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Plant Cell Reports

, Volume 38, Issue 8, pp 981–990 | Cite as

Altered levels of mitochondrial NFS1 affect cellular Fe and S contents in plants

  • Alejandro M. Armas
  • Manuel Balparda
  • Valeria R. Turowski
  • Maria V. Busi
  • Maria A. Pagani
  • Diego F. Gomez-CasatiEmail author
Original Article

Abstract

Key message

The ISC Fe–S cluster biosynthetic pathway would play a key role in the regulation of iron and sulfur homeostasis in plants.

Abstract

The Arabidopsis thaliana mitochondrial cysteine desulfurase AtNFS1 has an essential role in cellular ISC Fe–S cluster assembly, and this pathway is one of the main sinks for iron (Fe) and sulfur (S) in the plant. In different plant species it has been reported a close relationship between Fe and S metabolisms; however, the regulation of both nutrient homeostasis is not fully understood. In this study, we have characterized AtNFS1 overexpressing and knockdown mutant Arabidopsis plants. Plants showed alterations in the ISC Fe–S biosynthetic pathway genes and in the activity of Fe–S enzymes. Genes involved in Fe and S uptakes, assimilation, and regulation were up-regulated in overexpressing plants and down-regulated in knockdown plants. Furthermore, the plant nutritional status in different tissues was in accordance with those gene activities: overexpressing lines accumulated increased amounts of Fe and S and mutant plant had lower contents of S. In summary, our results suggest that the ISC Fe–S cluster biosynthetic pathway plays a crucial role in the homeostasis of Fe and S in plants, and that it may be important in their regulation.

Keywords

Iron Sulfur Fe–S clusters Cysteine desulfurase 

Notes

Acknowledgements

This work was supported by Grants from ANPCyT (PICT 2014-2184/2016-350/2016-0264). AMA and MB are research fellows from CONICET. VRT, MVB, MAP, and DFGC are research members from CONICET.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

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References

  1. Adam AC, Bornhövd C, Prokisch H, Neupert W, Hell K (2006) The Nfs1 interacting protein Isd11 has an essential role in Fe/S cluster biogenesis in mitochondria. EMBO J 25:174–183CrossRefGoogle Scholar
  2. Balk J, Lobreaux S (2005) Biogenesis of iron–sulfur proteins in plants. Trends Plant Sci 10:324–331CrossRefGoogle Scholar
  3. Balk J, Pilon M (2011) Ancient and essential: the assembly of iron–sulfur clusters in plants. Trends Plant Sci 16:218–226CrossRefGoogle Scholar
  4. Balk J, Schaedler TA (2014) Iron cofactor assembly in plants. Annu Rev Plant Biol 65:125–153CrossRefGoogle Scholar
  5. Bashir K, Ishimaru Y, Shimo H, Nagasaka S, Fujimoto M, Takanashi H, Tsutsumi N, An G, Nakanishi H, Nishizawa NK (2011) The rice mitochondrial iron transporter is essential for plant growth. Nat Commun 2:322CrossRefGoogle Scholar
  6. Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499–1510Google Scholar
  7. Busi MV, Maliandi MV, Valdez H, Clemente M, Zabaleta EJ, Araya A, Gomez-Casati DF (2006) Deficiency of Arabidopsis thaliana frataxin alters activity of mitochondrial Fe–S proteins and induces oxidative stress. Plant J 48:873–882CrossRefGoogle Scholar
  8. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefGoogle Scholar
  9. Colangelo EP, Guerinot ML (2004) The essential basic helix–loop–helix protein FIT1 is required for the iron deficiency response. Plant Cell 16:3400–3412CrossRefGoogle Scholar
  10. Connolly EL, Campbell NH, Grotz N, Prichard CL, Guerinot ML (2003) Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiol 133:1102–1110CrossRefGoogle Scholar
  11. Davidian J-C, Kopriva S (2010) Regulation of sulfate uptake and assimilation—the same or not the same? Mol Plant 3:314–325CrossRefGoogle Scholar
  12. Dos Santos PC, Dean DR, Hu Y, Ribbe MW (2004) Formation and insertion of the nitrogenase iron-molybdenum cofactor. Chem Rev 104:1159–1173CrossRefGoogle Scholar
  13. Eide D, Broderius M, Fett J, Guerinot ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci USA 93:5624–5628CrossRefGoogle Scholar
  14. Forieri I, Wirtz M, Hell R (2013) Toward new perspectives on the interaction of iron and sulfur metabolism in plants. Front Plant Sci 4:357CrossRefGoogle Scholar
  15. Forieri I, Sticht C, Reichelt M, Gretz N, Hawkesford MJ, Malagoli M, Wirtz M, Hell R (2017) System analysis of metabolism and the transcriptome in Arabidopsis thaliana roots reveals differential co-regulation upon iron, sulfur and potassium deficiency. Plant Cell Environ 40:95–107CrossRefGoogle Scholar
  16. Frazzon AP, Ramirez MV, Warek U, Balk J, Frazzon J, Dean DR, Winkel BS (2007) Functional analysis of Arabidopsis genes involved in mitochondrial iron–sulfur cluster assembly. Plant Mol Biol 64:225–240CrossRefGoogle Scholar
  17. Gigolashvili T, Kopriva S (2014) Transporters in plant sulfur metabolism. Front Plant Sci 5:442CrossRefGoogle Scholar
  18. Hatzfeld Y, Cathala N, Grignon C, Davidian JC (1998) Effect of ATP sulfurylase overexpression in bright yellow 2 tobacco cells. regulation of atp sulfurylase and SO4(2-) transport activities. Plant Physiol 116:1307–1313CrossRefGoogle Scholar
  19. Johnson DC, Dean DR, Smith AD, Johnson MK (2005) Structure, function, and formation of biological iron–sulfur clusters. Annu Rev Biochem 74:247–281CrossRefGoogle Scholar
  20. Kispal G, Csere P, Prohl C, Lill R (1999) The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. EMBO J 18:3981–3989CrossRefGoogle Scholar
  21. Kobayashi T, Nishizawa NK (2015) Intracellular iron sensing by the direct binding of iron to regulators. Front Plant Sci 6:155CrossRefGoogle Scholar
  22. Kolmert Å, Wikström P, Hallberg KB (2000) A fast and simple turbidimetric method for the determination of sulfate in sulfate-reducing bacterial cultures. J Microbiol Methods 41:179–184CrossRefGoogle Scholar
  23. Kopriva S (2006) Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot 97:479–495CrossRefGoogle Scholar
  24. Kopriva S, Rennenberg H (2004) Control of sulphate assimilation and glutathione synthesis: interaction with N and C metabolism. J Exp Bot 55:1831–1842CrossRefGoogle Scholar
  25. Kruft V, Eubel H, Jansch L, Werhahn W, Braun HP (2001) Proteomic approach to identify novel mitochondrial proteins in Arabidopsis. Plant Physiol 127:1694–1710CrossRefGoogle Scholar
  26. Land T, Rouault TA (1998) Targeting of a human iron–sulfur cluster assembly enzyme, nifs, to different subcellular compartments is regulated through alternative AUG utilization. Mol Cell 2:807–815CrossRefGoogle Scholar
  27. Leaden L, Pagani MA, Balparda M, Busi MV, Gomez-Casati DF (2016) Altered levels of AtHSCB disrupts iron translocation from roots to shoots. Plant Mol Biol 92:613–628CrossRefGoogle Scholar
  28. Lill R (2009) Function and biogenesis of iron–sulphur proteins. Nature 460:831CrossRefGoogle Scholar
  29. Lill R, Mühlenhoff U (2008) Maturation of iron–sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Annu Rev Biochem 77:669–700CrossRefGoogle Scholar
  30. Logan HM, Cathala N, Grignon C, Davidian JC (1996) Cloning of a cDNA encoded by a member of the Arabidopsis thaliana ATP sulfurylase multigene family. Expression studies in yeast and in relation to plant sulfur nutrition. J Biol Chem 271:12227–12233CrossRefGoogle Scholar
  31. Lu C, Cortopassi G (2007) Frataxin knockdown causes loss of cytoplasmic iron–sulfur cluster functions, redox alterations and induction of heme transcripts. Arch Biochem Biophys 457:111–122CrossRefGoogle Scholar
  32. Marschner H, Römheld V (1994) Strategies of plants for acquisition of iron. Plant Soil 165:261–264CrossRefGoogle Scholar
