Diversity of Frankia Strains, Actinobacterial Symbionts of Actinorhizal Plants

Chapter
Part of the Soil Biology book series (SOILBIOL, volume 37)

Abstract

Filamentous, sporangia-forming actinobacteria of the genus Frankia are best known for their symbiotic association with phylogenetically unrelated dicotyledonous plants, called actinorhizal plants, that results in the formation of root nodules. Frankia actively fixes nitrogen within these root nodules and for this purpose develops specialized thick-walled structures, termed vesicles, that are the site of nitrogen fixation in planta and ex planta. Analysis of the molecular phylogeny of cultured and uncultured Frankia strains consistently identifies four main clusters regardless of the typing locus used. Cluster 1 includes Frankia strains which associate with Betulaceae, Myricaceae, and Casuarinaceae plants (except Gymnostoma), while cluster 2 contains the uncultured Frankia microsymbionts of species from the Coriariaceae, Datiscaceae, and Rosaceae families as well as Ceanothus of the Rhamnaceae. Frankia strains in cluster 3 form effective nodules on plants from members of the Myricaceae, Rhamnaceae, Elaeagnaceae, and Gymnostoma of the Casuarinaceae. Cluster 4 forms a broad group of atypical Frankia strains (noninfective and/or nonnitrogen-fixing) that are unable to establish or reestablish an effective association with actinorhizal plants.

While the overall phylogenetic structure is strengthened by MLSA and AFLP approaches, this relationship only marginally overlaps phenotypic-based grouping using criteria that include morphology in planta and/or in vitro, chemotaxonomic properties, host infectivity and mode of infection, physiological traits, and DNA–DNA relatedness. Besides these differences, the limited number of strains studied and the variability of these strains from study to study have hindered the advancement of these phylogenetic groupings for use in describing Frankia species. The purpose of this review is to examine the diversity of Frankia with respect to the hypothesis of genome adaptation and Frankia strain diversity evolution as these strains have evolved from ecological versatility in soil environments to symbionts with diverse degrees of host infeodation in plant root nodules.

Keywords

Amplify Fragment Length Polymorphism Frankia Strain Actinorhizal Plant Obligate Symbiont Host Plant Range 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

MG was supported in part by a grant from the Ministère de l’Enseignement Supérieur et de la Recherche Scientifique–Tunisia (LabMBA-206) and a Visiting Scientist Program administered by the NH Agricultural Experimental Station at the University of New Hampshire. LST was supported in part by the Agriculture and Food Research Initiative Grant 2010-65108-20581 from the USDA National Institute of Food and Agriculture, the Hatch grant NH530, and the College of Life Sciences and Agriculture at the University of New Hampshire, Durham, NH. PN acknowledges receiving grant SESAM (2011–2013) from the French Agence Nationale de la Recherche (ANR).

References

  1. Akimov VN, Dobritsa SV (1992) Grouping of Frankia strains on the basis of DNA relatedness. Syst Appl Microbiol 15:372–379Google Scholar
  2. Akkermans ADL, Van Dijk C (1981) Non-leguminous root-nodule symbioses with actinomycetes and Rhizobium. In: Broughton JW (ed) Nitrogen fixation, vol 1. Academic, London, pp 57–103Google Scholar
  3. Alam MS, Garg SK, Agrawal P (2009) Studies on structural and functional divergence among seven WhiB proteins of Mycobacterium tuberculosis H37Rv. FEBS J 276:76–93PubMedGoogle Scholar
  4. Anderson MD, Ruess RW, Myrold DD, Taylor DL (2009) Host species and habitat affect nodulation by specific Frankia genotypes in two species of Alnus in interior Alaska. Oecologia 160:619–630PubMedGoogle Scholar
  5. Baker DD (1987) Relationships among pure cultured strains of Frankia based on host specificity. Physiol Plant 70:245–248Google Scholar
  6. Baker DD, Mullin BC (1994) Diversity of Frankia nodule endophytes of the actinorhizal shrub Ceanothus as assessed by RFLP patterns from single nodule lobes. Soil Biol Biochem 26:547–552Google Scholar
  7. Baker DD, Newcomb W, Torrey JG (1980) Characterization of an ineffective actinorhizal microsymbiont, Frankia sp. EuIl. Can J Microbiol 26:1072–1089PubMedGoogle Scholar
  8. Barabote RD, Xie G, Leu DH, Normand P, Necsulea A, Daubin V et al (2009) Complete genome of the cellulolytic thermophile Acidothermus cellulolyticus 11B provides insights into its ecophysiological and evolutionary adaptations. Genome Res 19:1033–1043PubMedGoogle Scholar
  9. Bates ST, Cropsey GW, Caporaso JG, Knight R, Fierer N (2011) Bacterial communities associated with the lichen symbiosis. Appl Environ Microbiol 77:1309–1314PubMedGoogle Scholar
  10. Bautista GH, Cruz HA, Nesme X, Valdés M, Mendoza HA, Fernandez MP (2011) Genomospecies identification and phylogenomic relevance of AFLP analysis of isolated and non-isolated strains of Frankia spp. Syst Appl Microbiol 34:200–206PubMedGoogle Scholar
  11. Becking JH (1970) Frankiaceae fam. nov. (Actinomycetales) with one new combination and six new species of the genus Frankia Brunchorst 1886, 174. Int J Syst Bacteriol 20:201–220Google Scholar
  12. Benson DR, Silvester WB (1993) Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 57:293–319PubMedGoogle Scholar
  13. Benson DR, Stephens DW, Clawson ML, Silvester WB (1996) Amplification of 16S rRNA genes from Frankia strains in root nodules of Ceanothus griseus, Coriaria arborea, Coriaria plumosa, Discaria toumatou, and Purshia tridentata. Appl Environ Microbiol 62:2904–2909PubMedGoogle Scholar
  14. Benson DR, Vanden Heuvel BD, Potter D (2004) Actinorhizal symbioses: diversity and biogeography. In: Gillings M (ed) Plant microbiology. BIOS Scientific, OxfordGoogle Scholar
  15. Berg RH (1983) Preliminary evidence for the involvement of suberization in infection of Casuarina. Can J Bot 61:2910–2918Google Scholar
  16. Berry A, Sunell L (1990) The infection process and nodule development. In: Schwintzer C, Tjepkema JD (eds) The biology of Frankia and actinorhizal plants. Academic, San Diego, CA, pp 61–81Google Scholar
  17. Berry AM, Harriott OT, Moreau RA, Osman SF, Benson DR, Jones AD (1993) Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc Natl Acad Sci USA 90:6091–6094PubMedGoogle Scholar
  18. Bloom RA, Mullin BC, Tate RL III (1989) DNA restriction patterns and DNA-DNA solution hybridization studies of Frankia isolates from Myrica pensylvanica (bayberry). Appl Environ Microbiol 55:2155–2160PubMedGoogle Scholar
  19. Bogusz D, Llewellyn DJ, Craig S, Dennis ES, Appleby CA, Peacock WJ (1990) Nonlegume hemoglobin genes retain organ-specific expression in heterologous transgenic plants. Plant Cell 2:633–641PubMedGoogle Scholar
  20. 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 58:1569–1576PubMedGoogle Scholar
