Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-09T14:54:17.569Z Has data issue: false hasContentIssue false

Genetics of plant-microbe nitrogen-fixing symbiosis

Published online by Cambridge University Press:  05 December 2011

G. C. Machray
Affiliation:
A.F.R.C. Research Group on Cyanobacteria and Department of Biological Sciences, University of Dundee, Dundee DD1 4HN
W. D. P. Stewart
Affiliation:
A.F.R.C. Research Group on Cyanobacteria and Department of Biological Sciences, University of Dundee, Dundee DD1 4HN
Get access

Synopsis

A wide variety of plant-microbe nitrogen-fixing symbioses which include cyanobacteria as the nitrogenfixing partner exist. While some information has been gathered on the biochemical changes in the cyanobacterium upon entering into symbiosis, very little is known about the accompanying changes at the genetic level. Much of our present knowledge of the organisation and control of expression of nitrogenfixation (nif) genes is derived from studies of the free-living diazotroph Klebsiella pneumoniae. This organism thus provides a model system and source of experimental material for the genetic analysis of symbiotic nitrogen fixation. We describe the use of cloned K. pneumoniae genes for nitrogen fixation and its regulation in the genetic analysis' of nitrogen fixation in cyanobacteria which can enter into symbiosis with plants. These studies reveal some dissimilarities in the organisation of nif genes and raise questions as to the genetic control of nitrogen fixation in symbiosis.

Type
Research Article
Copyright
Copyright © Royal Society of Edinburgh 1985

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alvarez-Morales, A., Dixon, R. and Merrick, M. 1984. Positive and negative control of the glnA ntrBC regulon in Klebsiella pneumoniae. EMBO J. 3, 501507.Google Scholar
Carr, N. G. and Whitton, B. A. (Eds). 1982. The Biology of Cyanobacteria. Oxford: Blackwell Scientific Publications.Google Scholar
De Bruijn, F. J., Sundaresan, V., Szeto, W. W., Ow, D. W. and Ausubel, F. M. 1984. Regulation of the nitrogen fixation (nif) genes of Klebsiella pneumoniae and Rhizobium mehloti: role of nitrogen regulation (nlr) genes. In Advances in Nitrogen Fixation Research, ed. Veeger, C. and Newton, W. E., pp. 627633. The Hague: Nijhoff/Junk.CrossRefGoogle Scholar
Dharmawardene, M. W. N., Haystead, A. and Stewart, W. D. P. 1973. Glutamine synthetase of the nitrogen-fixing alga Anabaena cylindrica. Arch. Microbiol. 90, 281295.Google ScholarPubMed
Dixon, R. A., Alvarez-Morales, A., Clements, J., Drummond, M., Merrick, M. and Postgate, J. 1984. Transcriptional control of the nif regulon in Klebsiella pneumoniae. In Advances in Nitrogen Fixation Research, ed. Veeger, C. and Newton, W. E., pp. 635642. The Hague: Nijhoff/Junk.Google Scholar
Espin, G., Alvarez-Morales, A., Cannon, F., Dixon, R. and Merrick, M. 1982. Cloning of the gln A, ntr B and ntr C genes of Klebsiella pneumoniae and studies of their role in regulation of the nitrogen fixation (nif) gene cluster. Mol. Gen. Genet. 186, 518524.Google Scholar
Fisher, R., Tuli, R. and Haselkorn, R. 1981. A cloned cyanobacterial gene for glutamine synthetase functions in Escherichia coli, but the enzyme is not adenylylated. Proc. Nam. Acad. Sci. U.S.A. 78, 33933397.Google Scholar
Fogg, G. E., Stewart, W. D. P., Fay, P. and Walsby, A. E. 1973. The Blue-Green Algae. London: Academic Press.Google Scholar
Haselkorn, R., Golden, J., Robinson, S. J., Avtges, P., Kranz, R. G. and Scolnik, P. A. 1985. Organisation of the genes for nitrogen fixation in cyanobacteria and photosynthetic bacteria. In Proc. Fourteenth Steenbock Symposium: Nitrogen Fixation and CO2 Metabolism, ed. Ludden, P. W. and Burris, J. E., pp. 8390. New York: Elsevier Science.Google Scholar
Hennecke, H. 1984. Organisation of Rhizobium symbiotic genes. In Advances in Nitrogen Fixation Research, ed. Veeger, C. and Newton, W. E., pp. 667668. The Hague: Nijhoff/Junk.Google Scholar
Johnson, W. C., Moran, C. P. and Losik, R. 1983. Two RNA polymerase sigma factors from Bacillus subtilis discriminate between overlapping promoters for a developmentally regulated gene. Nature, Land. 302, 800804.CrossRefGoogle ScholarPubMed
Kanemoto, R. H., Dowling-Paul, T., Lowery, R., Pope, M., Murrell, S. A., Saari, L. L. and Ludden, P. W. 1985. The regulation of nitrogenase in the photosynthetic bacterium Rhodospirilium rubrum. In Proc. Fourteenth Steenbock Symposium: Nitrogen Fixation and CO 2, Metabolism, ed. Ludden, P. W. and Burris, J. E., pp. 253260. New York: Elsevier Science.Google Scholar
Lea, P. J. and Miflin, B. J. 1975. Glutamine (amide): 2-oxoglutarate amino transferase in blue-green algae. Biochem. Soc. Trans. 3, 381384.CrossRefGoogle Scholar
Magasanik, B. 1982. Genetic control of nitrogen assimilation in bacteria. A. Rev. Genet. 16, 135168.Google Scholar
Mague, T. H., Weare, N. M. and Holm-Hansen, O. 1974. Nitrogen fixation in the North Pacific Ocean. Mar. Biol. 24, 109119.CrossRefGoogle Scholar
Mague, T. H., Mague, F. C. and Holm-Hansen, O. 1977. Physiology and chemical composition of nitrogen-fixing phytoplankton in the central North Pacific Ocean. Mar. Biol. 41, 213227.CrossRefGoogle Scholar
Meeks, J. C. Wolk, C. P., Lockau, W., Schilling, N., Schaffer, P. W. and Chien, W-S. 1978. Parthways of assimilation of [13N]N2 and by cyanobacteria with and without heterocysts. J. Bad. 134, 125130.Google Scholar
Millbank, J. W. 1974. Associations with blue-green algae. In The Biology of Nitrogen Fixation, ed. Quispel, A., pp. 238 264. Amsterdam/Oxford: North Holland Publishing Company.Google Scholar
Nuti, M. P., Lepidi, A. A., Prakash, R. K., Schilperoort, R. A. and Cannon, F. C. 1979. Evidence for nitrogen fixation (nif) genes on indigenous Rhizobium plasmids. Nature, Lond. 282, 533535.CrossRefGoogle Scholar
Obukowicz, M., Schaller, M. and Kennedy, G. S. 1981. Ultrastructure and phenolic histochemistry of the Cycas revoluta–Anabaena symbiosis. New Phytol. 87, 751759.CrossRefGoogle Scholar
Orr, J. and Haselkorn, R. 1982. Regulation of glutamine synthetase activity and synthesis in free-living and symbiotic Anabaena spp. J. Baet. 152, 626635.Google Scholar
Orr, J., Toan, N. D. and Haselkorn, R. 1978. Glutamine synthetase from two nitrogen-fixing cyanobacteria. Abst. Int. Symposium on Nitrogen Fixation (A27), Madison, Wisconsin.Google Scholar
Peters, G. A., Calvert, H. E., Kaplan, D., Ito, O. and Toia, R. E. Jr. 1982. The Azolla-Anabaena symbiosis: morphology, physiology and use. Israel J. Bot. 31, 305323.Google Scholar
Puhler, A., Aquilar, M. O., Hynes, M., Muller, P., Klipp, W., Priefer, U., Simon, R. and Weber, G. 1984. Advances in the genetics of free-living and symbiotic nitrogen fixing bacteria. In Advances in Nitrogen Fixation Research, ed. Veeger, C. and Newton, W. E., pp. 609619. The Hague: Nijhoff/Junk.CrossRefGoogle Scholar
Rai, A. N., Rowell, P. and Stewart, W. D. P. 1981a. Glutamate synthase activity in symbiotic cyanobacteria. J. Gen. Microbiol. 126, 515518.Google Scholar
Rai, A. N., Rowell, P. and Stewart, W. D. P. 1981b. 15N2 incorporation and metabolism in the lichen Pelligera aphthosa Willd. Planta 152, 544552.CrossRefGoogle ScholarPubMed
Rai, A. N., Rowell, P.and Stewart, W. D. P. 1983. Interactions between cyanobacterium and fungus during 15N2-incorporation and metabolism in the lichen Peltigera canina. Arch. Microbiol. 134, 136142.CrossRefGoogle Scholar
Rai, A. N., Rowell, P. and Stewart, W. D. P. 1984. Evidence for an ammonium transport system in freeliving and symbiotic cyanobacteria. Arch. Microbiol. 137, 241246.CrossRefGoogle Scholar
Ray, T. B., Peters, G. A., Toia, R. E. and Mayne, B. C. 1978. The Azolla-Anabaena azollae relationship. VII Distribution of ammonia assimilating enzymes, protein and chlorophyll between host and symbiont. Pi Physiol. 62, 463467.CrossRefGoogle ScholarPubMed
Rice, D., Mazur, B. J. and Haselkorn, R. 1982. Isolation and physical mapping of nitrogen fixation genes from the cyanobacterium Anabaena 7120. J. Biol. Chem. 257, 1315713163.CrossRefGoogle ScholarPubMed
Rigby, P. W. J., Dieckmann, M., Rhodes, C. and Berg, P. 1977. Labelling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase 1. J. Molec. Biol. 113, 237251.CrossRefGoogle Scholar
Rodgers, G. A. and Stewart, W. D. P. 1974. Physiological interactions of the blue-green alga Nostoc with the liverworts Anthoceros and Blasia. Br. Phycol J. 9, 223.Google Scholar
Rodgers, G. A. and Stewart, W. D. P. 1977. The cyanophyte-hepatic symbiosis–I. Morphology and physiology. New Phytol. 78, 441458.CrossRefGoogle Scholar
Ruvkun, G. B. and Ausubel, F. M. 1980. Interspecies homology of nitrogenase genes. Proc. Natn. Acad. Sci. U.S.A. 77, 191195.CrossRefGoogle ScholarPubMed
Sampaio, M. J. A. M., Rowell, P. and Stewart, W. D. P. 1979. Purification and some properties of glutamine synthetase from the nitrogen-fixing cyanobacteria Anabaena cylindrica and a Nostoc sp. J. Gen. Microbiol. 111, 181191.Google Scholar
Shine, J., Schofield, P. R., Weinman, J. J., Fellows, F., Badenoch-Jones, J., Morrison, N., Scott, K. F., Gresshoff, P. M., Watson, J. M. and Rolfe, B. G. 1984. Molecular cloning and organisation of genes involved in symbiotic nitrogen fixation in different Rhizobium species. In Advances in Nitrogen Fixation Research, ed. Veeger, C. and Newton, W. E., pp. 621625. The Hague: Nijhoff/Junk.CrossRefGoogle Scholar
Silvester, W. B. 1976. Endophyte adaptation in Gunnera-Nosloc symbiosis. In Symbiotic Nitrogen Fixation in Plants, ed. Nutman, P. S., pp. 521538. Cambridge: Cambridge University Press.Google Scholar
Smith, A. J. 1982. Modes of cyanobacterial carbon metabolism. In The Biology of Cyanobacteria, ed. Carr, N. G. and Whitton, B. A., pp. 4785. Oxford: Blackwell Scientific Publications.Google Scholar
Southern, E. M. 1975. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Molec. Biol. 98, 503517.CrossRefGoogle ScholarPubMed
Stacey, G., Tabita, F. R. and Van Baalen, C. 1977. Nitrogen and ammonia assimilation in the cyanobacteria: purification of glutamine synthetase from Anabaena sp. strain CA. J. Bad. 132, 596603.Google ScholarPubMed
Stewart, W. D. P. 1977. Present-day nitrogen-fixing plants. Ambio 6, 166173.Google Scholar
Stewart, W. D. P. 1980. Some aspects of structure and function in N2-fixing cyanobacteria. A. Rev. Microbiol. 34, 497536.CrossRefGoogle ScholarPubMed
Stewart, W. D. P. 1983. Natural environments–challenges to microbial success and survival. Symp. Soc. Gen. Microbiol. 15, 135.Google Scholar
Stewart, W. D. P., Haystead, A. and Dharmawardene, M. W. N. 1975. Nitrogen assimilation and metabolism in blue-green algae. In Nitrogen Fixation by Free-living Micro-organisms, ed. Stewart, W. D. P., I.B.P. Vol.6, pp. 129158. Cambridge: Cambridge University Press.Google Scholar
Stewart, W. D. P. and Rodgers, G. A. 1977. The cyanophyte-hepatic symbiosis–II. Nitrogen fixation and interchange of nitrogen and carbon. New Phytol. 78, 459471.CrossRefGoogle Scholar
Stewart, W. D. P. and Rowell, P. 1975. Effects of L-methionine-DL-sulphoximine on the assimilation of newly fixed NH3, acetylene reduction and heterocyst production in Anabaena cylindrica. Biochem. Biophys. Res. Commun. 65, 846856.Google Scholar
Stewart, W. D. P. and Rowell, P. 1977. Modifications of nitrogen-fixing algae in lichen symbiosis. Nature, Lond. 265, 371372.CrossRefGoogle Scholar
Stewart, W. D. P., Rowell, P. and Lockhart, C. M. 1979b. Associations of nitrogen-fixing prokaryotes with higher and lower plants. In Nitrogen Assimilation of Plants, ed. Hewitt, E. J. and Cutting, C. V., Proc. Sixth Long Ashton Symposium, pp. 4566. London: Academic Press.Google Scholar
Stewart, W. D. P., Rowell, P. and Rodgers, G. A. 1976. Nitrogen-fixing symbiotic systems. In Proc. Second Internal. Symp. on Photosynthetic Prokaryotes, ed. Codd, G. A. and Stewart, W. D. P., pp. 101106. Dundee: University of Dundee.Google Scholar
Stewart, W. D. P., Rowell, P. and Rai, A. N. 1983. Cyanobacteria-eukaryote plant symbioses. Ann. Microbiol. (Inst. Pasteur) 134B, 205228.Google Scholar
Stewart, W. D. P., Rowell, P., Cossar, J. D. and Kerby, N. W. 1985. Physiological studies on N2-fixing cyanobacteria. In Proc. Fourteenth Steenbock Symposium: Nitrogen Fixation and CO2 Fixation. New York: Elsevier Science.Google Scholar
Stewart, W. D. P., Rowell, P., Ladha, J. K. and Sampaio, M. J. A. M. 1979a. Blue-green algae (cyanobacteria)–some aspects related to their role as sources of fixed nitrogen in paddy soils. In Nitrogen and Rice, pp. 263285. Philippines: I.R.R.I.Google Scholar
Turner, N. E., Robinson, S. J. and Haselkorn, R. 1983. Different promoters for the Anabaena glutamine synthetase gene during growth using molecular or fixed nitrogen. Nature, Lond. 306, 337342.Google Scholar
Wolk, C. P., Thomas, J., Shaffer, P. W., Austin, S. M. and Galonsky, A. 1976. Pathway of nitrogen metabolism after fixation of 13N-labelled nitrogen gas by the cyanobacterium Anabaena cylindrica. J. Biol. Chem. 251, 50275034Google Scholar