Skip to main content
SpringerLink
Log in
Book cover

Plant Nitrogen Metabolism pp 43–63Cite as

Plant Genes Involved in Carbon and Nitrogen Assimilation in Root Nodules

  • Chapter

Part of the book series: Recent Advances in Phytochemistry ((RAPT,volume 23))

Abstract

The availability of reduced nitrogen is the most limiting factor in plant growth. In legume plants, nitrogen is provided by symbiotic bacteria (Rhizobium spp.) in exchange for carbon supplied by the host as photosynthates. A significant portion (25 to 30%) of the carbon received by nodules from photosynthates is returned to the shoot as nitrogenous solutes. Thus, not only are large amounts of energy required to support nitrogen fixation, but assimilation of that nitrogen is also energy intensive. It has been suggested that C02 fixation in the dark, catalyzed by phosphoenolpyruvate (PEP) carboxylase, can function as an anapleurotic pathway to supply part of the carbon skeleton needed for nitrogen assimilation.1 Legumes of temperate regions generally assimilate and export fixed nitrogen as amides, while the tropical legumes, e. g., soybean, synthesize ureides (allantoin and allantoic acid) that account for > 90% of the nitrogen in their xylem sap.2 Extensive studies have been carried out to calculate the carbon/nitrogen budget of several legumes, but our knowledge of the regulatory mechanisms controlling the expression of genes involved in carbon and nitrogen pathways in nodules is very limited. Moreover, we do not know how the regulation of these genes is affected by the supply of carbon and nitrogen and different levels of oxygen present in infected and uninfected cells of the nodules.

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. SCHUBERT, K.R. 1986. Products of biological nitrogen fixation in higher plants: synthesis, transport and metabolism. Annu Rev. Plant Physiol. 37: 539–574.

    Article  Google Scholar 

  2. McCLURE, P.E., D.W. ISRAEL. 1979. Transport of nitrogen in the xylem of soybean plants. Plant Physiol. 64: 411–416.

    Article  Google Scholar 

  3. ATKINS, C.A., R.M. RAINBIRD, J.S. PATE. 1980. Evidence for a purine pathway of ureide synthesis in nitrogen-fixing nodules of cowpea (Vigna unguiculata L. Walp). Z. Pflanzenphysiol. 97: 249–260.

    Google Scholar 

  4. BOLAND, M.J., J.F. HANKS, P.H.S. REYNOLDS, D.G. BLEVINS, N.E. TOLBERT, K.R. SCHUBERT. 1982. Subcellular organization of ureide biogenesis from glycolytic intermediates and ammonium in nitrogen-fixing soybean nodules. Planta 155: 45–51.

    Article  Google Scholar 

  5. TAJIMA, S., Y. YAMAMOTO. 1975. Enzymes of purine catabolism in soybean plants. Plant Cell Physiol. 16: 271–282.

    Google Scholar 

  6. SCHUBERT, K.R. 1981. Enzymes of purine biosynthesis and catabolism in Glycine max L. Plant Physiol. 68: 1115–1122.

    Article  Google Scholar 

  7. ATKINS, C.A. 1981. Metabolism of purine nucleotides to form ureides in nitrogen-fixing nodules of cowpea (Vigna unguiculata L. Walp). FEBS Lett. 125: 89–93.

    Article  Google Scholar 

  8. REYNOLDS, P.H.S., M.J. BOLAND, D.G. BLEVINS, K.R. SCHUBERT, D.D. RANDALL. 1982. Enzymes of amide and ureide biogenesis in developing soybean nodules. Plant Physiol. 69: 1334–1338.

    Article  Google Scholar 

  9. ATKINS, C.A., P.J. STORER, J.S. PATE. 1988. Pathways of nitrogen assimilation in cowpea nodules studied using 15N2 and allopurinol. Plant Physiol. 86: 204–207.

    Article  Google Scholar 

  10. VERMA, D.P.S., M.G. FORTIN. 1988. Nodule develop ment and formation of the endosymbiotic compartment. In The Molecular Biology of Nuclear Genes. (I.K. Vasil, ed.), Academic Press, New York, in press.

    Google Scholar 

  11. OAKS, A., B. HIREL. 1985. Nitrogen metabolism in roots. Annu. Rev. Plant Physiol. 36: 345–365.

    Article  Google Scholar 

  12. CULLIMORE, J.V., M. LARA, P.J. LEA, B.J. MIFLIN. 1983. Purification and properties of two forms of glutamine synthetase from the plant fraction of Phaseolus root nodules. Planta 147: 245–253.

    Article  Google Scholar 

  13. DUNN, K., R. DICKSTEIN, R. FEINBAUM, B.K. BURNETT, T.K. PETERMAN, G. THOIDIS, H.M. GOODMAN, F.M. AUSUBEL. 1988. Developmental regulation of nodule-specific genes in alfalfa root nodules. Mol. Plant Microbe Interactions 1: 66–75.

