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Variation in Frankia Populations of the Elaeagnus Host Infection Group in Nodules of Six Host Plant Species after Inoculation with Soil

  • Plant Microbe Interactions
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Abstract

The potential role of host plant species in the selection of symbiotic, nitrogen-fixing Frankia strains belonging to the Elaeagnus host infection group was assessed in bioassays with two Morella, three Elaeagnus, and one Shepherdia species as capture plants, inoculated with soil slurries made with soil collected from a mixed pine/grassland area in central Wisconsin, USA. Comparative sequence analysis of nifH gene fragments amplified from homogenates of at least 20 individual lobes of root nodules harvested from capture plants of each species confirmed the more promiscuous character of Morella cerifera and Morella pensylvanica that formed nodules with frankiae of the Alnus and the Elaeagnus host infection groups, while frankiae in nodules formed on Elaeagnus umbellata, Elaeagnus angustifolia, Elaeagnus commutata, and Shepherdia argentea generally belonged to the Elaeagnus host infection group. Diversity of frankiae of the Elaeagnus host infection groups was larger in nodules on both Morella species than in nodules formed on the other plant species. None of the plants, however, captured the entire diversity of nodule-forming frankiae. The distribution of clusters of Frankia populations and their abundance in nodules was unique for each of the plant species, with only one cluster being ubiquitous and most abundant while the remaining clusters were only present in nodules of one (six clusters) or two (two clusters) host plant species. These results demonstrate large effects of the host plant species in the selection of Frankia strains from soil for potential nodule formation and thus the significant effect of the choice of capture plant species in bioassays on diversity estimates in soil.

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References

  1. Akkermans ADL, Hahn D, Baker DD (1992) The family Frankiaceae. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H (eds) The prokaryotes: a handbook on the biology of bacteria: ecophysiology, isolation, identification, applications, vol II. Springer, Heidelberg, Germany, pp 1069–1084

    Google Scholar 

  2. Gordon JC, Dawson JO (1979) Potential uses of nitrogen-fixing trees and shrubs in commercial forestry. Bot Gaz 140(Suppl.):S88–S90

    Article  Google Scholar 

  3. Gordon JC (1983) Silvicultural systems and biological nitrogen fixation. In: Gordon JC, Wheeler CT (eds) Biological nitrogen fixation in forest ecosystems: Foundations and applications. Nijhoff/Junk, The Hague, Netherlands, pp 1–6

    Google Scholar 

  4. Dawson JO (1983) Dinitrogen fixation in forest ecosystems. Can J Microbiol 29:979–992

    CAS  Google Scholar 

  5. Dawson JO (1986) Actinorhizal plants: their use in forestry and agriculture. Outlook Agric 15:202–208

    Google Scholar 

  6. Crannell WK, Tanaka Y, Myrold DD (1994) Calcium and pH interaction on root nodulation of nursery-grown red alder (Alnus rubra Bong.) seedlings by Frankia. Soil Biol Biochem 26:607–614

    Article  CAS  Google Scholar 

  7. Griffiths AP, McCormick LH (1984) Effects of soil acidity on nodulation of Alnus glutinosa and viability of Frankia. Plant Soil 79:429–434

    Article  CAS  Google Scholar 

  8. Dawson JO, Kowalski DG, Dart PJ (1989) Variation with soil depth, topographic position and host species in the capacity of soils from an Australian locale to nodulate Casuarina and Allocasuarina seedlings. Plant Soil 118:1–11

    Article  Google Scholar 

  9. Schwintzer CR (1985) Effect of spring flooding on endophyte differentiation, nitrogenase activity, root growth and shoot growth in Myrica gale. Plant Soil 87:109–124

    Article  CAS  Google Scholar 

  10. Kohls SJ, Baker DD (1989) Effects of substrate nitrate concentration on symbiotic nodule formation in actinorhizal plants. Plant Soil 118:171–179

    Article  CAS  Google Scholar 

  11. Thomas KA, Berry AM (1989) Effects of continuous nitrogen application and nitrogen preconditioning on nodulation and growth of Ceanothus griseus var. horizontalis. Plant Soil 118:181–187

