Skip to main content
Log in

Ferritin (mRNA, protein) and iron concentrations during soybean nodule development

  • Update Section
  • Short Communication
  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

To study how iron-rich nodules concentrate and store iron, ferritin (mRNA, protein) was analyzed in developing soybean nodules and compared to nitrogenase (mRNA/activity) and leghemoglobin (mRNA, protein, heme). Both ferritin mRNA and protein concentrations increased early in nodulation. Later in nodulation ferritin protein declined, in contrast to the mRNA, as nitrogenase (mRNA and activity) increased and leghemoglobin (mRNA and protein) accumulated. A precursor/product relationship between iron stored in ferritin and iron in nitrogenase or leghemoglobin is suggested. The uncoordinated changes in ferritin mRNA and protein during nodulation contrast with nitrogenase mRNA and nitrogenase activity suggesting possible translational and posttranscriptional effects on ferritin expression.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

References

  1. Ahmed S, Evans HJ: Cobalt: a micronutrient element for the growth of soybean plants under symbiotic conditions. Soil Sci 90: 205–210 (1960).

    Google Scholar 

  2. Andrews S, Harrison PM, Guest JR: Cloning, sequencing and mapping of the bacterioferritin gene (bfv) of Escherichia coli K-12. J Bact 171: 3940–3947 (1989).

    PubMed  Google Scholar 

  3. Beaumont C, Dugast F, Renaudie F, Soyroujon M, Grandchamp B: Transcriptional regulation of ferritin in adult erythroid and liver cells of the mouse. J Biol Chem 264: 7498–7504 (1989).

    PubMed  Google Scholar 

  4. Bergerson FJ: The bacterial component of soybean root nodules; changes in respiratory activity, cell dry weight and nucleic acid content with increasing nodule age. J Gen Microbiol 19: 312–323 (1958).

    PubMed  Google Scholar 

  5. Bergerson FJ: Iron in the developing soybean nodule. Aust J Biol Sci 16: 916–919 (1963).

    Google Scholar 

  6. Brewin NJ: Development of the legume root nodule. Ann Rev Cell Biol 7: 191–226 (1991).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  8. Chou CC, Gotti RA, Fuller ML, Concannon P, Wong A, Chader S, Davis RC, Salser WA: Structure and expression of ferritin genes in a promyelocytic line that differentiates in vitro. Mol Cell Biol 6: 566–573 (1986).

    PubMed  Google Scholar 

  9. Cox F, Gestautas J, Rapaport B: Molecular cloning of cDNA corresponding to mRNA species whose steady state levels in the thyroid are enhanced by thyrotropin. J Biol Chem 263: 7060–7067 (1988).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  11. Fortin MG, Zelechowska M, Verma DPS: Specific targeting of membrane nodulins to the bacteroid enclosing compartment in soybean nodules. EMBO J 4: 3041–4036 (1985).

    Google Scholar 

  12. Fuhrmann M, Hennecke H: Coding properties of cloned nitrogenase structural genes from Rhizobium japonicum. Mol Gen Genet 187: 419–425 (1982).

    Google Scholar 

  13. Fuhrmann M, Hennecke H: Rhizobium japonicum nitrogenase Fe protein gene (nif H). J Bact 158: 1005–1011 (1984).

    PubMed  Google Scholar 

  14. Garbers C, Meckbach R, Mellor RB, Werner D: Protease (Thermolysis) inhibition activity in the peribacteroid space of Glycine max nodules. J Plant Physiol 132: 442–445 (1988).

    Google Scholar 

  15. Ko MP, Huang PY, Huang JS, Barker KR: Accumulation of phytoferritin and starch granules in developing nodules of soybean roots infected with Heterodera glycines. Cytol Histol 75: 159–164 (1985).

    Google Scholar 

  16. Laulhere JP, Lescure AM, Briat JF: Purification and characterization of ferritins from maize, pea and soybean seeds. J Biol Chem 263: 10289–10294 (1988).

    PubMed  Google Scholar 

  17. Laulhere JP, Labourre AM, Briat JF: Mechanisms of transition from plant ferritin to phytosiderin. J Biol Chem 264: 3629–3635 (1989).

    PubMed  Google Scholar 

  18. Laulhere JP, Laboure AM, Briat JF: Photoreduction and incorporation of iron into ferritins. Biochem J 269: 79–84 (1990).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  20. Lobreaux S, Briat JF: Ferritin accumulation and degradation in different organs of pea (Pisum sativum) during development. Biochem J 274: 601–606 (1991).

    PubMed  Google Scholar 

  21. Long S: Rhizobium-legume nodulation: life together in the underground. Cell 56: 203–214 (1989).

    Article  PubMed  Google Scholar 

  22. Manen JF, Simon P, vanSlooten JC, Osterias M, Frutiger S, Hughes J: A nodulin specifically expressed in nodules of winged bean is a protease inhibitor. Plant Cell 3: 259–270 (1991).

    Article  PubMed  Google Scholar 

  23. Marcker AM, Lund M, Jensen EO, Marcker KA: Transcription of soybean leghemoglobin genes during nodule development. EMBO J 3: 1691–1695 (1984).

    Google Scholar 

  24. McClure PR, Israel DW: Transport of nitrogen in the xylem of soybean plants. Plant Physiol 64: 4414–4416 (1979).

    Google Scholar 

  25. McKenzie RA, Yablonski MJ, Gillespie GY, Theil EC: Cross-links between intramolecular pairs of ferritin subunits: effects on both H and L subunits and on immunoreactivity of sheep spleen ferritin. Arch Biochem Biophys 272: 88–96 (1989).

    PubMed  Google Scholar 

  26. Munro HN, Linder MC: Ferritin: structure, biosynthesis and role in iron metabolism. Physiol Rev 58: 317–396 (1978).

    PubMed  Google Scholar 

  27. Nap JP, Bisseling T: The roots of nodulins. Physiol Plantarum 79: 407–414 (1990).

    Article  Google Scholar 

  28. Nap JP, Bisseling T: Developmental biology of a plant-prokaryote symbiosis: the legume root nodule. Science 250: 948–984 (1990).

    Google Scholar 

  29. O'Hara GW, Dilworth MJ, Boonkerd N, Parkian P: Iron deficiency specifically limits nodule development in peanut inoculated with Bradyrhizobium sp. New Phytol 108: 51–57 (1988).

    Google Scholar 

  30. Ragland M, Briat JF, Gagnon J, Laulhere JP, Massenet O, Theil EC: Evidence for conservation of ferritin sequences among plants and animals and for a transit peptide in soybean. J Biol Chem 263: 18339–18344 (1990).

    Google Scholar 

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

    PubMed  Google Scholar 

  32. Sczekan SR, Joshi JG: Isolation and characterization of ferritin from soybeans (Glycine max). J Biol Chem 262: 13780–13786 (1987).

    PubMed  Google Scholar 

  33. Seckback J: Studies on the detection of plant ferritin as influenced by iron supply to iron-deficient beans. J Ultrastruc Res 22: 413–423 (1968).

    Google Scholar 

  34. Seckback J: Ferreting out the secrets of plant ferritin-a review. J Plant Nutr 5: 369–394 (1982).

    Google Scholar 

  35. Sloger C: Symbiotic effectiveness and N2 fixation in nodulated soybean. Plant Physiol 44: 1666–1668 (1968).

    Google Scholar 

  36. Stripf R, Warner D: Differentiation of Rhizobium japonicum II. Enzymatic activities in bacteroids and plant cytoplasm. Z Naturforsch 33: 373–381 (1978).

    Google Scholar 

  37. Tang C, Robson AD, Dilworth MJ: The role of iron in nodulation and nitrogen fixation in Lupinus augustifolius L. New Phytol 114: 174–182 (1990).

    Google Scholar 

  38. Tang C, Robson AD, Dilworth MJ: A split root experiment shows that iron is required for nodule initiation in Lupinus augustifolius L. New Phytol 115: 61–67 (1990).

    Google Scholar 

  39. Terry RE, Sorensen KU, Jolley VD, Brown JC: The role of active Bradyrhizobium japonicum in iron stress response of soybeans. Plant Soil 130: 225–230 (1991).

    Google Scholar 

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

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  44. Van derMark F, Bienfait F, van denEnde N: Variable amounts of translatable ferritin mRNA in bean leaves with various iron contents. Biochem Biophys Res Comm 115: 463–469 (1983).

    PubMed  Google Scholar 

  45. Van derMark F, van denBriel W: Purification and partial characterization of ferritin from normal and iron-loaded leaves of Phaseolus vulgaris. Plant Sci 39: 55–60 (1985).

    Article  Google Scholar 

  46. Verma DPS, Ball S, Guerin C, Wanamaker L: Leghemoglobin biosynthesis in soybean root nodules. Characterization of the nascent and released peptides and the relative rates of synthesis of the major leghemoglobins. Biochemistry 18: 476–483 (1978).

    Google Scholar 

  47. Verma DPS: Nodulins and nodulin genes of Glycine max. Plant Mol Biol 7: 51–61 (1986).

    Google Scholar 

  48. Whatley JN: Variations in the basic pathway of chloroplast development. New Phytol 78: 407–420 (1977).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ragland, M., Theil, E.C. Ferritin (mRNA, protein) and iron concentrations during soybean nodule development. Plant Mol Biol 21, 555–560 (1993). https://doi.org/10.1007/BF00028813

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00028813

Key words

Navigation