    Article  Google Scholar 

  14. GEBHARDT, C., J.E. OLIVER, B.G. FORDE, R. SAARELAINEN, B.J. MIFLIN. 1986. Primary structure and differential expression of glutamine synthetase genes in nodules, roots and leaves of Phaseolus vulgaris. EMBO J. 5: 1429–1435.

    Google Scholar 

  15. TINGEY, S.V., E.L. WALKER, G.M. CORUZZI. 1987. Glutamine synthetase genes of pea encode distinct polypeptides which are differentially expressed in leaves, roots, and nodules. EMBO J. 6: 1–9.

    Google Scholar 

  16. CULLIMORE, J.V., D.A. LIGHTFOOT, M.J. BENNETT, F.L. CHEM, C. GEBHARDT, J. OLIVER, B.G. FORDE. 1988. Expression of glutamine synthetase and glutamate synthase in root nodules of Phaseolus vulgaris L. In Molecular Genetics of Plant-Microbe Interactions —1988. APS Press, St. Paul, Minnesota, pp. 340–345.

    Google Scholar 

  17. SENGUPTA-GOPALAN, C., J.W. PITAS. 1986. Expression of nodule-specific glutamine synthetase genes during nodule development in soybeans. Plant Mol. Biol. 7: 189–199.

    Article  Google Scholar 

  18. HIREL, B., C. BOUET, B. KING, D. LAYZELL, F. JACOBS, D.P.S. VERMA. 1987. Glutamine synthetase genes are regulated by ammonia provided externally or by symbiotic nitrogen fixation. EMBO J. 6: 1167–1171.

    Google Scholar 

  19. VERMA, D.P.S., M.G. FORTIN, J. STANLEY, V.P. MAURO, S. PUROHIT, N. MORRISON. 1986. Nodulins and nodulin genes. Plant Mol. Biol. 7: 51–61.

    Article  Google Scholar 

  20. FULLER, F., P.W. KUNSTNER, R. NGUYEN, D.P.S. VERMA. 1983. Soybean nodulin genes: analysis of cDNA clones reveals several major tissue-specific sequences in nitrogen-fixing root nodules. Proc. Nat. Acad. Sci. USA 80: 2594–2598.

    Article  ADS  Google Scholar 

  21. LANGSTON-UNKEFER, P.J., A.C. ROBINSON, T.J. KNIGHT, R.D. DURBIN. 1987. Inactivation of pea seed glutamine synthetase by the toxin, tabtoxinine-β-lactam. J. Biol. Chem. 262: 1608–1613.

    Google Scholar 

  22. KNIGHT, T.J., R. DICKSTEIN, C. SENGUPTA-COPALAN, P.J. UNKEFER. 1988. Enhancement of symbiotic N2 fixation in alfalfa and soybean. Fourth International Symposium on Molecular Genetics of Plant-Microbe Interactions, Acapulco, Mexico.

    Google Scholar 

  23. DELAUNEY, A.J., Z. TABAEIZADEH, D.P.S. VERMA. 1988. A stable bifunctional antisense transcript inhibiting gene expression in transgenic plants. Proc. Nat. Acad. Sci. USA 85: 4300–4304.

    Article  ADS  Google Scholar 

  24. SNAPP, S.S., C.P. VANCE. 1986. Asparagine biosynthesis in alfalfa (Medicago sativa L.) root nodules. Plant Physiol. 82: 390–395.

    Article  Google Scholar 

  25. REYNOLDS, P.M., K.J.F. FARNDEN. 1979. The involvement of aspartate aminotransferase in ammonia assimilation in Lupin nodules. Phytochemistry 18: 1625–1630.

    Article  Google Scholar 

  26. SHELP, B.J., C.A. ATKINS, P.J. STOVER, D.T. CAANVIN. 1983. Cellular and subcellular organization of patterns of ammonia assimilation and ureides synthesis in nodules of cow pea (Vigna unguiculata L. Walp). Arch. Biochem. Biophys. 224: 429–441.

    Article  Google Scholar 

  27. HENSON, C.A., M. COLINS, S.M. DUKE. 1982. Subcellular locationalization of enzymes of carbon and nitrogen metabolism in noduler of Medicago sativa. Plant Cell Physiol. 23: 227–235.

    Google Scholar 

  28. WOO, K.C. 1981. Ureide synthesis in a cell-free system from cowpea (Vigna unguiculata L. Walp). Plant Physiol. 37: 1156–1160.

    Article  Google Scholar 

  29. NGUYEN, T., M. ZELECHOWSKA, V. FOSTER, H. BERGMANN, D.P.S. VERMA. 1985. Primary structure of the soybean nodulin-35 gene encoding uricase II localized in the peroxisomes of uninfected cells of nodules. Proc. Nat. Acad. Sci. USA 82: 5040–5044.

    Article  ADS  Google Scholar 

  30. BERGMANN, H., E. PREDDIE, D.P.S. VERMA. 1983. Nodulin-35: a subunit of specific uricase (uricase II) induced and localized in the uninfected cells of soybean nodules. EMBO J. 2: 2333–2339.

    Google Scholar 

  31. NGUYEN, J., L. MACHAL, H. VIDEL, C. PERROT-RICHENMANN, P. GADAL. 1986. Immunochemical studies on xanthine dehydrogenase of soybean root nodule. Planta 167: 190–195.

    Article  Google Scholar 

  32. LEGOCKI, R., D.P.S. VERMA. 1979. A nodule-specific plant protein (Nodulin-35) from soybean. Science 205: 190–193.

    Article  ADS  Google Scholar 

  33. VERMA, D.P.S., A.J. DELAUNEY. 1988. Root nodule symbiosis: nodulins and nodulin genes. In Temporal and Spatial Regulation of Plant Genes. (D.P.S. Verma, R. Goldber, eds.), Springer Verlag, New York, pp. 169–199.

    Chapter  Google Scholar 

  34. GUTZ, H., H. HESLOT, V. LEUPOLEL. 1974. Schizosaccharomyces pombe 2. In Handbook of Genetics. (R.C. King, ed.), Plenum Press, New York, First Edition, pp. 395–446.

    Google Scholar 

  35. NIETO, D., R.A. WOODS. 1983. Studies on mutants affecting amidopyrophosphoribosyltransferase activity in Saccharomyces cerevisiae. Can. J. Microbiol. 29: 681–688.

    Google Scholar 

  36. FLURI, R., J.R. KINGHORN. 1985. The a!12 gene is required for the induction of the purine deamination pathway in Schizosaccharomyces pombe. J. Gen. Microbiol. 131: 527–532.

    Google Scholar 

  37. DasSARMA, S., E. TISCHER, H.M. GOODMAN. 1986. Plant glutamine synthetase complements a glnA mutation in Escherichia coli. Science 232: 1242–1244.

    Article  ADS  Google Scholar 

  38. LEE, M.G., P. NURSE. 1987. Complementation used to clone a human homologue of the fission yeast cell cycle control gene cdc2. Nature 327: 31–35.

    Article  ADS  Google Scholar 

  39. NIERLICH, D.P., B. MAGASANIK. 1965. Regulation of purine nucleotide synthesis by end-product inhibition. The effect of adenine and guanine ribonucleotides on the 5’-phosphoribosylpyro-phosphate amidotransferase of Aerobacter aerogenes. J. Biol. Chem. 240: 358–365.

    Google Scholar 

  40. MARTIN, D.W., N.T. OWEN. 1972. Repression and derepression of purine biosynthesis in mammalian hepatoma cells in culture. J. Biol. Chem. 247: 5477–5488.

    Google Scholar 

  41. MESSENGER, L.J., H. ZALKIN. 1979. Glutamine phosphoribosylpyrophosphate amidotransferase from Escherichia coli. J. Biol. Chem. 254: 3382–3389.

    Google Scholar 

  42. NAGY, M. 1970. Regulation of the biosynthesis of purine nucleotides in Schizosaccharomyces pombe. I. Properties of the phosphoribosylpyrophosphate: glutamine aminotransferase of the wild strain and of a mutant desensitized towards feedback modifiers. Biochim. Biophys. Acta 198: 471–481.

    Google Scholar 

  43. TSUDA, M., N. KATUNUMA, G. WEBER. 1979. Rat liver glutamine 5-phosphoribosyl-l-pyrophosphate amidotransferase (EC 2.4.2.14). Purification and properties. J. Biochem. 85: 1347–1354.

    Google Scholar 

  44. MANTSALA, P., H. ZALKIN. 1984. Glutamine nucleotide sequence of Saccharomyces cerevisiae Ade4 encoding phosphoribosylpyrophosphate amidotransferase. J. Biol. Chem. 259: 8478–8484.

    Google Scholar 

  45. REYNOLDS, P.H.S., D.G. BLEVINS, D.D. RANDALL. 1984. 5-Phosphoribosylpyrophosphate amidotransferase from soybean root nodules: kinetics and regulatory properties. Arch. Biochem. Biophys. 229: 623–631.

    Article  Google Scholar 

  46. KANIKO, Y., E.H. NEWCOMB. 1987. Cytochemical localization of uricase and catalase in developing root nodules of soybean. Protoplasma 140: 1–12.

    Article  Google Scholar 

  47. GOULD, S.J., G.A. KELLER, S. SUBRAMANI. 1987. Identification of a peroxisomal targetting signal at the carboxy terminus of firefly luciferase. J. Cell Biol. 105: 2923–2931.

    Article  Google Scholar 

  48. TRIPLETT, E.W. 1985. Intracellular nodule locali zation in nodule specificty of xanthine dehydrogenase in soybean. Plant Physiol. 77: 1004–1009.

    Article  Google Scholar 

  49. LARSEN, K., B.U. JOCHIMSEN. 1987. Appearance of purine-catabolizing enzymes in fix-plus and fix-minus root nodules on soybean and effect of oxygen on the expression of the enzymes in callus tissue. Plant Physiol. 85: 452–456.

    Article  Google Scholar 

  50. MINCHIN, F.R., R.J. SUMMERFIELD, P. HADLEY, E.H. ROBERTS, S. RAWSTHORNE. 1981. Carbon and nitrogen nutrition of nodulated roots of grain legumes. Plant Cell Environ. 4: 5–26.

    Article  Google Scholar 

  51. VERMA, D.P.S., K. NADLER. 1984. Legume-rhizobium symbiosis: host’s point of view. In Genes Involved in Microbe-Plant Interactions. (D.P.S. Verma, T. Hohn, eds.), Springer-Verlag, Wien, New York, pp. 58–93.

    Google Scholar 

  52. MORELL, M., L. COPELAND. 1985. Hexose kinases from the plant cytosolic fraction of soybean nodules. Plant Physiol. 79: 114–117.

    Article  Google Scholar 

  53. REIBACH, P.H., J.G. STREETER. 1983. Metabolism of 14C-labeled photosynthate and distribution of enzymes of glucose metabolism in soybean nodules. Plant Physiol. 72: 634–640.

    Article  Google Scholar 

  54. DELMAR, D.P. 1972. The purification and properties of sucrose synthetase from etiolated Phaseolus aureus seedlings. J. Biol. Chem. 247: 3822–3828.

    Google Scholar 

  55. GUPTA, M., P.S. CHOUREY, B. BURR, P.E. STILL. 1988. cDNAs of two non-allelic sucrose synthase genes in maize: cloning, expression, characterization and molecular mapping of the sucrose synthase-2 gene. Plant Mol. Biol. 10: 215–224.

    Article  Google Scholar 

  56. THUMMLER, F., D.P.S. VERMA. 1987. Nodulin 100 of soybean is the subunit of sucrose synthase regulated by the availability of free heme in nodules. J. Biol. Chem. 262: 14730–14736.

    Google Scholar 

  57. MORRISON, N., D.P.S. VERMA. 1987. A block in the endocytosis of Rhizobium allows cellular differentiation in nodules but affects the expression of some peribacteroid membrane nodulins. Plant Mol. Biol. 9: 185–196.

    Article  Google Scholar 

  58. FORREST, S. 1987. The metabolism of starch in effective and ineffective nodules of soybean. M.Sc. Thesis, McGill University, Canada.

    Google Scholar 

  59. BRISSON, N., H. GIROUX, M. ZOLLINGEN, A. CAMIRAND, C. SIMERD. 1988. Maturation and subcellular compartmentation of potato starch phosphorylase. J. Cell Biol., submitted.

    Google Scholar 

  60. KOHL, D.H., K.R. SCHUBERT, M.B. CARTER, C.H. HAGEDORN, G. SHEARER. 1988. Proline metabolism in N2-fixing root nodules: energy transfer and regulation of purine synthesis. Proc. Nat. Acac. Sci. USA 85: 2036–2040.

    Article  ADS  Google Scholar 

  61. SUGANUMA, H., M. KITOU, Y. YAMAMOTO. 1987. Carbon metabolism in relation to cellular organization of soybean root nodules and respiration of mitochondria aided by leghemoglobin. Plant Cell Physiol. 28: 113–122.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biotechnology Center and Department of Molecular Genetics, The Ohio State University, 43210, Columbus, Ohio, USA

    Desh Pal S. Verma

Authors
  1. Desh Pal S. Verma
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. University of lowa, Iowa City, Iowa, USA

    Jonathan E. Poulton

  2. University of South Florida, Tampa, Florida, USA

    John T. Romeo

  3. University of California, Davis, California, Davis, USA

    Eric E. Conn

Rights and permissions

Reprints and permissions

Copyright information

© 1989 Plenum Press, New York

About this chapter

Cite this chapter

Verma, D.P.S. (1989). Plant Genes Involved in Carbon and Nitrogen Assimilation in Root Nodules. In: Poulton, J.E., Romeo, J.T., Conn, E.E. (eds) Plant Nitrogen Metabolism. Recent Advances in Phytochemistry, vol 23. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-0835-5_2

Download citation

  • DOI: https://doi.org/10.1007/978-1-4613-0835-5_2

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4612-8106-1

  • Online ISBN: 978-1-4613-0835-5

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation