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Research progress on the biosynthesis and delivery of iron–sulfur clusters in the plastid

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Abstract

Iron–sulfur (Fe–S) clusters are ancient protein cofactors ubiquitously exist in organisms. They are involved in many important life processes. Plastids are semi-autonomous organelles with a double membrane and it is believed to originate from a cyanobacterial endosymbiont. By learning form the research in cyanobacteria, a Fe–S cluster biosynthesis and delivery pathway has been proposed and partly demonstrated in plastids, including iron uptake, sulfur mobilization, Fe–S cluster assembly and delivery. Fe–S clusters are essential for the downstream Fe–S proteins to perform their normal biological functions. Because of the importance of Fe–S proteins in plastid, researchers have made a lot of research progress on this pathway in recent years. This review summarizes the detail research progress made in recent years. In addition, the scientific problems remained in this pathway are also discussed.

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References

  • Balk J, Lobréaux S (2005) Biogenesis of iron–sulfur proteins in plants. Trends Plant Sci 10:324–331

    Article  CAS  PubMed  Google Scholar 

  • Bao Z, Qi X, Hong S et al (2017) Structure and mechanism of a group-I cobalt energy coupling factor transporter. Cell Res 27:675–687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berger N, Vignols F, Przybyla-Toscano J et al (2020a) Identification of client iron–sulfur proteins of the chloroplastic NFU2 transfer protein in Arabidopsis thaliana. J Exp Bot 71:4171–4187

    Article  CAS  PubMed  Google Scholar 

  • Berger N, Vignols F, Touraine B et al (2020b) A Global proteomic approach sheds new light on potential iron-sulfur client proteins of the chloroplastic maturation factor NFU3. Int J Mol Sci 21:8121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Briat J-F, Ravet K, Arnaud N et al (2010) New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants. Ann Bot 105:811–822

    Article  CAS  PubMed  Google Scholar 

  • Cheng N-H, Liu J-Z, Brock A et al (2006) AtGRXcp, an Arabidopsis chloroplastic glutaredoxin, is critical for protection against protein oxidative damage. J Biol Chem 281:26280–26288

    Article  CAS  PubMed  Google Scholar 

  • Conte SS, Lloyd AM (2010) The MAR1 transporter is an opportunistic entry point for antibiotics. Plant Signal Behav 5:49–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conte S, Stevenson D, Furner I, Lloyd A (2009) Multiple antibiotic resistance in Arabidopsis is conferred by mutations in a chloroplast-localized transport protein. Plant Physiol 151:559–573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duy D, Wanner G, Meda AR et al (2007) PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. Plant Cell 19:986–1006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duy D, Stübe R, Wanner G, Philippar K (2011) The chloroplast permease PIC1 regulates plant growth and development by directing homeostasis and transport of iron. Plant Physiol 155:1709–1722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eccleston JF, Petrovic A, Davis CT et al (2006) The kinetic mechanism of the SufC ATPase: the cleavage step is accelerated by SufB. J Biol Chem 281:8371–8378

    Article  CAS  PubMed  Google Scholar 

  • Ferro M, Brugière S, Salvi D et al (2010) AT-CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteomics 9:1063–1084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flint DH, Emptage MH (1988) Dihydroxy acid dehydratase from spinach contains a [2Fe-2S] cluster. J Biol Chem 263:3558–3564

    Article  CAS  PubMed  Google Scholar 

  • Gao H, Subramanian S, Couturier J et al (2013) Arabidopsis thaliana Nfu2 accommodates [2Fe–2S] or [4Fe–4S] clusters and is competent for in vitro maturation of chloroplast [2Fe–2S] and [4Fe–4S] cluster-containing proteins. Biochemistry 52:6633–6645

    Article  CAS  PubMed  Google Scholar 

  • Goldsmith-Fischman S, Kuzin A, Edstrom WC et al (2004) The SufE sulfur-acceptor protein contains a conserved core structure that mediates interdomain interactions in a variety of redox protein complexes. J Mol Biol 344:549–565

    Article  CAS  PubMed  Google Scholar 

  • Gupta V, Sendra M, Naik SG et al (2009) Native Escherichia coli SufA, coexpressed with SufBCDSE, purifies as a [2Fe−2S] protein and acts as an Fe−S transporter to Fe−S target enzymes. J Am Chem Soc 131:6149–6153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirabayashi K, Yuda E, Tanaka N et al (2015) Functional dynamics revealed by the structure of the SufBCD complex, a novel ATP-binding cassette (ABC) protein that serves as a scaffold for iron-sulfur cluster biogenesis. J Biol Chem 290:29717–29731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu X, Kato Y, Sumida A et al (2017) The SUFBC2D complex is required for the biogenesis of all major classes of plastid Fe-S proteins. Plant J 90:235–248

    Article  CAS  PubMed  Google Scholar 

  • Huet G, Daffé M, Saves I (2005) Identification of the Mycobacterium tuberculosis SUF machinery as the exclusive mycobacterial system of [Fe–S] cluster assembly: evidence for its implication in the pathogen’s survival. J Bacteriol 187:6137–6146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeon WB, Cheng J, Ludden PW (2001) Purification and characterization of membrane-associated CooC protein and its functional role in the insertion of nickel into carbon monoxide dehydrogenase from Rhodospirillum rubrum. J Biol Chem 276:38602–38609

    Article  CAS  PubMed  Google Scholar 

  • Jeong J, Guerinot ML (2009) Homing in on iron homeostasis in plants. Trends Plant Sci 14:280–285

    Article  CAS  PubMed  Google Scholar 

  • Jeong J, Cohu C, Kerkeb L et al (2008) Chloroplast Fe (III) chelate reductase activity is essential for seedling viability under iron limiting conditions. Proc Natl Acad Sci 105:10619–10624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson DC, Dean DR, Smith AD, Johnson MK (2005) Structure, function, and formation of biological iron-sulfur clusters. Annu Rev Biochem 74:247–281

    Article  CAS  PubMed  Google Scholar 

  • Kitaoka S, Wada K, Hasegawa Y et al (2006) Crystal structure of Escherichia coli SufC, an ABC-type ATPase component of the SUF iron–sulfur cluster assembly machinery. FEBS Lett 580:137–143

    Article  CAS  PubMed  Google Scholar 

  • Layer G, Gaddam SA, Ayala-Castro CN et al (2007) SufE transfers sulfur from SufS to SufB for iron-sulfur cluster assembly. J Biol Chem 282:13342–13350

    Article  CAS  PubMed  Google Scholar 

  • Léon S, Touraine B, Ribot C et al (2003) Iron-sulphur cluster assembly in plants: distinct NFU proteins in mitochondria and plastids from Arabidopsis thaliana. Biochem J 371:823–830

    Article  PubMed  PubMed Central  Google Scholar 

  • Lezhneva L, Amann K, Meurer J (2004) The universally conserved HCF101 protein is involved in assembly of [4Fe-4S]-cluster-containing complexes in Arabidopsis thaliana chloroplasts. Plant J 37:174–185

    Article  CAS  PubMed  Google Scholar 

  • Lill R (2009) Function and biogenesis of iron–sulphur proteins. Nature 460:831–838

    Article  CAS  PubMed  Google Scholar 

  • Lill R, Mühlenhoff U (2008) Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Annu Rev Biochem 77:669–700

    Article  CAS  PubMed  Google Scholar 

  • Lu J, Yang J, Tan G, Ding H (2008) Complementary roles of SufA and IscA in the biogenesis of iron–sulfur clusters in Escherichia coli. Biochem J 409:535–543

    Article  CAS  PubMed  Google Scholar 

  • Mapolelo DT, Zhang B, Randeniya S et al (2013) Monothiol glutaredoxins and A-type proteins: partners in Fe–S cluster trafficking. Dalt Trans 42:3107–3115

    Article  CAS  Google Scholar 

  • Mihara H, Esaki N (2002) Bacterial cysteine desulfurases: their function and mechanisms. Appl Microbiol Biotechnol 60:12–23

    Article  CAS  PubMed  Google Scholar 

  • Mihara H, Kurihara T, Yoshimura T, Esaki N (2000) Kinetic and mutational studies of three NifS homologs from Escherichia coli: mechanistic difference between l-cysteine desulfurase and l-selenocysteine lyase reactions. J Biochem 127:559–567

    Article  CAS  PubMed  Google Scholar 

  • Mihara H, Fujii T, Kato S et al (2002) Structure of external aldimine of Escherichia coli CsdB, an IscS/NifS homolog: implications for its specificity toward selenocysteine. J Biochem 131:679–685

    Article  CAS  PubMed  Google Scholar 

  • Morrissey J, Baxter IR, Lee J et al (2009) The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. Plant Cell 21:3326–3338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nachin L, Loiseau L, Expert D, Barras F (2003) SufC: an unorthodox cytoplasmic ABC/ATPase required for [Fe-S] biogenesis under oxidative stress. EMBO J 22:427–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narayana Murthy UM, Ollagnier-de-Choudens S, Sanakis Y et al (2007) Characterization of Arabidopsis thaliana SufE2 and SufE3: functions in chloroplast iron–sulfur cluster assembly and NAD synthesis. J Biol Chem 282:18254–18264

    Article  Google Scholar 

  • Nath K, Wessendorf RL, Lu Y (2016) A nitrogen-fixing subunit essential for accumulating 4Fe–4S-containing photosystem I core proteins. Plant Physiol 172:2459–2470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nath K, O’Donnell JP, Lu Y (2017) Chloroplastic iron-sulfur scaffold protein NFU3 is essential to overall plant fitness. Plant Signal Behav 12:e1282023

    Article  PubMed  PubMed Central  Google Scholar 

  • Ollagnier-de Choudens S, Nachin L, Sanakis Y et al (2003) SufA from Erwinia chrysanthemi: Characterization of a scaffold protein required for iron–sulfur cluster assembly. J Biol Chem 278:17993–18001

    Article  CAS  PubMed  Google Scholar 

  • Outten FW, Wood MJ, Muñoz FM, Storz G (2003) 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 278:45713–45719

    Article  CAS  PubMed  Google Scholar 

  • Outten FW, Djaman O, Storz G (2004) A suf operon requirement for Fe–S cluster assembly during iron starvation in Escherichia coli. Mol Microbiol 52:861–872

    Article  CAS  PubMed  Google Scholar 

  • Pilon-Smits EAH, Garifullina GF, Abdel-Ghany S et al (2002) Characterization of a NifS-like chloroplast protein from Arabidopsis. Implications for its role in sulfur and selenium metabolism. Plant Physiol 130:1309–1318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Przybyla-Toscano J, Roland M, Gaymard F et al (2018) Roles and maturation of iron–sulfur proteins in plastids. J Biol Inorg Chem 23:545–566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ranquet C, Ollagnier-de-Choudens S, Loiseau L et al (2007) Cobalt stress in Escherichia coli: the effect on the iron-sulfur proteins. J Biol Chem 282:30442–30451

    Article  CAS  PubMed  Google Scholar 

  • Rempel S, Stanek WK, Slotboom DJ (2019) Energy-coupling factor-type ATP-binding cassette transporters. Annu Rev Biochem 88:551–576

    Article  CAS  PubMed  Google Scholar 

  • Rey P, Becuwe N, Tourrette S, Rouhier N (2017) Involvement of Arabidopsis glutaredoxin S14 in the maintenance of chlorophyll content. Plant Cell Environ 40:2319–2332

    Article  CAS  PubMed  Google Scholar 

  • Roland M, Przybyla-Toscano J, Vignols F et al (2020) The plastidial Arabidopsis thaliana NFU1 protein binds and delivers [4Fe-4S] clusters to specific client proteins. J Biol Chem 295:1727–1742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saini A, Mapolelo DT, Chahal HK et al (2010) SufD and SufC ATPase activity are required for iron acquisition during in vivo Fe-S cluster formation on SufB. Biochemistry 49:9402–9412

    Article  CAS  PubMed  Google Scholar 

  • Satyanarayan MB, Zhao J, Zhang J et al (2021) Functional relationships of three NFU proteins in the biogenesis of chloroplastic iron-sulfur clusters. Plant Direct 5:e00303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schaaf G, Honsbein A, Meda AR et al (2006) AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. J Biol Chem 281:25532–25540

    Article  CAS  PubMed  Google Scholar 

  • Schwenkert S, Netz DJA, Frazzon J et al (2010) Chloroplast HCF101 is a scaffold protein for [4Fe-4S] cluster assembly. Biochem J 425:207–218

    Article  CAS  Google Scholar 

  • Shimoni-Shor E, Hassidim M, YUVAL-NAEH N, Keren NIR, (2010) Disruption of Nap14, a plastid-localized non-intrinsic ABC protein in Arabidopsis thaliana results in the over-accumulation of transition metals and in aberrant chloroplast structures. Plant Cell Environ 33:1029–1038

    Article  CAS  PubMed  Google Scholar 

  • Skovran E, Downs DM (2003) Lack of the ApbC or ApbE protein results in a defect in Fe-S cluster metabolism in Salmonella enterica serovar Typhimurium. J Bacteriol 185:98–106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solti Á, Kovács K, Müller B et al (2016) Does a voltage-sensitive outer envelope transport mechanism contributes to the chloroplast iron uptake? Planta 244:1303–1313

    Article  CAS  PubMed  Google Scholar 

  • Takahashi Y, Tokumoto U (2002) A Third bacterial system for the assembly of iron-sulfur clusters with homologs in Archaea and plastids. J Biol Chem 277:28380–28383

    Article  CAS  PubMed  Google Scholar 

  • Tarantino D, Morandini P, Ramirez L et al (2011) Identification of an Arabidopsis mitoferrinlike carrier protein involved in Fe metabolism. Plant Physiol Biochem 49:520–529

    Article  CAS  PubMed  Google Scholar 

  • Tokumoto U, Kitamura S, Fukuyama K, Takahashi Y (2004) Interchangeability and distinct properties of bacterial Fe-S cluster assembly systems: functional replacement of the isc and suf operons in Escherichia coli with the nifSU-like operon from Helicobacter pylori. J Biochem 136:199–209

    Article  CAS  PubMed  Google Scholar 

  • Touraine B, Boutin J, Marion-Poll A et al (2004) Nfu2: a scaffold protein required for [4Fe–4S] and ferredoxin iron-sulphur cluster assembly in Arabidopsis chloroplasts. Plant J 40:101–111

    Article  CAS  PubMed  Google Scholar 

  • Touraine B, Vignols F, Przybyla-Toscano J et al (2019) Iron–sulfur protein NFU2 is required for branched-chain amino acid synthesis in Arabidopsis roots. J Exp Bot 70:1875–1889

    Article  CAS  PubMed  Google Scholar 

  • Van Hoewyk D, Abdel-Ghany SE, Cohu CM et al (2007) Chloroplast iron-sulfur cluster protein maturation requires the essential cysteine desulfurase CpNifS. Proc Natl Acad Sci 104:5686–5691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verrier PJ, Bird D, Burla B et al (2008) Plant ABC proteins–a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159

    Article  CAS  PubMed  Google Scholar 

  • Vigani G, Solti Á, Thomine S, Philippar K (2019) Essential and detrimental—an update on intracellular iron trafficking and homeostasis. Plant Cell Physiol 60:1420–1439

    Article  CAS  PubMed  Google Scholar 

  • Vinella D, Brochier-Armanet C, Loiseau L et al (2009) Iron-sulfur (Fe/S) protein biogenesis: phylogenomic and genetic studies of A-type carriers. PLoS Genet 5:e1000497

    Article  PubMed  PubMed Central  Google Scholar 

  • von Lena V, Jiyoung P, Roland S et al (2019) A Novel prokaryote-Type ECF/ABC transporter module in chloroplast metal homeostasis. Front Plant Sci 10:e1264

    Article  Google Scholar 

  • Wollers S, Layer G, Garcia-Serres R et al (2010) Iron-sulfur (Fe-S) cluster assembly: the SufBCD complex is a new type of Fe-S scaffold with a flavin redox cofactor. J Biol Chem 285:23331–23341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu XM, Møller SG (2006) AtSufE is an essential activator of plastidic and mitochondrial desulfurases in Arabidopsis. EMBO J 25:900–909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yabe T, Morimoto K, Kikuchi S et al (2004) The Arabidopsis chloroplastic NifU-like protein CnfU, which can act as an iron-sulfur cluster scaffold protein, is required for biogenesis of ferredoxin and photosystem I. Plant Cell 16:993–1007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye H, Abdel-Ghany SE, Anderson TD et al (2006) CpSufE activates the cysteine desulfurase CpNifS for chloroplastic Fe-S cluster formation. J Biol Chem 281:8958–8969

    Article  CAS  PubMed  Google Scholar 

  • Yuda E, Tanaka N, Fujishiro T et al (2017) Mapping the key residues of SufB and SufD essential for biosynthesis of iron-sulfur clusters. Sci Rep 7:e9387

    Article  Google Scholar 

  • Zhang J, Bai Z, Ouyang M et al (2021) The DnaJ proteins DJA6 and DJA5 are essential for chloroplast iron–sulfur cluster biogenesis. EMBO J 40:e106742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by the National Natural Science Foundation of China under Grant No. 32000197, the China Postdoctoral Science Foundation under Grant No. 2019T120467.

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Authors and Affiliations

  1. International Research Laboratory of Agriculture and Agri-Product Safety of the Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China

    Bing Yang, Chenyun Xu, Yuting Cheng, Ting Jia & Xueyun Hu

  2. Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou, 225009, China

    Bing Yang, Chenyun Xu, Yuting Cheng & Xueyun Hu

  3. College of Bioscience and Biotechnology, Yangzhou University, Yangzhou, 225009, China

    Bing Yang, Chenyun Xu, Yuting Cheng & Xueyun Hu

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  1. Bing Yang
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  2. Chenyun Xu
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  3. Yuting Cheng
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  4. Ting Jia
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TJ and XH conceived the idea. BY, CX, YC, TJ and XH wrote and evaluated the manuscript.

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Correspondence to Ting Jia or Xueyun Hu.

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Communicated by Wusheng Liu.

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Yang, B., Xu, C., Cheng, Y. et al. Research progress on the biosynthesis and delivery of iron–sulfur clusters in the plastid. Plant Cell Rep 42, 1255–1264 (2023). https://doi.org/10.1007/s00299-023-03024-7

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