Abstract
Iron (Fe) is an intriguing nutrient due to its dual nature. Its redox properties make it essential for different vital processes in plant cells. But an excess of Fe can be toxic as it catalyses the formation of reactive oxygen species. Therefore Fe homeostasis must be tightly regulated. Different mechanisms contribute to the regulation, including the control of uptake, the intracellular chelation by different molecules and the partitioning into the organelles and storage locations. Despite its high abundance in soil, Fe solubility is extremely low. Fe availability represents a significant constraint to plant growth and plants have developed distinct strategies to ensure Fe solubilisation and uptake. The Fe-S clusters in the electron transport chain of mitochondria and chloroplasts represent an important sink of Fe. Recent observations suggest that a co-regulation exists between Fe and sulfur metabolism. This is most likely the outcome of the high demand for Fe and S required for the biosynthesis of Fe-S clusters. In the following chapter the uptake strategies and their regulation mechanisms will be introduced. Moreover, different aspects of the regulation of Fe homeostasis in the cell will be presented, including the partitioning in the organelles. In the last section different evidences towards the interaction between Fe and S metabolism will be discussed.
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References
Astolfi S, Zuchi S, Hubberten H-M, Pinton R, Hoefgen R (2010) Supply of sulphur to S-deficient young barley seedlings restores their capability to cope with iron shortage. J Exp Bot 61:799–806
Astolfi S, Zuchi S, Neumann G, Cesco S, Di Toppi LS, Pinton R (2012) Response of barley plants to Fe deficiency and Cd contamination as affected by S starvation. J Exp Bot 63:1241–1250
Balk J, Pilon M (2011) Ancient and essential: the assembly of iron–sulfur clusters in plants. Trends Plant Sci 16:218–226
Barberon M, Zelazny E, Robert S, Conejero G, Curie C, Friml J, Vert G (2011) Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proc Natl Acad Sci U S A 108:E450–E458
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
Bauer P, Ling HQ, Guerinot ML (2007) FIT, the FER-like iron deficiency induced transcription factor in Arabidopsis. Plant Physiol Biochem 45:260–261
Bernard DG, Cheng Y, Zhao Y, Balk J (2009) An allelic mutant series of ATM3 reveals its key role in the biogenesis of cytosolic iron-sulfur proteins in Arabidopsis. Plant Physiol 151:590–602
Briat JF, Duc C, Ravet K, Gaymard F (2010) Ferritins and iron storage in plants. Biochim Biophys Acta 1800:806–814
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
Cailliatte R, Schikora A, Briat JF, Mari S, Curie C (2010) High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell 22:904–917
Cakmak I, Erenoglu B, Gülüt K, Derici R, Römheld V (1998) Light-mediated release of phytosiderophores in wheat and barley under iron or zinc deficiency. Plant Soil 202:309–315
Chan KX, Wirtz M, Phua SY, Estavillo GM, Pogson BJ (2013) Balancing metabolites in drought: the sulfur assimilation conundrum. Trends Plant Sci 18:18–29
Chu HH, Chiecko J, Punshon T, Lanzirotti A, Lahner B, Salt DE, Walker EL (2010) Successful reproduction requires the function of Arabidopsis Yellow Stripe-Like1 and Yellow Stripe-Like3 metal-nicotianamine transporters in both vegetative and reproductive structures. Plant Physiol 154:197–210
Chu H-H, Conte SS, Chan Rodriguez D, Vasques K, Punshon T, Salt DE, Walker EL (2013) Arabidopsis thaliana Yellow Stripe1-Like4 and Yellow Stripe1-Like6 localize to internal cellular membranes and are involved in metal ion homeostasis. Front Plant Sci 4. doi:10.3389/fpls.2013.00283
Ciaffi M, Paolacci AR, Celletti S, Catarcione G, Kopriva S, Astolfi S (2013) Transcriptional and physiological changes in the S assimilation pathway due to single or combined S and Fe deprivation in durum wheat (Triticum durum L.) seedlings. J Exp Bot 64:1663–1675
Cohen CK, Fox TC, Garvin DF, Kochian LV (1998) The role of iron-deficiency stress responses in stimulating heavy-metal transport in plants. Plant Physiol 116:1063–1072
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, Fett JP, Guerinot ML (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14:1347–1357
Couturier J, Touraine B, Briat J-F, Gaymard F, Rouhier N (2013) The iron-sulfur cluster assembly machineries in plants: current knowledge and open questions. Front Plant Sci 4. doi:10.3389/fpls.2013.00259
Curie C, Alonso JM, Le Jean M, Ecker JR, Briat JF (2000) Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J 347(Pt 3):749–755
Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409:346–349
Curie C, Cassin G, Couch D, Divol F, Higuchi K, Le Jean M, Misson J, Schikora A, Czernic P, Mari S (2009) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann Bot 103:1–11
Deinlein U, Weber M, Schmidt H, Rensch S, Trampczynska A, Hansen TH, Husted S, Schjoerring JK, Talke IN, Kramer U, Clemens S (2012) Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation. Plant Cell 24:708–723
Divol F, Couch D, Conejero G, Roschzttardtz H, Mari S, Curie C (2013) The Arabidopsis Yellow Stripe LIKE4 and 6 transporters control iron release from the chloroplast. Plant Cell 25:1040–1055
Duc C, Cellier F, Lobreaux S, Briat JF, Gaymard F (2009) Regulation of iron homeostasis in Arabidopsis thaliana by the clock regulator time for coffee. J Biol Chem 284:36271–36281
Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144:197–205
Duy D, Wanner G, Meda AR, Von Wiren N, Soll J, Philippar K (2007) PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. Plant Cell 19:986–1006
Eckhardt U, Mas Marques A, Buckhout TJ (2001) Two iron-regulated cation transporters from tomato complement metal uptake-deficient yeast mutants. Plant Mol Biol 45:437–448
Forieri I, Wirtz M, Hell R (2013) Towards new perspectives on the interaction of iron and sulfur metabolism in plants. Front Plant Sci 4. doi:10.3389/fpls.2013.00357
Haydon MJ, Kawachi M, Wirtz M, Hillmer S, Hell R, Kramer U (2012) Vacuolar nicotianamine has critical and distinct roles under iron deficiency and for zinc sequestration in Arabidopsis. Plant Cell 24:724–737
Hell R, Stephan U (2003) Iron uptake, trafficking and homeostasis in plants. Planta 216:541–551
Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y, Suzuki K, Nakazono M, Nakanishi H, Mori S, Nishizawa NK (2009) Rice OsYSL15 is an iron-regulated iron (III)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings. J Biol Chem 284:3470–3479
Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, Kobayashi T, Wada Y, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2006) Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J 45:335–346
Jeong J, Cohu C, Kerkeb L, Pilon M, Connolly EL, Guerinot ML (2008) Chloroplast Fe(III) chelate reductase activity is essential for seedling viability under iron limiting conditions. Proc Natl Acad Sci U S A 105:10619–10624
Kerkeb L, Mukherjee I, Chatterjee I, Lahner B, Salt DE, Connolly EL (2008) Iron-induced turnover of the Arabidopsis IRON-REGULATED TRANSPORTER1 metal transporter requires lysine residues. Plant Physiol 146:1964–1973
Kim SA, Punshon T, Lanzirotti A, Li L, Alonso JM, Ecker JR, Kaplan J, Guerinot ML (2006) Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314:1295–1298
Klatte M, Schuler M, Wirtz M, Fink-Straube C, Hell R, Bauer P (2009) The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiol 150:257–271
Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation and regulation in higher plants. Annu Rev Plant Biol 63:131–152
Kobayashi T, Nakayama Y, Itai RN, Nakanishi H, Yoshihara T, Mori S, Nishizawa NK (2003) Identification of novel cis-acting elements, IDE1 and IDE2, of the barley IDS2 gene promoter conferring iron-deficiency-inducible, root-specific expression in heterogeneous tobacco plants. Plant J 36:780–793
Kobayashi T, Ogo Y, Itai RN, Nakanishi H, Takahashi M, Mori S, Nishizawa NK (2007) The transcription factor IDEF1 regulates the response to and tolerance of iron deficiency in plants. Proc Natl Acad Sci U S A 104:19150–19155
Kobayashi T, Itai RN, Ogo Y, Kakei Y, Nakanishi H, Takahashi M, Nishizawa NK (2009) The rice transcription factor IDEF1 is essential for the early response to iron deficiency and induces vegetative expression of late embryogenesis abundant genes. Plant J 60:948–961
Kobayashi T, Ogo Y, Aung MS, Nozoye T, Itai RN, Nakanishi H, Yamakawa T, Nishizawa NK (2010) The spatial expression and regulation of transcription factors IDEF1 and IDEF2. Ann Bot 105:1109–1117
Kobayashi T, Itai RN, Aung MS, Senoura T, Nakanishi H, Nishizawa NK (2012) The rice transcription factor IDEF1 directly binds to iron and other divalent metals for sensing cellular iron status. Plant J 69:81–91
Kushnir S, Babiychuk E, Storozhenko S, Davey MW, Papenbrock J, De Rycke R, Engler G, Stephan UW, Lange H, Kispal G, Lill R, Van Montagu M (2001) A mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell 13:89–100
Lanquar V, Lelievre F, Bolte S, Hames C, Alcon C, Neumann D, Vansuyt G, Curie C, Schroder A, Kramer U, Barbier-Brygoo H, Thomine S (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 24:4041–4051
Lill R (2009) Function and biogenesis of iron-sulphur proteins. Nature 460:831–838
Lin YF, Liang HM, Yang SY, Boch A, Clemens S, Chen CC, Wu JF, Huang JL, Yeh KC (2009) Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. New Phytol 182:392–404
Ling HQ, Koch G, Baumlein H, Ganal MW (1999) Map-based cloning of chloronerva, a gene involved in iron uptake of higher plants encoding nicotianamine synthase. Proc Natl Acad Sci U S A 96:7098–7103
Ling HQ, Bauer P, Bereczky Z, Keller B, Ganal M (2002) The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. Proc Natl Acad Sci U S A 99:13938–13943
Lingam S, Mohrbacher J, Brumbarova T, Potuschak T, Fink-Straube C, Blondet E, Genschik P, Bauer P (2011) Interaction between the bHLH transcription factor FIT and ETHYLENE INSENSITIVE3/ETHYLENE INSENSITIVE3-LIKE1 reveals molecular linkage between the regulation of iron acquisition and ethylene signaling in Arabidopsis. Plant Cell 23:1815–1829
Liu Z, Hong SW, Escobar M, Vierling E, Mitchell DL, Mount DW, Hall JD (2003) Arabidopsis UVH6, a homolog of human XPD and yeast RAD3 DNA repair genes, functions in DNA repair and is essential for plant growth. Plant Physiol 132:1405–1414
Long TA, Tsukagoshi H, Busch W, Lahner B, Salt DE, Benfey PN (2010) The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell 22:2219–2236
Marschner H (1995) Mineral nutrition of higher plants. Academic/Harcourt Brace & Company, London, pp 313–324
Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667
Morrissey J, Guerinot ML (2009) Iron uptake and transport in plants: the good, the bad, and the ionome. Chem Rev 109:4553–4567
Morrissey J, Baxter IR, Lee J, Li L, Lahner B, Grotz N, Kaplan J, Salt DE, Guerinot ML (2009) The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. Plant Cell 21:3326–3338
Nakanishi H, Yamaguchi H, Sasakuma T, Nishizawa NK, Mori S (2000) Two dioxygenase genes, Ids3 and Ids2, from Hordeum vulgare are involved in the biosynthesis of mugineic acid family phytosiderophores. Plant Mol Biol 44:199–207
Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33:633–650
Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2011) Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J Biol Chem 286:5446–5454
Ogo Y, Itai RN, Nakanishi H, Inoue H, Kobayashi T, Suzuki M, Takahashi M, Mori S, Nishizawa NK (2006) Isolation and characterization of IRO2, a novel iron-regulated bHLH transcription factor in graminaceous plants. J Exp Bot 57:2867–2878
Ogo Y, Kobayashi T, Nakanishi Itai R, Nakanishi H, Kakei Y, Takahashi M, Toki S, Mori S, Nishizawa NK (2008) A novel NAC transcription factor, IDEF2, that recognizes the iron deficiency-responsive element 2 regulates the genes involved in iron homeostasis in plants. J Biol Chem 283:13407–13417
Ogo Y, Itai RN, Kobayashi T, Aung MS, Nakanishi H, Nishizawa NK (2011) OsIRO2 is responsible for iron utilization in rice and improves growth and yield in calcareous soil. Plant Mol Biol 75:593–605
Palmgren MG (2001) Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817–845
Petit JM, Van Wuytswinkel O, Briat JF, Lobreaux S (2001) Characterization of an iron-dependent regulatory sequence involved in the transcriptional control of AtFer1 and ZmFer1 plant ferritin genes by iron. J Biol Chem 276:5584–5590
Ravet K, Touraine B, Boucherez J, Briat JF, Gaymard F, Cellier F (2009) Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis. Plant J 57:400–412
Rellan-Alvarez R, Giner-Martinez-Sierra J, Orduna J, Orera I, Rodriguez-Castrillon JA, Garcia-Alonso JI, Abadia J, Alvarez-Fernandez A (2010) Identification of a tri-iron (III), tri-citrate complex in the xylem sap of iron-deficient tomato resupplied with iron: new insights into plant iron long-distance transport. Plant Cell Physiol 51:91–102
Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697