  33. Martelli A, Wattenhofer-Donze M, Schmucker S, Bouvet S, Reutenauer L, Puccio H (2007) Frataxin is essential for extramitochondrial Fe–S cluster proteins in mammalian tissues. Hum Mol Genet 16:2651–2658CrossRefGoogle Scholar
  34. Maruyama-Nakashita A, Nakamura Y, Tohge T, Saito K, Takahashi H (2006) Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 18:3235–3251CrossRefGoogle Scholar
  35. Mihara H, Kurihara T, Yoshimura T, Soda K, Esaki N (1997) Cysteine sulfinate desulfinase, a NIFS-like protein of Escherichia coli with selenocysteine lyase and cysteine desulfurase activities. J Biol Chem 272:22417–22424CrossRefGoogle Scholar
  36. Nakai Y, Yoshihara Y, Hayashi H, Kagamiyama H (1998) cDNA cloning and characterization of mouse nifS-like protein, m-Nfs1: mitochondrial localization of eukaryotic NifS-like proteins. FEBS Lett 433:143–148CrossRefGoogle Scholar
  37. Palmgren MG (2001) PLANT PLASMA MEMBRANE H + -ATPases: powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817–845CrossRefGoogle Scholar
  38. Paolacci AR, Celletti S, Catarcione G, Hawkesford MJ, Astolfi S, Ciaffi M (2014) Iron deprivation results in a rapid but not sustained increase of the expression of genes involved in iron metabolism and sulfate uptake in tomato (Solanum lycopersicum L.) seedlings. J Integr Plant Biol 56:88–100CrossRefGoogle Scholar
  39. Patzer SI, Hantke K (1999) SufS is a NifS-like protein, and SufD is necessary for stability of the [2Fe-2S] FhuF protein in Escherichia coli. J Bacteriol 181:3307–3309Google Scholar
  40. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29:e45CrossRefGoogle Scholar
  41. Poburski D, Boerner JB, Koenig M, Ristow M, Thierbach R (2016) Time-resolved functional analysis of acute impairment of frataxin expression in an inducible cell model of Friedreich ataxia. Biol Open 5:654–661CrossRefGoogle Scholar
  42. Reyt G, Boudouf S, Boucherez J, Gaymard F, Briat JF (2015) Iron- and ferritin-dependent reactive oxygen species distribution: impact on Arabidopsis root system architecture. Mol Plant 8:439–453CrossRefGoogle Scholar
  43. Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697CrossRefGoogle Scholar
  44. Rubio LM, Ludden PW (2005) Maturation of nitrogenase: a biochemical puzzle. J Bacteriol 187:405–414CrossRefGoogle Scholar
  45. Tan G, Napoli E, Taroni F, Cortopassi G (2003) Decreased expression of genes involved in sulfur amino acid metabolism in frataxin-deficient cells. Hum Mol Genet 12:1699–1711CrossRefGoogle Scholar
  46. Tripodi K, Podestá F (2003) Purification and characterization of an NAD-dependent malate dehydrogenase from leaves of the crassulacean acid metabolism plant Aptenia cordifolia. Plant Physiol Biochem 41:97–105CrossRefGoogle Scholar
  47. Vauclare P, Kopriva S, Fell D, Suter M, Sticher L, von Ballmoos P, Krahenbuhl U, den Camp RO, Brunold C (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5′-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J 31:729–740CrossRefGoogle Scholar
  48. Vigani G, Briat JF (2016) Impairment of respiratory chain under nutrient deficiency in plants: does it play a role in the regulation of iron and sulfur responsive genes? Front Plant Sci 6:1185CrossRefGoogle Scholar
  49. Vigani G, Bashir K, Ishimaru Y, Lehman M, Casiraghi FM, Nakanishi H, Seki M, Geigenberger P, Zocchi G, Nishizawa NK (2016) Knocking down mitochondrial iron transporter (MIT) reprograms primary and secondary metabolism in rice plants. J Exp Bot 67:1357–1368CrossRefGoogle Scholar
  50. Vigani G, Pii Y, Celletti S, Maver M, Mimmo T, Cesco S, Astolfi S (2018) Mitochondria dysfunctions under Fe and S deficiency: is citric acid involved in the regulation of adaptive responses? Plant Physiol Biochem 126:86–96CrossRefGoogle Scholar
  51. Weigel D, Glazebrook J (2002) Arabidopsis. A laboratory manual. Cold Spring Harbor Laboratory Press, New York, p 354Google Scholar
  52. Werhahn W, Niemeyer A, Jänsch L, Kruft V, Schmitz UK, Braun H-P (2001) Purification and characterization of the preprotein translocase of the outer mitochondrial membrane from Arabidopsis. Identification of multiple forms of TOM20. Plant Physiol 125:943–954CrossRefGoogle Scholar
  53. Wiedemann N, Urzica E, Guiard B, Müller H, Lohaus C, Meyer HE, Ryan MT, Meisinger C, Mühlenhoff U, Lill R (2006) Essential role of Isd11 in mitochondrial iron–sulfur cluster synthesis on Isu scaffold proteins. EMBO J 25:184–195CrossRefGoogle Scholar
  54. Yoon T, Cowan J (2003) Iron–sulfur cluster biosynthesis. Characterization of frataxin as an iron donor for assembly of [2Fe–2S] clusters in ISU-type proteins. J Am Chem Soc 125:6078–6084CrossRefGoogle Scholar
  55. Yuan Y, Wu H, Wang N, Li J, Zhao W, Du J, Wang D, Ling H-Q (2008) FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Res 18:385–397CrossRefGoogle Scholar
  56. Zheng L, White RH, Cash VL, Jack RF, Dean DR (1993) Cysteine desulfurase activity indicates a role for NIFS in metallocluster biosynthesis. Proc Natl Acad Sci USA 90:2754–2758CrossRefGoogle Scholar
  57. Zuchi S, Cesco S, Varanini Z, Pinton R, Astolfi S (2009) Sulphur deprivation limits Fe-deficiency responses in tomato plants. Planta 230:85–94CrossRefGoogle Scholar
  58. Zuchi S, Watanabe M, Hubberten HM, Bromke M, Osorio S, Fernie AR, Celletti S, Paolacci AR, Catarcione G, Ciaffi M, Hoefgen R, Astolfi S (2015) The interplay between sulfur and iron nutrition in tomato. Plant Physiol 169:2624–2639Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Centro de Estudios Fotosintéticos y Bioquímicos (CEFOBI-CONICET)Universidad Nacional de RosarioRosarioArgentina
  2. 2.Instituto de Investigaciones Biotecnológicas, IIB-INTECH, CONICET-UNSAMChascomúsArgentina

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