved in the sequestration of heavy metal ions in the vacuoles of S. cerevisiae (Szczypka et al., 1994; Li et al., 1997), Schizosaccharomyces pombe (Ortiz et al., 1995), and higher plants (Tommasini et al., 1998). To investigate whether IDI7 is involved in responses to heavy metal stresses, induction of IDI7 in barley roots and leaves in response to treatments with excess copper, manganese, and zinc was examined. As shown in Fig. 6, IDI7 transcripts did not accumulate in leaves in response to these treatments. In roots, manganese treatment induced a slight accumulation of IDI7 transcripts, while copper and zinc treatments did not have any significant effect. However, the degree of induction in roots was much less with manganese than that observed during Fe-deficiency.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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A new Fe-deficiency-inducible cDNA, IDI7, which encodes a putative ABC transporter protein with a TMD and a NBD was isolated. IDI7 is thought to be a novel half-type ABC transporter protein, and it is expected to function as either a homo- or heterodimer. IDI7 was found to have strong amino acid similarity to several members of the MDR/TAP family of ABC transporters from vertebrates, fungi, and higher plants (Bauer et al., 1999
; Klein et al., 1999; Saurin et al., 1999). Phylogenetic analysis revealed that IDI7 belongs to the half-type TAP-related subfamily. IDI7 and its putative orthologues from A. thaliana and tomato are more closely related to TAP-related half-type ABC proteins than plant MDR proteins, and comprise a new subfamily in higher plants. In a recent complete inventory of the A. thaliana ABC protein superfamily, two TAP-related half-type transporters were categorized in the TAP subfamily (Sánchez-Fernández et al., 2001).
The transiently expressed IDI7::GFP fusion protein clearly localized to the tonoplasts in cultured tobacco cells. No signals were observed at the plasma membrane or in vacuoles, the cytosol, or the nucleus; IDI7 is therefore believed to be a tonoplast ABC transporter. Plant homologues of multidrug-resistance-associated proteins (MRPs) have been isolated from A. thaliana (Rea et al., 1998; Rea, 1999). They transport a wide variety of substrates into vacuoles, including glutathione conjugates and chlorophyll catabolites; their involvement in xenobiotic and heavy metal tolerance (Lu et al., 1997, 1998; Tommasini et al., 1998), or root development and stomata movement (Gaedeke et al., 2001) has been suggested. Only AtMRP2 has been localized to the tonoplast (Liu et al., 2001). IDI7 is the second class of tonoplast ABC transporter in higher plants. All the functionally characterized eukaryotic ABC transporters mediate either the excretion of substrates from the cytosol, or their export from the cytosol into organelles, but not their import into the cytoplasm (Saurin et al., 1999). IDI7 is thought to be involved in the export of certain substrates from the cytosol to the vacuoles.
The abundance of IDI7 mRNA was strongly correlated with iron nutritional status, and induction by Fe-deficiency was restricted to roots, suggesting that IDI7 is involved in the physiological adaptation of barley roots to Fe-deficiency. What kind of molecules does IDI7 transport across tonoplasts? Several hypotheses for IDI7 function can be proposed, based on the biochemical evidence present in barley roots under Fe-deficient conditions. The synthesis and secretion of phytosiderophores are the most dynamic events in adaptation to an Fe-deficient environment in graminaceous plants (Takagi, 1976; Römheld, 1987). Phytosiderophores are synthesized from three molecules of methionine (Mori and Nishizawa, 1987; Shojima et al., 1990; Higuchi et al., 1999; Takahashi et al., 1999). The daily secretion of phytosiderophores by Fe-deficient barley roots amounts to approximately 1% of the roots’ dry weight. Synthesis of phytosiderophores may require the transport of specific molecules, such as precursors and by-products, between the cytosol and vacuoles. It is thought that phytosiderophores are secreted as monovalent anions via anion channels (Sakaguchi et al., 1999). The secretion of large amounts of phytosiderophores causes various biochemical changes in root cells, such as cation–anion imbalance and pH changes in the cytosol. These cytosolic changes are compensated for by the so-called pH-stat mechanism, in which organic acids are synthesized or decarboxylated to regulate the anion concentration and proton production (Davies, 1986). IDI7 may transport specific molecules across the tonoplast, such as by-products and organic acids accumulated in the cytosol, facilitating the synthesis and secretion of phytosiderophores.
