Skip to main content
Log in

Ferritin gene organization: Differences between plants and animals suggest possible kingdom-specific selective constraints

  • Articles
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Ferritin, a protein widespread in nature, concentrates iron −1011−1012-fold above the solubility within a spherical shell of 24 subunits; it derives in plants and animals from a common ancestor (based on sequence) but displays a cytoplasmic location in animals compared to the plastid in contemporary plants. Ferritin gene regulation in plants and animals is altered by development, hormones, and excess iron; iron signals target DNA in plants but mRNA in animals. Evolution has thus conserved the two end points of ferritin gene expression, the physiological signals and the protein structure, while allowing some divergence of the genetic mechanisms.

Comparison of ferritin gene organization in plants and animals, made possible by the cloning of a dicot (soy-bean) ferritin gene presented here and the recent cloning of two monocot (maize) ferritin genes, shows evolutionary divergence in ferritin gene organization between plants and animals but conservation among plants or among animals; divergence in the genetic mechanism for iron regulation is reflected by the absence in all three plant genes of the IRE, a highly conserved, noncoding sequence in vertebrate animal ferritin mRNA. In plant ferritin genes, the number of introns (n = 7) is higher than in animals (n = 3). Second, no intron positions are conserved when ferritin genes of plants and animals are compared, although all ferritin gene introns are in the coding region; within kingdoms, the intron positions in ferritin genes are conserved. Finally, secondary protein structure has no apparent relationship to intron/exon boundaries in plant ferritin genes, whereas in animal ferritin genes the correspondence is high. The structural differences in introns/exons among phylogenetically related ferritin coding sequences and the high conservation of the gene structure within plant or animal kingdoms suggest that kingdom-specific functional constraints may exist to maintain a particular intron/exon pattern within ferritin genes. In the case of plants, where ferritin gene intron placement is unrelated to triplet codons or protein structure, and where ferritin is targeted to the plastid, the selection pressure on gene organization may relate to RNA function and plastid/nuclear signaling.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Andrews SC, Harrison PM, Guest JR (1989) Cloning, sequencing, and mapping of the bacterioferritin gene (bfr) of Escherichia coli K-12. J Bacteriol 171:3940–3947

    CAS  PubMed  Google Scholar 

  • Andrews SC, Smith JMA, Yewdall SJ, Guest JR, Harrison PM (1991) Bacterioferritins and ferritins are distantly related in evolution. FEBS Lett 293:164–168

    Article  CAS  PubMed  Google Scholar 

  • Andrews SC, Arosio P, Bottke W, Briat J-F, Von Darl M, Harrison PM, Laulhere J-P, Levi S, Lobreaux S, Yewdall SJ (1992) Structure, function, and evolution of ferritins. J Inorg Biochem 47:161–174

    Article  CAS  PubMed  Google Scholar 

  • Banyard SH, Stammers DK, Harrison PM (1978) Electron density map of apoferritin at 2.8 A resolution. Nature 271:282–284

    Article  CAS  PubMed  Google Scholar 

  • Bäumlein H, Nagy I, Villarroel R (1992) Cis-analysis of a seed protein gene promoter: the conservative RY repeat CATGCATG within the legumin box is essential for tissue-specific expression of a legumin gene. Plant J 2:233–238

    PubMed  Google Scholar 

  • Beaumont C, Jain SK, Bogard M, Nordmann Y, Drysdale J (1987) Ferritin synthesis in differentiating friend erythroleukemic cells. J Biol Chem 262:10619–10623

    CAS  PubMed  Google Scholar 

  • Biedenkapp H, Borgmeyer U, Sippel AE, Klempnauer K-H (1988) Viral myb oncogene encodes a sequence-specific DNA-binding activity. Nature 335:835–837

    Article  CAS  PubMed  Google Scholar 

  • Blake CCF (1985) Exons and the evolution of proteins. Int Rev Cytol 93:149–185

    CAS  PubMed  Google Scholar 

  • Bottke W, Von Darl M, Harrison PM (1994) cDNA cloning and deduced amino acid sequence of two ferritins: soma ferritin and yolk ferritin, from the snail Lymnaea stagnalis L Eur J Biochem 222: 353–357

    PubMed  Google Scholar 

  • Brandl R, Mann E, Springe M (1992) Estimate of monocot-dicot divergence through tRNA sequences from chloroplasts. Proc R Soc Lond [Biol] 24713–24717

  • Brown JEB, Theil EC (1978) Red cells, ferritin and iron storage during amphibian development. J Biol Chem 253:2673–2678

    CAS  PubMed  Google Scholar 

  • Chazenbalk GD, Wadsworth HL, Rapoport B (1990) Transcriptional regulation of ferritin H messenger RNA levels in FRTL5 rat thyroid cells by thyrotropin. J Biol Chem 265:666–670

    CAS  PubMed  Google Scholar 

  • Costanzo F, Colombo M, Staempfli S, Santoro C, Marone M, Frank R, Delius H, Cortese R (1986) Structure of gene and pseudogenes of human apoferritin H. Nucleic Acids Res 14:721–736

    CAS  PubMed  Google Scholar 

  • Craik CS, Sprang S, Fletterick R, Rutter WJ (1982) Intron-exon splice junctions map at protein surfaces. Nature 299:180–182

    Article  CAS  PubMed  Google Scholar 

  • Crichton RR (1990) Proteins of iron storage and transport. Adv Protein Chem 40:281–353

    CAS  PubMed  Google Scholar 

  • Daniels-McQueen S, Ray A, Walden WE, Ray BK, Brown PH, Thach RE (1988) Nucleotide sequence of cDNA encoding rabbit ferritin L chain. Nucleic Acids Res 16:7741–7741

    CAS  PubMed  Google Scholar 

  • Darnell JE (1978) Implications of RNA splicing in evolution of eukaryotic cells. Science 202:1257–1260

    CAS  PubMed  Google Scholar 

  • Darnell JE, Doolittle WF (1986) Speculations on the early course of evolution. Proc Natl Acad Sci USA 83:1271–1275

    CAS  PubMed  Google Scholar 

  • Dickey LF, Sreedharan S, Theil EC, Didsbury JR, Wang YH, Kaufman RE (1987) Differences in the regulation of messenger RNA for housekeeping and specialized-cell ferritin. J Biol Chem 262:7901–7907

    PubMed  Google Scholar 

  • Didsbury JR, Theil EC, Kaufman RE, Dickey LF (1986) Multiple red cell ferritin mRNAs, which code for an abundant protein in the embryonic cell type, analyzed by cDNA sequence and by primer extension of the 5′-untranslated regions. J Biol Chem 261:949–955

    CAS  PubMed  Google Scholar 

  • Dietzel J, Hirzmann J, Preis D, Symmons P, Kunz W (1992) Ferritins of Schistosoma mansoni: sequence comparison and expression in female and male worms. Mol Biochem Parasitol 50:245–254

    Article  CAS  PubMed  Google Scholar 

  • Dixon B, Walker B, Kimmins W, Pohajdak B (1992) A nematode hemoglobin gene contains an intron previously thought to be unique to plants. J Mol Evol 35:131–136

    Article  CAS  PubMed  Google Scholar 

  • Doolittle WF (1978) Genes in pieces: were they ever together? Nature 272:581–582

    Article  Google Scholar 

  • Drysdale JW, Munro HN (1966) Regulation of synthesis and turnover of ferritin in rat liver. J Biol Chem 241:3630–3637

    CAS  PubMed  Google Scholar 

  • Fobis-Loisy I, Loridon K, Lobreaux S, Lebrun M, Briat J-F (1995) Structure and differential expression of two maize ferritin genes in response to iron and abscisic acid. Eur J Biochem 231:609–619

    Article  CAS  PubMed  Google Scholar 

  • Gerl M, Jaenicke R (1988) Self-assembly of apoferritin from horse spleen after reversible chemical modification with 1,3 dimethylmaleic anhydride. Biochemistry 27:4089–4096

    Article  CAS  PubMed  Google Scholar 

  • Gilbert W (1978) Why genes in pieces? Nature 271:501

    Article  CAS  PubMed  Google Scholar 

  • Gilbert W (1985) Genes in pieces revisited. Science 228:823–824

    CAS  PubMed  Google Scholar 

  • Goldscmidt-Clermont M, Rahire M (1986) Sequence, evolution and differential expression of the two genes encoding variant small subunits of ribulose bisphosphate carboxylase/oxygenase in chlamydomonas reinhardtii. J Mol Biol 191:421–432

    Google Scholar 

  • Goodall GJ, Kiss T, Filipowicz W (1991) Nuclear RNA splicing and small nuclear RNAs and their genes in higher plants. Oxf Surv Plant Mol Cell Biol 7:255–296

    CAS  Google Scholar 

  • Grossman MJ, Hinton SM, Minak-Bernero V, Slaughter C, Stiefel EI (1992) Unification of the ferritin family of proteins. Proc Natl Acad Sci USA 89:2419–2423

    CAS  PubMed  Google Scholar 

  • Harrison PM, Lilley TH (1990) Ferritin. In: Loehr TM (ed) Iron carriers and iron proteins. VCH, Weinheim, p 353

    Google Scholar 

  • Harrison PM, Ford GC, Smith JMA, White JL (1991) The location of exon boundaries in the multimeric iron storage protein ferritin. Biol Metals 4:95–99

    Article  CAS  Google Scholar 

  • Infante AA, Infante D, Rimland J (1993) Ferritin gene expression is developmentally regulated and induced by heat shock in sea urchin embryos. J Dev Genet 14:58–68

    CAS  Google Scholar 

  • Karin M, Haslinger A, Heguy A, Dietlin T, Cooke T (1987) Metal-responsive elements act as positive modulators of human metallothionein-IIA enhancer activity. Mol Cell Biol 7:606–613

    CAS  PubMed  Google Scholar 

  • Kersanach R, Brinkmann H, Liaud M-F, De-Xing Z, Martin W, Cerff R (1994) Five identical intron positions in ancient duplicated genes of eubacterial origin. Nature 367:387–389

    Article  CAS  PubMed  Google Scholar 

  • Kimata Y, Theil EC (1994) Posttranscriptional regulation of ferritin during nodule development in soybean. Plant Physiol 104:263–270

    Article  CAS  PubMed  Google Scholar 

  • Klausner RD, Rouault TA, Harford JB (1993) Regulating the fate of mRNA: the control of cellular iron metabolism. Cell 72:19–28

    Article  CAS  PubMed  Google Scholar 

  • Laulhere J-P, Laboure A-M, Briat J-F (1989) Mechanism of the transition from plant ferritin to phytosiderin. J Biol Chem 264:3629–3635

    CAS  PubMed  Google Scholar 

  • Lee VD, Stapleton M, Huang B (1991) Genomic structure of chlamydomonas caltractin. Evidence for intron insertion suggests a probable genealogy for the EF-hand superfamily of proteins. J Mol Biol 221:175–191

    Article  CAS  PubMed  Google Scholar 

  • Leibold EA, Munro HN (1987) Characterization and evolution of the expressed rat ferritin light subunit gene and its pseudogene family. J Biol Chem 262:7335–7341

    CAS  PubMed  Google Scholar 

  • Lescure A-M, Proudhon D, Pesey H, Ragland M, Theil EC, Briat J-F (1991) Ferritin gene transcription is regulated by iron in soybean cell cultures. Proc Natl Acad Sci USA 88:8222–8226

    CAS  PubMed  Google Scholar 

  • Lewin R (1984) Surprise finding with insect globin genes. Science 226:328

    Google Scholar 

  • Liaud M-F, Brinkmann H, Cerff R (1992) The beta-tubulin gene family of pea: primary structures, genomic organization and intron-dependent evolution of genes. Plant Mol Biol 18:639–651

    Article  CAS  PubMed  Google Scholar 

  • Linder MC, Moor JR, Scott LE, Munro HN (1972) Prenatal and post-natal changes in the content and species of ferritin in rat liver. Biochem J 129:455–1162

    CAS  PubMed  Google Scholar 

  • Lobreaux S, Briat J-F (1991) Ferritin accumulation and degradation in different organs of pea during development. Biochem J 274:601–606

    CAS  PubMed  Google Scholar 

  • Lobreaux S, Yewdall SJ, Briat J-F, Harrison PM (1992a) Amino acid sequence and predicted three dimensional structure of pea seed (pisum sativum) ferritin. Biochem J 288:931–939

    CAS  Google Scholar 

  • Lobreaux S, Massenet O, Briat J-F (1992b) Iron induces ferritin synthesis in maize plantlets. Plant Mol Biol 19:563–575

