Abstract
Expression of Frankia genes involved in nitrogen fixation was studied in Alnus glutinosa nodules using the in situ hybridization technique. The results show that high level expression of nif genes does not occur immediately upon infection of cortical cells by Frankia. Also, only in the infected cells near the tips of the nodule lobes, nif genes are expressed at high levels. In the majority of infected cells, nif gene expression is rather low.
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Akkermans A D L and vanDijk C 1981 Non-leguminous root-nodule symbiosis with actinomycetes and Rhizobium. In Nitrogen Fixation, Vol.1. Ecology. Ed. W JBroughton. pp 57–103 Oxford University Press, Oxford, UK.
Arigoni F, Kaminski P A, Celli J and Elmerich C 1992 Transcriptional analysis of the fixABCXORF1 region of Azorhizobium caulinodans suggests post-transcriptional processing of the fixABCXORF1 mRNA. Mol. Gen. Genet. 235, 422–431.
Arigoni F, Kaminski P A, Hennecke H and Elmerich C 1991 Nucleotide sequence of the fixABC region of Azorhizobium caulinodans OR5571: similarity of the fixB product with eukaryotic flavoproteins, characterization of fixX, and identification of nifW. Mol. Gen. Genet. 225, 514–520.
Baker D D and Mullin B C 1992 Actinorhizal symbioses. In Biological Nitrogen Fixation Eds. G SStacey, R HBurris and H JEvans. pp 259–292. Chapman and Hall, New York.
Benson D R and Silvester W B 1993 Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol. Rev. 57, 293–319.
Berry A M, Harriot O T, Moreau R A, Osman S F, Benson D R and Jones A D 1993 Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc. Natl. Acad. Sci. USA 90, 6091–6094.
Berry A M and Sunell L A 1990 The infection process and nodule development. In The Biology of Frankia and Actinorhizal Plants. Eds. D RSchwintzer and J DTjepkema. pp 61–81. Academic Press. New York.
Berry A M and Torrey J G 1979 Isolation and characterization in vivo and in vitro of an actinomycetous endophyte from Alnus rubra Bong. In Symbiotic Nitrogen Fixation in the Management of Temperate Forests. Eds. J CGordon, C TWheeler and D APerry, pp 69–84. Oregon State University, Corvallis, Oregon, USA.
Burgess D and Peterson R L 1987 Development of Alnus japonica root nodules after inoculation with Frankia strain HFPArI3. Can. J. Bot. 65, 1647–1657.
Fontaine M F, Lancelle S A and Torrey J G 1984 Initiation and ontogeny of vesicles in cultured Frankia sp. strain HFPArI3. J. Bacteriol. 160, 921–927.
Hirsch A M 1992 Developmental biology of legume nodulation. New Phytol. 122, 211–237.
Hoagland D R and Arnon D T 1950 California Agriculture Experiment Station Circular 347. University of California, Berkely, CA, USA.
Huss-Danell K and Bergman B 1990 Nitrogenase in Frankia from root nodules of Alnus incana (L.) Moench: immunolocalization of the Fe-and MoFe proteins during vesicle differentiation. New Phytol 116, 443–455.
Kim S and Burgess B K 1994 Purification and characterization of nitrogenase from a ΔnifW strain of Azotobacter vinelandii. J. Biol. Chem. 269, 4215–4220.
Klipp W, Reiländer H, Schlüter A, Krey R and Pühler A 1989 The Rhizobium meliloti fdxN gene encoding a ferredoxin-like protein is necessary for nitrogen fixation and is cotranscribed with nifA and nifB Mol. Gen. Genet. 216, 293–302.
Lalonde M 1979 Techniques and observations of the nitrogen fixing Alnus root nodule symbiosis. In Recent Advances in Biological Nitrogen Fixation. Ed. N SSubba Rao. pp 421–434. Oxford and IBH, New Delhi, India.
Lalonde M and Knowles R 1975 Ultrastructure, composition, and biogenesis of the encapsulation material surrounding the endophyte in Alnus crispa var. mollis root nodules. Can. J. Bot. 53, 1951–1971.
Liu Q and Berry A M 1991 Localization and characterization of pectic polysaccharides in roots and root nodules of Ceanothus spp. during intercellular infection by Frankia Protoplasma 163, 93–101.
Meesters T M, vanGenesen S T and Akkermans A D L 1985 Growth, acetylene reduction activity and localization of nitrogenase in relation to vesicle formation in Frankia strains Cc 1.17 and Cp1.2. Arch. Microbiol. 143, 189–194.
Meesters T M 1987 Localization of nitrogenase in vesicles of Frankia sp. Cc 1.17 by immunogoldlabelling on ultrathin cryosections. Arch. Microbiol. 146, 327–331.
Merrick M J 1992 Regulation of nitrogen fixation genes in freeliving and symbiotic bacteria. In Biological Nitrogen Fixation. Eds. GStacey, R HBurris and H JEvans. pp 835–876. Chapman and Hall, New York.
Mian S and Bond G 1978 The onset of nitrogen fixation in young alder plants and its relation to differentiation in the nodular endophyte. New Phyol. 80, 187–192.
Mirza S, Pawlowski K, Hafeez F Y, Chaudhary A H and Akkermans A D L 1994 Ultrastructure of the endophyte and localization of nifH transcripts in root nodules of Coriaria nepalensis Wall. by in sity hybridization. New Phytol. 126, 131–136.
Murry M A, Zhang Y and Torrey J G 1985 Effect of oxygen on vesicle formation, acetylene reduction and oxygen-uptake kinetics in Frankia sp. HFPCcI3 isolated from Casuarina cunninghamiana. Can. J. Microbiol. 31, 804–809.
Noridge N A and Benson D R 1986 Isolation and nitrogen-fixing activity of Frankia sp. strain CpI1 vesicles. J. Bacteriol. 166, 301–305.
Paul W and Merrick M 1989 The roles of the nifW, nifZ and nifM genes of Klebsiella pneumoniae in nitrogenase biosynthesis. Eur. J. Biochem. 178, 675–682.
Prin Y, Mallein-Gerin F and Simonet P 1993 Identification and localization of Frankia strains in Alnus nodules by in situ hybridization of nifH mRNA with strain-specific oligonucleotide probes. J. Exp. Bot. 44, 815–820.
Schwintzer C R, Berry A M and Disney L D 1982 Seasonal patterns of root nodule growth, endophyte morphology, nitrogenase activity, and shoot development in Myrica gale Can. J. Bot. 60, 746–757.
Simonet P, Normand P and Bardin R 1988a Conservation of nif sequences in Frankia. Mol. Gen. Genet. 231, 238–246.
Simonet P, Normand P and Bardin R 1988b Heterologous hybridization of Frankia DNA to Rhizobium meliloti and Klebsiella pneumoniae nif genes. FEMS Microbiol. Lett. 55, 141–146.
Souillard N and Sibold L 1989 Primary structure, functional organization and expression of nitrogenase structural genes of the thermophilic archaebacterium Methanococcus thermolithotrophicus. Mol. Microbiol. 3, 541–551.
Torrey J G 1985 The site of nitrogenase in Frankia in free-living culture and in symbiosis In Nitrogen Fixation Research Progress. Eds. H JEvans, P JBottomley and W ENewton. pp 293–299. Martinus Nijhoff, New York.
Trinick M H and Galbraith J 1976 Structure of root nodules formed by Rhizobium on the non-legume Trema cannabina var. scabra. Arch. Microbiol. 108, 159–166.
Van deWiel C, Scheres B, Franssen H J, vanLammeren A, vanKammen A and Bisseling T 1990 The early nodulin transcript ENOD 2 is located in the nodule parenchyma (inner cortex) of pea and soybean root nodules. EMBO J. 9, 1–7.
Wang S-Z, Chen J-S and Johnson J L 1988 The presence of five nifH-like sequences in Clostridium pasteurianum: sequence divergence and transcription properties. Nucl. Acids Res. 16, 439–454.
Yang W-C, Horvath B, Hontelez J, vanKammen A and Bisseling T 1991 In situ localization of Rhizobium mRNAs in pea root nodules: nifA and nifH localization. Mol. Plant-Microbe Int. 4, 464–468.
Yanish-Perron C, Vieira J and Messing J 1985 Improved M13 cloning vectors and host strains: nucleotide sequence of the M13mp18 and pUC19 vectors. Gene 33, 103–110.
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Pawlowski, K., Akkermans, A.D.L., van Kammen, A. et al. Expression of Frankia nif genes in nodules of Alnus glutinosa . Plant Soil 170, 371–376 (1995). https://doi.org/10.1007/BF00010491
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DOI: https://doi.org/10.1007/BF00010491