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


Journal

Plant cell reports
ISSN: 1432-203X
Titre abrégé: Plant Cell Rep
Pays: Germany
ID NLM: 9880970

Informations de publication

Date de publication:
Aug 2023
Historique:
received: 28 01 2023
accepted: 27 04 2023
medline: 17 7 2023
pubmed: 10 5 2023
entrez: 10 5 2023
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 37160773
doi: 10.1007/s00299-023-03024-7
pii: 10.1007/s00299-023-03024-7
doi:

Substances chimiques

Iron E1UOL152H7
Sulfur 70FD1KFU70
Iron-Sulfur Proteins 0

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

1255-1264

Subventions

Organisme : National Natural Science Foundation of China
ID : 32000197
Organisme : China Postdoctoral Science Foundation
ID : 2019T120467

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Balk J, Lobréaux S (2005) Biogenesis of iron–sulfur proteins in plants. Trends Plant Sci 10:324–331
pubmed: 15951221 doi: 10.1016/j.tplants.2005.05.002
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
pubmed: 28322252 pmcid: 5520853 doi: 10.1038/cr.2017.38
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
pubmed: 32240305 doi: 10.1093/jxb/eraa166
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
pubmed: 33143294 pmcid: 7672563 doi: 10.3390/ijms21218121
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
pubmed: 19482877 doi: 10.1093/aob/mcp128
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
pubmed: 16829529 doi: 10.1074/jbc.M601354200
Conte SS, Lloyd AM (2010) The MAR1 transporter is an opportunistic entry point for antibiotics. Plant Signal Behav 5:49–52
pubmed: 20592808 pmcid: 2835957 doi: 10.4161/psb.5.1.10142
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
pubmed: 19675150 pmcid: 2754617 doi: 10.1104/pp.109.143487
Duy D, Wanner G, Meda AR et al (2007) PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. Plant Cell 19:986–1006
pubmed: 17337631 pmcid: 1867359 doi: 10.1105/tpc.106.047407
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
pubmed: 21343424 pmcid: 3091129 doi: 10.1104/pp.110.170233
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
pubmed: 16431905 doi: 10.1074/jbc.M513455200
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
pubmed: 20061580 pmcid: 2877971 doi: 10.1074/mcp.M900325-MCP200
Flint DH, Emptage MH (1988) Dihydroxy acid dehydratase from spinach contains a [2Fe-2S] cluster. J Biol Chem 263:3558–3564
pubmed: 2831190 doi: 10.1016/S0021-9258(18)68961-6
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
pubmed: 24032747 doi: 10.1021/bi4007622
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
pubmed: 15522304 doi: 10.1016/j.jmb.2004.08.074
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
pubmed: 19366265 pmcid: 2677299 doi: 10.1021/ja807551e
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
pubmed: 26472926 pmcid: 4705970 doi: 10.1074/jbc.M115.680934
Hu X, Kato Y, Sumida A et al (2017) The SUFBC
pubmed: 28103400 doi: 10.1111/tpj.13483
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
pubmed: 16109955 pmcid: 1196142 doi: 10.1128/JB.187.17.6137-6146.2005
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
pubmed: 11507093 doi: 10.1074/jbc.M104945200
Jeong J, Guerinot ML (2009) Homing in on iron homeostasis in plants. Trends Plant Sci 14:280–285
pubmed: 19375375 doi: 10.1016/j.tplants.2009.02.006
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
pubmed: 18647837 pmcid: 2492473 doi: 10.1073/pnas.0708367105
Johnson DC, Dean DR, Smith AD, Johnson MK (2005) Structure, function, and formation of biological iron-sulfur clusters. Annu Rev Biochem 74:247–281
pubmed: 15952888 doi: 10.1146/annurev.biochem.74.082803.133518
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
pubmed: 16364320 doi: 10.1016/j.febslet.2005.11.058
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
pubmed: 17350958 doi: 10.1074/jbc.M608555200
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
pubmed: 12553879 pmcid: 1223333 doi: 10.1042/bj20021946
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
pubmed: 14690502 doi: 10.1046/j.1365-313X.2003.01952.x
Lill R (2009) Function and biogenesis of iron–sulphur proteins. Nature 460:831–838
pubmed: 19675643 doi: 10.1038/nature08301
Lill R, Mühlenhoff U (2008) Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Annu Rev Biochem 77:669–700
pubmed: 18366324 doi: 10.1146/annurev.biochem.76.052705.162653
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
pubmed: 17941825 doi: 10.1042/BJ20071166
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
doi: 10.1039/c2dt32263c
Mihara H, Esaki N (2002) Bacterial cysteine desulfurases: their function and mechanisms. Appl Microbiol Biotechnol 60:12–23
pubmed: 12382038 doi: 10.1007/s00253-002-1107-4
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
pubmed: 10739946 doi: 10.1093/oxfordjournals.jbchem.a022641
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
pubmed: 11983074 doi: 10.1093/oxfordjournals.jbchem.a003151
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
pubmed: 19861554 pmcid: 2782287 doi: 10.1105/tpc.109.069401
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
pubmed: 12554644 pmcid: 140745 doi: 10.1093/emboj/cdg061
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
doi: 10.1074/jbc.M701428200
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