    Article  CAS  Google Scholar 

  • Lobreaux S, Hardy T, Briat J-F (1993) Abscisic acid is involved in the iron-induced synthesis of maize ferritin. EMBO J 12:651–657

    CAS  PubMed  Google Scholar 

  • Marcotte WR, Russell SH, Quatrano RS (1989) Abscissic acid-responsive sequences from the Em gene of wheat. Plant Cell 1: 969–976

    CAS  PubMed  Google Scholar 

  • Mertz JR, Theil EC (1983) Subunit dimers in sheep spleen apoferritin. J Biol Chem 258:11719–11726

    CAS  PubMed  Google Scholar 

  • Moskaitis JE, Pastori RL, Schoenberg D (1990) Sequence of Xenopus laevis ferritin mRNA. Nucleic Acids Res 18:2184–2184

    CAS  PubMed  Google Scholar 

  • Munro HN (1990) Iron regulation of ferritin gene expression. J Cell Biochem 44:107–115

    Article  CAS  PubMed  Google Scholar 

  • Murray MT, White K, Munro HN (1987) Conservation of ferritin heavy subunit gene structure: implications for the regulation of ferritin gene expression. Proc Natl Acad Sci USA 84:7438–7442

    CAS  PubMed  Google Scholar 

  • Murre C, McCaw PS, Baltimore D (1989) A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughter-less, MyoLD, and myc proteins. Cell 56:777–783

    Article  CAS  PubMed  Google Scholar 

  • Ohama T, Kumazaki T, Hori H, Osawa S (1984) Evolution of multi-cellular animals as deduced from 5S rRNA sequences: a possible early emergence of the mesozoa. Nucleic Acids Res 12:5101–5108

    CAS  PubMed  Google Scholar 

  • Patthy L (1987) Intron-dependent evolution: preferred types of exons and inrons. FEBS Lett 214:1–7

    Article  CAS  PubMed  Google Scholar 

  • Patthy L (1990) Homology of a domain of the growth hormone and prolactin receptor family with type III modules of fibronectin. Cell 61:13–14

    Article  CAS  PubMed  Google Scholar 

  • Pearson L, Meagher RB (1990) Diverse soybean actin transcripts contain a large intron in the 5′ untranslated leader: structural similarity to vertebrate muscle actin genes. Plant Mol Biol 14:513–526

    Article  CAS  PubMed  Google Scholar 

  • Proudhon D, Briat J-F, Lescure A-M (1989) Iron induction of ferritin synthesis in soybean cell suspensions. Plant Physiol 90:586–590

    CAS  Google Scholar 

  • Quigley F, Martin W, Cerff R (1988) Intron conservation across the prokaryote-eukaryote boundary: Structure of the nuclear gene for chloroplast glyceraldehyde-3-phosphate dehydrogenase from maize. Proc Natl Acad Sci USA 85:2672–2676

    CAS  PubMed  Google Scholar 

  • Ragland M, Briat J-F, Gagnon J, Laulhere J-P, Massenet O, Theil EC (1990) Evidence for a conservation of ferritin sequences among plants and animals and for a transit peptide in soybean. J Biol Chem 265:18339–18344

    CAS  PubMed  Google Scholar 

  • Ragland M, Theil EC (1993) Ferritin and iron are developmentally regulated in nodules. Plant Mol Biol 21:555–560

    Article  CAS  PubMed  Google Scholar 

  • Rice DW, Ford GC, White JL, Smith JMA, Harrison PM (1983) The spacial structure of horse spleen apoferritin. In: Theil EC, Eichorn GL, Marzilli G (eds) Advances in inorganic biochemistry 5 iron binding proteins without cofactors or sulfur clusters. Elsevier Science, New York, pp 39–50

    Google Scholar 

  • Rogers JH (1990) The role of introns in evolution. FEBS Lett 268: 339–343

    Article  CAS  PubMed  Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain termination inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    CAS  PubMed  Google Scholar 

  • Santoro C, Maron M, Ferrone M, Costanzo F, Colombo M, Minganti C, Cortese R, Silengo L (1986) Cloning of the gene coding for human L apoferritin. Nucleic Acids Res 14:2863–2876

    CAS  PubMed  Google Scholar 

  • Saunders SE, Burke JF (1990) Rapid isolation of miniprep DNA for double strand sequencing. Nucleic Acids Res 18:4948

    CAS  PubMed  Google Scholar 

  • Schaefer FV, Theil EC (1981) The effect of iron on the synthesis and amount of ferritin in red blood cells during ontogeny. J Biol Chem 256:1711–1715

    CAS  PubMed  Google Scholar 

  • Shull GE, Theil EC (1982) Translational control of ferritin synthesis by iron in embryonic reticulocytes of the bullfrog. J Biol Chem 257: 14187–14191

    CAS  PubMed  Google Scholar 

  • Shull GE, Theil EC (1983) Regulation of ferritin mRNA: a possible gene-sparing phenomenon. J Biol Chem 258:7921–7923

    CAS  PubMed  Google Scholar 

  • Spence MJ, Henzl MT, Lammers PJ (1991) The structure of a Phaseolus vulgaris cDNA encoding the iron storage protein ferritin. Plant Mol Biol 17:499–504

    Article  CAS  PubMed  Google Scholar 

  • Stefanini S, Vechinni P, Chiancone E (1987) On the mechanism of horse spleen apoferritin assembly: a sedimentation velocity and circular dichroism study. Biochemistry 26:1831–1837

    Article  CAS  PubMed  Google Scholar 

  • Stevens PW, Dodgson JB, Engel JD (1987) Structure and expression of the chicken ferritin H-subunit gene. Mol Cell Biol 7:1751–1758

    CAS  PubMed  Google Scholar 

  • Szczyglowski K, Szabados L, Fujimoto SY, Silver D, deBruijn FJ (1994) Site-specific mutagenesis of the nodule-infected cell expression (NICE) element and the AT-rich element ATRE-BS2 of the Sesbania rostrata leghemoglobin g1b3 promoter. Plant Cell 6:312–317

    Article  Google Scholar 

  • Takeda S, Ohta M, Ebina S, Nagayama K (1993) Cloning, expression and characterization of horse L-ferritin in escherichia coli. Biochim Biophys Acta 1174:218–220

    CAS  PubMed  Google Scholar 

  • Theil EC (1978) The induction of ferritin synthesis in circulating larval red blood cells. J Biol Chem 253:2902–2904

    CAS  PubMed  Google Scholar 

  • Theil EC, Brenner WE (1981) The ferritin content of human red blood cells during the replacement of embryonic cells by fetal cells. Dev Biol 84:481–484

    Article  CAS  Google Scholar 

  • Theil EC (1981) Red cell ferritin and iron storage during the early hemoglobin switch. In: Stamatoyannopoulos G, Nienhuis A (eds) Hemoglobins in development and differentiation. Alan R. Liss, New York, p 423

    Google Scholar 

  • Theil EC (1987) Ferritin: structure, gene regulation, and cellular function in animals, plants and microorganisms. Annu Rev Biochem 56:289–315

    Article  CAS  PubMed  Google Scholar 

  • Theil EC (1990a) Regulation of ferritin and transferrin receptor (TR) mRNAs. J Biol Chem 265:4771–4774

    CAS  Google Scholar 

  • Theil EC (1990b) The ferritin family of iron storage proteins. Adv Enzymol 63:421–449

    CAS  Google Scholar 

  • Theil EC (1994) Iron regulatory elements (IREs): a family of mRNA non-coding sequences. Biochem J 304:1–11

    PubMed  Google Scholar 

  • Theil EC, Toshiharu H (1993) Plant and microbial ferritins. In: Iron chelation in plants and soil microorganisms 5. Academic Press, San Diego, pp 133–156

    Google Scholar 

  • Tittiger C, Whyard S, Walker VK (1993) A novel intron site in the triosephosphate isomerase gene from the mosquito Culex tarsalis. Nature 361:470–472

    Article  CAS  PubMed  Google Scholar 

  • Torti SW, Kwak EL, Miller SC, Miller LL, Ringold GM, Myambo KB, Young AP, Torti FM (1988) The molecular cloning and characterization of murine ferritin heavy chain, a tumor necrosis factor inducible gene. J Biol Chem 263:12638–12644

    CAS  PubMed  Google Scholar 

  • Traut TW (1988) Do exons code for structural or functional units in proteins? Proc Natl Acad Sci USA 85:2944–2948

    CAS  PubMed  Google Scholar 

  • Trikha J, Waldo GS, Lewandowski FA, Ha A, Theil EC, Weber PC, Allewell NM (1994) Crystallization and structural analysis of bull-frog red cell L-subunit ferritins. Proteins 18:107–118

    Article  CAS  PubMed  Google Scholar 

  • Trikha J, Theil EC, Allewell NM (1995) High resolution crystal structures of amphibian red cell L ferritin: potential roles for structural plasticity and solvation in function. J Mol Biol 248:949–967

    Article  CAS  PubMed  Google Scholar 

  • Van Der Mark F, Van Der Briel W, Huisman HG (1983) Phytoferritin is synthesized in vitro as a high molecular weight precursor. Biochem J 214: 943–950

    PubMed  Google Scholar 

  • Van Wuytswinkel O, Savino G, Briat J-F (1995a) Purification and characterization of recombinant pea seed ferritins expressed in escherichia coli: influence of amino terminus deletions on protein solubility and in vitro core formation. Biochem J 305:253–261

    Google Scholar 

  • Wade VJ, Levi S, Arosio P, Treffry A, Harrison PM, Mann S (1991) Influence of site directed modifications on formation of iron cores in ferritin. J Mol Biol 221:1443–1452

    Article  CAS  PubMed  Google Scholar 

  • Waldo GS, Ling J, Sanders-Loehr J, Theil EC (1993) Formation of an Fe(III)-tyrosinate complex during biomineralization of H-subunit ferritin. Science 259:796–798

    CAS  PubMed  Google Scholar 

  • Waldo GS, Theil EC (1995) Ferritin and iron biomineralization. In: Suslick KS (ed) Comprehensive supramolecular chemistry, bioinorganic systems 5. Pergamon Press, Oxford (in press)

    Google Scholar 

  • Waldo GS, Wright E, Wang ZH, Briat J-F, Theil EC, Sayers DE (1995) Formation of the ferritin iron mineral occurs in plastids: an X-ray absorption spectroscopy (exafs) study. Plant Physiol 109:797–802

    Article  CAS  PubMed  Google Scholar 

  • White K, Munro HN (1988) Induction of ferritin subunit synthesis by iron is regulated at both the transcriptional and translational levels. J Biol Chem 263:8938–8942

    CAS  PubMed  Google Scholar 

  • Wicks RE, Entsch B (1993) Functional genes found for three different plant ferritin subunits in the legume vigna unguiculata. Bioch Biophys Res Commun 192:813–819

    CAS  Google Scholar 

  • Wolfe KH, Goug M, Yang YW, Sharp PM, Li WH (1989) Date of the monocot-dicot divergence from chloroplast DNA sequence data. Proc Natl Acad Sci USA 86:6201–6205

    CAS  PubMed  Google Scholar 

  • Wolter FP, Fritz CC, Willmitzer L, Shell J, Schreier PH (1988) rbcS genes in solarium Tuberosum: conservation of transit peptide and exon shuffling during evolution. Proc Natl Acad Sci USA 85:846–850

    CAS  PubMed  Google Scholar 

  • Wright HT (1993) Introns and higher-order structure in the evolution of serpins. J Mol Evol 36:136–143

    Article  CAS  Google Scholar 

  • Yachaou A, Renaudie F, Grandchamp B, Beaumont C (1989) Nucleotide sequence of the mouse ferritin H chain gene. Nucleic Acids Res 17:8005–8005

    Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki (1994) A novel cis-acting element in anArabidopsis gene is involved in responsiveness to drought, low temperature, or high-salt stress. Plant Cell 6:251–264

    Article  CAS  PubMed  Google Scholar 

  • Zahringer J, Baliga BS, Munro FIN (1976) Novel mechanism for translational control of ferritin synthesis by iron. Proc Natl Acad Sci USA 73:857–861

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Correspondence to: E.C. Theil

Rights and permissions

Reprints and permissions

About this article

Cite this article

Proudhon, D., Wei, J., Briat, J.F. et al. Ferritin gene organization: Differences between plants and animals suggest possible kingdom-specific selective constraints. J Mol Evol 42, 325–336 (1996). https://doi.org/10.1007/BF02337543

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02337543

Key words

Navigation