Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1996 Jun 11;93(12):5682–5687. doi: 10.1073/pnas.93.12.5682

A new hemoglobin gene from soybean: a role for hemoglobin in all plants.

C R Anderson 1, E O Jensen 1, D J LLewellyn 1, E S Dennis 1, W J Peacock 1
PMCID: PMC39120  PMID: 8650152

Abstract

We have isolated a new hemoglobin gene from soybean. It is expressed in cotyledons, stems of seedlings, roots, young leaves, and in some cells in the nodules that are associated with the nitrogen-fixing Bradyrhizobium symbiont. This contrasts with the expression of the leghemoglobins, which are active only in the infected cells of the nodules. The deduced protein sequence of the new gene shows only 58% similarity to one of the soybean leghemoglobins, but 85-87% similarity to hemoglobins from the nonlegumes Parasponia, Casuarina, and barley. The pattern of expression and the gene sequence indicate that this new gene is a nonsymbiotic legume hemoglobin. The finding of this gene in legumes and similar genes in other species strengthens our previous suggestion that genomes of all plants contain hemoglobin genes. The specialized leghemoglobin gene family may have arisen from a preexisting nonsymbiotic hemoglobin by gene duplication.

Full text

PDF
5686

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Appleby C. A., Tjepkema J. D., Trinick M. J. Hemoglobin in a nonleguminous plant, parasponia: possible genetic origin and function in nitrogen fixation. Science. 1983 May 27;220(4600):951–953. doi: 10.1126/science.220.4600.951. [DOI] [PubMed] [Google Scholar]
  2. Bogusz D., Appleby C. A., Landsmann J., Dennis E. S., Trinick M. J., Peacock W. J. Functioning haemoglobin genes in non-nodulating plants. Nature. 1988 Jan 14;331(6152):178–180. doi: 10.1038/331178a0. [DOI] [PubMed] [Google Scholar]
  3. Burke T. J., Callis J., Vierstra R. D. Characterization of a polyubiquitin gene from Arabidopsis thaliana. Mol Gen Genet. 1988 Aug;213(2-3):435–443. doi: 10.1007/BF00339613. [DOI] [PubMed] [Google Scholar]
  4. Christensen T., Dennis E. S., Peacock J. W., Landsmann J., Marcker K. A. Hemoglobin genes in non-legumes: cloning and characterization of a Casuarina glauca hemoglobin gene. Plant Mol Biol. 1991 Feb;16(2):339–344. doi: 10.1007/BF00020566. [DOI] [PubMed] [Google Scholar]
  5. Gallusci P., Dedieu A., Journet E. P., Huguet T., Barker D. G. Synchronous expression of leghaemoglobin genes in Medicago truncatula during nitrogen-fixing root nodule development and response to exogenously supplied nitrate. Plant Mol Biol. 1991 Sep;17(3):335–349. doi: 10.1007/BF00040629. [DOI] [PubMed] [Google Scholar]
  6. Hirano H. Microsequence analysis of winged bean seed proteins electroblotted from two-dimensional gel. J Protein Chem. 1989 Feb;8(1):115–130. doi: 10.1007/BF01025083. [DOI] [PubMed] [Google Scholar]
  7. Hyldig-Nielsen J. J., Jensen E. O., Paludan K., Wiborg O., Garrett R., Jørgensen P., Marcker K. A. The primary structures of two leghemoglobin genes from soybean. Nucleic Acids Res. 1982 Jan 22;10(2):689–701. doi: 10.1093/nar/10.2.689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Jacobsen-Lyon K., Jensen E. O., Jørgensen J. E., Marcker K. A., Peacock W. J., Dennis E. S. Symbiotic and nonsymbiotic hemoglobin genes of Casuarina glauca. Plant Cell. 1995 Feb;7(2):213–223. doi: 10.1105/tpc.7.2.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Konieczny A. Nucleotide sequence of lupin leghemoglobin I cDNA. Nucleic Acids Res. 1987 Aug 25;15(16):6742–6742. doi: 10.1093/nar/15.16.6742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lee J. S., Verma D. P. Structure and chromosomal arrangement of leghemoglobin genes in kidney bean suggest divergence in soybean leghemoglobin gene loci following tetraploidization. EMBO J. 1984 Dec 1;3(12):2745–2752. doi: 10.1002/j.1460-2075.1984.tb02205.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lehtovaara P., Lappalainen A., Ellfolk N. The amino acid sequence of pea (Pisum sativum) leghemoglobin. Biochim Biophys Acta. 1980 May 29;623(1):98–106. doi: 10.1016/0005-2795(80)90012-4. [DOI] [PubMed] [Google Scholar]