Organic acids, such as citrate and malate, accumulate in the roots of both monocots and dicots grown under Fe-deficient conditions (Landsberg, 1981). It is not clear whether organic acid accumulation in the roots of monocots is related to the synthesis or secretion of phytosiderophores, but accumulated organic acids are transported into vacuoles or exported to the xylem (De Vos et al., 1986; Bienfait et al., 1989). Transport of malate or citrate into isolated tonoplast vesicles has been studied in various plant species. These transport events were shown, and believed to be pH-dependent, or inside-positive electrical membrane potential-dependent (Ratajczak et al., 1994; Martinoia and Ratajczak, 1997). However, the possibility cannot be ruled out that unknown ABC transporters are involved in the transport of organic acids across the tonoplast.
It is known that Fe-deficiency causes accumulation of heavy metal ions in roots, including manganese, copper, and zinc (Cohen et al., 1998). Vacuoles have an important role in resistance to heavy metals in yeasts and higher plants (Steffens, 1990; Vögeli-Lange and Wagner, 1990; Li et al., 1997). In S. cerevisiae and S. pombe, involvement of ABC transporters, ScYCF1 (Szczypka et al., 1994; Li et al., 1997) and HMT1 (Ortiz et al., 1995), respectively, in heavy metal resistance is well documented. At present, among ABC proteins isolated from higher plants, only AtMRP3 has been shown to suppress the Cd2+-hyper-sensitivity of the yeast ycf1 strain (Tommasini et al., 1998). Since accumulation of IDI7 mRNA was much less with excess concentrations of heavy metals than with Fe-deficiency, it is unlikely that IDI7 is involved in the sequestration of metal ions into vacuoles.
At present, it is not known which kind of molecules IDI7 transports across the tonoplasts. Further analysis of the IDI7 ABC transporter will reveal the specific role of vacuoles in the adaptive response of root cells of higher plants to Fe-deficiency.
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Acknowledgments |
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We thank Dr Yasuo Niwa (University of Shizuoka, Japan) for providing the pblue-sGFP(S65T)-NOS SK.
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Notes |
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4 To whom correspondence should be addressed. Fax: +81358418009. E-mail: asmori{at}mail.ecc.u\|[hyphen]\|tokyo.ac.jp
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References |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Bahram S, Arnold D, Bresnahan M, Strominger JL, Spies T. 1991. Two putative subunits of a peptide pump encoded in the human major histocompatibility complex class II region. Proceedings of the National Academy of Sciences, USA 88, 10094–10098.
Bauer BE, Wolfger H, Kuchler K. 1999. Inventory and function of yeast ABC proteins: about sex, stress, pleiotropic drug and heavy metal resistance. Biochimica et Biophysica Acta 1461, 217–236.[Medline]
Bienfait HF, Lubberding HJ, Heutink P, Lindner L, Visser J, Kaptein R, Dijkstra K. 1989. Rhizosphere acidification by iron-deficient bean plants: the role of trace amounts of divalent metal ions. Plant Physiology 90, 359–364.
Blake-Kalff MMA, Coleman JOD. 1996. Detoxification of xenobiotics by plant cells: characterization of vacuolar amphiphilic organic anion transporters. Planta 200, 426–431.
Brown JC. 1978. Mechanism of iron uptake by plants. Plant, Cell and Environment 1, 249–257.
