Light-regulated expression of the Arabidopsis thaliana ferredoxin A gene involves both transcriptional and post-transcriptional processes

Vorst, Oscar; Dam, Frans; Weisbeek, Peter; Smeekens, Sjef

doi:10.1046/j.1365-313x.1993.03060793.x

Cited by 22 publications

(31 citation statements)

References 13 publications

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“…On alignment (see Fig. 1A), AtFd1 and AtFd2 share many residues specific to leaf type Fds, and in support of this, light regulation of the AtFd2 gene has been reported (Vorst et al, 1993). On the basis of amino acid sequence comparison, AtFd3 encodes a typical root type Fd, and Wang et al (2000) found expression of this gene was nitrate inducible, reminiscent of a root type Fd from maize (Matsumura et al, 1997).…”

Section: The Arabidopsis Genome Contains Four Genes Coding For Three mentioning

confidence: 66%

“…Work using maize (Zea mays) has exposed functional differences between these Fd types; the rate of light-dependent NADP ϩ reduction being higher with leaf type (photosynthetic) than root type (non-photosynthetic), and the root type being more efficiently reduced by NADPH than the leaf type (Hase et al, 1991b;Onda et al, 2000). In addition, root type Fd was found to mediate a more efficient electron flow from FNR to SiR, in a reconstruction of the root type sulfite reduction electron cascade (Yonekura-Sakakibara et al, 2000).One Arabidopsis Fd gene has previously been cloned (Somers et al, 1990), and its expression was found to be light regulated and specific to chloroplast-containing tissues (Vorst et al, 1993). A second Arabidopsis Fd gene is up-regulated in response to nitrogen availability (Wang et al, 2000).…”

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“…One Arabidopsis Fd gene has previously been cloned (Somers et al, 1990), and its expression was found to be light regulated and specific to chloroplast-containing tissues (Vorst et al, 1993). A second Arabidopsis Fd gene is up-regulated in response to nitrogen availability (Wang et al, 2000).…”

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A Post Genomic Characterization of Arabidopsis Ferredoxins

et al. 2004

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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 M r 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 (Ϫ350 to Ϫ450 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), Fd is best known for a photosynthetic role: accepting electrons from photosystem I (PSI) and donating them to the enzyme Fd:NADP ϩ oxidoreductase (FNR) for photoreduction of NADP ϩ (Arnon, 1989). Donation of electrons by Fd has now been demonstrated to many other plastid enzymes essential for cellular processes, including nitrogen assimilation (nitrite reductase), sulfur assimilation (sulfite reductase [SiR]), amino acid synthesis (Glnoxoglutarate amino transferase), fatty acid synthesis (fatty acid desaturase), and redox regulation (Fd: thioredoxin reductase) (Knaff, 1996). In addition to PSI, Fd may be reduced by NADPH oxidation in a reversal of the FNR reaction (Suzuki et al., 1985). This enables Fd-dependent metabolism to continue under non-photosynthetic conditions, such as in root plastids.Fds are present as multiple isoforms in many plants and algae (Bertini et al., 2002). In higher plants, those predominantly expressed in photosynthetic tissues can be crudely divided from those that are not on the basis of primary sequence (Wada et al., 1986). Work using maize (Zea mays) has exposed functional differences between these Fd types; the rate of light-dependent NA...

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Section: The Arabidopsis Genome Contains Four Genes Coding For Three mentioning

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A Post Genomic Characterization of Arabidopsis Ferredoxins

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“…Arabidopsis, changes in mRNA abundance in light-grown versus dark-adapted plants occur in the absence of corresponding changes in the transcriptional activity of isolated nuclei (Dickey et ai., 1992b;Vorst et al, 1993), and the 5' portion of a pea Fed-7::GUS (P-glucuronidase) chimeric mRNA is stabilized in the light, whereas reporter sequences in the 3' portion of the transcript are degraded (Dickey et al, 1992b).…”

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“…However, other data provide indirect support for a post-transcriptional model. In both tobacco andTo whom correspondence should be addressed.Arabidopsis, changes in mRNA abundance in light-grown versus dark-adapted plants occur in the absence of corresponding changes in the transcriptional activity of isolated nuclei (Dickey et ai., 1992b;Vorst et al, 1993), and the 5' portion of a pea Fed-7::GUS (P-glucuronidase) chimeric mRNA is stabilized in the light, whereas reporter sequences in the 3' portion of the transcript are degraded (Dickey et al, 1992b).Recent reports indicate that the stability of an mRNA often depends on its translational activity, whereas in other cases, translation may be required for rapid mRNA turnover (for reviews, see Cleveland and Yen, 1989;Gallie, 1993;Sachs, 1993;Sullivan and Green, 1993). Recent reports using polysome-based in vitro mRNA degradation systems suggest that in some of these cases, mRNA turnover may be linked to translation (Brewer and Ross, 1990;Byrne et al, 1993;Tanzer and Meagher, 1994).…”

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Light modulation of ferredoxin mRNA abundance requires an open reading frame.

et al. 1994

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Ferredoxin I (Fed-l) mRNA abundance is modulated by an Interna1 light regulatory element that includes sequences both L'and 3'of the translational initiation site. To test the hypothesis that the light response mediated by this element might be coupled to translation, we transformed tobacco plants with gene constructs blocked in translational initiation or elongation. Here, we report that such mutations abollsh the light response ln vivo. A nonsense mutation could be rescued by restorlng the open reading frame with a different sequence, even when the new codon caused an amino acld substitution. Our data establlsh that the light response requires a translatable reading frame and thus pmvide strong circumstantial evidence for post-transcriptional modulation of Fed-1 mRNA levels. The Fed-1 system 1s presently the only higher plant example of a developmentally regulated change in mRNA abundance that requires translation of the affected mRNA. INTRODUCTIONFerredoxin I (Fed-7) is a nuclear gene encoding chloroplast ferredoxin in Pisum (Dobres et al., 1987; Dickey et al., 1992a). Like most genes encoding plastid proteins, Fed-7 is expressed more strongly in the light than in the dark. However, its light response differs in severa1 respects from those of other wellcharacterized light-responsive genes (Kaufman et al., 1986) and involves different molecular events (Thompson, 1988;Thompson and White, 1991;Neuhaus et al., 1993). Among the important differences is the fact that a major light response element in the pea Fed-7 gene is located within the transcription unit (Elliott et al., 1989), while other light-responsive genes are regulated mainly by upstream elements (Thompson and White, 1991;Kuhlemeier, 1992). We have recently shown that the Fed-7 interna1 light regulatory element (iLRE) is located within the 5' portion of the transcribed sequence and that it includes portions of both the leader and coding region (Dickey et ai., 1992b).The location of the Fed-7 iLRE within the transcribed portion of an intronless gene rules out transcriptional regulatory mechanisms that depend on upstream control elements and is consistent with models in which light modulates mRNA abundance by directly or indirectly affecting its rate of degradation. Direct observation of a light effect on mRNA stability has thus far been prevented by the fact that Ad-7 mRNA is stabilized when cellular RNA synthesis is inhibited by actinomycin-D (G.C. Allen, unpublished data). However, other data provide indirect support for a post-transcriptional model. In both tobacco andTo whom correspondence should be addressed.Arabidopsis, changes in mRNA abundance in light-grown versus dark-adapted plants occur in the absence of corresponding changes in the transcriptional activity of isolated nuclei (Dickey et ai., 1992b;Vorst et al., 1993), and the 5' portion of a pea Fed-7::GUS (P-glucuronidase) chimeric mRNA is stabilized in the light, whereas reporter sequences in the 3' portion of the transcript are degraded (Dickey et al., 1992b).Recent reports indicate that ...

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Light-regulated expression of the Arabidopsis thaliana ferredoxin gene requires sequences upstream and downstream of the transcription initiation site

et al. 1995

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The effect of light on the expression of the Arabidopsis thaliana ferredoxin gene (fedA) was studied in mature tobacco plants. In light-treated leaves of tobacco plants transformed with a full-length ferredoxin gene, fedA-specific mRNA levels were more than twenty fold higher than in dark-treated controls. This indicates that all components for regulation of the Arabidopsis ferredoxin gene are present in tobacco. To identify light-regulatory elements in the fedA gene, we have tested a set of chimeric genes containing various parts of the fedA gene for light-dependent expression in mature tobacco plants. A fedA promoter-GUS fusion gene was not light-responsive, indicating that the 5'-upstream promoter region is not sufficient for light regulation. Fusion genes in which different transcribed regions of the fedA gene were expressed from the CaMV 35S promoter showed only limited light regulation, if any at all. This indicates that, like the fedA upstream region, the region downstream of the transcription start site is also not sufficient for full light regulation. The combined results suggest that for full light-regulated expression of the fedA gene, both the promoter region and sequences downstream of the transcription start site are required.

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Light-regulated expression of the Arabidopsis thaliana ferredoxin A gene involves both transcriptional and post-transcriptional processes

Cited by 22 publications

References 13 publications

A Post Genomic Characterization of Arabidopsis Ferredoxins

A Post Genomic Characterization of Arabidopsis Ferredoxins

Light modulation of ferredoxin mRNA abundance requires an open reading frame.

Light-regulated expression of the Arabidopsis thaliana ferredoxin gene requires sequences upstream and downstream of the transcription initiation site

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