pubmed: 27784767 pmcid: 5129733 doi: 10.1104/pp.16.01564
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
pubmed: 28102753 pmcid: 5351725 doi: 10.1080/15592324.2017.1282023
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
pubmed: 12637501 doi: 10.1074/jbc.M300285200
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
pubmed: 12941942 doi: 10.1074/jbc.M308004200
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
pubmed: 15101990 doi: 10.1111/j.1365-2958.2004.04025.x
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
pubmed: 12427997 pmcid: 166651 doi: 10.1104/pp.102.010280
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
pubmed: 29349662 pmcid: 6006212 doi: 10.1007/s00775-018-1532-1
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
pubmed: 17642475 doi: 10.1074/jbc.M702519200
Rempel S, Stanek WK, Slotboom DJ (2019) Energy-coupling factor-type ATP-binding cassette transporters. Annu Rev Biochem 88:551–576
pubmed: 30485755 doi: 10.1146/annurev-biochem-013118-111705
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
pubmed: 28741719 doi: 10.1111/pce.13036
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
pubmed: 31911438 pmcid: 7008376 doi: 10.1074/jbc.RA119.011034
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
pubmed: 20857974 doi: 10.1021/bi1011546
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
pubmed: 33553997 pmcid: 7851846 doi: 10.1002/pld3.303
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
pubmed: 16790430 doi: 10.1074/jbc.M601062200
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
doi: 10.1042/BJ20091290
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
pubmed: 20132520 doi: 10.1111/j.1365-3040.2010.02124.x
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
pubmed: 12486045 pmcid: 141979 doi: 10.1128/JB.185.1.98-106.2003
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
pubmed: 27541495 doi: 10.1007/s00425-016-2586-3
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
pubmed: 12089140 doi: 10.1074/jbc.C200365200
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
pubmed: 21371898 doi: 10.1016/j.plaphy.2011.02.003
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
pubmed: 15496591 doi: 10.1093/jb/mvh104
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
pubmed: 15361144 doi: 10.1111/j.1365-313X.2004.02189.x
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
pubmed: 30785184 doi: 10.1093/jxb/erz050
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
pubmed: 17372218 pmcid: 1838476 doi: 10.1073/pnas.0700774104
Verrier PJ, Bird D, Burla B et al (2008) Plant ABC proteins–a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159
pubmed: 18299247 doi: 10.1016/j.tplants.2008.02.001
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
pubmed: 31093670 doi: 10.1093/pcp/pcz091
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
pubmed: 19478995 pmcid: 2682760 doi: 10.1371/journal.pgen.1000497
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
doi: 10.3389/fpls.2019.01264
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
pubmed: 20460376 pmcid: 2906325 doi: 10.1074/jbc.M110.127449
Xu XM, Møller SG (2006) AtSufE is an essential activator of plastidic and mitochondrial desulfurases in Arabidopsis. EMBO J 25:900–909
pubmed: 16437155 pmcid: 1383551 doi: 10.1038/sj.emboj.7600968
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
pubmed: 15031412 pmcid: 412872 doi: 10.1105/tpc.020511
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
pubmed: 16455656 doi: 10.1074/jbc.M512737200
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
doi: 10.1038/s41598-017-09846-2
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
pubmed: 33855718 pmcid: 8246258 doi: 10.15252/embj.2020106742

Auteurs

Bing Yang (B)

International Research Laboratory of Agriculture and Agri-Product Safety of the Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China.
Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou, 225009, China.
College of Bioscience and Biotechnology, Yangzhou University, Yangzhou, 225009, China.

Chenyun Xu (C)

International Research Laboratory of Agriculture and Agri-Product Safety of the Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China.
Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou, 225009, China.
College of Bioscience and Biotechnology, Yangzhou University, Yangzhou, 225009, China.

Yuting Cheng (Y)

International Research Laboratory of Agriculture and Agri-Product Safety of the Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China.
Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou, 225009, China.
College of Bioscience and Biotechnology, Yangzhou University, Yangzhou, 225009, China.

Ting Jia (T)

International Research Laboratory of Agriculture and Agri-Product Safety of the Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China. tingj2012@yzu.edu.cn.

Xueyun Hu (X)

International Research Laboratory of Agriculture and Agri-Product Safety of the Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China. xyhulab@yzu.edu.cn.
Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou, 225009, China. xyhulab@yzu.edu.cn.
College of Bioscience and Biotechnology, Yangzhou University, Yangzhou, 225009, China. xyhulab@yzu.edu.cn.

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