Role of Nfu1 and Bol3 in iron-sulfur cluster transfer to mitochondrial clients

eLife

Volumn 5, Issue AUGUST, 2016, Pages

  Melber, Andrew ^a,b   Na, Un ^a,b   Vashisht, Ajay ^c   Weiler, Benjamin D ^d   Lill, Roland ^d,e   Wohlschlegel, James A ^c   Winge, Dennis R ^a,b  

^a UNIVERSITY OF UTAH HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d PHILIPPS UNIVERSITY MARBURG   (Germany)

^e Offensive for the Development of Scientific and Economic Excellence of the State of Hesse LOEWE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAREDOXIN; IRON SULFUR PROTEIN; BOL1 PROTEIN, S CEREVISIAE; BOL3 PROTEIN, S CEREVISIAE; MITOCHONDRIAL PROTEIN; NFU1 PROTEIN, S CEREVISIAE; PROTEOME; SACCHAROMYCES CEREVISIAE PROTEIN;

AEROBIC METABOLISM; ARTICLE; BINDING AFFINITY; BOL3 GENE; DNA REPAIR; ENZYME ACTIVITY; FUNGAL GENE; GENE MUTATION; IMMUNOBLOTTING; MASS SPECTROMETRY; MITOCHONDRIAL RESPIRATION; NFU1 GENE; POLYMERASE CHAIN REACTION; PROTEIN ASSEMBLY; PROTEIN PURIFICATION; PROTEIN TRANSPORT; PROTEOMICS; SIZE EXCLUSION CHROMATOGRAPHY; YEAST; ENZYMOLOGY; GENETICS; METABOLISM; MITOCHONDRION; SACCHAROMYCES CEREVISIAE; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; IRON-SULFUR PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PROTEOME; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84986200954     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.15991     Document Type: Article

References (69)

1. Al-Hassnan ZN, Al-Dosary M, Alfadhel M, Faqeih EA, Alsagob M, Kenana R, Almass R, Al-Harazi OS, Al-Hindi H, Malibari OI, Almutari FB, Tulbah S, Alhadeq F, Al-Sheddi T, Alamro R, AlAsmari A, Almuntashri M, Alshaalan H, Al-Mohanna FA, Colak D, et al. 2015. ISCA2 mutation causes infantile neurodegenerative mitochondrial disorder. Journal of Medical Genetics 52:186–194. doi: 10.1136/jmedgenet-2014-102592
2. Angelini S, Gerez C, Ollagnier-de Choudens S, Sanakis Y, Fontecave M, Barras F, Py B. 2008. NfuA, a new factor required for maturing Fe/S proteins in Escherichia coli under oxidative stress and iron starvation conditions. Journal of Biological Chemistry 283:14084–14091. doi: 10.1074/jbc.M709405200
3. Atkinson A, Smith P, Fox JL, Cui TZ, Khalimonchuk O, Winge DR. 2011. The LYR protein Mzm1 functions in the insertion of the Rieske Fe/S protein in yeast mitochondria. Molecular and Cellular Biology 31:3988–3996. doi: 10.1128/MCB.05673-11
4. Baker PR, Friederich MW, Swanson MA, Shaikh T, Bhattacharya K, Scharer GH, Aicher J, Creadon-Swindell G, Geiger E, MacLean KN, Lee WT, Deshpande C, Freckmann ML, Shih LY, Wasserstein M, Rasmussen MB, Lund AM, Procopis P, Cameron JM, Robinson BH, et al. 2014. Variant non ketotic hyperglycinemia is caused by mutations in LIAS, BOLA3 and the novel gene GLRX5. Brain 137:366–379. doi: 10.1093/brain/awt328
5. Banci L, Brancaccio D, Ciofi-Baffoni S, Del Conte R, Gadepalli R, Mikolajczyk M, Neri S, Piccioli M, Winkelmann J. 2014. [2Fe-2S] cluster transfer in iron-sulfur protein biogenesis. PNAS 111:6203–6208. doi: 10.1073/pnas.1400102111
6. Bandyopadhyay S, Naik SG, O’Carroll IP, Huynh BH, Dean DR, Johnson MK, Dos Santos PC. 2008. A proposed role for the Azotobacter vinelandii NfuA protein as an intermediate iron-sulfur cluster carrier. Journal of Biological Chemistry 283:14092–14099. doi: 10.1074/jbc.M709161200
7. Biederbick A, Stehling O, Rösser R, Niggemeyer B, Nakai Y, Elsä sser HP, Lill R. 2006. Role of human mitochondrial Nfs1 in cytosolic iron-sulfur protein biogenesis and iron regulation. Molecular and Cellular Biology 26:5675–5687. doi: 10.1128/MCB.00112-06
8. Boutigny S, Saini A, Baidoo EE, Yeung N, Keasling JD, Butland G. 2013. Physical and functional interactions of a monothiol glutaredoxin and an iron sulfur cluster carrier protein with the sulfur-donating radical S-adenosyl-L-methionine enzyme MiaB. Journal of Biological Chemistry 288:14200–14211. doi: 10.1074/jbc.M113.460360
9. Brancaccio D, Gallo A, Mikolajczyk M, Zovo K, Palumaa P, Novellino E, Piccioli M, Ciofi-Baffoni S, Banci L. 2014. Formation of [4Fe-4S] clusters in the mitochondrial iron-sulfur cluster assembly machinery. Journal of the American Chemical Society 136:16240–16250. doi: 10.1021/ja507822j
10. Bridwell-Rabb J, Fox NG, Tsai CL, Winn AM, Barondeau DP. 2014. Human frataxin activates Fe-S cluster biosynthesis by facilitating sulfur transfer chemistry. Biochemistry 53:4904–4913. doi: 10.1021/bi500532e
11. Cameron JM, Janer A, Levandovskiy V, Mackay N, Rouault TA, Tong WH, Ogilvie I, Shoubridge EA, Robinson BH. 2011. Mutations in iron-sulfur cluster scaffold genes NFU1 and BOLA3 cause a fatal deficiency of multiple respiratory chain and 2-oxoacid dehydrogenase enzymes. The American Journal of Human Genetics 89:486–495. doi: 10.1016/j.ajhg.2011.08.011
12. Cicchillo RM, Lee KH, Baleanu-Gogonea C, Nesbitt NM, Krebs C, Booker SJ. 2004. Escherichia coli lipoyl synthase binds two distinct [4Fe-4S] clusters per polypeptide. Biochemistry 43:11770–11781. doi: 10.1021/ bi0488505
13. Cicchillo RM, Booker SJ. 2005. Mechanistic investigations of lipoic acid biosynthesis in Escherichia coli: both sulfur atoms in lipoic acid are contributed by the same lipoyl synthase polypeptide. Journal of the American Chemical Society 127:2860–2861. doi: 10.1021/ja042428u
14. Ciesielski SJ, Schilke BA, Osipiuk J, Bigelow L, Mulligan R, Majewska J, Joachimiak A, Marszalek J, Craig EA, Dutkiewicz R. 2012. Interaction of J-protein co-chaperone Jac1 with Fe-S scaffold Isu is indispensable in vivo and conserved in evolution. Journal of Molecular Biology 417:1–12. doi: 10.1016/j.jmb.2012.01.022
15. Cociorva D, Tabb D L, Yates JR. 2007. Validation of tandem mass spectrometry database search results using DTASelect. Current Protocols in Bioinformatics Chapter 13:Unit 13.4:13.4.1–13.4.14. doi: 10.1002/0471250953.bi1304s16
16. Cronan JE. 2014. The structure of lipoyl synthase, a remarkable enzyme that performs the last step of an extraordinary biosynthetic pathway. Biochemical Journal 464:e1–3. doi: 10.1042/BJ20141061
17. Debray FG, Stü mpfig C, Vanlander AV, Dideberg V, Josse C, Caberg JH, Boemer F, Bours V, Stevens R, Seneca S, Smet J, Lill R, van Coster R. 2015. Mutation of the iron-sulfur cluster assembly gene IBA57 causes fatal infantile leukodystrophy. Journal of Inherited Metabolic Disease 38:1147–1153. doi: 10.1007/s10545-015-9857-1
18. Elias JE, Gygi SP. 2007. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nature Methods 4:207–214. doi: 10.1038/nmeth1019
19. Fazius F, Shelest E, Gebhardt P, Brock M. 2012. The fungal a-aminoadipate pathway for lysine biosynthesis requires two enzymes of the aconitase family for the isomerization of homocitrate to homoisocitrate. Molecular Microbiology 86:1508–1530. doi: 10.1111/mmi.12076
20. Fernandes L, Rodrigues-Pousada C, Struhl K. 1997. Yap, a novel family of eight bZIP proteins in Saccharomyces cerevisiae with distinct biological functions. Molecular and Cellular Biology 17:6982–6993. doi: 10.1128/MCB.17.12.6982
21. Ferrer-Cortès X, Font A, Bujan N, Navarro-Sastre A, Matalonga L, Arranz JA, Riudor E, del Toro M, Garcia-Cazorla A, Campistol J, Briones P, Ribes A, Tort F. 2013. Protein expression profiles in patients carrying NFU1 mutations. Contribution to the pathophysiology of the disease. Journal of Inherited Metabolic Disease 36:841–847. doi: 10.1007/s10545-012-9565-z
22. Florens L, Carozza MJ, Swanson SK, Fournier M, Coleman MK, Workman JL, Washburn MP. 2006. Analyzing chromatin remodeling complexes using shotgun proteomics and normalized spectral abundance factors. Methods 40:303–311. doi: 10.1016/j.ymeth.2006.07.028
23. Fox NG, Das D, Chakrabarti M, Lindahl PA, Barondeau DP. 2015. Frataxin accelerates [2Fe-2S] cluster formation on the human Fe-S assembly complex. Biochemistry 54:3880–3889. doi: 10.1021/bi5014497
24. Gao H, Subramanian S, Couturier J, Naik SG, Kim SK, Leustek T, Knaff DB, Wu HC, Vignols F, Huynh BH, Rouhier N, Johnson MK. 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. doi: 10.1021/bi4007622
25. Gelling C, Dawes IW, Richhardt N, Lill R, Mü hlenhoff U. 2008. Mitochondrial Iba57p is required for Fe/S cluster formation on aconitase and activation of radical SAM enzymes. Molecular and Cellular Biology 28:1851–1861. doi: 10.1128/MCB.01963-07
26. Gerber J, Mü hlenhoff U, Lill R. 2003. An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1. EMBO Reports 4:906–911. doi: 10.1038/sj.embor.embor918
27. Glick BS, Pon LA. 1995. Isolation of highly purified mitochondria from Saccharomyces cerevisiae. Methods in Enzymology 260:213–223. doi: 10.1016/0076-6879(95)60139-2
28. Hiltunen JK, Schonauer MS, Autio KJ, Mittelmeier TM, Kastaniotis AJ, Dieckmann CL. 2009. Mitochondrial fatty acid synthesis type II: more than just fatty acids. Journal of Biological Chemistry 284:9011–9015. doi: 10.1074/jbc.R800068200
29. Hiltunen JK, Autio KJ, Schonauer MS, Kursu VAS, Dieckmann CL, Kastaniotis AJ. 2010. Mitochondrial fatty acid synthesis and respiration. Biochimica Et Biophysica Acta (BBA) 1797:1195–1202. doi: 10.1016/j.bbabio.2010.03.006
30. Jacobson MR, Cash VL, Weiss MC, Laird NF, Newton WE, Dean DR. 1989. Biochemical and genetic analysis of the nifUSVWZM cluster from Azotobacter vinelandii. MGG Molecular & General Genetics 219:49–57. doi: 10.1007/BF00261156
31. Kaiser P, Wohlschlegel J. 2005. Identification of ubiquitination sites and determination of ubiquitin-chain architectures by mass spectrometry. Methods in Enzymology 399:266–277. doi: 10.1016/S0076-6879(05)99018-6
32. Kelstrup CD, Young C, Lavallee R, Nielsen ML, Olsen JV. 2012. Optimized fast and sensitive acquisition methods for shotgun proteomics on a quadrupole orbitrap mass spectrometer. Journal of Proteome Research 11:3487–3497. doi: 10.1021/pr3000249
33. Kim KD, Chung WH, Kim HJ, Lee KC, Roe JH. 2010. Monothiol glutaredoxin Grx5 interacts with Fe-S scaffold proteins Isa1 and Isa2 and supports Fe-S assembly and DNA integrity in mitochondria of fission yeast. Biochemical and Biophysical Research Communications 392:467–472. doi: 10.1016/j.bbrc.2010.01.051
34. Kim HJ, Jeong MY, Na U, Winge DR. 2012. Flavinylation and assembly of succinate dehydrogenase are dependent on the C-terminal tail of the flavoprotein subunit. Journal of Biological Chemistry 287:40670–40679. doi: 10.1074/jbc.M112.405704
35. Lange H, Kaut A, Kispal G, Lill R. 2000. A mitochondrial ferredoxin is essential for biogenesis of cellular iron-sulfur proteins. PNAS 97:1050–1055. doi: 10.1073/pnas.97.3.1050
36. Li H, Outten CE. 2012. Monothiol CGFS glutaredoxins and BolA-like proteins: [2Fe-2S] binding partners in iron homeostasis. Biochemistry 51:4377–4389. doi: 10.1021/bi300393z
37. Li H, Mapolelo DT, Randeniya S, Johnson MK, Outten CE. 2012. Human glutaredoxin 3 forms [2Fe-2S]-bridged complexes with human BolA2. Biochemistry 51:1687–1696. doi: 10.1021/bi2019089
38. Lill R, Mü hlenhoff U. 2008. Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Annual Review of Biochemistry 77:669–700. doi: 10.1146/annurev.biochem.76.052705.162653
39. Lill R, Hoffmann B, Molik S, Pierik AJ, Rietzschel N, Stehling O, Uzarska MA, Webert H, Wilbrecht C, Mü hlenhoff U. 2012. The role of mitochondria in cellular iron–sulfur protein biogenesis and iron metabolism. Biochimica Et Biophysica Acta (BBA) 1823:1491–1508. doi: 10.1016/j.bbamcr.2012.05.009
40. Limberg G, Klaffke W, Thiem J. 1995. Conversion of aldonic acids to their corresponding 2-keto-3-deoxy-analogs by the non-carbohydrate enzyme dihydroxy acid dehydratase (DHAD). Bioorganic & Medicinal Chemistry 3: 487–494. doi: 10.1016/0968-0896(95)00072-O
41. Liu Y, Qi W, Cowan JA. 2009. Iron-sulfur cluster biosynthesis: functional characterization of the N- and C-terminal domains of human NFU. Biochemistry 48:973–980. doi: 10.1021/bi801645z
42. Longtine MS, McKenzie A, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953–961. doi: 10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U
43. Lossos A, Stü mpfig C, Stevanin G, Gaussen M, Zimmerman BE, Mundwiller E, Asulin M, Chamma L, Sheffer R, Misk A, Dotan S, Gomori JM, Ponger P, Brice A, Lerer I, Meiner V, Lill R. 2015. Fe/S protein assembly gene IBA57 mutation causes hereditary spastic paraplegia. Neurology 84:659–667. doi: 10.1212/WNL.0000000000001270
44. Majewska J, Ciesielski SJ, Schilke B, Kominek J, Blenska A, Delewski W, Song JY, Marszalek J, Craig EA, Dutkiewicz R. 2013. Binding of the chaperone Jac1 protein and cysteine desulfurase Nfs1 to the iron-sulfur cluster scaffold Isu protein is mutually exclusive. Journal of Biological Chemistry 288:29134–29142. doi: 10.1074/jbc.M113.503524
45. Michalski A, Damoc E, Hauschild JP, Lange O, Wieghaus A, Makarov A, Nagaraj N, Cox J, Mann M, Horning S. 2011. Mass spectrometry-based proteomics using Q Exactive, a high-performance benchtop quadrupole Orbitrap mass spectrometer. Molecular & Cellular Proteomics 10:M111.011015. doi: 10.1074/mcp.M111.011015
46. Mühlenhoff U, Richter N, Pines O, Pierik AJ, Lill R. 2011. Specialized function of yeast Isa1 and Isa2 proteins in the maturation of mitochondrial [4Fe-4S] proteins. Journal of Biological Chemistry 286:41205–41216. doi: 10.1074/jbc.M111.296152
47. Na U, Yu W, Cox J, Bricker DK, Brockmann K, Rutter J, Thummel CS, Winge DR. 2014. The LYR factors SDHAF1 and SDHAF3 mediate maturation of the iron-sulfur subunit of succinate dehydrogenase. Cell Metabolism 20: 253–266. doi: 10.1016/j.cmet.2014.05.014
48. Navarro-Sastre A, Tort F, Stehling O, Uzarska MA, Arranz JA, Del Toro M, Labayru MT, Landa J, Font A, Garcia-Villoria J, Merinero B, Ugarte M, Gutierrez-Solana LG, Campistol J, Garcia-Cazorla A, Vaquerizo J, Riudor E, Briones P, Elpeleg O, Ribes A, et al. 2011. A fatal mitochondrial disease is associated with defective NFU1 function in the maturation of a subset of mitochondrial Fe-S proteins. The American Journal of Human Genetics 89:656–667. doi: 10.1016/j.ajhg.2011.10.005
49. Nishio K, Nakai M. 2000. Transfer of iron-sulfur cluster from NifU to apoferredoxin. Journal of Biological Chemistry 275:22615–22618. doi: 10.1074/jbc.C000279200
50. Nizon M, Boutron A, Boddaert N, Slama A, Delpech H, Sardet C, Brassier A, Habarou F, Delahodde A, Correia I, Ottolenghi C, de Lonlay P. 2014. Leukoencephalopathy with cysts and hyperglycinemia may result from NFU1 deficiency. Mitochondrion 15:59–64. doi: 10.1016/j.mito.2014.01.003
51. Parent A, Elduque X, Cornu D, Belot L, Le Caer JP, Grandas A, Toledano MB, D’Autré aux B. 2015. Mammalian frataxin directly enhances sulfur transfer of NFS1 persulfide to both ISCU and free thiols. Nature Communications 6:5686. doi: 10.1038/ncomms6686
52. Pierrel F, Bestwick ML, Cobine PA, Khalimonchuk O, Cricco JA, Winge DR. 2007. Coa1 links the Mss51 post-translational function to Cox1 cofactor insertion in cytochrome c oxidase assembly. The EMBO Journal 26: 4335–4346. doi: 10.1038/sj.emboj.7601861
53. Py B, Gerez C, Angelini S, Planel R, Vinella D, Loiseau L, Talla E, Brochier-Armanet C, Garcia Serres R, Latour JM, Ollagnier-de Choudens S, Fontecave M, Barras F. 2012. Molecular organization, biochemical function, cellular role and evolution of NfuA, an atypical Fe-S carrier. Molecular Microbiology 86:155–171. doi: 10.1111/j.1365-2958.2012.08181.x
54. Roret T, Tsan P, Couturier J, Zhang B, Johnson MK, Rouhier N, Didierjean C. 2014. Structural and spectroscopic insights into BolA-glutaredoxin complexes. Journal of Biological Chemistry 289:24588–24598. doi: 10.1074/jbc.M114.572701
55. Schilke B, Voisine C, Beinert H, Craig E. 1999. Evidence for a conserved system for iron metabolism in the mitochondria of Saccharomyces cerevisiae. PNAS 96:10206–10211. doi: 10.1073/pnas.96.18.10206
56. Schmucker S, Martelli A, Colin F, Page A, Wattenhofer-Donzé M, Reutenauer L, Puccio H. 2011. Mammalian frataxin: an essential function for cellular viability through an interaction with a preformed ISCU/NFS1/ISD11 iron-sulfur assembly complex. PLoS One 6:e16199. doi: 10.1371/journal.pone.0016199
57. Schonauer MS, Kastaniotis AJ, Hiltunen JK, Dieckmann CL. 2008. Intersection of RNA processing and the type II fatty acid synthesis pathway in yeast mitochondria. Molecular and Cellular Biology 28:6646–6657. doi: 10.1128/MCB.01162-08
58. Seyda A, Newbold RF, Hudson TJ, Verner A, MacKay N, Winter S, Feigenbaum A, Malaney S, Gonzalez-Halphen D, Cuthbert AP, Robinson BH. 2001. A novel syndrome affecting multiple mitochondrial functions, located by microcell-mediated transfer to chromosome 2p14-2p13. The American Journal of Human Genetics 68:386–396. doi: 10.1086/318196
59. Sheftel AD, Wilbrecht C, Stehling O, Niggemeyer B, Elsä sser HP, Mü hlenhoff U, Lill R. 2012. The human mitochondrial ISCA1, ISCA2, and IBA57 proteins are required for [4Fe-4S] protein maturation. Molecular Biology of the Cell 23:1157–1166. doi: 10.1091/mbc.E11-09-0772
60. Tabb DL, McDonald WH, Yates JR. 2002. DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. Journal of Proteome Research 1:21–26. doi: 10.1021/pr015504q
61. Tong W-H, Jameson GNL, Huynh BH, Rouault TA. 2003. Subcellular compartmentalization of human Nfu, an iron-sulfur cluster scaffold protein, and its ability to assemble a [4Fe-4S] cluster. PNAS 100:9762–9767. doi: 10.1073/pnas.1732541100
62. Tsai CL, Barondeau DP. 2010. Human frataxin is an allosteric switch that activates the Fe-S cluster biosynthetic complex. Biochemistry 49:9132–9139. doi: 10.1021/bi1013062
63. Uzarska MA, Dutkiewicz R, Freibert SA, Lill R, Mü hlenhoff U. 2013. The mitochondrial Hsp70 chaperone Ssq1 facilitates Fe/S cluster transfer from Isu1 to Grx5 by complex formation. Molecular Biology of the Cell 24:1830–1841. doi: 10.1091/mbc.E12-09-0644
64. Webert H, Freibert SA, Gallo A, Heidenreich T, Linne U, Amlacher S, Hurt E, Mü hlenhoff U, Banci L, Lill R. 2014. Functional reconstitution of mitochondrial Fe/S cluster synthesis on Isu1 reveals the involvement of ferredoxin. Nature Communications 5:5013. doi: 10.1038/ncomms6013
65. Willems P, Wanschers BF, Esseling J, Szklarczyk R, Kudla U, Duarte I, Forkink M, Nooteboom M, Swarts H, Gloerich J, Nijtmans L, Koopman W, Huynen MA. 2013. BOLA1 is an aerobic protein that prevents mitochondrial morphology changes induced by glutathione depletion. Antioxidants & Redox Signaling 18:129–138. doi: 10.1089/ars.2011.4253
66. Wittig I, Braun HP, Schägger H. 2006. Blue native PAGE. Nature Protocols 1:418–428. doi: 10.1038/nprot.2006.62
67. Wohlschlegel JA. 2009. Identification of SUMO-conjugated proteins and their SUMO attachment sites using proteomic mass spectrometry. Methods in Molecular Biology 497:33–49. doi: 10.1007/978-1-59745-566-4_3
68. Xu T, Venable JD, Park SK, Cociorva D, Lu B, Liao L, Wohlschlegel J, Hewel J, Yates JR. 2006. ProLuCID, a fast and sensitive tandem mass spectra-based protein identification program. Molecular & Cellular Proteomics 5: S174.
69. Yabe T, Morimoto K, Kikuchi S, Nishio K, Terashima I, Nakai M. 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. The Plant Cell Online 16:993–1007. doi: 10.1105/tpc.020511