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First published online December 18, 2003; 10.1104/pp.103.032755 Plant Physiology 134:255-264 (2004) © 2004 American Society of Plant Biologists A Post Genomic Characterization of Arabidopsis Ferredoxins1Division of Enzymology, Osaka University, 3–2 Yamadaoka, Suita, Osaka 565–0871, Japan (G.T.H., Y.K.-A., T.H.); and Department of Applied Chemistry and Biochemistry, Kumammoto University, 2–39–1 Kurokami 860–8555, Japan (I.T.)
In higher plant plastids, ferredoxin (Fd) is the unique soluble electron carrier protein located in the stroma. Consequently, a wide variety of essential metabolic and signaling processes depend upon reduction by Fd. The currently available plant genomes of Arabidopsis and rice (Oryza sativa) contain several genes encoding putative Fds, although little is known about the proteins themselves. To establish whether this variety represents redundancy or specialized function, we have recombinantly expressed and purified the four conventional [2Fe-2S] Fd proteins encoded in the Arabidopsis genome and analyzed their physical and functional properties. Two proteins are leaf type Fds, having relatively low redox potentials and supporting a higher photosynthetic activity. One protein is a root type Fd, being more efficiently reduced under nonphotosynthetic conditions and supporting a higher activity of sulfite reduction. A further Fd has a remarkably positive redox potential and so, although redox active, is limited in redox partners to which it can donate electrons. Immunological analysis indicates that all four proteins are expressed in mature leaves. This holistic view demonstrates how varied and essential soluble electron transfer functions in higher plants are fulfilled through a diversity of Fd proteins.
Ferredoxin (Fd) is a soluble, low Mr protein that mediates transfer of one electron from a donor to an acceptor. The redox active center is a [2Fe-2S] cluster that confers a highly negative redox potential on the protein (-350 to -450 mV), making Fd a powerful reductant. The [2Fe-2S] cluster is ligated by four highly conserved Cys residues.
A broad spectrum of redox metabolism in higher plant plastids involves Fd. Although the name Fd was first used to describe a non-photosynthetic bacterial protein involved in nitrogen fixation (Mortenson et al., 1962
Fds are present as multiple isoforms in many plants and algae (Bertini et al., 2002
One Arabidopsis Fd gene has previously been cloned (Somers et al., 1990 We have recombinantly expressed and purified all conventional [2Fe-2S] Fds encoded in the Arabidopsis genome, and we present here a detailed analysis of the physical and functional properties of the individual proteins, with confirmation of their expression in mature plants.
The Arabidopsis Genome Contains Four Genes Coding for Three Different Types of [2Fe-2S] Fd
Using the amino acid sequence of maize FdI, a National Center for Biotechnology Information BLAST2.0 search of the Arabidopsis genome (http://www.arabidopsis.org) identified six sequences with significant similarity. Of these, four were considered conventional Fds, because they shared more than 35% amino acid identity with maize FdI and conserved most structural features common to [2Fe-2S] Fd proteins from other higher plants (as represented within the 88 sequences compiled by Bertini et al. [2002
The phylogram of mature Fd proteins shown in Figure 1B illustrates further that AtFd1 and AtFd2 are leaf type Fds and AtFd3 is a root type Fd. AtFd4 is grouped close to root type Fds, but the long evolutionary distance makes it unclear whether AtFd4 shares a recent common ancestor with root type Fds. DNA sequences coding for mature AtFd proteins were chemically synthesized, and the proteins were expressed recombinantly in Escherichia coli and then purified for detailed biochemical analysis. We consider the Chloro-P-predicted transit peptide cleavage site for AtFd1 unlikely because it includes residues highly conserved in mature Fds and that of AtFd3 unlikely because it includes seven residues before the conserved N terminus of many mature Fd proteins as determined by chemical sequencing. Therefore the first amino acid for recombinant expression was estimated by comparison with known mature Fd protein sequences and is given in Figure 1A as the first capital letter of AtFd proteins. In the case of AtFd3 and AtFd4, an additional Met residue was introduced as a transcription start site at the N terminus (see supplementary information for full nucleotide sequence details).
Although all expressed AtFd sequences were similar in length and predicted mass (97 amino acids and 10.5 kD, 97 amino acids and 10.4 kD, 99 amino acids and 10.7 kD, and 100 amino acids and 10.9 kD for AtFd1, AtFd2, AtFd3, and AtFd4, respectively), there was wide variation in mobility during SDS-PAGE (Fig. 2A, left panel). Fd proteins contain a high proportion of negatively charged residues, reducing the SDS bound from the standard 1 to 1.4 molecules per peptide bond and resulting in migration to a position of higher perceived molecular mass (Huisman et al., 1978
Fds are known to interact with electron transfer partners mainly through a network of salt bridges (Akashi et al., 1999
The spectra of all purified recombinant AtFd proteins, shown in Figure 2B, are typical of plant Fds, with the exception of a unique red shift in the spectrum of AtFd4 around 340 to 390 nm. We have cultivated AtFd4-expressing bacteria at 37°C, 30°C, and 25°C, which might result in alteration in peptide synthesis and cluster formation, and we observed no variation in the spectra of AtFd4 purified from such cells. We speculate that this red shift may be due to variation from the normal microenvironment of Fd [2Fe-2S] clusters and not a result of the artificial heterologous expression system.
Efficiency of electron transfer between Fd and its partner enzymes is dependent not only on protein-protein interaction but is also determined by the redox potential of the Fd [2Fe-2S] cluster relative to that of its partner enzyme. We therefore measured the redox potential of AtFd proteins by cyclic voltammetry. Figure 3A shows cyclic voltammograms of the current generated when Fd proteins interact with an electrode as its potential is decreased then increased. Calculated redox potentials (Fig. 3B) of AtFd1 and AtFd2 (-425 and -433 mV, respectively) are close to that of maize leaf Fd and considerably lower than the FAD moiety of maize leaf FNR, consistent with the physiological direction of electron flow in photosynthesis. The redox potential of AtFd3 is -337 mV, close to that of maize root type Fd, NADPH, and maize root FNR, and therefore favorable for efficient electron flow from catabolically generated NADPH to Fd, such as occurs in roots. At -152 mV, the redox potential of AtFd4 is remarkably high for a Fd molecule, implying that electron donation would only be efficient to a more restricted number of redox proteins with a similar or still higher redox potential. Other proteins containing plant type [2Fe-2S] clusters do have higher redox potentials than classical leaf and root type Fds, such as mitochondrial adrenodoxin (-250 mV according to Huang and Kimura [1983
Actual measurements of electron transfer are presented in Figure 4, and average kinetic parameters for interaction of AtFds with electron transfer partners are recorded in Table I. We measured a significant difference in the affinity of root and leaf type Fds for electron transport between PSI and leaf type FNR. The leaf type Fds, AtFd1 and AtFd2, have a higher efficiency in mediating transfer of photosynthetic reductant, with Km values approximately 20 times lower than the root type AtFd3. AtFd4 showed no NADP+ photoreduction activity, presumably because its higher redox potential (Fig. 3B) prevented electron donation to leaf type FNR. We consider it likely that AtFd4 is reduced by PSI, because illumination of thylakoids resulted in a AtFd4 concentration-dependent decrease in OD422, consistent with reduction of the [2Fe-2S] cluster (results not shown).
Under non-photosynthetic conditions, Fd is reduced by FNR using NADPH, and this reaction was replicated in vitro with leaf type FNR (Fig. 4B) and with root type FNR (Fig. 4C). Leaf FNR has almost interchangeable kinetic parameters with leaf and root type Fds. However, root type FNR has a comparatively reduced affinity for leaf type Fds AtFd1 and AtFd2. These results are consistent with an efficient role for AtFd3 in transfer of non-photosynthetically derived reductant. AtFd4 shows a very high activity in both of these reactions, combined with a low affinity for both FNR molecules. In this assay, Fd reduces cytochrome c, and the relatively high redox potential of AtFd4 is no barrier to electron transfer, because cytochrome c has an even more positive redox potential of around +250 mV (Margalit and Schejter, 1973 SiR is a Fd-dependent enzyme catalyzing reduction of sulfite to sulfide. Figure 4D shows sulfite reduction supported by a NADPH, root FNR, Fd reduction system. Root type AtFd3 is a more efficient electron donor than leaf type AtFd1 and AtFd2, having a higher activity for this reaction and a higher affinity for SiR. Probably due to its relatively high redox potential, AtFd4 is unable to support sulfite reduction in this system.
To confirm the presence of AtFd proteins in the plant, we performed immunodetection studies using antibodies specific to leaf and root type Fds. Neither antibody reacted efficiently with AtFd4, so we generated a new antibody to detect this protein. As model tissues, we chose mature Arabidopsis leaves and roots and prepared crude extracts from them. The leaf extract was fractionated into 70% saturated (NH4)2SO4 soluble and precipitated fractions. The antibody specific to leaf type Fds detects two bands corresponding to AtFd1 and AtFd2 mainly in the soluble fraction from leaves and not in roots, after SDS-PAGE (Fig. 5A). These leaf proteins also behave similarly to AtFd1 and AtFd2 during native PAGE (data not shown). To further confirm that the two proteins detected by the antibody specific to leaf type Fds are AtFd1 and AtFd2, we compared their chromatographic behaviors with those of recombinant AtFds using an anion exchange column. The two proteins are eluted at an identical NaCl concentration to recombinant AtFd1 and AtFd2 (Fig. 5, B and C).
The specific root type Fd antibody detected a band at a similar position to AtFd3, in the root extract and in the leaf (NH4)2SO4 soluble fraction (Fig. 5A). This assignment was also confirmed by elution profile over anion exchange chromatography, as described above (Fig. 5, B and C), and by comparison of migration over native PAGE (Fig. 5C, ii). The antibody raised against AtFd4 is highly specific, 10 times less recombinant AtFd4 than for all other controls gave a strongly reacting band. Despite this specific, high titer of the antibody, the AtFd4 protein is so scarce in leaf tissues that 7.5 times more leaf protein was loaded onto the gel to detect a protein corresponding to recombinant AtFd4. The protein is detected in the (NH4)2SO4-precipitated fraction, but not in root protein extract. We also confirmed that this protein is eluted in the equivalent fraction to recombinant AtFd4 during anion exchange chromatography (Fig. 5, B and D). Precipitation of leaf AtFd4 in 70% saturated (NH4)2SO4 contrasts with the recombinant protein, although we have observed that a greater proportion of AtFd4 than other AtFds was precipitated by this treatment during purification of recombinant proteins from E. coli. Its entire precipitation may indicate a complex with another protein in vivo, which is still less soluble in solutions of (NH4)2SO4. Densitometric comparison of leaf AtFd signals, obtained on the western blots, with standard curves of recombinant protein, blotted onto the same membrane, indicates that putative AtFd2 is most abundant and comprises around 90% of all leaf Fd, with putative AtFd1 and AtFd3 contributing around 7% and 3%, respectively, whereas the putative AtFd4 makes up just 0.05% of total leaf Fd. The possibility of Fd antibodies cross-reacting with the two Fd-like proteins in the Arabidopsis genome and leading to misidentification of AtFd proteins cannot be absolutely discounted. However, we consider it very unlikely given the number of bands detected, their behavior during PAGE and on anion exchange columns, and the high specificity of the antibodies, IgG reacting to conserved Fd sequences having being removed during antibody purification (see "Materials and Methods").
We have characterized all conventional [2Fe-2S] Fd proteins encoded within the Arabidopsis genome, following recombinant expression and purification. Three basic types of protein are encoded, corresponding to classic leaf type Fds, a classic root type Fd, and a previously undescribed high redox potential type Fd.
Two leaf type Fds, AtFd1 and AtFd2, are present and, in all parameters so far measured, appear very similar. Both leaf type Fds have relatively negative redox potentials and have the highest affinity for NADP+ photoreduction of all of the Fd proteins measured. Using recombinant maize Fd proteins Hase et al. (1991b
AtFd3 is the only root type Fd in the Arabidopsis genome. This is in contrast to maize, where two separate isoforms have been described (Matsumura et al., 1997 In addition to previously described Fd types, the Arabidopsis genome also contains a gene coding for AtFd4, a protein that shares some homology with root type Fds, but is evolutionarily distant. The AtFd4 sequence contains substitutions of two residues known to make a large contribution to the negative redox potential of Fds, and this probably contributes to its remarkably positive redox potential of around -150 mV, which likely prevents it from efficiently donating electrons to FNR or SiR. It is, however, redox active and donates electrons to cytochrome c in assays of leaf type and root type FNR with very high activity. A putative AtFd4 protein was detected at very low levels in mature leaves using an antibody specific for AtFd4, and its salting out behavior in (NH4)2SO4 indicates that it may be complexed to another protein(s) in vivo. Its low expression and our failure to detect it in roots may explain why, as yet, no expressed sequence tag is available. The number of redox proteins to which AtFd4 is capable of donating electrons is much more restricted than for other Fds, so it may have some kind of signaling function, perhaps when expressed in a specific cell type or under certain conditions. These questions would be best answered by a promoter expression study, and the identification of AtFd4-interacting proteins. In conclusion, variation between Arabidopsis Fd sequences has been shown in this study to confer different functional characteristics on the individual proteins. We can now begin to see how different Fd isoproteins have the capacity to support a wide range of physiological roles under varying conditions. Studies of protein-protein interaction and expression pattern will further clarify the physiological roles of separate Fd proteins.
Gene Construction, Recombinant Expression, and Purification
Arabidopsis Fd genomic sequences were identified by a BLAST search of the Arabidopsis Information Resource (http://www.arabidopsis.org/Blast/) using maize (Zea mays) FdI amino acid sequence. Stop codons were confirmed by comparison with cDNAs, where available, and cleavage sites of chloroplast transit peptides were estimated by comparison with known mature sequences. Sixteen oligonucleotides (oligos) of approximately 30 bp, corresponding to the coding and template strands of each mature amino acid sequence, were designed with increased A/T ratio in the first 60 bp from the 5' end to increase expression level in Escherichia coli (Matsumura et al., 1999
Spectra were measured on a UV-2500PC spectrophotometer (Shimadzu, Tokyo). Redox potential was calculated as the midpoint of cyclic voltammetric measurements made at room temperature versus a standard hydrogen electrode at pH 7.5 as described by Taniguchi et al. (1997
Photoreduction of NADP+ was measured at 340 nm in a final volume of 1 mL containing: 50 mM HEPES-NaOH, pH 7.5, 100 mM NaCl, 1 mM MgCl2, 0.2 mM NADP+, 10 µg of chlorophyll spinach (Spinacia oleracea) thylakoid membranes and 0.01 to 40 µM Fd. The assay was started by illuminating the cuvette with an LH7 red light source (Hansatech, Kings Lynn, UK), perpendicular to the light path of the spectrophotometer. Measurements of NADPH-dependent Fd reduction by FNR were performed as described by Onda et al. (2000
Mature leaves and roots from healthy 3-week-old wild-type Arabidopsis plants (Columbia ecotype) were purchased from Green Gold Biosystem (Okayama, Japan). The plants were grown under a 16-h-light (light intensity, 70 µmol m-2 s-1)/8-h-dark regime and treated with fertilizer from Hyponex, Corp. Ltd (Tokyo) with final NH4 and NO3 concentrations of 1.4 and 0.64 mM, respectively. Proteins were extracted into 50 mM Tris-HCl, pH 7.5, 50 mM NaCl, 1 mM MgCl2, 1 mM EDTA, 5% (w/v) polyclar A, 5 mM phenylmethylsulfonyl fluoride, and 1x protease inhibitor cocktail (Nacalai tesque, Kyoto). The extract was desalted, and remaining micelles and thylakoids were precipitated at 30% saturated (NH4)2SO4. A crude Fd fraction was generated by precipitating the majority of proteins at 70% saturated (NH4)2SO4. Precipitated proteins were re-suspended, and both fractions were dialyzed against 50 mM Tris HCl, pH 7.5, and 1 mM MgCl2.
Native gradient PAGE was performed as described by Kimata and Hase (1989
Two milligrams of maize FdI, maize FdIII (purified as described by Matsumura et al. [1999
An ÄKTA prime chromatographic system was used in combination with a RESOURCE Q 6-mL anion exchange column (both from Amersham Biosciences, Tokyo). Proteins were loaded on the column in 50 mM Tris-HCl, pH 7.5, 50 mM NaCl, and 1 mM MgCl2. A mix of 50 µM each recombinant AtFd was used, and peak identity was confirmed by western blotting. Leaf proteins were loaded as the equivalent to 100 mg of total leaf protein. After extensive washing with the same buffer, elution was performed over a 100-mL gradient from 0.05 to 1 M NaCl.
Gene bank accession numbers for Fd genes are AtFd1 (At1g10960), AtFd2 (At1g60950), AtFd3 (At2g27510), AtFd4 (At5g10000), and Arabidopsis Fd-like protein encoding genes (At1g32550, At4g14890). Accession numbers for proteins are, rice (Oryza sativa) leaf (BAA06436, rice root (BAA06456, maize I (P27787), maize II (T01170), maize III (P27788), radish (Raphanus sativus) leaf (JX0088), radish root (P1493), spinach I (P00221), spinach II (P00224), and sweet orange (S62722).
Upon request, all novel materials described in this publication will be made available in a timely manner for noncommercial research purposes, subject to the requisite permission from any third-party owners of all or parts of the material. Obtaining permissions will be the responsibility of the requestor. Received September 8, 2003; returned for revision September 30, 2003; accepted October 12, 2003.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.032755.
1 This work was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (15G50320). * Corresponding author; e-mail enzyme{at}protein.osaka-u.ac.jp; fax 81–6–6879–8613.
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