  21. Bosco M, Jamann S, Chapelon C, Simonet P, Normand P (1994) Frankia microsymbiont in Dryas drummondii nodules is closely related to the microsymbiont of Coriaria and genetically distinct from other characterized Frankia strains. In: Hegazi HA, Fayez M, Monib M (eds) Nitrogen fixation with non-legumes. The American University in Cairo Press, Cairo, pp 173–183Google Scholar
  22. Callaham D, Del Tredici P, Torrey JG (1978) Isolation and cultivation in vitro of the actinomycete causing root nodulation in Comptonia. Science 199:899–902PubMedGoogle Scholar
  23. Chávez M, Carú M (2007) Genetic diversity of Frankia microsymbionts in root nodules from Colletia hystrix (Clos.) plants by sampling at a small-scale. World J Microbiol Biotechnol 22:813–820Google Scholar
  24. Chouaia B, Crotti E, Brusetti L, Daffonchio D, Essoussi I, Nouioui I, Sbissi I, Ghodhbane-Gtari F, Gtari M, Vacherie B, Barbe V, Médigue C, Gury J, Pujic P, Normand P (2012) Genome sequence of Blastococcus saxobsidens DD2, a stone-inhabiting bacterium. J Bacteriol 194:2752–2753PubMedGoogle Scholar
  25. Clawson ML, Benson DR (1999) Natural diversity of Frankia strains in actinorhizal root nodules from promiscuous hosts in the family Myricaceae. Appl Environ Microbiol 65:4521–4527PubMedGoogle Scholar
  26. Clawson ML, Benson DR, Stephens DW, Resch SC, Silvester WB (1997) Typical Frankia infect actinorhizal plants exotic to New Zealand. New Zealand J Bot 35:361–367Google Scholar
  27. Clawson ML, Carú M, Benson DR (1998) Diversity of Frankia strains in root nodules of plants from the families Elaeagnaceae and Rhamnaceae. Appl Environ Microbiol 64:3539–3543PubMedGoogle Scholar
  28. Clawson ML, Bourret A, Benson DR (2004) Assessing the phylogeny of Frankia-actinorhizal plant nitrogen-fixing root nodule symbioses with Frankia 16S rRNA and glutamine synthetase gene sequences. Mol Phylogenet Evol 31:131–138PubMedGoogle Scholar
  29. Coenye T, Schouls LM, Govan JR, Kersters K, Vandamme P (1999) Identification of Burkholderia species and genomovars from cystic fibrosis patients by AFLP fingerprinting. Int J Syst Bacteriol 4:1657–1666Google Scholar
  30. Cournoyer B, Lavire C (1999) Analysis of Frankia evolutionary radiation using glnII sequences. FEMS Microbiol Letts 177:29–34Google Scholar
  31. Dai Y, Cao J, Tang X, Zhang C (2004) Diversity of Frankia in nodules of Alnus nepalensis at Gaoligong mountains revealed by IGS, PCR-RFLP analysis. Chin J Appl Ecol 15:186–190Google Scholar
  32. Dai Y, Zhang C, Xiong Z, Zhang Z (2005) Correlations between the ages of Alnus host species and the genetic diversity of associated endosymbiotic Frankia strains from nodules. Sci China C Life Sci 48:76–81PubMedGoogle Scholar
  33. Daubin V, Lerat E, Perrière G (2003) The source of laterally transferred genes in bacterial genomes. Genome Biol 4:R57PubMedGoogle Scholar
  34. Dawson JO (2007) The ecology of actinorhizal plants. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing actinorhizal symbioses nitrogen fixation: applications and research progress, vol 6. Springer, Dordrecht, pp 199–234Google Scholar
  35. den Hengst CD, Buttner MJ (2008) Redox control in actinobacteria. Biochim Biophys Acta 1780:1201–1216Google Scholar
  36. Diem H, Dommergues Y (1983) The isolation of Frankia from nodules of Casuarina. Can J Bot 61:2822–2825Google Scholar
  37. Dobritsa SV (1998) Grouping of Frankia strains on the basis of susceptibility to antibiotics, pigment production and host specificity. Int J Syst Evol Microbiol 48:1265–1275Google Scholar
  38. Doyle JJ (2011) Phylogenetic perspectives on the origins of nodulation. Mol Plant Microbe Interact 24:1289–1295PubMedGoogle Scholar
  39. Fernandez MP, Meugnier H, Grimont PAD, Bardin R (1989) Deoxyribonucleic acid relatedness among members of the genus Frankia. Int J Syst Bacteriol 39:424–429Google Scholar
  40. Gao B, Gupta RS (2012) Phylogenetic framework and molecular signatures for the main clades of the phylum Actinobacteria. Microbiol Mol Biol Rev 76:66–112PubMedGoogle Scholar
  41. Ghodhbane-Gtari F, Nouioui I, Chair M, Boudabous A, Gtari M (2010) 16S-23S rRNA intergenic spacer region variability in the genus Frankia. Microb Ecol 60:487–495PubMedGoogle Scholar
  42. Gtari M, Dawson JO (2011) An overview of actinorhizal plants in Africa. Funct Plant Biol 38:653–661Google Scholar
  43. Gtari M, Brusetti L, Skander G, Mora D, Boudabous A, Daffonchio D (2004) Isolation of Elaeagnus-compatible Frankia from soils collected in Tunisia. FEMS Microbiol Lett 234:349–355PubMedGoogle Scholar
  44. Gtari M, Brusetti L, Hassen A, Mora D, Daffonchio D, Boudabous A (2007a) Genetic diversity among Elaeagnus compatible Frankia strains and sympatric-related nitrogen-fixing actinobacteria revealed bynifH sequence analysis. Soil Biol Biochem 39:372–377Google Scholar
  45. Gtari M, Daffonchio D, Boudabous A (2007b) Assessment of the genetic diversity of Frankia microsymbionts of Elaeagnus angustifolia L. plants growing in a Tunisian date-palm oasis by analysis of PCR amplified nifD-K intergenic spacer. Can J Microbiol 53:440–445PubMedGoogle Scholar
  46. Gtari M, Daffonchio D, Boudabous A (2007c) Occurrence and diversity of Frankia in Tunisian soil. Physiol Plant 130:372–379Google Scholar
  47. Gtari M, Ghodhbane-Gtari F, Nouioui I, Beauchemin N, Tisa LS (2012) Phylogenetic perspectives of nitrogen-fixing actinobacteria. Arch Microbiol 194:3–11PubMedGoogle Scholar
  48. Hahn D (2008) Polyphasic taxonomy of the genus Frankia. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing actinorhizal symbioses. Springer, Dordrecht, pp 25–47Google Scholar
  49. Hahn D, Lechevalier M, Fischer A, Stackebrandt E (1989) Evidence for a close phylogenetic relationship between members of the genera Frankia, Geodermatophilus, and “Blastococcus” and emendation of the family Frankiaceae. Syst Appl Microbiol 11:236–242Google Scholar
  50. Hahn D, Nickel A, Dawson JO (1999) Assessing Frankia populations in plants and soil using molecular methods. FEMS Microbiol Ecol 29:215–227Google Scholar
  51. He XH, Chen LG, Hu XQ, Asghar S (2004) Natural diversity of nodular microsymbionts of Myrica rubra. Plant Soil 262:229–239Google Scholar
  52. Honerlage W, Hahn D, Zepp K, Zyer J, Normand P (1994) A hypervariable region provides a discriminative target for specific characterization of uncultured and cultured Frankia. Syst Appl Microbiol 17:433–443Google Scholar
  53. Huguet V, McCray Batzli J, 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 67:2116–2122PubMedGoogle Scholar
  54. 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 6:1032–1041PubMedGoogle Scholar
  55. Huguet V, Gouy M, Normand P, Zimpfer JF, Fernandez MP (2005a) Molecular phylogeny of Myricaceae: a reexamination of host-symbiont specificity. Mol Phylogenet Evol 34:557–568PubMedGoogle Scholar
  56. Huguet V, Land EO, Casanova JG, Zimpfer JF, Fernandez MP (2005b) Genetic diversity of Frankia microsymbionts from the relict species Myrica faya (Ait.) and Myrica rivas-martinezii (S.) in Canary Islands and Hawaii. Microb Ecol 49:617–625PubMedGoogle Scholar
  57. Huss-Danell K (1997) Actinorhizal symbioses and their N2 fixation. New Phytol 136:375–405Google Scholar
  58. Igual JM, Valverde A, Velázquez E, Regina IS, Rodríguez-Barrueco C (2006) Natural diversity of nodular microsymbionts of Alnus glutinosa in the Tormes River Basin. Plant Soil 280:373–383Google Scholar
  59. Ivanova N, Sikorski J, Jando M, Munk C, Lapidus A, Glavina Del Rio T, Copeland A, Tice H, Cheng JF, Lucas S, Chen F, Nolan M, Bruce D, Goodwin L, Pitluck S, Mavromatis K, Mikhailova N, Pati A, Chen A, Palaniappan K, Land M, Hauser L, Chang YJ, Jeffries CD, Meincke L, Brettin T, Detter JC, Rohde M, Göker M, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP (2010) Complete genome sequence of Geodermatophilus obscurus type strain (G-20). Stand Genomic Sci 2:158–167PubMedGoogle Scholar
  60. Jamann S, Fernandez MP, Moiroud A (1992) Genetic diversity of Elaeagnaceae-infective Frankia strains isolated from various soils. Acta Oecol 13:395–405Google Scholar
  61. Jamann S, Fernandez MP, Normand P (1993) Typing method for N2-fixing bacteria based on PCR-RFLP–application to the characterization of Frankia strains. Mol Ecol 2:17–26PubMedGoogle Scholar
  62. Jeong SC, Myrold DD (1999) Genomic fingerprinting of Frankia microsymbionts from Ceanothus copopulations using repetitive sequences and polymerase chain reactions. Can J Bot 77:1220–1230Google Scholar
  63. Käppel M, Wartenberg H (1958) Der Formenwechsel des Actinomyces alni Peklo in den M, Wurzeln von Alnus glutinosa Gaertner. Arch Mikrobiol 30:46–63Google Scholar
  64. Kennedy PG, Schouboe JL, Rogers RH, Weber MG, Nadkarni NM (2010) Frankia and Alnus rubra canopy roots: an assessment of genetic diversity, propagule availability, and effects on soil nitrogen. Microb Ecol 59:214–220PubMedGoogle Scholar
  65. Khan A, Myrold DD, Misra AK (2007) Distribution of Frankia genotypes occupying Alnus nepalensis nodules with respect to altitude and soil characteristics in the Sikkim Himalayas. Physiol Plant 130:364–371Google Scholar
  66. Khan A, Myrold DD, Misra AK (2009) Molecular diversity of Frankia from root nodules of Hippophae salicifolia D.Don found in Sikkim. Indian J Microbiol 49:196–200PubMedGoogle Scholar
  67. Konstantinidis KT, Tiedje JM (2004) Trends between gene content and genome size in prokaryotic species with larger genomes. Proc Natl Acad Sci USA 101:3160–3165PubMedGoogle Scholar
  68. Krumholz GD, Chval MS, McBride MJ, Tisa LS (2003) Germination and physiological properties of Frankia spores. Plant Soil 254:57–67Google Scholar
  69. Lalonde M (1979) Immunological and ultrastructural demonstration of nodulation of the European Alnus glutinosa (L.) Gaertn. host plant by an actinomycetal isolate from the North American Comptonia peregrina (L.) Coult. root nodule. Bot Gaz 140(suppl):S35–S43Google Scholar
  70. Lawrence JG, Hendrickson H (2005) Genome evolution in bacteria: order beneath chaos. Curr Opin Microbiol 8:572–578PubMedGoogle Scholar
  71. Lechevalier MP (1994) Taxonomy of the genus Frankia (Actinomycetales). Int J Syst Bacteriol 44:1–8Google Scholar
  72. Lechevalier MP, Lechevalier HA (1979) The taxonomic position of the actinomycetic endophytes. In: Wheeler CT, Perry DA, Gordon JC (eds) Symbiotic nitrogen fixation in the management of temperate forests. Forest Research Laboratory, Oregon State University, Corvallis, OR, pp 111–122Google Scholar
  73. Lechevalier MP, Ruan JS (1984) Physiology and chemical diversity of Frankia spp. isolated from nodules of Comptonia peregrina (L.) Coult. and Ceanothus americanus L. Plant Soil 78:15–22Google Scholar
  74. Lechevalier MP, Baker D, Horriere F (1983) Physiology, chemistry, serology, and infectivity of two Frankia isolates from Alnus incana subsp. rugosa. Can J Bot 61:2826–2833Google Scholar
  75. Lumini E, Bosco M (1999) Polymerase chain reaction-restriction fragment length polymorphisms for assessing and increasing biodiversity of Frankia culture collections. Can J Bot 77:1261–1269Google Scholar
  76. Lumini E, Bosco M, Fernandez MP (1996) PCR-RFLP and total DNA homology revealed three related genomic species among broad-host-range Frankia strains. FEMS Microbiol Ecol 21:303–311Google Scholar
  77. Margheri MC, Vagnoli L, Favilli F, Sili C (1985) Proprieta morfofisiologiche di Frankia ceppo EanII57 da Elaeagnus angustifolia, infettivo su Alnus glutinosa. Ann Microbiol 35:143–153Google Scholar
  78. Maunuksela L, Zepp K, Koivula T, Zeyer J, Haahtela K, Hahn D (1999) Analysis of Frankia populations in three soils devoid of actinorhizal plants. FEMS Microbiol Ecol 28:11–21Google Scholar
  79. Mian S, Bond G, Rodriguez-Barrueco C (1976) Effective and ineffective root nodules in Myrica faya. Proc R Soc Lond B 194:285–293Google Scholar
  80. Mirza MS, Hameed S, Akkermans ADL (1994a) Genetic diversity of Datisca cannabina-compatible Frankia strains as determined by sequence analysis of the PCR-amplified 16S rRNA gene. Appl Environ Microbiol 60:2371–2376PubMedGoogle Scholar
  81. Mirza MS, Akkermans WM, Akkermans ADL (1994b) PCR-amplified 16S rRNA sequence analysis to confirm nodulation of Datisca cannabina L. by the endophyte of Coriaria nepalensis Wall. Plant Soil 160:147–152Google Scholar
  82. Mirza BS, Welsh A, Rasul G, Rieder JP, Paschke MW, Hahn D (2009) Variation in Frankia populations of the Elaeagnus host infection group in nodules of six host plant species after inoculation with soil. Microb Ecol 58:384–393PubMedGoogle Scholar
  83. Mort A, Normand P, Lalonde M (1983) 2-O-Methyl-D-Mannose, a key sugar in the taxonomy of Frankia. Can J Microbiol 29:993–1002Google Scholar
  84. 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 99:714–721Google Scholar
  85. Nagashima Y, Tani C, Yamamoto M, Sasakawa H (2008) Host range of Frankia strains isolated from actinorhizal plants growing in Japan and their relatedness based on 16S rDNA. Soil Sci Plant Nutr 54:379–386Google Scholar
  86. Nalin R, Normand P, Domenach AM (1997) Distribution and N2-fixing activity of Frankia strains in relation with soil depth. Physiol Plant 99:732–738Google Scholar
  87. Nasr H, Domenach AM, Ghorbel MH, Benson DR (2007) Divergence in symbiotic interactions between same genotypic PCR–RFLP Frankia strains and different Casuarinaceae species under natural conditions. Physiol Plant 130:400–408Google Scholar
  88. Navarro E, Nalin R, Gauthier D, Normand P (1997) The nodular microsymbionts of Gymnostoma spp. are Elaeagnus-infective Frankia strains. Appl Environ Microbiol 63:1610–1616PubMedGoogle Scholar
  89. Navarro E, Jaffre T, Gauthier D, Gourbiere F, Rinaudo G, Simonet P, Normand P (1999) Distribution of Gymnostoma spp. Microsymbiotic Frankia strains in New Caledonia is related to soil type and to host-plant species. Mol Ecol 8:1781–1788PubMedGoogle Scholar
  90. Nazaret S, Simonet P, Normand P, Bardin R (1989) Genetic diversity among Frankia strains isolated from Casuarina nodules. Plant Soil 118:241–247Google Scholar
  91. Nazaret S, Cournoyer B, Normand P, Simonet P (1991) Phylogenetic relationships among Frankia genomic species determined by use of amplified 16S rDNA sequences. J Bacteriol 173:4072–4078PubMedGoogle Scholar