    Article  Google Scholar 

  12. Sanginga N, Danso SKA, Bowen GD (1989) Nodulation and growth response of Allocasuarina and Casuarina species to phosphorus fertilization. Plant Soil 118:125–132

    Article  Google Scholar 

  13. Yang Y (1995) The effect of phosphorus on nodule formation and function in the Casuarina–Frankia symbiosis. Plant Soil 176:161–169

    Article  CAS  Google Scholar 

  14. Prat D (1989) Effects of some pure and mixed Frankia strains on seedling growth in different Alnus species. Plant Soil 113:31–38

    Article  Google Scholar 

  15. Hall RB, McNabb HSj, Maynard CA, Green TL (1979) Toward development of optimal Alnus glutinosa symbiosis. Bot Gaz 140(Suppl.):S120–S126

    Article  Google Scholar 

  16. Huss-Danell K (1997) Actinorhizal symbioses and their N2 fixation. New Phytol 136:375–405

    Article  CAS  Google Scholar 

  17. Benson DR, Silvester WB (1993) Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 57:293–319

    PubMed  CAS  Google Scholar 

  18. Schwintzer CR, Tjepkema JD (1990) The biology of Frankia and actinorhizal plants. Academic, San Diego

    Google Scholar 

  19. Huss-Danell K, Myrold DD (1994) Intragenic variation in nodulation of Alnus: Consequences for quantifying Frankia nodulation units in soil. Soil Biol Biochem 26:525–531

    Article  Google Scholar 

  20. Baker DD (1987) Relationships among pure cultured strains of Frankia based on host specificity. Physiol Plant 70:245–248

    Article  Google Scholar 

  21. Hahn D, Starrenburg MJC, Akkermans ADL (1988) Variable compatibility of cloned Alnus glutinosa ecotypes against ineffective Frankia strains. Plant Soil 107:233–243

    Article  Google Scholar 

  22. Myrold DD, Hilger AB, Huss-Danell K, Martin KJ (1994) Use of molecular methods to enumerate Frankia in soil. In: Ritz K, Dighton J, Giller KE (eds) Beyond the biomass. Wiley, Chichester, UK, pp 127–136

    Google Scholar 

  23. Maunuksela L, Hahn D, Haahtela K (2000) Effect of freezing of soils on nodulation capacities of total and specific Frankia populations. Symbiosis (Rehovot) 29:107–120

    Google Scholar 

  24. Dobritsa SV, Novik SN, Stupar OS (1990) Infectivity and host specificity of strains of Frankia. Microbiol (NY) 59:210–214

    Google Scholar 

  25. Huang JB, Zhao ZY, Chen GX, Liu HC (1985) Host range of Frankia endophytes. Plant Soil 87:61–65

    Article  Google Scholar 

  26. Benson DR, Dawson J (2007) Recent advances in the biogeography and genecology of symbiotic Frankia and its host plants. Physiol Plant 130:318–330

    Article  CAS  Google Scholar 

  27. Soil Survey Staff (2008) Web Soil Survey. Natural Resources Conservation Service, US Department of Agriculture. Available online at http://websoilsurveynrcsusdagov/. Cited 25 July 2008

  28. Huss-Danell K (1978) Nitrogenase activity measurements in intact plants of Alus incana. Physiol Plant 43:372–376

    Article  CAS  Google Scholar 

  29. Normand P, Simonet P, Bardin R (1988) Conservation of nif sequences in Frankia. Mol Gen Genet 213:238–246

    Article  PubMed  CAS  Google Scholar 

  30. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  31. Versalovic J, de Bruijn FJ, Lupski JR (1998) Repetitive sequence-based PCR (rep-PCR) DNA fingerprinting of bacterial genomes. In: de Bruijn FJ, Lupski JR, Weinstock GM (eds) Bacterial genomes: physical structure and analysis. Chapman and Hall, New York, NY, pp 437–454

    Google Scholar 

  32. Rademaker JLW, de Bruijn FJ (1997) Characterization and classification of microbes by rep-PCR genomic fingerprinting and computer-assisted pattern analysis. In: Caetano-Anollés G, Gresshoff PM (eds) DNA markers: protocols, applications and overviews. Wiley, New York, NY, pp 151–171

    Google Scholar 

  33. Dombek PE, Johnson LK, Zimmerley ST, Sadowsky MJ (2000) Use of repetitive DNA sequences and the PCR to differentiate Escherichia coli isolates from human and animal sources. Appl Environ Microbiol 66:2572–2577

    Article  PubMed  CAS  Google Scholar 

  34. Kukanskis KA, Siddiquee Z, Shohet RV, Garner HR (1999) Mix of sequencing technologies for sequence closure: an example. BioTechniques 28:630–634

    Google Scholar 

  35. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  36. Maddison WP, Maddison DR (1999) MacClade: analysis of phylogeny and character evolution. Sinauer, Sunderland, MA

    Google Scholar 

  37. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (* and other methods). Sinauer, Sunderland, MA

    Google Scholar 

  38. Felsenstein J (1985) Confidence limits of phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  39. Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. System Biol 42:182–192

    Google Scholar 

  40. Posada D, Crandell KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  41. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics Appl Note 17:754–755

    Article  CAS  Google Scholar 

  42. Huelsenbeck JP, Larget B, Miller RE, Ronquist F (2002) Potential applications and pitfalls of Bayesian inference of phylogeny. System Biol 51:673–688

    Article  Google Scholar 

  43. Stamatakis A (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:btl446

    Article  CAS  Google Scholar 

  44. Stamatakis A (2006) Phylogenetic models of rate heterogeneity: a high performance computing perspective. In: Proceedings 20th IEEE International Parallel & Distributed Processing Symposium, Rhodos, Greece. Available online at http://www.hicomb.org/HiCOMB2006/proceedings.html

  45. Akimov VN, Dobritsa SV (1992) Grouping of Frankia strains on the basis of DNA relatedness. Syst Appl Microbiol 15:372–379

    CAS  Google Scholar 

  46. An CS, Riggsby WS, Mullin BC (1985) Relationships of Frankia isolates based on deoxyribonucleic acid homology studies. Int J Syst Bacteriol 35:140–146

    Article  CAS  Google Scholar 

  47. Fernandez MP, Meugnier H, Grimont PAD, Bardin R (1989) Deoxyribonucleic acid relatedness among members of the genus Frankia. Int J Syst Bacteriol 39:424–429

    Google Scholar 

  48. Page RDM (1996) TREEVIEW: An application to display phylogenetic trees on personal computers. Comp Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  49. Tamura K, Dudley J, Nei M, Kumar S (2007) Molecular evolutionary genetics analysis (MEGA) software version 4. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  50. Clawson ML, Benson DR (1999) Natural diversity of Frankia strains in actinorhizal root nodules from promiscuous hosts in the family Myricaceae. Appl Environ Microbiol 65:4521–4527

    PubMed  CAS  Google Scholar 

  51. Clawson ML, Caru M, Benson DR (1998) Diversity of Frankia strains in root nodules of plants from the families Elaeagnaceae and Rhamnaceae. Appl Environ Microbiol 64:3539–3543

    PubMed  CAS  Google Scholar 

  52. Clawson ML, Gawronski J, Benson DR (1999) Dominance of Frankia strains in stands of Alnus incana subsp. rugosa and Myrica pensylvanica. Can J Bot 77:1203–1207

    Article  Google Scholar 

  53. Huguet V, Batzli JM, Zimpfer JF, Normand P, Dawson JO, Fernandez MP (2001) Diversity and specificity of Frankia strains in nodules of sympatric Myrica gale, Alnus incana, and Shepherdia canadensis determined by rrs gene polymorphism. Appl Environ Microbiol 67:2116–2122

    Article  PubMed  CAS  Google Scholar 

  54. Margheri MC, Bosco M, Vagnoli L, Favilli F (1989) Compatibility of Frankia strains belonging to different host-specificity groups with Alnus glutinosa. A. incana and A. cordata. Ann Microbiol Enzimol 39:247–255

    Google Scholar 

  55. Bosco M, Fernandez MP, Simonet P, Materassi R, 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

    PubMed  CAS  Google Scholar 

  56. Simonet P, Navarro E, Rouvier C, Reddell P, Zimpfer J, Dommergues Y, Bardin R, Combarro P, Hamelin J, Domenach AM, Gourbiere F, Prin Y, Dawson JO, Normand P (1999) Co-evolution between Frankia populations and host plants in the family Casuarinaceae and consequent patterns of global dispersal. Environ Microbiol 1:525–533

    Article  PubMed  CAS  Google Scholar 

  57. Simonet P, Haurat J, Normand P, Bardin R, Moiroud A (1986) Localization of nif genes on a large plasmid in Frankia sp. strain ULQ0132105009. Mol Gen Genet 204:492–495

    Article  CAS  Google Scholar 

  58. Hirsch AM, McKhann HI, Reddy A, Liao J, Fang Y, Marshall CR (1995) Assessing horizontal transfer of nifHDK genes in Eubacteria: nucleotide sequence of nifK from Frankia strain HFPCcI3. Mol Biol Evol 12:16–27

    PubMed  CAS  Google Scholar 

  59. Manjula M, Rakesh T (1990) Cluster analysis of genes for nitrogen fixation from several diazotrophs. J Genet 69:67–78

    Article  Google Scholar 

  60. Murry MA, Konopka AS, Pratt SD, Vandergon TL (1997) The use of PCR-based typing methods to assess the diversity of Frankia nodule endophytes of the actinorhizal shrub Ceanothus. Physiol Plant 99:714–721

    Article  CAS  Google Scholar 

  61. Murry MA, Zhang D, Schneider M, De Bruijn FJ (1995) Use of repetitive sequences and the polymerase chain reaction (rep-PCR) to fingerprint the genomes of Frankia isolates. Symbiosis 19:223–240

    CAS  Google Scholar 

  62. Versalovic J, Schneider M, De Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 5:25–40

    CAS  Google Scholar 

  63. Torrey JG (1990) Cross-inoculation within Frankia and host-endosymbiont associations. In: Schwintzer CR, Tjepkema JD (eds) The biology of Frankia and actinorhizal plants. Academic, New York, USA, pp 83–106

    Google Scholar 

  64. Huguet V, Mergeay M, Cervantes E, Fernandez MP (2004) Diversity of Frankia strains associated to Myrica gale in Western Europe: impact of host plant (Myrica vs. Alnus) and of edaphic factors. Environ Microbiol 6:1032–1041

    Article  PubMed  CAS  Google Scholar 

  65. Chávez M, Carú M (2006) Genetic diversity of Frankia microsymbionts in root nodules from Colletia hystrix (Clos.) plants by sampling at a small-scale. World J Microbiol Biotechnol 22:813–820

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank Dr. Laura G. Perry and the Restoration Ecology Laboratory Crew (Liza Bodistow, Bryan Brown, Jeremy Buss, Chris Herron, Lilly Hines, Tim Hoelzle, Ben Hoffman, Erin Klamper, Katie Legg, Mandy Roesch, Travis Talbot, Hannah Varani, Will Vieth) for development of protocols, propagation of plant species, maintenance of the experiment, and harvesting plants. The authors are indebted to the Texas State Department of Biology, the National Science Foundation (GK-12 grant No. 0742306), and the Higher Education Commission of Pakistan for financial support.

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Authors and Affiliations

  1. Department of Biology, Texas State University, 601 University Drive, San Marcos, TX, 78666, USA

    Babur S. Mirza, Allana Welsh, Ghulam Rasul & Dittmar Hahn

  2. Plant Microbiology Division, National Institute for Biotechnology & Genetic Engineering (NIBGE), P.O. Box 577, Jhang Road, Faisalabad, Pakistan

    Ghulam Rasul

  3. Department of Forest, Rangeland, and Watershed Stewardship, Colorado State University, Fort Collins, CO, 80523-1472, USA

    Julie P. Rieder & Mark W. Paschke

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  1. Babur S. Mirza
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Correspondence to Dittmar Hahn.

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Mirza, B.S., Welsh, A., Rasul, G. et al. Variation in Frankia Populations of the Elaeagnus Host Infection Group in Nodules of Six Host Plant Species after Inoculation with Soil. Microb Ecol 58, 384–393 (2009). https://doi.org/10.1007/s00248-009-9513-0

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