Chen CJ, Chin JE, Ueda K, Clark DP, Pastan I, Gottesman MM, Roninson IB. 1986. Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell 47, 381–389.[Web of Science][Medline]
Chiu WI, Niwa Y, Zeng W, Hirano T, Kobayashi H, Sheen J. 1996. Engineered GFP as a vital reporter in plants. Current Biology 6, 325–330.[Web of Science][Medline]
Cohen CK, Fox TC, Garvin DF, Kochian LV. 1998. The role of iron-deficiency stress responses in stimulating heavy-metal transport in plants. Plant Physiology 116, 1063–1072.
Davies DD. 1986. The fine control of cytosolic pH. Physiologia Plantarum 67, 702–706.
Davies TGE, Theodoulou FL, Hallahan DL, Forde BG. 1997. Cloning and characterization of a novel P-glycoprotein homologue from barley. Gene 199, 195–202.[Web of Science][Medline]
Dean M, Allikmets R, Gerrard B, Stewart C, Kistler A, Sfafer B, Michaelis S, Strathern J. 1994. Mapping and sequence of two yeast genes belonging to the ATP-binding casserre superfamily. Yeast 10, 377–383.[Web of Science][Medline]
De Vos CR, Lubberding HJ, Bienfait HF. 1986. Rhizosphere acidification as a response to iron deficiency in bean plants. Plant Physiology 81, 842–846.
Dudler R, Hertig C. 1992. Structure of an mdr-like gene from Arabidopsis thaliana: evolutionary implications. Journal of Biological Chemistry 267, 5882–5888.
Gaedeke N, Klein M, Kolukisaoglu U, Forestier C, Müller A, Ansorge M, Becker D, Mamnun Y, Kuchler K, Schulz B, Mueller-Roeber B, Martinoia E. 2001. The Arabidopsis thaliana ABC transporter AtMRP5 controls root development and stomata movement. The EMBO Journal 20, 1875–1887.[Web of Science][Medline]
Higgins CF. 1992. ABC transporters: from microorganisms to man. Annual Review of Cell Biology 8, 67–113.[Web of Science]
Higuchi K, Suzuki K, Nakanishi H, Yamaguchi H, Nishizawa NK, Mori S. 1999. Cloning of nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores. Plant Physiology 199, 471–479.
Hogue DL, Liu L, Ling V. 1998. Identification and characterization of a mammalian mitochondrial ATP-binding cassette membrane protein. Journal of Molecular Biology 285, 379–389.
Klein I, Sarkadi B, Váradi A. 1999. An inventory of the human ABC proteins. Biochimica et Biophysica Acta 1461, 237–262.[Medline]
Kushnir S, Babiychuk E, Storozhenko S, Davey MW, Papenbrock J, Rycke RD, Engler G, Stephan UW, Lange H, Kispal G, Lill R, Montagu MV. 2001. A mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. The Plant Cell 13, 89–100.
Kyte J, Doolittle RF. 1982. A simple method for displaying the hydropathic character of a protein. Journal of Molecular Biology 157, 105–132.[Web of Science][Medline]
Landsberg EC. 1981. Organic acid synthesis and release of hydrogen ions in response to Fe deficiency stress of mono- and dicotyledonous plant species. Journal of Plant Nutrition 3, 579–591.
Li ZS, Lu YP, Zhen RG, Szczypka M, Thiele DJ, Rea PA. 1997. A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis (glutathionato) cadmium. Proceedings of the National Academy of Sciences, USA 94, 42–47.
Liu GS, Sánchez-Fernández R, Li ZS, Rea PA. 2001. Enhanced multispecificity of Arabidopsis vacuolar multidrug resistance-associated protein-type ATP-binding cassette transporter, AtMRP2. Journal of Biological Chemistry 276, 8648–8656.
Lu YP, Li ZS, Rea PA. 1997. AtMRP1 gene of Arabidopsis encodes a glutathione S-conjugate pump: isolation and functional definition of a plant ATP-binding cassette transporter gene. Proceedings of the National Academy of Sciences, USA 94, 8243–8248.
Lu YP, Li ZS, Drozdowicz YM, Hortensteiner S, Martinoia E, Rea PA. 1998. AtMRP2, an Arabidopsis ATP-binding cassette transporter able to transport glutathione S-conjugates and chlorophyll catabolites: functional comparisons with AtMRP1. The Plant Cell 10, 1–18.
Maeshima M. 2000. Vacuolar H+-pyrophosphatase. Biochimica et Biophysica Acta 1465, 37–51.[Medline]
Martinoia E, Ratajczak R. 1997. Transport of organic molecules across the tonoplast. Advances in Botanical Research 25, 366–400.
Martinoia E, Rentsch D. 1994. Malate compartmentation-responses to a complex metabolism. Annual Review of Plant Physiology and Plant Molecular Biology 45, 447–467.[Web of Science]
Mori S, Nishizawa NK. 1987. Methionine as a dominant precursor of phytosiderophore in graminaceae plants. Plant and Cell Physiology 28, 1081–1092.
Murray MG, Thompson WF. 1980. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8, 4321–4325.
Nagata T, Nemoto Y, Hasegawa S. 1992. Tobacco BY-2 cell line as the ‘HeLa’ cells in the cell biology of higher plants. International Review of Cytology 132, 1–30.
Nakanishi H, Okumura N, Umehara Y, Nishizawa NK, Chino M, Mori S. 1993. Expression of a gene specific for iron deficiency (Ids3) in the roots of Hordeum vulgare. Plant and Cell Physiology 34, 401–410.
Okumura N, Nishizawa NK, Umehara Y, Ohata T, Mori S. 1992. Iron deficiency specific cDNA (Ids1) with two homologous cysteine rich MT domains from the roots of barley. Journal of Plant Nutrition 15, 2157–2172.
Okumura N, Nishizawa NK, Umehara Y, Ohata T, Nakanishi H, Yamaguchi T, Chino M, Mori S. 1994. A dioxygenase gene (Ids2) expressed under iron deficiency conditions in the roots of Hordeum vulgare. Plant Molecular Biology 25, 705–719.[Web of Science][Medline]
Ortiz DF, Ruscitti T, McCue KF, Ow DW. 1995. Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. Journal of Biological Chemistry 270, 4721–4728.
Ratajczak R. 2000. Structure, function and regulation of the plant vacuolar H+-translocating ATPase. Biochimica et Biophysica Acta 1465, 17–36.[Medline]
Ratajczak R, Kemna I, Lüttge U. 1994. Characteristics, partial purification and reconstitution of the vacuolar malate transporter of the CAM plant Kalanchoë daigremontiana Hamet et Perrier de la Bâthie. Planta 195, 226–236.[Web of Science]
Raven JA. 1985. Regulation of pH and generation of osmolarity in vascular plants: a cost–benefit analysis in relation to efficiency of energy, nitrogen and water. New Phytologist 101, 25–77.[Web of Science]
Rea PA. 1999. MRP subfamily ABC transporters from plants and yeast. Journal of Experimental Botany 50, 895–913.[Abstract]
Rea PA, Li ZS, Lu YP, Drozdowicz YM. 1998. From vacuolar GS-X pumps to multispecific ABC transporters. Annual Review of Plant Physiology and Plant Molecular Biology 49, 727–760.[Web of Science]
Römheld V. 1987. Different strategies for iron acquisition in higher plants. Physiologia Plantarum 70, 231–234.
Sakaguchi T, Nishizawa NK, Nakanishi H, Yoshimura E, Mori S. 1999. The role of potassium in the secretion of mugineic acids family phytosiderophores from iron-deficient barley roots. Plant and Soil 215, 221–227.[Web of Science]
Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd edn. New York: Cold Spring Harbor Laboratory Press.
Sánchez-Fernández R, Davies TGE, Coleman JOD, Rea PA. 2001. The Arabidopsis thaliana ABC protein superfamily: a complete inventory. Journal of Biological Chemistry (in press).
Saurin W, Hofnung M, Dassa E. 1999. Getting in or out: early segregation between importers and exporters in the evolution of ATP-binding cassette (ABC) transporters. Journal of Molecular Evolution 48, 22–41.[Web of Science][Medline]
Serrano R, Mulet JM, Rios G, Marquez JA, De Larrinoa IF, Leube MP, Mendizabal I, Pascual-Ahuir A, Proft M, Ros R, Montesinos C. 1999. A glimpse of the mechanisms of ion homeostasis during salt stress. Journal of Experimental Botany 50, 1023–1036.[Abstract]
Shojima S, Nishizawa NK, Fushiya S, Nozoe S, Irifune T, Mori S. 1990. Biosynthesis of phytosiderophores: in vitro biosynthesis of 2'-deoxymugineic acid from L-methionine and nicotianamine. Plant Physiology 93, 1497–1503.
Suzuki K, Itai R, Suzuki K, Nakanishi H, Nishizawa NK, Yoshimura E, Mori S. 1998. Formate dehydrogenase, an enzyme of anaerobic metabolism, is induced by iron deficiency in barley roots. Plant Physiology 116, 725–732.
Steffens JC. 1990. The heavy metal-binding peptides of plants. Annual Review of Plant Physiology and Plant Molecular Biology 41, 553–575.[Web of Science]
Szczypka MS, Wemmie JA, Moye-Rowley WS, Thiele DJ. 1994. A yeast metal resistance protein similar to human cystis fibrosis transmembrane conductance regulator (CFTR) and multidrug resistance-associated protein. Journal of Biological Chemistry 269, 22853–22857.
Takagi S. 1976. Naturally occurring iron-chelating compounds in oat- and rice-root washing. I. Activity measurement and preliminary characterization. Soil Science and Plant Nutrition 22, 4232–4233.
Takahashi M, Yamaguchi H, Nakanishi H, Shioiri T, Nishizawa NK, Mori S. 1999. Cloning two genes for nicotianamine aminotransferase, a critical enzyme in iron acquisition (Strategy II) in graminaceous plants. Plant Physiology 121, 947–956.
Theodoulou FL. 2000. Plant ABC transporters. Biochimica et Biophysica Acta 1465, 79–103.[Medline]
Tommasini R, Vogt E, Fromenteau M, Hörtensteiner S, Matile P, Amrhein N, Martinoia E. 1998. An ABC-transporter of Arabidopsis thaliana has both glutathione-conjugate and chlorophyll catabolite transport activity. The Plant Journal 13, 773–780.[Web of Science][Medline]
Trowsdale J, Hanson I, Mockridge I, Beck S, Townsend A, Kelly A. 1990. Sequences encoded in the class II region of the MHC related to the ‘ABC’ superfamily of transporters. Nature 348, 741–744.[Medline]
Vögeli-Lange R, Wagner GJ. 1990. Subcellular localization of cadmium and cadmium binding peptides in tobacco leaves. Plant Physiology 92, 1086–1093.
Wink M. 1993. The plant vacuole: a multifunctional compartment. Journal of Experimental Botany 44, 231–246.
Wink M. 1997. Compartmentation of secondary metabolites and xenobiotics in plant vacuoles. Advances in Botanical Research 25, 141–169.
Yamaguchi H, Nakanishi H, Nishizawa NK, Mori S. 2000. Isolation and characterization of IDI2, a new Fe-deficiency induced cDNA from barley roots, which encodes a protein related to the 
subunit of eukaryotic initiation factor 2B (eIF2B ). Journal of Experimental Botany 51, 2001–2007.
Yamaguchi Y, Kasano M, Terada T, Sato R, Maeda M. 1999. An ABC transporter homologous to TAP proteins. FEBS Letters 457, 231–236.[Web of Science][Medline]
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