Skip to main content
SpringerLink
Log in

A soybean coproporphyrinogen oxidase gene is highly expressed in root nodules

  • Research Article
  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

In plants the enzyme coproporphyrinogen oxidase catalyzes the oxidative decarboxylation of coproporphyrinogen III to protoporphyrinogen IX in the heme and chlorophyll biosynthesis pathway(s).

We have isolated a soybean coproporphyrinogen oxidase cDNA from a cDNA library and determined the primary structure of the corresponding gene. The coproporphyrinogen oxidase gene encodes a polypeptide with a predicted molecular mass of 43 kDa. The derived amino acid sequence shows 50% similarity to the corresponding yeast amino acid sequence. The main difference is an extension of 67 amino acids at the N-terminus of the soybean polypeptide which may function as a transit peptide.

A full-length coproporphyrinogen oxidase cDNA clone complements a yeast mutant deleted of the coproporphyrinogen oxidase gene, thus demonstrating the function of the soybean protein.

The soybean coproporphyrinogen oxidase gene is highly expressed in nodules at the stage where several late nodulins including leghemoglobin appear. The coproporphyrinogen oxidase mRNA is also detectable in leaves but at a lower level than in nodules while no mRNA is detectable in roots.

The high level of coproporphyrinogen oxidase mRNA in soybean nodules implies that the plant increases heme production in the nodules to meet the demand for additional heme required for hemoprotein formation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Alderson A, Sabelli PA, Dickinson JR, Cole D, Richardson M, Kreis M, Shewry PR, Halford NG: Complementation of snf1, a mutation affecting global regulation of carbon metabolism in yeast, by a plant protein kinase cDNA. Proc Natl Acad Sci USA 88: 8602–8605 (1991).

    Google Scholar 

  2. Appleby CA: Leghemoglobin and Rhizobium respiration. Annu Rev Plant Physiol 35: 443–478 (1984).

    Google Scholar 

  3. Bogard M, Camadro J, Nordmann Y, Labbe P: Purification and properties of mouse liver coproporphyrinogen oxidase. Eur J Biochem 181: 417–421 (1989).

    Google Scholar 

  4. Brown JWS: A catalogue of splice junction and putative branch point sequence from plant introns. Nucl Acids Res 14: 9549–9559 (1986).

    Google Scholar 

  5. deBruijn FJ, Felix G, Grunenberg B, Hoffmann HJ, Metz B, Ratet P, Simons-Schreier A, Szabados L, Welters P, Schell J: Regulation of plant genes specifically induced in nitrogen-fixing nodules: role of cis-acting factors in leghemoglobin gene expression. Plant Mol Biol 13: 319–325 (1989).

    Google Scholar 

  6. Camadro J, Chambon H, Jolles J, Labbe P: Purification and properties of coproporphyrinogen oxidase from the yeast Saccharomyces cerevisiae. Eur J Biochem 156: 579–587 (1986).

    Google Scholar 

  7. Castelfranco PA, Weinstein JD, Schwarcz S, Pardo AD, Wezelman BE: The Mg insertion step in chlorophyll biosynthesis. Arch Biochem Biophys 192: 592–598 (1979).

    Google Scholar 

  8. Cutting JA, Schulman HM: The site of heme synthesis in soybean root nodules. Biochim Biophys Acta 192: 486–493 (1969).

    Google Scholar 

  9. Dean C, Tamaki S, Dunsmuir P, Favreau M, Katayama C, Dooner H, Bedbrook J: mRNA transcripts of several plant genes are polyadenylated at multiple sites in vivo. Nucl Acids Res 14: 2229–2240 (1986).

    Google Scholar 

  10. Dickstein R, Scheier DC, Fowle WH, Ausubel FM: Nodules elicited by Rhizobium meliloti heme mutants are arrested at an early stage of development. Mol Gen Genet 230: 423–432 (1991).

    Google Scholar 

  11. Frustaci JM, O'Brian MR: Characterization of a Bradyrhizobium japonicum ferrochelatase mutant and isolation of the hemH gene. J Bact 174: 4223–4229 (1992).

    Google Scholar 

  12. Guerinot ML, Chelm BK: Bacterial δ-aminolevulinic acid synthase activity is not essential for leghemoglobin formation in the soybean/Bradyrhizobium japonicum symbiosis. Proc Natl Acad Sci USA 86: 1837–1841 (1986).

    Google Scholar 

  13. vonHeijne G, Steppuhn J, Herrmann RG, Domain structure of mitochondrial and chloroplast targeting peptides. Eur J Biochem 180: 535–545 (1989).

    Google Scholar 

  14. Hsu WP, Miller GW: Coproporphyrinogenase in tobacco. Biochem J 117: 215–220 (1970).

    Google Scholar 

  15. Ito H, Fukuda Y, Murata K, Kimura A: Transformation of intact yeast cells treated with alkali cations. J Bact 153: 163–168 (1983).

    Google Scholar 

  16. Jacobs NJ, Borotz SE, Guerinot ML: Protoporphyrinogen oxidation, a step in heme synthesis in soybean root nodules and free-living rhizobia. J Bact 171: 573–576 (1989).

    Google Scholar 

  17. Jacobs JM, Jacobs NJ, Borotz SE, Guerinot ML: Effects of the photobleaching herbicide, acofluorfenmethyl, on protoporphyrinogen oxidation in barley organelles, soybean root nodules, and bacteria. Arch Biochem Biophys 280: 369–375 (1990).

    Google Scholar 

  18. Joshi CP: An inspection of the domain between putative TATA box and translation start site in 79 plant genes. Nucl Acids Res 15: 6643–6653 (1987).

