Skip to main content
SpringerLink
Log in

Molecular analysis of actinorhizal symbiotic systems: Progress to date

  • Chapter
Current Issues in Symbiotic Nitrogen Fixation

Part of the book series: Developments in Plant and Soil Sciences ((DPSS,volume 72))

  • 205 Accesses

Abstract

The application of molecular tools to questions related to the genetics, ecology and evolution of actinorhizal symbiotic systems has been especially fruitful during the past two years. Host plant phylogenies based on molecular data have revealed markedly different relationships among host plants than have previously been suspected and have contributed to the development of new hypotheses on the origin and evolution of actinorhizal symbiotic systems. Molecular analyses of host plant gene expression in developing nodules have confirmed the occurrence of nodulin proteins and in situ hybridization techniques have been successfully adapted to permit the study of the spatial and temporal patterns of gene expression within actinorhizal nodules. The use of heterologous probes in combination with nucleotide sequence analysis have allowed a number of nif genes to be mapped on the Frankia chromosome which will ultimately contribute to the development of hypotheses related to nif gene regulation in Frankia. The use of both 16S and 23S rDNA nucleotide sequences has allowed the construction of phylogenetic trees that can be tested for congruence with symbiotic characters. In addition the development of Frankia- specific gene probes and amplification primers have contributed to studies on the genetic diversity and distribution of Frankia in the soil.

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

Access this chapter

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 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover 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

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Akimov V N and Dobritsa S V 1992 Grouping of Frankia strains on the basis of DNA relatedness. System. Appl. Microbiol. 15, 372–379.

    Article  CAS  Google Scholar 

  • Akkermans A D L, Hahn D and Mirza M S 1991 Molecular ecology of Frankia: Advantages and disadvantages of the use of DNA probes. Plant and Soil 137, 49–54.

    Article  CAS  Google Scholar 

  • Akkermans A D L, Mirza M S, Harmsen H J M, Blok H J, Herron P R, Sessitsch A and Akkermans W M 1994 Molecular ecology of microbes: A review of promises, pitfalls and true progress. FEMS Microbiol. Rev. 15, 185–194.

    Article  CAS  Google Scholar 

  • An C S, Hong J S and Mullin B C 1995a nif-gene organization and nucleotide sequence of nif K and nif E from Frankia FaCl strain. 10th Int. Conf. on Frankia and Actinorhizal Plants, Davis, CA, August 6-11 (Abstract). Dept. of Environmental Horticulture, UC Davis, Davis, CA, USA.

    Google Scholar 

  • An C S, Oh B S, Twigg P G and Mullin B C 1995b Nucleotide sequence of nif V from Frankia FaCl strain. 10th Int. Conf. on Frankia and Actinorhizal Plants, Davis, CA, August 6-11. (Abstract). Dept. of Environmental Horticulture, UC Davis,Davis, CA, USA.

    Google Scholar 

  • Baker D and O’Keefe D 1984 A modified sucrose fractionation procedure for the isolation of frankiae from actinorhizal root nodules and soil samples. Plant and Soil 78, 23–28.

    Article  Google Scholar 

  • Baker D D and Mullin B C 1994 Diversity of Frankia nodule endo-phytes of the actinorhizal shrub Ceanothus as assessed by RFLP patterns from single nodule lobes. Soil Biol. Biochem. 26, 547–552.

    Article  Google Scholar 

  • Benson D R and Silvester W B 1993 Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol. Rev. 57, 293–319.

    PubMed  CAS  Google Scholar 

  • Berry A M, McIntyre L and McCully M E 1986 Fine structure of root hair infection leading to nodulation in the Frankia-Alnus symbiosis. Can. J. Bot. 64, 292–305.

    Article  Google Scholar 

  • Bogusz D, Gherbi H, Nassar A, Franche C and Duhoux E 1995 Characterization of transcripts expressed in actinorhizal nodules of Casuarina glauca. 10th Int. Conf. on Frankia and Actinorhizal Plants, Davis CA, August 6-11. (Abstract). Dept. of Environmental Horticulture, UC Davis, Davis, CA, USA.

    Google Scholar 

  • Bosco M, Fernandez M P, Simonet P, Materassi R and Normand P 1992 Evidence that some Frankia sp. strains are able to cross boundaries between Alnus and Elaeagnus host specificity groups. Appl. Environ. Microbiol. 58, 1569–1576.

    CAS  Google Scholar 

  • Carlson D, Kuebler H and Twigg P 1995 Using the reverse transcriptase-based polymerase chain reaction (RT-PCR) to amplify a glutamine synthetase cDNA from nodules of Elaeagnus augustifolia10th Int. Conf. on Frankia and Actinorhizal Plants, Davis CA, August 6-11. (Abstract). Dept. of Environmental Horticulture, UC Davis, Davis, CA, USA.

    Google Scholar 

  • Chase M, Soltis D E, Olmstead R G, Morgan D, Les D H, Mishler B D, Duvall M R, Price R, Hills H G, Qiu Y, Kron K A, Rettig J H, Conti E, Palmer J D, Manhart J R, Sytsma K J, Michaels H J, Kress W J, Donoghue J D, Clark W D, Hedrén M, Gaut B S, Jansen R K, Kim K-J, Wimpee C F, Smith J F, Furnier G R, Straus S H, Xiang Q, Plunkett G M, Soltis P S, Swensen S M, Eguiarte L E, Learn G H Jr, Barrett S C, Graham S and Albert V A 1993 Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Ann. Missouri Bot. Garden 80, 528–580.

    Article  Google Scholar 

  • Conklin D S, McMaster J A, Culbertson and Kung C 1992 COT1, a gene involved in cobalt accumulation in Saccharomyces cerevisiae. Molec. Cell. Biol. 12, 3678–3688.

    PubMed  CAS  Google Scholar 

  • Cournoyer B and Normand P 1990 Uptake of macromolecules by Frankia. In Nitrogen Fixation: Achievements and objectives. Eds. P M Gresshoff, L E Roth, G Stacey and W E Newton. Chapman and Hall, New York, USA. 256 p.

    Google Scholar 

  • Cronquist A 1988 The evolution and classification of flowering plants. New York Botanical Garden, Bronx, New York, USA.

    Google Scholar 

  • De Bruijn F J 1992 Use of repetitive (repetitive extragenic palindromic and enterobacterial repetitive intergenic consensus) sequences and the polymerase chain reaction to fingerprint the genomes of Rhizobium meliloti and other soil bacteria. Appl. Environ. Microbiol. 58, 2180–2187.

    PubMed  Google Scholar 

  • Diouf D, Gherbi H, Prin Y, Franche C, Duhoux E and Bogusz D 1995 Hairy root nodulation of Casuarina glauca-a system for the study of symbiotic gene-expression in an actinorhizal tree. Molec. Plant Microbe Interact 8, 532–537.

    Article  CAS  Google Scholar 

  • Dobritsa S V, Baker D D and Mullin B C 1995 DNA amplification fingerprinting of Frankia genomes using ERIC and REP primers. 10th Int. Conf. on Frankia and Actinorhizal Plants, Davis, CA, August 6–11 (Abstract). Dept. of Environmental Horticulture, UC Davis, Davis, CA, USA.

    Google Scholar 

  • Doyle J J 1994 Phylogeny of the legume family: An approach to understanding of the origins of nodulation. Annu. Rev. Ecol. Syst. 25, 325–349.

    Article  Google Scholar 

  • Fernandez W P, Meugnier M, Grimont P A D and Bardin R 1989 Deoxyribonucleic acid relatedness among members of the genus Frankia. Int. J. Syst. Bacteriol. 39, 424–429.

    Article  Google Scholar 

  • Fleming A I, Wittenberg J B, Wittenberg B A, Dudman W F and Appleby C A 1987 The purification, characterization and ligand-binding kinetics of hemoglobins from root nodules of the non-leguminous Casuarina glauca-Frankia symbiosis. Biochem. Biophys. Acta 911, 209–220.

    Article  CAS  Google Scholar 

  • Franche C, Ndiaye A, Bogusz D, Gherbi H, Diouf D, Auguy F and Duhoux E 1995 Genetic transformations of Allocasuarina verticillata by Agrobacterium tumefaciens. 10th Int. Conf. on Frankia and Actinorhizal Plants, Davis, CA, August 6-11. (Abstract). Dept. of Environmental Horticulture, UC Davis, Davis, CA, USA.

    Google Scholar 

  • Ganesh G, Misra A K, Chepelon C and Normand P 1994 Morphological and molecular characterization of Frankia sp. iisolates from nodules of Alnus nepalensis Don. Arch. Microbiol. 161, 152–155.

    PubMed  CAS  Google Scholar 

  • Goetting-Minesky M P and Mullin B C 1994 Differential gene expression in an actinorhizal symbiosis: Evidence for a nodule-specific cysteine proteinase. Proc. Natl. Acad. Sci. USA 91, 9891–9895.

    Article  PubMed  CAS  Google Scholar 

  • Guan C, Akkermans A D L, van Kammen A, Bisseling T and Pawlowski K 1995 Expression of a homologue of fatty acid reductase in actinorhizal nodules of Alnus glutinosa and in Arabidopsis thaliana. 10th Int. Conf. on Frankia and Actinorhizal Plants, Davis, CA, August 6-11. (Abstract). Dept. of Environmental Horticulture, UC Davis, Davis, CA, USA.

    Google Scholar 

  • Hahn D, Dorsch M, Stackebrandt E and Akkermans A D L 1989a Synthetic oligonucleotide probes for identification of Frankia strains. Plant and Soil 118, 211–219.

    Article  CAS  Google Scholar 

  • Hahn D, Lechevalier M P, Fischer A and Stackebrandt E 1989b Evidence for a close phylogenetic relationship between members of the genera Frankia, Geodermatophilus, and “Blastococcus” and emendation of the family Frankiaceae. Syst. Appl. Microbiol. 11, 236–242.

    Article  CAS  Google Scholar 

  • Hahn D, Kester R, Starrenburg M J C and Akkermans A D L 1990a Extraction of ribosomal RNA from soil for detection of Frankia with oligonucleotide probes. Arch. Microbiol. 154, 329–335.

    Article  PubMed  CAS  Google Scholar 

  • Hahn D, Starrenburg M J C and Akkermans A D L 1990b Oligonucleotide probes that hybridize with rRNA as a tool to study Frankia strains in root nodules. Appl. Environ. Microbiol. 56, 1342–1346.

    PubMed  CAS  Google Scholar 

  • Harriott O T, Hosted T J and Bensen D R 1995 Sequences of nif X, nif W, nif Z, nif B and two ORF in the Frankia nitrogen fixation gene cluster. Gene 161, 63–67.

    Article  PubMed  CAS  Google Scholar 

  • Hönerlage W, Hahn D, Zepp K, Zeyer J and Normand P 1994 A hypervariable 23S rRNA region provides a discriminating target for specific characterization of uncultured and cultured Frankia. Syst. Appl. Microbiol. 17, 433–443.

    Article  Google Scholar 

  • Jacobsen-Lyon K, Jensen E O, Jorgensen J-E, Marcker K A, Peacock W J and Dennis E S 1995 Symbiotic and non-symbiotic haemoglobin genes in Casuarina glauca. Plant Cell 7, 213–223.

    PubMed  CAS  Google Scholar 

  • Jamann S, Fernandez M P and Moiroud A 1992 Genetic diversity of Elaeagnaceae-infective Frankia strains isolated from various soils. Acta Ecol. 13, 395–405.

    Google Scholar 

  • Jamann S, Fernandez M P and Normand P 1993 Typing method for N2-fixing bacteria based on PCR-RFLP-application to the characterization of Frankia strains. Molec. Ecol. 2, 17–26.

    Article  CAS  Google Scholar 

  • Lechevalier M P 1994 Taxonomy of the genus Frankia (Actinomycetales) Int. J. Syst. Bacteriol. 44, 1–8.

    Article  Google Scholar 

  • Liu Q and Berry A M 1991 The infection process and nodule initiation in the Frankia-Ceanothus root nodule symbiosis: A structural and histochemical study. Protoplasma 163, 82–92.

    Article  Google Scholar 

  • Lundquist P-O 1993 Dynamics of nitrogenase in the Frankia-Alnus incana symbiosis. PhD Dissertation, University of Umeå, Sweden.

    Google Scholar 

  • Lundquist P-O and Vance C P 1995 Cloning of genes involved in nitrogen and carbon metabolism of Alnus incana root nodules. 10th Int. Conf. on Frankia and Actinorhizal Plants, Davis, CA, August 6-11. (Abstract). Dept of Environmental Horticulture, UC Davis, Davis, CA, USA.

    Google Scholar 

  • Maggia L, Nazaret S and Simonet P 1992 Molecular characterization of Frankia isolates from Castuarina equisetifolia root nodules harvested in West Africa (Senegal and Gambia). Acta Ecol. 13, 453–461.

    Google Scholar 

  • McEwan N R, Wheeler C T and Milner J J 1994 Strain discrimination of cultured and symbiotic Frankia by RFLP-PCR. Soil Biol. Biochem. 26, 541–545.

    Article  Google Scholar 

  • McEwan N R and Wheeler C T 1995 PCR on the gram-positive organism Frankia without prior DNA extraction. TIG 11, 168.

    Google Scholar 

  • Miller I M and Baker D D 1986 Nodulation of actinorhizal plants by Frankia strains capable of both root hair infection and intercellular penetration. Protoplasma 131, 82–91.

    Article  Google Scholar 

  • Mirza M S, Akkermans W M and Akkermans A D L 1994a PCR-amplified 16S rRNA sequence analysis to confirm nodulation of Datisca cannabina L. by the endophyte of Coriaria nepalensis Wall. Plant and Soil 160, 147–152.

    Article  CAS  Google Scholar 

  • Mirza M S, Hameed S and Akkermans ADL 1994c Genetic diversity of Datisca cannabina- compatible Frankia strains as determined by sequence analysis of the PCR-amplified 16S rRNA gene. Appl. Environ. Microbiol. 60, 2371–2376.

    PubMed  CAS  Google Scholar 

  • Murza M S, Hahn D and Akkermans A D L 1992 Isolation and characterization of Frankia strains from Coriaria nepalensis. Syst Appl. Microbiol. 15, 289–295.

    Article  Google Scholar 

  • Mirza M S, Hahn D, Dobritsa S V and Akkermans A D L 1994b Phylogenetic studies on uncultured Frankia populations in nodules of Datisca cannabina. Can. J. Microbiol. 40, 313–318.

    Article  PubMed  CAS  Google Scholar 

  • Mirza M S, Pawlowski K, Hafeez F Y, Chaudhary A M and Akkermans A D L 1994d Ultrastructure of the endophyte and localization of nif H transcripts in root nodules of Coriaria nepalensis Wall by in situ hybridization. New Phytol. 126, 131–136.

    Google Scholar 

  • Mullin B C, Goetting-Minesky M P and Twigg P 1993 Differential gene expression in the development of actinorhizal root nodules. In New Horizons in Nitrogen Fixation. Eds. R. Palacios, J Mora and W E Newton, pp 309–314. Kluwer Academic Publishers, Boston, USA.

    Google Scholar 

  • Murry M A, Konopka A S, Pratt S D and Davis S D 1995 The use of PCR-based typing methods to assess the diversity and phylogenetic relationships of nodule endophytes of Ceanothus. 10th Int. Conf. on Frankia and Actinorhizal Plants, Davis, CA, August 6-11. (Abstract). Dept of Environmental Horticulture, UC Davis, Davis, CA, USA.

    Google Scholar 

  • Myrold D D and Huss-Danell K 1994 Population dynamics of Alnus- infective Frankia in a forest soil with and without host trees. Soil Biol. Biochem. 26, 533–540.

    Article  Google Scholar 

  • Nalin R, Domenach A-M and Normand P 1995 Molecular structure of the Frankia spp. nifD-K intergenic spacer and design of Frankia genus compatible primer. Molec. Ecol. 4, 483–491.

    CAS  Google Scholar 

  • Nazaret S, Cournoyer B, Normand P and Simonet P 1991 Phylogenetic relationships among Frankia genomic species determined by use of amplified 16S rDNA sequences. J. Bacteriol. 173, 4072–4078.

    PubMed  CAS  Google Scholar 

  • Nazaret S, Simonet P, Normand P and Bardin R 1989 Genetic diversity among Frankia isolated from Casuarina nodules. Plant and Soil 118, 241–247.

    Article  CAS  Google Scholar 

  • Newcomb W and Wood S M 1987 Morphogenesis and fine structure of Frankia (Actinomycetales): The microsymbiont of nitrogen-fixing actinorhizal root nodules. In International Review of Cytology, Vol. 109. Eds. G H Bourne, K W Joen and M Friedlander, pp 1–88. Academic Press, New York, USA.

    Google Scholar 

  • Nick G, Paget E, Simonet P, Moiroud A and Normand P 1992 The nodular endophytes of Coriaria spp. form a distinct lineage within the genus Frankia. Mol. Ecol. 1, 175–181.

    CAS  Google Scholar 

  • Normand P and Bousquet J 1989 Phylogeny of nitrogenase sequences in Frankia and other nitrogen-fixing microorganisms. J. Mol. Evol. 29, 436–447.

    Article  PubMed  CAS  Google Scholar 

  • Normand P, Cournoyer B, Somonet P and Nazaret S 1992a Analysis of a ribosomal RNA operon in the actinomycete Frankia. Gene 111, 119–124.

    Article  PubMed  CAS  Google Scholar 

  • Normand P, Gouy M, Cournoyer B and Simonet P 1992b Nucleotide sequence of nifD from Frankia alni strain ArI3: phylogenetic inferences. Mol. Biol. Evol. 9, 495–506.

    PubMed  CAS  Google Scholar 

  • Normand P, Simonet P, Prin Y and Moiroud A 1987 Formation and regeneration of Frankia protoplasts. Physiol. Plant. 70, 259–266.

    Article  CAS  Google Scholar 

  • Pawlowski K, Akkermans A D L, van Kammen A and Bisseling T 1995 Expression of Frankia nif genes in nodules of Alnus glutinosa. Plant and Soil 170, 371–376.

    Article  CAS  Google Scholar 

  • Picard C, Ponsonnet C, Paget E, Nesme X and Simonet P 1992 Detection and enumeration of bacteria in soil by direct DNA extraction and polymerase chain reaction. Appl. Environ. Microbiol. 58, 2717–2722.

    PubMed  CAS  Google Scholar 

  • Prin Y, Mallein-Gerin F and Simonet P 1993 Identification and localization of Frankia strains in Alnus nodules by in situ hybridization of nif H mRNA with strain-specific oligonucleotide probes. J.Exp. Bot. 44, 815–820.

    Article  Google Scholar 

  • Ribeiro A, Akkermans A, van Kammen A, Bisseling T and Pawlowski K 1995 A nodule-specific gene encoding a subtilisin-like protease is expressed in early stages of actinorhizal nodule development. Plant Cell 7, 785–794.

    PubMed  CAS  Google Scholar 

  • Schwencke J and Selim S 1995 Deforming factors of Casuarina root hairs (dnF) are induced in Frankia by flavonoids from Casuarina seeds. 10th Int. Conf. on Frankia and Actinorhizal Plants, Davis, CA, August 6-11. (Abstract). Dept of Environmental Horticulture, UC Davis, Davis, CA, USA.

    Google Scholar 

  • Séquin A and Lalonde M 1993 Modification of polypeptide patterns during nodule development in the Frankia-Alnus symbiosis. Symbiosis 15, 135–149.

    Google Scholar 

  • Sellstedt A, Wullings B, Nyström U and Gustafsson P 1992 Identification of Casuarina-Frankia strains by use of polymerase chain reaction (PCR) with arbitrary primers. FEMS Microbiol. Lett. 93, 1–6.

    Article  CAS  Google Scholar 

  • Simonet P, Bosco M, Chapelon C, Moiroud A and Normand P 1994 Molecular characterization of Frankia microsymbionts from spore-positive and spore-negative nodules in a natural alder stand. Appl. Environ. Microbiol. 60, 1335–1341.

    PubMed  CAS  Google Scholar 

  • Simonet P, Grosjean M-C, Misra A K, Nazaret S, Cournoyer B and Normand P 1991 Frankia genus-specific characterization by polymerase chain reaction. Appl. Environ. Microbiol. 57, 3278–3286.

    PubMed  CAS  Google Scholar 

  • Simonet P, Le N T, du Cros E T and Bardin R 1988 Identification of Frankia strains by direct DNA hybridization of crushed nodules. Appl. Environ. Microbiol. 54, 2500–2503.

    PubMed  CAS  Google Scholar 

  • Simonet P, Normand P, Moiroud A and Bardin R 1990 Identification of Frankia strains in nodules by hybridization of polymerase chain reaction products with strain-specific oligonucleotide probes. Arch. Microbiol. 153, 235–240.

    Article  PubMed  CAS  Google Scholar 

  • Soltis D E, Soltis P S, Morgan D R, Swensen S M, Mullin B C, Dowd J M and Martin P G 1995 Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc. Natl. Acad. Sci. USA 92, 2647–2651.

    Article  PubMed  CAS  Google Scholar 

  • Sprent J I 1994 Evolution and diversity in the legume-Rhizobium symbiosis: Chaos theory? Plant and Soil 161, 1–10.

    Article  Google Scholar 

  • Swensen S 1996 The evolution of actinorhizal symbiosis: evidence for multiple origins of the symbiotic association. Am. J. Bot (In press).

    Google Scholar 

  • Suharjo U K S and Tjepkema T D 1995 Occurrence of hemoglobin in the nitrogen-fixing root-nodules of Alnus glutinosa. Physiol. Plant 95, 247–252.

    Article  CAS  Google Scholar 

  • Swensen S and Mullin B 1996 Phylogenetic relationships among actinorhizal plants: The impact of molecular systematics and implications for the evolution of actinorhizal symbiosis. Physiol. Plant (In press).

    Google Scholar 

  • Swensen S M, Mullin B C and Chase M 1994 Phylogenetic affinities of the Datiscaceae based on analysis of nucleotide sequences from the plastid rbcL gene. Syst. Bot. 19, 157–168.

    Article  Google Scholar 

  • Tisa L S and Ensign J C 1987 Formation and regeneration of protoplasts of the actinorhizal nitrogen-fixing actinomycete Frankia. Appl. Environ. Microbiol. 53, 53–56.

    PubMed  CAS  Google Scholar 

  • Tjepkema J D 1983 Hemoglobins in the nitrogen-fixing root nodules of actinorhizal plants. Can. J. Bot. 61, 2924–2929.

    Article  CAS  Google Scholar 

  • Twigg P G 1993 Isolation of a nodule-specific cDNA encoding a putative glycine-rich protein from Alnus glutinosa. PhD Dissertation University of Tennessee, Knoxville, TN, USA.

    Google Scholar 

  • Twigg P G, Kuebler H and Mullin B C 1995a NS85: A nodule enhanced cDNA from Alnus glutinosa encodes a glutamine synthetase. 10th Int. Conf. on Frankia and Actinorhizal Plants, Davis, CA, August 6-11. (Abstract). Dept. of Environmental Horticulture, UC Davis, Davis, CA, USA.

    Google Scholar 

  • Twigg P G, Pawlowski K and Mullin B 1995b NS84: A nodule-specific cDNA from Alnus glutinosa encoding a putative glycinerich protein. 10th Int. Conf. on Frankia and Actinorhizal Plants, Davis, CA, August 6-11. (Abstract). Dept. of Environmental Horticulture, UC Davis, Davis, CA, USA.

    Google Scholar 

  • Wigington J, Bock J V, Battershell T and Johnson J D 1995 Cloning and characterization of a Frankia ArI5 DNA fragment with promoter activity. 10th Int. Conf. on Frankia and Actinorhizal Plants, Davis CA, August 6-11. (Abstract). Dept. of Environmental Horticulture, UC Davis, Davis, CA, USA.

    Google Scholar 

  • Wülfing C, Lombardero J and Pluckthun A 1994 An Escherichia coli protein consisting of a domain homologous to FK506-binding proteins (FKBP) and a new metal binding motif. J. Biol. Chem. 269, 2895–2901.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botany and The Center for Legume Research, The University of Tennessee, Knoxville, TN 37996, USA

    Beth C. Mullin

  2. Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, Pushchino, Moscow Region, 142292, Russia

    Svetlana V. Dobritsa

Authors
  1. Beth C. Mullin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Svetlana V. Dobritsa
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

G. H. Elkan R. G. Upchurch

Rights and permissions

Reprints and permissions

Copyright information

© 1996 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Mullin, B.C., Dobritsa, S.V. (1996). Molecular analysis of actinorhizal symbiotic systems: Progress to date. In: Elkan, G.H., Upchurch, R.G. (eds) Current Issues in Symbiotic Nitrogen Fixation. Developments in Plant and Soil Sciences, vol 72. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-5700-1_2

Download citation

  • DOI: https://doi.org/10.1007/978-94-011-5700-1_2

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-6404-0

  • Online ISBN: 978-94-011-5700-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation