Trends in Plant Science
ReviewAncient and essential: the assembly of iron–sulfur clusters in plants
Section snippets
The basics of Fe–S cluster assembly
Iron–sulfur (Fe–S) clusters are cofactors of proteins that function in vital processes such as respiration, photosynthesis, sulfur and nitrogen assimilation, amino acid and purine metabolism, plant hormone and coenzyme synthesis, DNA repair and translation (see Box 1 and Supplementary Table S1). Plants and algae are particularly rich in Fe–S proteins, both in diversity and abundance, owing to their photo-autotrophic life style. Fe–S proteins are found in the plastids, mitochondria, cytosol and
The sulfur mobilization (SUF)-like machinery in the plastids
Chloroplasts harbor their own Fe–S cluster assembly system (Table 1) which was largely inherited from their cyanobacterial evolutionary ancestor. The source of sulfur is cysteine but the source of Fe is not known. Although it has been assumed that the iron-sequestering protein ferritin could be a source of Fe it is now clear that this is not the case from the analysis of Arabidopsis triple ferritin mutants [14]. By contrast, it seems that ferritin serves to sequester iron in order to prevent
The plastid contains several scaffolds and carrier proteins
A number of plastid proteins have been identified that bind and transfer Fe–S clusters in vitro, and could function either as a scaffold for cluster assembly or as carrier/transfer proteins. These are the SUFBCD complex, NFU1-3, HCF101, SUFA (CpISCA), GRXS14 or GRXS16 (Table 1 and Figure 1a).
The SUFBCD proteins are best characterized in E. coli. They form a BC2D complex with structural homology to non-integral ABC proteins. SufB can assemble a labile 4Fe–4S cluster, and binds FADH2 [26]. The BC2
The iron–sulfur cluster (ISC) pathway in the mitochondria
Plant mitochondria operate the so-called ISC pathway for the assembly of Fe–S clusters (Table 2 and Figure 1b). Key features of this pathway are a group-I cysteine desulfurase [18], and a single-domain scaffold protein (IscU/ISU). The isc gene cluster in E. coli also encodes an IscA protein, chaperones and ferredoxin [48], whereas additional proteins assisting the core machinery have been identified in yeast mitochondria 1, 10.
In the first stage of cluster assembly, persulfide is delivered by
Mitochondrial dependence and the emerging cytosolic iron–sulfur cluster assembly (CIA) pathway in the cytosol
Direct functional evidence for the cytosolic Fe–S cluster assembly pathway in plants is fragmentary, but a number of recent reports indicate that the situation is similar to that in Baker's yeast: (i) Cytosolic Fe–S proteins depend on ISC components and a mitochondrial ABC transporter; (ii) localization results show that most ISC proteins are exclusively mitochondrial (except HSCB and HSCA1 [56]); and (iii) highly conserved CIA proteins are present in the cytosol (Table 2 and Figure 1c).
The
Conclusions and future prospects
A fairly complete draft of the pathways of Fe–S cluster assembly in the plastids, mitochondria and cytosol is now available. The plastids generate Fe–S clusters for their own requirements, whereas the mitochondria provide both their resident clusters and play a role in the assembly of cytosolic/nuclear Fe–S proteins. The general localization of the SUF proteins to the plastids and the ISC proteins to the mitochondria reflects their inheritance through their cyanobacterial and α-proteobacterial
Acknowledgements
Janneke Balk is supported by a University Research Fellowship from the Royal Society. Her research on Fe–S protein biogenesis is supported by grants from the EU FP7, BBSRC and the Wellcome Trust. Research in the laboratory of Marinus Pilon is supported by a grant from the US National Science Foundation (Grant # NSF-MCB 0950726). We would like to thank Delphine Bernard and the reviewers for helpful comments to the manuscript and figures.
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2022, Plant Physiology and BiochemistryCitation Excerpt :Compared with previous reports, we found that the gene members involved in the Fe-S cluster assembly mechanism are slightly different among distinct plant species (Table 2). Compared with annual plants, like Arabidopsis (Balk and Pilon, 2011), rice (Liang et al., 2014) and soybean (Qin et al., 2015), strawberry genome lacks genes encoding scaffold proteins, such as ISU2, ISU3 and NFU5 (Table 2). In particular, the expression levels of ISU3 and NFU5 genes in Arabidopsis were extremely low, and these two genes may be pseudogenes or have no specific functions (Leon et al., 2003), implying that non-functional scaffold proteins in plant mitochondrial ISC assembly machinery are more likely to be lost during the long-term evolution, and a smaller number of active scaffold proteins may be used in the Fe metabolism of perennial fruit crops, including strawberry and peach (Song et al., 2014b).