    Google Scholar 

  19. Keegstra K, Olsen LJ, Theg SM: Chloroplastic precursors and their transport across the envelope membranes. Annu Rev Plant Physiol Plant Mol Biol 40: 471–501 (1989).

    Google Scholar 

  20. Larsen K, Jochimsen BU: Expression of nodule-specific uricase in soybean callus tissue is regulated by oxigen. EMBO J 5: 15–19 (1986).

    Google Scholar 

  21. Leong SA, Ditta GS, Helinski DR: Heme biosynthesis in Rhizobium. J Biol Chem 257: 8724–8730 (1982).

    Google Scholar 

  22. Lütcke HA, Chow KC, Mickel FS, Moss KS, Kern HF, Scheele GA: Selection of AUG initiation codons differs in plants and animals. EMBO J 6: 43–48 (1987).

    Google Scholar 

  23. Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1982).

    Google Scholar 

  24. Marcker A, Lund M, Jensen EØ, Marcker KA: Transcription of the soybean leghemoglobin genes during nodule development. EMBO J 3: 1691–1695 (1984).

    Google Scholar 

  25. Minet M, Dufour M, Lacroute F: Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J 2: 417–422 (1992).

    Google Scholar 

  26. Mohapatra SS, Pühler A: Detection of nodule specific pomypeptides from effective and ineffective root nodules of Medicago sativa L. Plant Physiol 126: 269–281 (1986).

    Google Scholar 

  27. Nadler KD, Avissar YJ: Heme synthesis in soybean root nodules. Plant Physiol 60: 433–436 (1977).

    Google Scholar 

  28. Newcomb W: Nodule morphogenesis and differentiation. In: Bourne GH, Danielli JF, Jeon KW (eds) International Review of Cytology, suppl. 13: Biology of the Rhizobiaceae, pp. 247–298. Academic Press, New York (1981).

    Google Scholar 

  29. Pawlowski K, Gough SP, Kannangara CG, deBruijn FJ: Characterization of a 5-aminolevulinic acid synthase mutant of Azorhizobium caulinodans ORS571. Mol Plant-Microb Interact 6: 35–44 (1993).

    Google Scholar 

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

    Google Scholar 

  31. Sangwan I, O'Brian MR: Evidence for an interorganismic heme biosynthetic pathway in symbiotic soybean root nodules. Science 251: 1220–1222 (1991).

    Google Scholar 

  32. Sangwan I, O'Brian MR: Characterization of δ-aminolevulinic acid formation in soybean root nodules. Plant Physiol 98: 1074–1079 (1992).

    Google Scholar 

  33. Sentenac H, Bonneaud N, Minet M, Lacroute F, Salmon J, Gaymard R, Grignon C: Cloning and expression in yeast of a plant potassium ion transport system. Science 256: 663–665 (1992).

    Google Scholar 

  34. Sikorski RS and Hieter P: A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19–27 (1989).

    Google Scholar 

  35. Smith AG, Marsh O, Elder GH: Investigation of the subcellular location of the tetrapyrrole biosynthesis enzyme coproporphyrinogen oxidase in higher plants. Biochem J 292: 503–508 (1993).

    Google Scholar 

  36. Stanley J, Dowling DN, Broughton WJ: Cloning of hemA from Rhizobium sp. NGR234 and symbiotic phenotype of a gene-directed mutant in diverse legume genera. Mol Gen Genet 215: 32–37 (1988).

    Google Scholar 

  37. Vasse J, deBilly F, Camut S, Truchet G: Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J Bact 172: 4295–4306 (1990).

    Google Scholar 

  38. Weinstein JD, Castelfranco PA: Protoporphyrin IX biosynthesis from glutamate in isolated greening chloroplast. Arch Biochem Biophys 178: 671–673 (1977).

    Google Scholar 

  39. Yoshinaga T, Sano S: Coproporphyrinogen oxidase. J Biol Chem 255: 4722–4726 (1980).

    Google Scholar 

  40. Yoshinaga T, Sano S: Coproporphyrinogen oxidase. J Biol Chem 255: 4727–4731 (1980).

    Google Scholar 

  41. Zagorec M, Labbe-Bois R: Negative control of yeast coproporphyrinogen oxidase synthesis by heme and oxygen J Biol Chem 261: 2506–2509 (1986).

    Google Scholar 

  42. Zagorec M, Buhler J, Treich I, Keng T, Guarente L, Labbe-Bois R: Isolation, sequence, and regulation by oxygen of the yeast HEM13 gene coding for coproporphyrinogen oxidase. J Biol Chem 263: 9718–9724 (1988).

    Google Scholar 

  43. Xue Z, Larsen K, Jochimsen BU: Oxygen regulation of uricase and sucrose synthase synthesis in soybean callus tissue is exerted at the mRNA level. Plant Mol Biol 16: 899–906 (1991).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Gene Expression, Department of Molecular Biology, University of Aarhus, Gustav Wieds Vej 10, DK-8000, Aarhus C, Denmark

    Ole Madsen, Lene Sandal, Niels N. Sandal & Kjeld A. Marcker

Authors
  1. Ole Madsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lene Sandal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Niels N. Sandal
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kjeld A. Marcker
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Madsen, O., Sandal, L., Sandal, N.N. et al. A soybean coproporphyrinogen oxidase gene is highly expressed in root nodules. Plant Mol Biol 23, 35–43 (1993). https://doi.org/10.1007/BF00021417

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00021417

Key words

Search

Navigation