Trends in Plant Science
Biogenesis of iron–sulfur proteins in plants
Section snippets
Fe–S protein biogenesis in the photosynthetic eukaryote
Iron–sulfur (Fe–S) clusters are chemically simple but functionally versatile, prosthetic groups of proteins that are central to the basic processes of life, including photosynthesis, respiration and nitrogen fixation. These co-factors were identified ∼40 years ago; spinach ferredoxin was one of the first Fe–S proteins to be described 1, 2. For a long time it was thought that Fe–S proteins assembled spontaneously because this could be achieved chemically in a reaction tube. A growing number of
Fe–S cluster proteins
As the name indicates, Fe–S clusters are built of iron and acid-labile sulfide. Different types of clusters have been described, the [2Fe–2S] and the [4Fe–4S] clusters being the more commonly encountered (Figure 1a) (reviewed in Ref. [3]). Fe–S clusters are usually bound to the polypeptide chain through the interaction of the iron atoms with cysteine residues. Exceptions include the Rieske proteins, where the [2Fe–2S] cluster is ligated by two cysteines and two histidines. The chemical
Biogenesis of Fe–S proteins
The assembly of biological Fe–S clusters in bacteria and yeast has recently been reviewed in some detail 16, 17, therefore only a brief summary is given here. For a summary of the older literature on chloroplasts and cyanobacteria, see Ref. [18]. Fe–S clusters can be assembled in apoproteins in vitro in the presence of S2−, Fe2+ or Fe3+, and a thiol compound, such as dithiothreitol [19]. However, the conditions are unlikely to resemble Fe–S co-factor assembly in vivo because sulfide and ferric
Plastids
In vitro import studies of the ferredoxin precursor have demonstrated the ability of chloroplasts to mature the imported apo-protein into a functional holo-ferredoxin [22]. Moreover, Yasuhiro Takahashi et al. pioneered the Fe–S biogenesis process in intact [21] and lysed 42, 43 spinach chloroplasts using apo-ferredoxin and 35S labelled cysteine as a sulfur donor. Their results revealed the existence of an Fe–S assembly process in the stroma that was dependent on both ATP and light-derived
Plant mitochondria
One of the two NifS-like proteins encoded in the nuclear genome of Arabidopsis is localized in the mitochondria [44] (Table 2 and Figure 2). AtNFS1 is a group I cysteine desulfurase, as opposed to the group II (SufS-like) enzyme residing in the plastids. The potato NFS1 homologue was purified from a mitochondrial matrix protein fraction as a component facilitating the last step of biotin synthesis [60]. Supported by the recently solved crystal structure of biotin synthase [6], it is most likely
Conclusions
There is now sufficient evidence to state that both plastids and mitochondria are capable of assembling their resident Fe–S proteins. This is an important function of these organelles that became evident from recent reports on ‘primitive’ organisms that have lost the capacity for photosynthesis or respiration. Surprisingly, the malaria parasite has kept its apicoplasts [72] and Giardia does have mitochondria after all [73] – their dressed-down organelles appear to have retained the Fe–S cluster
Acknowledgements
We are grateful to The Royal Society (UK) and CNRS for funding our research positions. We apologize for not being able to cite all articles touching on Fe–S protein biogenesis in plants.
References (75)
Electron spin resonance spectra of spinach ferredoxin
Biochem. Biophys. Res. Commun.
(1966)- et al.
On the magnetic resonance of spinach ferredoxin
J. Biol. Chem.
(1966) Iron–sulfur clusters: formation, perturbation, and physiological functions
Plant Physiol. Biochem.
(1999)S-adenosylmethionine radical enzymes
Bioorg. Chem.
(2004)- et al.
Fe–S proteins in sensing and regulatory functions
Curr. Opin. Chem. Biol.
(1999) Balancing acts: molecular control of mammalian iron metabolism
Cell
(2004)- et al.
A role for iron–sulfur clusters in DNA repair
Curr. Opin. Chem. Biol.
(2005) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis
Cell
(2002)ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase
Cell
(2002)- et al.
Iron–sulfur-protein biogenesis in eukaryotes
Trends Biochem. Sci.
(2005)
The reconstitution of clostridial ferredoxin
Biochem. Biophys. Res. Commun.
A novel L-cysteine/cystine C–S-lyase directing [2Fe–2S] cluster formation of Synechocystis ferredoxin
J. Biol. Chem.
Studies on the synthesis of the Fe–S cluster of dihydroxy-acid dehydratase in Escherichia coli crude extract – isolation of O-acetylserine sulfhydrylases A and B and beta-cystathionase based on their ability to mobilize sulfur from cysteine and to participate in Fe–S cluster synthesis
J. Biol. Chem.
Characterization of iron–sulfur protein assembly in isolated mitochondria. A requirement for ATP, NADH, and reduced iron
J. Biol. Chem.
Formation of iron–sulfur clusters in bacteria – an emerging field in bioinorganic chemistry
Curr. Opin. Chem. Biol.
Assembly of iron–sulfur clusters – identification of an iscSUA–hscBA–fdx gene cluster from Azotobacter vinelandii
J. Biol. Chem.
Biogenesis of iron–sulfur proteins in eukaryotes: a novel task of mitochondria that is inherited from bacteria
Biochim. Biophys. Acta
A third bacterial system for the assembly of iron–sulfur clusters with homologs in Archaea and plastids
J. Biol. Chem.
Biogenesis of Fe–S cluster by the bacterial Suf system: SufS and SufE form a new type of cysteine desulfurase
J. Biol. Chem.
The SufE protein and the SufBCD complex enhance SufS cysteine desulfurase activity as part of a sulfur transfer pathway for Fe–S cluster assembly in Escherichia coli
J. Biol. Chem.
SufA from Erwinia chrysanthemi: characterization of a scaffold protein required for iron–sulfur cluster assembly
J. Biol. Chem.
Iron–molybdenum cofactor biosynthesis in Azotobacter vinelandii requires the iron protein of nitrogenase
J. Biol. Chem.
Evolution and classification of P-loop kinases and related proteins
J. Mol. Biol.
AtNAP1 represents an atypical SufB protein in Arabidopsis plastids
J. Biol. Chem.
Unique genetic compartmentalization of the SUF system in cryptophytes and characterization of a SufD mutant in Arabidopsis thaliana
FEBS Lett.
A novel protein for photosystem I biogenesis
J. Biol. Chem.
The plant biotin synthase reaction. Identification and characterization of essential mitochondrial accessory protein components
J. Biol. Chem.
Isolation and characterization of Arabidopsis thaliana ISU1 gene
Biochim. Biophys. Acta
Functional and molecular characterization of the frataxin homolog from Arabidopsis thaliana
FEBS Lett.
The plant ABC transporter superfamily: the functions of a few and identities of many
Unique features of plant mitochondrial sulfhydryl oxidase
J. Biol. Chem.
Assembly of photosystem I. II. Rubredoxin is required for the in vivo assembly of F(X) in Synechococcus sp. PCC 7002 as shown by optical and EPR spectroscopy
J. Biol. Chem.
Iron–sulfur proteins: ancient structures, still full of surprises
J. Biol. Inorg. Chem.
Crystal structure of biotin synthase, an S-adenosylmethionine-dependent radical enzyme
Science
Iron regulatory proteins and the molecular control of mammalian iron metabolism
Annu. Rev. Nutr.
The chloroplastic protein import machinery contains a Rieske-type iron–sulfur cluster and a mononuclear iron-binding protein
EMBO J.
Protein import into chloroplasts involves redox-regulated proteins
EMBO J.
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