  12. Metz B. A., Welters P., Hoffmann H. J., Jensen E. O., Schell J., de Bruijn F. J. Primary structure and promoter analysis of leghemoglobin genes of the stem-nodulated tropical legume Sesbania rostrata: conserved coding sequences, cis-elements and trans-acting factors. Mol Gen Genet. 1988 Oct;214(2):181–191. doi: 10.1007/BF00337709. [DOI] [PubMed] [Google Scholar]
  13. Miao G. H., Verma D. P. Soybean nodulin-26 gene encoding a channel protein is expressed only in the infected cells of nodules and is regulated differently in roots of homologous and heterologous plants. Plant Cell. 1993 Jul;5(7):781–794. doi: 10.1105/tpc.5.7.781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Nap J. P., Bisseling T. Developmental biology of a plant-prokaryote symbiosis: the legume root nodule. Science. 1990 Nov 16;250(4983):948–954. doi: 10.1126/science.250.4983.948. [DOI] [PubMed] [Google Scholar]
  15. Ramlov K. B., Laursen N. B., Stougaard J., Marcker K. A. Site-directed mutagenesis of the organ-specific element in the soybean leghemoglobin lbc3 gene promoter. Plant J. 1993 Sep;4(3):577–580. doi: 10.1046/j.1365-313x.1993.04030577.x. [DOI] [PubMed] [Google Scholar]
  16. Richardson M., Dilworth M. J., Scawen M. D. The amino acid sequence of leghaemoglobin I from root nodules of broad bean (Vicia faba L.). FEBS Lett. 1975 Mar 1;51(1):33–37. doi: 10.1016/0014-5793(75)80849-0. [DOI] [PubMed] [Google Scholar]
  17. Sherman D. R., Guinn B., Perdok M. M., Goldberg D. E. Components of sterol biosynthesis assembled on the oxygen-avid hemoglobin of Ascaris. Science. 1992 Dec 18;258(5090):1930–1932. doi: 10.1126/science.1470914. [DOI] [PubMed] [Google Scholar]
  18. Stougaard J., Sandal N. N., Grøn A., Kühle A., Marcker K. A. 5' Analysis of the soybean leghaemoglobin lbc(3) gene: regulatory elements required for promoter activity and organ specificity. EMBO J. 1987 Dec 1;6(12):3565–3569. doi: 10.1002/j.1460-2075.1987.tb02686.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Szczyglowski K., Szabados L., Fujimoto S. Y., Silver D., de Bruijn F. J. Site-specific mutagenesis of the nodule-infected cell expression (NICE) element and the AT-rich element ATRE-BS2* of the Sesbania rostrata leghemoglobin glb3 promoter. Plant Cell. 1994 Mar;6(3):317–332. doi: 10.1105/tpc.6.3.317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Taylor E. R., Nie X. Z., MacGregor A. W., Hill R. D. A cereal haemoglobin gene is expressed in seed and root tissues under anaerobic conditions. Plant Mol Biol. 1994 Mar;24(6):853–862. doi: 10.1007/BF00014440. [DOI] [PubMed] [Google Scholar]
  21. Wiborg O., Hyldig-Nielsen J. J., Jensen E. O., Paludan K., Marcker K. A. The nucleotide sequences of two leghemoglobin genes from soybean. Nucleic Acids Res. 1982 Jun 11;10(11):3487–3494. doi: 10.1093/nar/10.11.3487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Wiborg O., Hyldig-Nielsen J. J., Jensen E. O., Paludan K., Marcker K. A. The structure of an unusual leghemoglobin gene from soybean. EMBO J. 1983;2(3):449–452. doi: 10.1002/j.1460-2075.1983.tb01443.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Zhu H., Riggs A. F. Yeast flavohemoglobin is an ancient protein related to globins and a reductase family. Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):5015–5019. doi: 10.1073/pnas.89.11.5015. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES