Skip to main content
PMC home page
Plant Physiology logoLink to Plant Physiology
. 1994 Apr;104(4):1411–1417. doi: 10.1104/pp.104.4.1411

Plant delta-aminolevulinic acid dehydratase. Expression in soybean root nodules and evidence for a bacterial lineage of the Alad gene.

C M Kaczor 1, M W Smith 1, I Sangwan 1, M R O'Brian 1
PMCID: PMC159307  PMID: 8016269

Abstract

We isolated a soybean (Glycine max) cDNA encoding the heme and chlorophyll synthesis enzyme delta-aminolevulinic acid (ALA) dehydratase by functional complementation of an Escherichia coli hemB mutant, and we designated the gene Alad. ALA dehydratase was strongly expressed in nodules but not in uninfected roots, although Alad mRNA was only 2- to 3-fold greater in the symbiotic tissue. Light was not essential for expression of Alad in leaves of dark-grown etiolated plantlets as discerned by mRNA, protein, and enzyme activity levels; hence, its expression in subterranean nodules was not unique in that regard. The data show that soybean can metabolize the ALA it synthesizes in nodules, which argues in favor of tetrapyrrole formation by the plant host in that organ. Molecular phylogenetic analysis of ALA dehydratases from 11 organisms indicated that plant and bacterial enzymes have a common lineage not shared by animals and yeast. We suggest that plant ALA dehydratase is descended from the bacterial endosymbiont ancestor of chloroplasts and that the Alad gene was transferred to the nucleus during plant evolution.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

Selected References

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

  1. Bauer C. E., Bollivar D. W., Suzuki J. Y. Genetic analyses of photopigment biosynthesis in eubacteria: a guiding light for algae and plants. J Bacteriol. 1993 Jul;175(13):3919–3925. doi: 10.1128/jb.175.13.3919-3925.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bishop T. R., Frelin L. P., Boyer S. H. Nucleotide sequence of rat liver delta-aminolevulinic acid dehydratase cDNA. Nucleic Acids Res. 1986 Dec 22;14(24):10115–10115. doi: 10.1093/nar/14.24.10115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bishop T. R., Hodes Z. I., Frelin L. P., Boyer S. H. Cloning and sequence of mouse erythroid delta-aminolevulinate dehydratase cDNA. Nucleic Acids Res. 1989 Feb 25;17(4):1775–1775. doi: 10.1093/nar/17.4.1775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burke D. H., Alberti M., Hearst J. E. bchFNBH bacteriochlorophyll synthesis genes of Rhodobacter capsulatus and identification of the third subunit of light-independent protochlorophyllide reductase in bacteria and plants. J Bacteriol. 1993 Apr;175(8):2414–2422. doi: 10.1128/jb.175.8.2414-2422.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Caetano-Anollés G., Gresshoff P. M. Plant genetic control of nodulation. Annu Rev Microbiol. 1991;45:345–382. doi: 10.1146/annurev.mi.45.100191.002021. [DOI] [PubMed] [Google Scholar]
  6. Dickstein R., Scheirer D. C., Fowle W. H., Ausubel F. M. Nodules elicited by Rhizobium meliloti heme mutants are arrested at an early stage of development. Mol Gen Genet. 1991 Dec;230(3):423–432. doi: 10.1007/BF00280299. [DOI] [PubMed] [Google Scholar]
  7. Frustaci J. M., O'Brian M. R. Analysis of the Bradyrhizobium japonicum hemH gene and its expression in Escherichia coli. Appl Environ Microbiol. 1993 Aug;59(8):2347–2351. doi: 10.1128/aem.59.8.2347-2351.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Frustaci J. M., O'Brian M. R. Characterization of a Bradyrhizobium japonicum ferrochelatase mutant and isolation of the hemH gene. J Bacteriol. 1992 Jul;174(13):4223–4229. doi: 10.1128/jb.174.13.4223-4229.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Frustaci J. M., Sangwan I., O'Brian M. R. Aerobic growth and respiration of a delta-aminolevulinic acid synthase (hemA) mutant of Bradyrhizobium japonicum. J Bacteriol. 1991 Feb;173(3):1145–1150. doi: 10.1128/jb.173.3.1145-1150.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gray M. W. The evolutionary origins of organelles. Trends Genet. 1989 Sep;5(9):294–299. doi: 10.1016/0168-9525(89)90111-x. [DOI] [PubMed] [Google Scholar]
  11. Hansson M., Rutberg L., Schröder I., Hederstedt L. The Bacillus subtilis hemAXCDBL gene cluster, which encodes enzymes of the biosynthetic pathway from glutamate to uroporphyrinogen III. J Bacteriol. 1991 Apr;173(8):2590–2599. doi: 10.1128/jb.173.8.2590-2599.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Li J. M., Russell C. S., Cosloy S. D. The structure of the Escherichia coli hemB gene. Gene. 1989 Jan 30;75(1):177–184. doi: 10.1016/0378-1119(89)90394-6. [DOI] [PubMed] [Google Scholar]
  13. Madsen O., Sandal L., Sandal N. N., Marcker K. A. A soybean coproporphyrinogen oxidase gene is highly expressed in root nodules. Plant Mol Biol. 1993 Oct;23(1):35–43. doi: 10.1007/BF00021417. [DOI] [PubMed] [Google Scholar]
  14. Nadler K. D., Avissar Y. J. Heme Synthesis in Soybean Root Nodules: I. On the Role of Bacteroid delta-Aminolevulinic Acid Synthase and delta-Aminolevulinic Acid Dehydrase in the Synthesis of the Heme of Leghemoglobin. Plant Physiol. 1977 Sep;60(3):433–436. doi: 10.1104/pp.60.3.433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Porra R. J. A rapid spectrophotometric assay for ferrochelatase activity in preparations containing much endogenous hemoglobin and its application to soybean root-nodule preparations. Anal Biochem. 1975 Sep;68(1):289–298. doi: 10.1016/0003-2697(75)90707-1. [DOI] [PubMed] [Google Scholar]
  16. Sangwan I., O'Brian M. R. Expression of the soybean (Glycine max) glutamate 1-semialdehyde aminotransferase gene in symbiotic root nodules. Plant Physiol. 1993 Jul;102(3):829–834. doi: 10.1104/pp.102.3.829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Sangwan I., O'brian M. R. Characterization of delta-Aminolevulinic Acid Formation in Soybean Root Nodules. Plant Physiol. 1992 Mar;98(3):1074–1079. doi: 10.1104/pp.98.3.1074. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Smith A. G. Subcellular localization of two porphyrin-synthesis enzymes in Pisum sativum (pea) and Arum (cuckoo-pint) species. Biochem J. 1988 Jan 15;249(2):423–428. doi: 10.1042/bj2490423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Udvardi M. K., Kahn M. L. Isolation and analysis of a cDNA clone that encodes an alfalfa (Medicago sativa) aspartate aminotransferase. Mol Gen Genet. 1991 Dec;231(1):97–105. doi: 10.1007/BF00293827. [DOI] [PubMed] [Google Scholar]
  20. Verma DPS. Signals in Root Nodule Organogenesis and Endocytosis of Rhizobium. Plant Cell. 1992 Apr;4(4):373–382. doi: 10.1105/tpc.4.4.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Wetmur J. G., Bishop D. F., Cantelmo C., Desnick R. J. Human delta-aminolevulinate dehydratase: nucleotide sequence of a full-length cDNA clone. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7703–7707. doi: 10.1073/pnas.83.20.7703. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES