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.
Similar content being viewed by others
References
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 25:174–183
Balk J, Lobreaux S (2005) Biogenesis of iron–sulfur proteins in plants. Trends Plant Sci 10:324–331
Balk J, Pilon M (2011) Ancient and essential: the assembly of iron–sulfur clusters in plants. Trends Plant Sci 16:218–226
Balk J, Schaedler TA (2014) Iron cofactor assembly in plants. Annu Rev Plant Biol 65:125–153
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 2:322
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 13:1499–1510
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 48:873–882
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Colangelo EP, Guerinot ML (2004) The essential basic helix–loop–helix protein FIT1 is required for the iron deficiency response. Plant Cell 16:3400–3412
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 133:1102–1110
Davidian J-C, Kopriva S (2010) Regulation of sulfate uptake and assimilation—the same or not the same? Mol Plant 3:314–325
Dos Santos PC, Dean DR, Hu Y, Ribbe MW (2004) Formation and insertion of the nitrogenase iron-molybdenum cofactor. Chem Rev 104:1159–1173
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 93:5624–5628
Forieri I, Wirtz M, Hell R (2013) Toward new perspectives on the interaction of iron and sulfur metabolism in plants. Front Plant Sci 4:357
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 40:95–107
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 64:225–240
Gigolashvili T, Kopriva S (2014) Transporters in plant sulfur metabolism. Front Plant Sci 5:442
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 116:1307–1313
Johnson DC, Dean DR, Smith AD, Johnson MK (2005) Structure, function, and formation of biological iron–sulfur clusters. Annu Rev Biochem 74:247–281
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 18:3981–3989
Kobayashi T, Nishizawa NK (2015) Intracellular iron sensing by the direct binding of iron to regulators. Front Plant Sci 6:155
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 41:179–184
Kopriva S (2006) Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot 97:479–495
Kopriva S, Rennenberg H (2004) Control of sulphate assimilation and glutathione synthesis: interaction with N and C metabolism. J Exp Bot 55:1831–1842
Kruft V, Eubel H, Jansch L, Werhahn W, Braun HP (2001) Proteomic approach to identify novel mitochondrial proteins in Arabidopsis. Plant Physiol 127:1694–1710
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 2:807–815
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 92:613–628
Lill R (2009) Function and biogenesis of iron–sulphur proteins. Nature 460:831
Lill R, Mühlenhoff U (2008) Maturation of iron–sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Annu Rev Biochem 77:669–700
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 271:12227–12233
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 457:111–122
Marschner H, Römheld V (1994) Strategies of plants for acquisition of iron. Plant Soil 165:261–264
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 16:2651–2658
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 18:3235–3251
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 272:22417–22424
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 433:143–148
Palmgren MG (2001) PLANT PLASMA MEMBRANE H + -ATPases: powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817–845
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 56:88–100
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 181:3307–3309
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29:e45
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 5:654–661
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 8:439–453
Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697
Rubio LM, Ludden PW (2005) Maturation of nitrogenase: a biochemical puzzle. J Bacteriol 187:405–414
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 12:1699–1711
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 41:97–105
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 31:729–740
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 6:1185
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 67:1357–1368
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 126:86–96
Weigel D, Glazebrook J (2002) Arabidopsis. A laboratory manual. Cold Spring Harbor Laboratory Press, New York, p 354
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 125:943–954
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 25:184–195
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 125:6078–6084
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 18:385–397
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 90:2754–2758
Zuchi S, Cesco S, Varanini Z, Pinton R, Astolfi S (2009) Sulphur deprivation limits Fe-deficiency responses in tomato plants. Planta 230:85–94
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 169:2624–2639
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Emmanuel Guiderdoni.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Armas, A.M., Balparda, M., Turowski, V.R. et al. Altered levels of mitochondrial NFS1 affect cellular Fe and S contents in plants. Plant Cell Rep 38, 981–990 (2019). https://doi.org/10.1007/s00299-019-02419-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-019-02419-9