Skip to main content
Plant Physiology logoLink to Plant Physiology
. 1992 Mar;98(3):1074–1079. doi: 10.1104/pp.98.3.1074

Characterization of δ-Aminolevulinic Acid Formation in Soybean Root Nodules 1

Indu Sangwan 1, Mark R O'Brian 1
PMCID: PMC1080310  PMID: 16668729

Abstract

Formation of the heme precursor δ-aminolevulinic acid (ALA) was studied in soybean root nodules elicited by Bradyrhizobium japonicum. Glutamate-dependent ALA formation activity by soybean (Glycine max) in nodules was maximal at pH 6.5 to 7.0 and at 55 to 60°C. A low level of the plant activity was detected in uninfected roots and was 50-fold greater in nodules from 17-day-old plants; this apparent stimulation correlated with increases in both plant and bacterial hemes in nodules compared with the respective asymbiotic cells. The glutamate-dependent ALA formation activity was greatest in nodules from 17-day-old plants and decreased by about one-half in those from 38-day-old plants. Unlike the eukaryotic ALA formation activity, B. japonicum ALA synthase activity was not significantly different in nodules than in cultured cells, and the symbiotic activity was independent of nodule age. The lack of symbiotic induction of B. japonicum ALA synthase indicates either that ALA formation is not rate-limiting, or that ALA synthase is not the only source of ALA for bacterial heme synthesis in nodules. Plant cytosol from nodules catalyzed the formation of radiolabeled ALA from U-[14C]glutamate and 3,4-[3H]glutamate but not from 1-[14C]glutamate, and thus, operation of the C5 pathway could not be confirmed.

Full text

PDF
1074

Selected References

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

  1. Avissar Y. J., Beale S. I. Biosynthesis of Tetrapyrrole Pigment Precursors : Formation and Utilization of Glutamyl-tRNA for delta-Aminolevulinic Acid Synthesis by Isolated Enzyme Fractions from Chlorella Vulgaris. Plant Physiol. 1988 Nov;88(3):879–886. doi: 10.1104/pp.88.3.879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Avissar Y. J., Beale S. I. Identification of the enzymatic basis for delta-aminolevulinic acid auxotrophy in a hemA mutant of Escherichia coli. J Bacteriol. 1989 Jun;171(6):2919–2924. doi: 10.1128/jb.171.6.2919-2924.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Avissar Y. J., Nadler K. D. Stimulation of tetrapyrrole formation in Rhizobium japonicum by restricted aeration. J Bacteriol. 1978 Sep;135(3):782–789. doi: 10.1128/jb.135.3.782-789.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Avissar Y. J., Ormerod J. G., Beale S. I. Distribution of delta-aminolevulinic acid biosynthetic pathways among phototrophic bacterial groups. Arch Microbiol. 1989;151(6):513–519. doi: 10.1007/BF00454867. [DOI] [PubMed] [Google Scholar]
  5. Beale S. I. Biosynthesis of the Tetrapyrrole Pigment Precursor, delta-Aminolevulinic Acid, from Glutamate. Plant Physiol. 1990 Aug;93(4):1273–1279. doi: 10.1104/pp.93.4.1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Elliott T., Avissar Y. J., Rhie G. E., Beale S. I. Cloning and sequence of the Salmonella typhimurium hemL gene and identification of the missing enzyme in hemL mutants as glutamate-1-semialdehyde aminotransferase. J Bacteriol. 1990 Dec;172(12):7071–7084. doi: 10.1128/jb.172.12.7071-7084.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Guerinot M. L., Chelm B. K. Bacterial delta-aminolevulinic acid synthase activity is not essential for leghemoglobin formation in the soybean/Bradyrhizobium japonicum symbiosis. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1837–1841. doi: 10.1073/pnas.83.6.1837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ilag L. L., Jahn D., Eggertsson G., Söll D. The Escherichia coli hemL gene encodes glutamate 1-semialdehyde aminotransferase. J Bacteriol. 1991 Jun;173(11):3408–3413. doi: 10.1128/jb.173.11.3408-3413.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jahn D., Michelsen U., Söll D. Two glutamyl-tRNA reductase activities in Escherichia coli. J Biol Chem. 1991 Feb 5;266(4):2542–2548. [PubMed] [Google Scholar]
  11. Kannangara C. G., Gough S. P., Bruyant P., Hoober J. K., Kahn A., von Wettstein D. tRNA(Glu) as a cofactor in delta-aminolevulinate biosynthesis: steps that regulate chlorophyll synthesis. Trends Biochem Sci. 1988 Apr;13(4):139–143. doi: 10.1016/0968-0004(88)90071-0. [DOI] [PubMed] [Google Scholar]
  12. Keng T., Guarente L. Constitutive expression of the yeast HEM1 gene is actually a composite of activation and repression. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9113–9117. doi: 10.1073/pnas.84.24.9113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Leong S. A., Ditta G. S., Helinski D. R. Heme biosynthesis in Rhizobium. Identification of a cloned gene coding for delta-aminolevulinic acid synthetase from Rhizobium meliloti. J Biol Chem. 1982 Aug 10;257(15):8724–8730. [PubMed] [Google Scholar]
  14. Li J. M., Brathwaite O., Cosloy S. D., Russell C. S. 5-Aminolevulinic acid synthesis in Escherichia coli. J Bacteriol. 1989 May;171(5):2547–2552. doi: 10.1128/jb.171.5.2547-2552.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lien L. F., Beattie D. S. Comparisons and modifications of the colorimetric assay for delta-aminolevulinic acid synthase. Enzyme. 1982;28(2-3):120–132. doi: 10.1159/000459096. [DOI] [PubMed] [Google Scholar]
  16. McClung C. R., Somerville J. E., Guerinot M. L., Chelm B. K. Structure of the Bradyrhizobium japonicum gene hemA encoding 5-aminolevulinic acid synthase. Gene. 1987;54(1):133–139. doi: 10.1016/0378-1119(87)90355-6. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. O'Brian M. R., Kirshbom P. M., Maier R. J. Tn5-induced cytochrome mutants of Bradyrhizobium japonicum: effects of the mutations on cells grown symbiotically and in culture. J Bacteriol. 1987 Mar;169(3):1089–1094. doi: 10.1128/jb.169.3.1089-1094.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. O'Brian M. R., Maier R. J. Expression of cytochrome o in hydrogen uptake constitutive mutants of Rhizobium japonicum. J Bacteriol. 1985 Feb;161(2):507–514. doi: 10.1128/jb.161.2.507-514.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. O'Brian M. R., Maier R. J. Involvement of cytochromes and a flavoprotein in hydrogen oxidation in Rhizobium japonicum bacteroids. J Bacteriol. 1983 Aug;155(2):481–487. doi: 10.1128/jb.155.2.481-487.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. O'Brian M. R., Maier R. J. Molecular aspects of the energetics of nitrogen fixation in Rhizobium-legume symbioses. Biochim Biophys Acta. 1989 May 30;974(3):229–246. doi: 10.1016/s0005-2728(89)80239-7. [DOI] [PubMed] [Google Scholar]
  22. O'Neill G. P., Söll D. Transfer RNA and the formation of the heme and chlorophyll precursor, 5-aminolevulinic acid. Biofactors. 1990 Oct;2(4):227–235. [PubMed] [Google Scholar]
  23. Ratet P., Pawlowski K., Schell J., de Bruijn F. J. The Azorhizobium caulinodans nitrogen-fixation regulatory gene, nifA, is controlled by the cellular nitrogen and oxygen status. Mol Microbiol. 1989 Jun;3(6):825–838. doi: 10.1111/j.1365-2958.1989.tb00231.x. [DOI] [PubMed] [Google Scholar]
  24. Sangwan I., O'brian M. R. Evidence for an inter-organismic heme biosynthetic pathway in symbiotic soybean root nodules. Science. 1991 Mar 8;251(4998):1220–1222. doi: 10.1126/science.251.4998.1220. [DOI] [PubMed] [Google Scholar]
  25. Streeter J. G. Carbohydrate, organic Acid, and amino Acid composition of bacteroids and cytosol from soybean nodules. Plant Physiol. 1987 Nov;85(3):768–773. doi: 10.1104/pp.85.3.768. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES