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First published online February 22, 2008; 10.1105/tpc.107.057554 The Plant Cell 20:438-451 (2008) © 2008 American Society of Plant Biologists Identification of a Novel Adenine Nucleotide Transporter in the Endoplasmic Reticulum of Arabidopsis[W]
a Pflanzenphysiologie, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany 2 Address correspondence to tjaden{at}rhrk.uni-kl.de.
Many metabolic reactions in the endoplasmic reticulum (ER) require high levels of energy in the form of ATP, which is important for cell viability. Here, we report on an adenine nucleotide transporter residing in the ER membranes of Arabidopsis thaliana (ER-ANT1). Functional integration of ER-ANT1 in the cytoplasmic membrane of intact Escherichia coli cells reveals a high specificity for an ATP/ADP antiport. Immunodetection in transgenic ER-ANT1-C-MYC-tag Arabidopsis plants and immunogold labeling of wild-type pollen grain tissue using a peptide-specific antiserum reveal the localization of this carrier in ER membranes. Transgenic ER-ANT1-promoter-β-glucuronidase Arabidopsis lines show high expression in ER-active tissues (i.e., pollen, seeds, root tips, apical meristems, or vascular bundles). Two independent ER-ANT1 Arabidopsis knockout lines indicate a high physiological relevance of ER-ANT1 for ATP transport into the plant ER (e.g., disruption of ER-ANT1 results in a drastic retardation of plant growth and impaired root and seed development). In these ER-ANT1 knockout lines, the expression levels of several genes encoding ER proteins that are dependent on a sufficient ATP supply (i.e., BiP [for luminal binding protein] chaperones, calreticulin chaperones, Ca2+-dependent protein kinase, and SEC61) are substantially decreased.
A major difference feature between prokaryotes and eukaryotes is the high degree of compartmentalization in the latter, allowing an improved regulation of complex metabolism, and the simultaneous presence of pathways of opposite direction (e.g., the reductive and the oxidative pentose phosphate cycle in photosynthetic cells). The lumens of the endoplasmic reticulum (ER) and Golgi apparatus are the subcellular sites where glycosylation, sulfation, and phosphorylation of secretory and membrane-bound proteins, proteoglycans, and lipids occur (Hirschberg et al., 1998  ). The correct folding and assembling of proteins and peptides, disulfide bond formation, and protein polymerization in the ER lumen indicate a strong demand for energy in this compartment, and ATP serves as the energy source for the reactions mentioned above (Abeijon et al., 1997). Both the size and charge of nucleotides prevent free flux across biological membranes, making a specific carrier protein for the translocation of cytosolic ATP into the ER lumen necessary.
In eukaryotic cells, different groups of intracellular adenine nucleotide transport proteins have been elucidated at the molecular level. First, the mitochondrial ADP/ATP carrier (AAC) is the most prominent member of the mitochondrial carrier family (MCF). MCFs occur as homodimers, each monomer exhibiting six predicted transmembrane domains (TMDs) with a molecular mass of
Although several biochemical studies have revealed ATP transport across the ER membrane (Abeijon et al., 1997
Sequence Analysis of ER-ANT1 An ER-ANT1 cDNA clone was isolated from first-strand cDNA of Arabidopsis leaves. The deduced amino acid sequence was aligned with the three mitochondrial AAC isoforms (AAC1 to AAC3) from Arabidopsis (Figure 1 ), since phylogenetic analyses classify ER-ANT1 as a member of the MCF forming a monophyletic subcluster with mitochondrial AACs (Picault et al., 2004 ). The amino acid sequence of ER-ANT1 consists of three tandem repeats of  100 residues exhibiting six putative transmembrane helices. Three conserved mitochondrial energy transfer signatures, a characteristic of membrane proteins of the MCF (Leroch et al., 2005), were also identified (Figure 1). A comparison of ER-ANT1 with mitochondrial AAC homologs revealed a high sequence similarity to AAC1 to AAC3 of 62, 61, and 63%, respectively. However, in contrast with AAC1 to AAC3, ER-ANT1 does not possess a putative N-terminal transit peptide (Figure 1), which is strictly required for targeting plant AACs to the inner mitochondrial membrane (Murcha et al., 2005).
A comprehensive study of amino acids essential for the function of mitochondrial AACs suggests a putative biochemical function for ER-ANT1 as an ATP/ADP transporter. For example, the importance of basic amino acid residues for the function of AAC2 from Saccharomyces cerevisiae was investigated previously by site-directed mutagenesis. Six Arg residues and one Lys (R96, R204, R252, R253, R254, R294, and K38) were found to be crucial for the ADP/ATP transport activity of the yeast mitochondrial AAC2 (Nelson et al., 1993 ). The corresponding amino acids in At ER-ANT1 (R83, R192, R240, R241, R242, L282, and K25) are almost identical, with the exception that R294 is replaced by L282 (Figure 1).
Furthermore, the structure of the bovine AAC1 monomer was solved at a resolution of 2.2 Å by x-ray crystallography (Pebay-Peyroula et al., 2003 A second cationic cluster was found near the bottom of the bovine AAC1 translocation channel, comprising four Lys (K91, K95, K106, and K198) and two Arg (R104 and R187) residues, which are postulated to be involved in the carrier function. This cationic cluster of six basic amino acids is also conserved in At ER-ANT1 (K95, K99, K106, K108, K203, and R192), but R104 of the bovine AAC1 is replaced in At ER-ANT1 by the similarly charged K106 as in plant mitochondrial At AAC1 to AAC3 (Figure 1). Next to the two cationic clusters, a Tyr ladder motif was identified in the proposed translocation channel of the bovine AAC1. This motif, formed by the residues Y186, Y190, and Y194, was suggested to guide ADP translocation along the Tyr rings. Interestingly, the corresponding Tyr ladder is completely conserved in At ER-ANT1 (Y191, Y195, and Y199; Figure 1). The high conservation of amino acid residues critical for the function of mitochondrial AACs strongly indicates a putative biochemical function for At ER-ANT1 as an adenylate transport protein.
Functional Expression of ER-ANT1 in E. coli Cells
Uptake studies with radioactively labeled [  -32P]ATP or [-32P]ADP into intact bacterial cells harboring ER-ANT1 clearly revealed the time-linear import of both nucleotides for at least 25 min. By contrast, noninduced E. coli control cells were not able to transport ATP or ADP at significant rates (Figure 2B). The nucleotide uptake was strictly dependent on the membrane intactness of E. coli cells (see Supplemental Figure 1 online). The import of radioactively labeled [-32P]ATP or [-32P]ADP by the recombinant ER-ANT1 into E. coli cells displayed typical Michaelis-Menten kinetics, with apparent Km values of 343.7 ± 20.4 µM and 327.3 ± 24.4 µM for ATP and ADP, respectively. Competition experiments with 26 different potential substrates showed that ER-ANT1 has a high specificity for transporting ATP and ADP similar to the mitochondrial isoform AAC1 (Table 1
). The [-32P]ATP import catalyzed by ER-ANT1 could be reduced with nonlabeled ATP or ADP to below 44 or 38% of the control value, respectively. All other metabolic intermediates tested exerted no substantial influence on the [-32P]ATP transport rate (Table 1).
We also determined the influence of common inhibitors on the [ -32P]ATP uptake catalyzed by ER-ANT1 in comparison with the mitochondrial AAC1 isoform from Arabidopsis (Table 1). As expected, the mitochondrial AAC1 is highly sensitive to bongkrekic acid (BKA) and carboxyatractyloside (CAT). The inhibition with 10 µM BKA and 1 mM CAT reduced the [-32P]ATP uptake mediated by At AAC1 to 30.4 and 47.5%, respectively (Table 1). Remarkably, these two highly specific inhibitors of mitochondrial AACs (Leroch et al., 2005) showed no inhibitory effect on the [-32P]ATP uptake catalyzed by ER-ANT1 at the given concentrations (Table 1). In addition, no significant inhibition of the ER-ANT1–mediated nucleotide transport was observed in the presence of pyridoxal-5'-phosphate (PLP) or mersalyl (Table 1), which are known as efficient inhibitors of plastidic (PLP) and peroxisomal (PLP and mersalyl) adenine nucleotide transporters (Palmieri et al., 2001; Leroch et al., 2005). Only N-ethylmaleimide, which does not exert any influence on the mitochondrial AAC1, exhibited a significant inhibitory effect of up to 71% on the nucleotide transport rate of ER-ANT1 (Table 1).
To analyze whether ER-ANT1 mediates a nucleotide exchange, we performed back-exchange experiments with E. coli cells harboring ER-ANT1. For this, E. coli cells were preloaded with radioactively labeled [
Subcellular Localization of ER-ANT1
To resolve the membrane location of ER-ANT1, sucrose density gradient centrifugation with total membranes of Arabidopsis was performed either in the presence or absence of Mg2+. The association of ribosomes with the ER is Mg2+-dependent, and removal of the divalent cation results in the dissociation of ribosomes from the ER and the diagnostic redistribution of ER from higher to lower density on the gradient (Chen et al., 2002 ). Fractions from the sucrose gradient were screened for the presence of the ER-ANT1-C-MYC-tag as well as for the calreticulin marker specific for ER membranes (Pagny et al., 2000). In the absence of Mg2+, ER-ANT1-C-MYC-tag and the ER marker calreticulin cofractionated (Figure 3B, lanes 11 and 12). In the gradient containing Mg2+, both ER-ANT1-C-MYC-tag and the ER marker calreticulin shifted to the bottom fractions of the gradient without the loss of colocalization (Figure 3B, lanes 6 and 7). Since other membranes, like the plasma membrane, the vacuolar membrane, or the mitochondrial membrane, did not show any similar shift in gradient position dependent upon the presence of Mg2+ (Figure 3B; cf. Chen et al., 2002), this observation shows the ER localization of At ER-ANT1.
To confirm these data, we conducted a second totally independent approach. For these localization studies, we chose Arabidopsis wild-type pollen grain tissues, since pollen shows the highest levels of ER-ANT1 transcript (pollen, 99,714;
Expression Analyses of ER-ANT1
Physiological Analyses of ER-ANT1 Arabidopsis Knockout Lines To provide the first insight into the physiological role of ER-ANT1 as an adenine nucleotide transporter localized in the ER, we made use of transgenic plants. Two independent heterozygous ER-ANT1::T-DNA Arabidopsis mutants carrying a T-DNA insert in exon 2 were provided by the SALK library (Figure 5A ). After backcrossing, homozygous knockout lines were identified by PCR and the absence of ER-ANT1 transcript was verified by RT-PCR.
Interestingly, 24-d-old homozygous ER-ANT1 knockout plants of both SALK lines grown on soil under ambient conditions exhibited a dramatic growth retardation compared with wild-type plants (Figure 5B). Due to the high ER-ANT1-promoter activity, particularly in the root tips, we assumed that the root development of ER-ANT1 knockout plants was most likely impaired under these growth conditions. Thus, we analyzed the germination and early development of the ER-ANT1 knockout seeds in sterile culture supplemented with agar at various concentrations (0.5 to 1.5%). Interestingly, root development of both ER-ANT1 knockout mutants was improved when grown on low-agar medium, which facilitates the penetration of developing root tips (Figure 5C). At an agar concentration of 0.5%, the root development of ER-ANT1 knockout mutants was similar to that in wild-type roots (Figure 5C). Therefore, prior to growth on soil, we incubated plants for the first 12 d on sterile medium with 0.5% agar. The improved growth of ER-ANT1 knockout plants enabled us to carry out further physiological studies. However, ER-ANT1 knockout plants exhibited, after 3 to 4 months of growth, a dumose compact, bushy phenotype with several parallel flower buds still very delayed in growth compared with wild-type plants (Figure 5D). In contrast with the short generation cycle of 6 weeks of Arabidopsis wild-type plants, ER-ANT1 knockout mutants extended their generation cycle up to 6 months, until seed harvest was possible. During the flowering stage, ER-ANT1 knockout plants presented a reduced size accompanied by the loss of apical dominance compared with wild-type plants (Figure 5E).
ER chaperones are known to be high consumers of luminal ATP and play an important role in ER metabolism (Hirschberg et al., 1998
To investigate any putative influence of ER-ANT1 on seed development, we analyzed the seeds of both ER-ANT1 knockout lines compared with wild-type seeds. For the quantification of the 1000-seed weight and the lipid and protein contents, fully developed seeds from wild-type and ER-ANT1 knockout plants were harvested from mature siliques. Seeds of ER-ANT1 knockout plants exhibited morphological alterations compared with wild-type seeds. ER-ANT1 seeds were translucent and smaller in size than wild-type seeds (Figure 7A ). The average 1000-seed weight for wild-type seeds was 20 mg, which fully concurs with previous studies (Jako et al., 2001). By contrast, the 1000-seed weight in ER-ANT1 knockout seeds decreased to 45% (Figure 7B). The seed oil content of ER-ANT1 knockout seeds decreased drastically to 30% compared with wild-type seeds (Figure 7C). In addition, both ER-ANT1 knockout lines also exhibited a significant decrease of 50% in the seed protein levels (Figure 7D). Apparently, the observed reduction in seed weight of ER-ANT1 knockout seeds can be attributed mainly to the loss of storage oil and protein.
Necessity of ATP Transport into the ER In eukaryotes, ATP transport has been shown to occur across ER membranes, but the corresponding carrier proteins have not been identified at the molecular level (Mayinger et al., 1995 ; Abeijon et al., 1997; Kochendörfer et al., 1999). The occurrence of an adenine nucleotide transporter in the ER membrane is essential to provide the ER lumen with ATP for the following reasons. (1) Protein translocation through the ER membrane can only occur in the presence of luminal ATP, because the transfer of bound protein precursors into the translocation pore and the subsequent transport is mediated by ATP-dependent ER chaperones (Schatz and Dobberstein, 1996; Lyman and Schekman, 1997). (2) Other ATP-dependent chaperones are crucial for the proper folding and assembly of ER or secretory proteins inside the organelle throughout the transport process (Pfeffer and Rothman, 1987). (3) For the glycosylation and phosphorylation of proteins, proteoglycans, or lipids, ATP is either required to energize the corresponding reactions or serves as a direct substrate inside the ER lumen (Hirschberg et al., 1998). (4) Protein trafficking between the ER and the Golgi within the secretory pathway depends on luminal ATP, since this metabolite is required for fundamental steps in the transport process, such as the regeneration of GTP used by GTPases (Brandizzi et al., 2002).
Identification of an Adenine Nucleotide Exchanger Localized in the ER Membrane of Arabidopsis
The identification of ER-ANT1 in ER membranes is in full concordance with previous observations that typical MCF carriers reside in other subcellular membranes, including plastids, glyoxisomes, and peroxisomes (Picault et al., 2004
(1) In contrast with the mitochondrial AAC1 to AAC3 isoforms, ER-ANT1 lacks any cleavable N-terminal transit peptide (Figure 1), which is necessary for the efficient insertion of plant AACs into the inner mitochondrial membranes (Murcha et al., 2005 (2) Moreover, our in planta localization experiments showed the integration of ER-ANT1 in ER membranes. The immunodetection of ER-ANT1-C-MYC-tag fusion protein in transgenic Arabidopsis and the immunogold labeling in wild-type pollen grain tissue using an At ER-ANT1–specific antiserum prove that ER-ANT1 resides in ER membranes (Figure 3).
(3) The remarkable ER-ANT1 insensitivity to BKA and CAT distinguishes biochemically ER-ANT1 from mitochondrial AACs, which are highly sensitive to both inhibitors (Table 1) (Haferkamp et al., 2002
(4) As mentioned above, several ER chaperones (e.g., BiP chaperones) are high ATP consumers and essential for the constitutive function of the plant ER. In Arabidopsis and soybean (Glycine max), several BiP proteins play an important role in the biosynthesis of ER-related proteins in ER-active tissues (Sung et al., 2001
(5) The deletion of an ATPase gene (MIA, for Male gametogenesis Impaired Anthers) located in the ER membranes of Arabidopsis mutants is linked to defects in the secretory pathway accompanied by significantly impaired pollen development and male fertility (Jakobsen et al., 2005
Physiological Relevance of ER-ANT1 in the Metabolism of Arabidopsis
The ER proteins involved in protein translocation, phosphorylation, and proper folding are dependent on an adequate luminal ATP level (Hirschberg et al., 1998
Moreover, the plant ER plays an important role in lipid metabolism (White et al., 2000
Seed storage proteins are all initially synthesized in the ER. The formation of specific disulfide bonds and assembly into dimers or trimers occurs in the ER lumen before sorting to protein storage vacuoles (Gruis et al., 2004
The biochemical and molecular physiological analyses of ER-ANT1, a novel ATP/ADP transporter residing in ER membranes of higher plants, provide the first insights into the physiological importance of the energy supply for the ER–Golgi system. Approximately one-third of all cellular proteins are translocated and processed in the ER lumen, which requires an enormous amount of energy (Shen et al., 2002
Nevertheless, an absolute lack of ATP inside the ER lumen should be lethal for ER-ANT1 knockout mutants. Thus, we predict a low basic ATP supply by an alternative transport system in plant ER membranes. Recently, it was proposed that a voltage-dependent anion channel residing in ER membranes might mediate ATP transport into the ER lumen (Shoshan-Barmatz and Israelson, 2005
Cultivation of Plants Arabidopsis thaliana (ecotype Columbia) plants were grown in a climate-controlled chamber on soil at 22 to 24°C and 120 µmol·m–2·s–1. For short-day growth conditions, light was given for 10 h/d; for long-day conditions, light was present for 16 h/d. For improved root growth of knockout lines, surface-sterilized seeds were sown on Murashige and Skoog plates as described earlier (Reiser et al., 2004 ).
ER-ANT1 Knockout Mutants
cDNA Constructs
Heterologous Expression of ER-ANT1 in E. coli
Staining for GUS Activity
Quantitative Real-Time RT-PCR
Membrane Fractionation and Analyses from Arabidopsis Plants
Immunogold Labeling and Transmission Electron Microscopy
Accession Numbers
Supplemental Data
We gratefully acknowledge critical reading of the manuscript by Zeina Tjaden. We thank Rebecca Boston (North Carolina State University), Wolfgang Michalke (Freiburg University), and Masayoshi Maeshima (Nagoya University) for antibodies. Work in the laboratory of J.T. was financially supported by the Deutsche Forschungsgemeinschaft (Grant TJ 5/1-3) and by the Stiftung Rheinland-Pfalz für Innovation (Grant 15202-386261/766).
1 These authors contributed equally to this work.  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.plantcell.org) is: Joachim Tjaden (tjaden{at}rhrk.uni-kl.de).
[W] Online version contains Web-only data. www.plantcell.org/cgi/doi/10.1105/tpc.107.057554 Received December 14, 2007; Revision received January 25, 2008. accepted February 7, 2008.
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[Lu and Hrabak, 2002
