FdC1, a Novel Ferredoxin Protein Capable of Alternative Electron Partitioning, Increases in Conditions of Acceptor Limitation at Photosystem I

Abstract

In higher plants, [2Fe-2S] ferredoxin (Fd) proteins are the unique electron acceptors from photosystem I (PSI).. Whereas FdC1 was capable of electron transfer with FNR, redox potentiometry showed that it had a more positive redox potential than photosynthetic Fds by around 220 mV. These results indicate that FdC1 electron donation to FNR is prevented because it is thermodynamically unfavorable. Based on our data, we speculate that FdC1 has a specific function in conditions of acceptor limitation at PSI, and channels electrons away from NADP ؉ photoreduction.Ferredoxins (Fds) 3 are small soluble electron carrier proteins. In the final reaction of photosynthetic electron transfer (PET), photosystem I (PSI) donates electrons to Fd (1), which acts as the soluble electron donor to various acceptors in the chloroplast stroma and can also return electrons to the thylakoid in cyclic electron flow (CET) (2). The electron cascade to supply carbon fixation requires photoreduction of NADP ϩ by Fd, catalyzed by Fd-NADP(H) oxidoreductase (FNR) (3). Many other plastid enzymes accept electrons directly from Fd for metabolic processes. These include, but are not limited to, nitrite reductase and sulfite reductase, which are essential for assimilation of inorganic nitrogen and sulfur, respectively, and Fd-dependent glutamine oxoglutarate aminotransferase and fatty acid desaturase, which catalyze key steps in amino acid and fatty acid metabolism, respectively (4). In addition, Fd donation to thioredoxin via the Fd:thioredoxin reductase translates the redox state of the electron transfer chain into a regulatory signal controlling the activity of many enzymes (5). Fds are also capable of accepting electrons from NADPH via FNR, in a reversal of the photosynthetic reaction (6), allowing electron donation from reduced Fd to different acceptors under non-photosynthetic conditions. Most higher plants studied possess genes for several different Fd isoproteins (7-9). There is always an isoprotein that is more abundant in non-photosynthetic tissues and has higher affinity than photosynthetic and PetF-type Fds for FNR in the non-photosynthetic (often called "root") cascade (9, 10), where electrons are transferred from NADPH to Fd. In all plants for which we possess significant EST and cDNA information at least 2 separate photosynthetic isoproteins have been identified (7,8). In the C4-plant maize, different functions have been identified for two of the leaf-type Fds (11). There is a higher demand for ATP (which is disproportionately produced in CET) in the bundle sheath cells of NADP ϩ malic enzyme type C4 plants, and maize FdI and FdII are differentially expressed in mesophyll and bundle sheath cells, respectively (12). FdII has decreased affinity for FNR (13) and demonstrates a higher activity in CET around the photosystems, whereas FdI drives linear electron flow (11). In C3 plants, this spatial distribution is not observed, but duplicate photosynthetic Fds are still present, and there is some evi-* This work was supported by Deutsche For...

A Program for Iron Economy during Deficiency Targets Specific Fe Proteins

“…There are several FDX isoforms in Arabidopsis (Hanke et al, 2004). Due to the possible partial redundancy of ferredoxin isoforms, mutants in FDX2 show mild phenotypes (Hanke and Hase, 2008;Voss et al, 2011). This may also explain why in Fe deficiency we see FDX2 protein decrease early (day 2), but we do not see effects on photosynthesis until later (day 4) when also the cytochrome-b 6 f complex and to a lesser extent PSI and the NDHK subunit of the NDH complex become affected.…”

“…Genetic loss of FDX2 is reported to result in mild phenotypes and affected mainly photoreduction of NADP, while cyclic electron flow via the less abundant FDX1 isoform or alternative Fe-S proteins may help maintain NPQ in FDX2 mutants (Voss et al, 2011;Liu et al, 2013). Chlorophyll fluorescence measurements indicated that both FPSII, which is indicative of linear electron flow, and NPQ, which depends on both linear and cyclic electron flow (Maxwell and Johnson, 2000), are affected by Fe deficiency.…”

“…Does the down-regulation of FDX2 make sense in the context of Fe economy? In regard to this question, it is of interest to see if photosynthesis-related symptoms of Fe deficiency resemble published phenotypes of ferredoxin mutants (Hanke and Hase, 2008;Voss et al, 2011;Liu et al, 2013). There are several FDX isoforms in Arabidopsis (Hanke et al, 2004).…”

N-Terminal Structure of Maize Ferredoxin:NADP+ Reductase Determines Recruitment into Different Thylakoid Membrane Complexes

“…Arabidopsis thaliana plants were all Columbia ecotype and grown under long-day conditions, basically as described previously (Voss et al, 2011). Membrane and soluble protein fractions were prepared from whole plants and isolated chloroplasts and subjected to native-PAGE or SDS-PAGE and immunoblotting as described previously .…”

Expression of the Minor Isoform Pea Ferredoxin in Tobacco Alters Photosynthetic Electron Partitioning and Enhances Cyclic Electron Flow

“…Higher-plant Fds are encoded by a small gene family, with distinct isoforms present in chloroplasts and nonphotosynthetic plastids (Hanke et al, 2004;Voss et al, 2008Voss et al, , 2011. Chloroplasts from C3 plants contain at least two isoforms that accumulate to different levels and share a high degree of sequence identity (Hanke et al, 2004).…”