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. 1994 Jan;104(1):263–270. doi: 10.1104/pp.104.1.263

Posttranscriptional regulation of ferritin during nodule development in soybean.

Y Kimata 1, E C Theil 1
PMCID: PMC159185  PMID: 8115547

Abstract

During soybean (Glycine max) nodule development, induced ferritin mRNA concentration remains elevated while the protein concentration decreases 4- to 5-fold (M. Ragland and E.C. Theil [1993] Plant Mol Biol 21: 555-560). Investigation of posttranscriptional regulation of nodule ferritin during development showed that ferritin mRNA was efficiently translated based on polyribosome size in vivo, protein synthesis (0.8% of total protein) in vitro, and protein synthesis in intact nodules. Ferritin, a plastid protein, was processed in both immature and mature nodules. In chimeric mRNA, soybean ferritin mRNA sequences blocked the function of the iron regulatory element (IRE), the cis regulatory element of animal ferritin mRNA; the IRE regulates chimeric animal mRNAs. The absence of translational regulation of ferritin in plants contrasts with ferritin regulation in animals. Thus, ferritin regulation has diverged during evolution, whereas structure of the mature protein has been conserved. Ferritin in mature soybean nodules is apparently regulated after translation, possibly in analogy with such plastid proteins as chlorophyll-binding proteins D1, CP43, LHCI, and LHCII, the small subunit of ribulose-bisphosphate carboxylase, and apoplastocyanin. An autocatalytic mechanism observed in vivo for degradation of plastid protein D1 and in vitro for pea ferritin during iron release could explain the ferritin decreases in mature nodules.

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Selected References

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  1. Apel K. Phytochrome-induced appearance of mRNA activity for the apoprotein of the light-harvesting chlorophyll a/b protein of barley (Hordeum vulgare). Eur J Biochem. 1979 Jun;97(1):183–188. doi: 10.1111/j.1432-1033.1979.tb13101.x. [DOI] [PubMed] [Google Scholar]
  2. Dickey L. F., Wang Y. H., Shull G. E., Wortman I. A., 3rd, Theil E. C. The importance of the 3'-untranslated region in the translational control of ferritin mRNA. J Biol Chem. 1988 Mar 5;263(7):3071–3074. [PubMed] [Google Scholar]
  3. Dix D. J., Lin P. N., Kimata Y., Theil E. C. The iron regulatory region of ferritin mRNA is also a positive control element for iron-independent translation. Biochemistry. 1992 Mar 17;31(10):2818–2822. doi: 10.1021/bi00125a024. [DOI] [PubMed] [Google Scholar]
  4. Dix D. J., Lin P. N., McKenzie A. R., Walden W. E., Theil E. C. The influence of the base-paired flanking region on structure and function of the ferritin mRNA iron regulatory element. J Mol Biol. 1993 May 20;231(2):230–240. doi: 10.1006/jmbi.1993.1278. [DOI] [PubMed] [Google Scholar]
  5. Haile D. J., Rouault T. A., Harford J. B., Kennedy M. C., Blondin G. A., Beinert H., Klausner R. D. Cellular regulation of the iron-responsive element binding protein: disassembly of the cubane iron-sulfur cluster results in high-affinity RNA binding. Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11735–11739. doi: 10.1073/pnas.89.24.11735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hentze M. W., Caughman S. W., Rouault T. A., Barriocanal J. G., Dancis A., Harford J. B., Klausner R. D. Identification of the iron-responsive element for the translational regulation of human ferritin mRNA. Science. 1987 Dec 11;238(4833):1570–1573. doi: 10.1126/science.3685996. [DOI] [PubMed] [Google Scholar]
  7. Hill K. L., Merchant S. In Vivo Competition between Plastocyanin and a Copper-Dependent Regulator of the Chlamydomonas reinhardtii Cytochrome c(6) Gene. Plant Physiol. 1992 Sep;100(1):319–326. doi: 10.1104/pp.100.1.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hunt T., Luca F. C., Ruderman J. V. The requirements for protein synthesis and degradation, and the control of destruction of cyclins A and B in the meiotic and mitotic cell cycles of the clam embryo. J Cell Biol. 1992 Feb;116(3):707–724. doi: 10.1083/jcb.116.3.707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kennedy M. C., Mende-Mueller L., Blondin G. A., Beinert H. Purification and characterization of cytosolic aconitase from beef liver and its relationship to the iron-responsive element binding protein. Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11730–11734. doi: 10.1073/pnas.89.24.11730. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Klaff P., Gruissem W. Changes in Chloroplast mRNA Stability during Leaf Development. Plant Cell. 1991 May;3(5):517–529. doi: 10.1105/tpc.3.5.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Klausner R. D., Rouault T. A., Harford J. B. Regulating the fate of mRNA: the control of cellular iron metabolism. Cell. 1993 Jan 15;72(1):19–28. doi: 10.1016/0092-8674(93)90046-s. [DOI] [PubMed] [Google Scholar]
  12. Lescure A. M., Proudhon D., Pesey H., Ragland M., Theil E. C., Briat J. F. Ferritin gene transcription is regulated by iron in soybean cell cultures. Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):8222–8226. doi: 10.1073/pnas.88.18.8222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Li H. M., Theg S. M., Bauerle C. M., Keegstra K. Metal-ion-center assembly of ferredoxin and plastocyanin in isolated chloroplasts. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6748–6752. doi: 10.1073/pnas.87.17.6748. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lobreaux S., Briat J. F. Ferritin accumulation and degradation in different organs of pea (Pisum sativum) during development. Biochem J. 1991 Mar 1;274(Pt 2):601–606. doi: 10.1042/bj2740601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lobréaux S., Hardy T., Briat J. F. Abscisic acid is involved in the iron-induced synthesis of maize ferritin. EMBO J. 1993 Feb;12(2):651–657. doi: 10.1002/j.1460-2075.1993.tb05698.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ragland M., Briat J. F., Gagnon J., Laulhere J. P., Massenet O., Theil E. C. Evidence for conservation of ferritin sequences among plants and animals and for a transit peptide in soybean. J Biol Chem. 1990 Oct 25;265(30):18339–18344. [PubMed] [Google Scholar]
  17. Ragland M., Theil E. C. Ferritin (mRNA, protein) and iron concentrations during soybean nodule development. Plant Mol Biol. 1993 Feb;21(3):555–560. doi: 10.1007/BF00028813. [DOI] [PubMed] [Google Scholar]
  18. Schmidt G. W., Mishkind M. L. Rapid degradation of unassembled ribulose 1,5-bisphosphate carboxylase small subunits in chloroplasts. Proc Natl Acad Sci U S A. 1983 May;80(9):2632–2636. doi: 10.1073/pnas.80.9.2632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Shipton C. A., Barber J. Characterisation of photoinduced breakdown of the D1-polypeptide in isolated reaction centres of Photosystem II. Biochim Biophys Acta. 1992 Jan 30;1099(1):85–90. [PubMed] [Google Scholar]
  20. Shipton C. A., Barber J. Photoinduced degradation of the D1 polypeptide in isolated reaction centers of photosystem II: evidence for an autoproteolytic process triggered by the oxidizing side of the photosystem. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6691–6695. doi: 10.1073/pnas.88.15.6691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Theil E. C. The IRE (iron regulatory element) family: structures which regulate mRNA translation or stability. Biofactors. 1993 May;4(2):87–93. [PubMed] [Google Scholar]
  22. Wang Y. H., Sczekan S. R., Theil E. C. Structure of the 5' untranslated regulatory region of ferritin mRNA studied in solution. Nucleic Acids Res. 1990 Aug 11;18(15):4463–4468. doi: 10.1093/nar/18.15.4463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Zähringer J., Baliga B. S., Munro H. N. Novel mechanism for translational control in regulation of ferritin synthesis by iron. Proc Natl Acad Sci U S A. 1976 Mar;73(3):857–861. doi: 10.1073/pnas.73.3.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. van der Mark F., Bienfait F., van den Ende H. Variable amounts of translatable ferritin mRNA in bean leaves with various iron contents. Biochem Biophys Res Commun. 1983 Sep 15;115(2):463–469. doi: 10.1016/s0006-291x(83)80167-3. [DOI] [PubMed] [Google Scholar]

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