Rogers EE, Guerinot ML (2002) FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell 14:1787–1799
Romheld V, Marschner H (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol 80:175–180
Santi S, Schmidt W (2009) Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol 183:1072–1084
Schuler M, Keller A, Backes C, Philippar K, Lenhof H-P, Bauer P (2011) Transcriptome analysis by GeneTrail revealed regulation of functional categories in response to alterations of iron homeostasis in Arabidopsis thaliana. BMC Plant Biol 11:87
Schuler M, Rellan-Alvarez R, Fink-Straube C, Abadia J, Bauer P (2012) Nicotianamine functions in the phloem-based transport of iron to sink organs, in pollen development and pollen tube growth in Arabidopsis. Plant Cell 24:2380–2400
Seckback J (1982) Ferreting out the secrets of plant ferritin − a review. J Plant Nutr 5:369–394
Shin LJ, Lo JC, Chen GH, Callis J, Fu H, Yeh KC (2013) IRT1 DEGRADATION FACTOR1, a RING E3 ubiquitin ligase, regulates the degradation of IRON-REGULATED TRANSPORTER1 in Arabidopsis. Plant Cell 25:3039–3051
Sivitz AB, Hermand V, Curie C, Vert G (2012) Arabidopsis bHLH100 and bHLH101 control iron homeostasis via a FIT-independent pathway. PLoS One 7:e44843
Tarantino D, Petit JM, Lobreaux S, Briat JF, Soave C, Murgia I (2003) Differential involvement of the IDRS cis-element in the developmental and environmental regulation of the AtFer1 ferritin gene from Arabidopsis. Planta 217:709–716
Tarantino D, Santo N, Morandini P, Casagrande F, Braun H-P, Heinemeyer J, Vigani G, Soave C, Murgia I (2010) AtFer4 ferritin is a determinant of iron homeostasis in Arabidopsis thaliana heterotrophic cells. J Plant Physiol 167:1598–1605
Teng YS, Su YS, Chen LJ, Lee YJ, Hwang I, Li HM (2006) Tic21 is an essential translocon component for protein translocation across the chloroplast inner envelope membrane. Plant Cell 18:2247–2257
Varotto C, Maiwald D, Pesaresi P, Jahns P, Salamini F, Leister D (2002) The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. Plant J 31:589–599
Vert G, Briat JF, Curie C (2001) Arabidopsis IRT2 gene encodes a root-periphery iron transporter. Plant J 26:181–189
Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot ML, Briat JF, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–1233
Vert GA, Briat JF, Curie C (2003) Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals. Plant Physiol 132:796–804
Vigani G, Zocchi G, Bashir K, Philippar K, Briat JF (2013) Signals from chloroplasts and mitochondria for iron homeostasis regulation. Trends Plant Sci 18:305–311
Von Wiren N, Mori S, Marschner H, Romheld V (1994) Iron inefficiency in maize mutant ys1 (Zea mays L. cv Yellow-Stripe) is caused by a defect in uptake of iron phytosiderophores. Plant Physiol 106:71–77
Wang HY, Klatte M, Jakoby M, Baumlein H, Weisshaar B, Bauer P (2007) Iron deficiency-mediated stress regulation of four subgroup Ib BHLH genes in Arabidopsis thaliana. Planta 226:897–908
Waters BM, Blevins DG, Eide DJ (2002) Characterization of FRO1, a pea ferric-chelate reductase involved in root iron acquisition. Plant Physiol 129:85–94
Yi Y, Guerinot ML (1996) Genetic evidence that induction of root Fe(III) chelate reductase activity is necessary for iron uptake under iron deficiency. Plant J 10:835–844
Yuan Y, Wu H, Wang N, Li J, Zhao W, Du J, Wang D, Ling HQ (2008) FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Res 18:385–397
Zancani M, Peresson C, Biroccio A, Federici G, Urbani A, Murgia I, Soave C, Micali F, Vianello A, Macrì F (2004) Evidence for the presence of ferritin in plant mitochondria. Eur J Biochem 271:3657–3664
Zheng L, Ying Y, Wang L, Wang F, Whelan J, Shou H (2010) Identification of a novel iron regulated basic helix-loop-helix protein involved in Fe homeostasis in Oryza sativa. BMC Plant Biol 10:166
Zuchi S, Cesco S, Varanini Z, Pinton R, Astolfi S (2009) Sulphur deprivation limits Fe-deficiency responses in tomato plants. Planta 230:85–94
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Forieri, I., Hell, R. (2014). Micronutrient Use Efficiency – Cell Biology of Iron and Its Metabolic Interactions in Plants. In: Hawkesford, M., Kopriva, S., De Kok, L. (eds) Nutrient Use Efficiency in Plants. Plant Ecophysiology, vol 10. Springer, Cham. https://doi.org/10.1007/978-3-319-10635-9_5
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