  92. Nesme X, Normand P, Tremblay FM, Lalonde M (1985) Nodulation speed of Frankia sp. on Alnus glutinosa, Alnus crispa, and Myrica gale. Can J Bot 63:1292–1295Google Scholar
  93. Nick G, Paget E, Simonet P, Moiroud A, Normand P (1992) The nodular endophytes of Coriaria sp. form a distinct lineage within the genus Frankia. Mol Ecol 1:175–181PubMedGoogle Scholar
  94. Normand P, Benson DR (2012) Order XVI Frankiales. In: Goodfellow M et al (eds) Bergey’s manual of systematic bacteriology, vol 5, 2nd edn, The actinobacteria. Springer, New York, NY, pp 508–510Google Scholar
  95. Normand P, Chapelon C (1997) Direct characterization of Frankia and of close phylogenetic neighbors from an Alnus viridis rhizosphere. Physiol Plant 99:722–731Google Scholar
  96. Normand P, Lalonde M (1982) Evaluation of Frankia strains isolated from provenances of two Alnus species. Can J Microbiol 28:1133–1142Google Scholar
  97. Normand P, Orso S, Cournoyer B, Jeannin P, Chapelon C, Dawson J, Evtushenko L, Misra AK (1996) Molecular phylogeny of the genus Frankia and related genera and emendation of family Frankiaceae. Int J Syst Bacteriol 46:1–9PubMedGoogle Scholar
  98. Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, Bickhart DM, Choisne N, Couloux A, Cournoyer B, Cruveiller S, Daubin V, Demange N, Francino MP, Goltsman E, Huang Y, Kopp OR, Labarre L, Lapidus A, Lavire C, Marechal J, Martinez M, Mastronunzio JE, Mullin BC, Niemann J, Pujic P, Rawnsley T, Rouy Z, Schenowitz C, Sellstedt A, Tavares F, Tomkins JP, Vallenet D, Valverde C, Wall LG, Wang Y, Medigue C, Benson DR (2007) Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res 17:7–15PubMedGoogle Scholar
  99. Normand P, Gury J, Pujic P, Chouaia B, Crotti E, Brusetti L, Daffonchio D, Vacherie B, Barbe V, Médigue C, Calteau A, Ghodhbane-Gtari F, Essoussi I, Nouioui I, Abbassi-Ghozzi I, Gtari M (2012) Genome sequence of radio-resistant Modestobacter marinus strain BC501, a representative actinobacterium thriving on calcareous stone surfaces. J Bacteriol 194(17):4773–4774. doi: 10.1128/JB.01029-12 PubMedGoogle Scholar
  100. Nouioui I, Ghodhbane-Gtari F, Beauchemin NJ, Tisa LS, Gtari M (2011) Phylogeny of members of the Frankia genus based on gyrB, nifH and glnII sequences. Antonie Van Leeuwenhoek 100:579–587PubMedGoogle Scholar
  101. Oakley B, North M, Franklin JF, Hedlund BP, Staley JT (2004) Diversity and distribution of Frankia strains symbiotic with Ceanothus in California. Appl Environ Microbiol 70:6444–6452PubMedGoogle Scholar
  102. Ochman H (2005) Genomes on the shrink. Proc Natl Acad Sci USA 102:11959–11960PubMedGoogle Scholar
  103. Oono R, Schmitt I, Sprent JI, Denison RF (2010) Multiple evolutionary origins of legume traits leading to extreme rhizobial differentiation. New Phytol 187:508–520PubMedGoogle Scholar
  104. Pérez NO, Olivera H, Vásquez L, Valdés M (1999) Genetic characterization of Mexican Frankia strains nodulating Casuarina equisetifolia. Can J Bot 77:1214–1219Google Scholar
  105. Perradin Y, Mottet M, Lalonde M (1983) Influence of phenolics on in vitro growth of Frankia strains. Can J Bot 61:2807–2814Google Scholar
  106. Persson T, Benson DR, Normand P, Vanden Heuvel B, Pujic P, Chertkov O, Teshima H, Bruce DC, Detter C, Tapia R, Han S, Han J, Woyke T, Pitluck S, Pennacchio L, Nolan M, Ivanova N, Pati A, Land ML, Pawlowski K, Berry AM (2011) Genome sequence of “Candidatus Frankia datiscae” Dg1, the uncultured microsymbiont from nitrogen-fixing root nodules of the dicot Datisca glomerata. J Bacteriol 193:7017–7018PubMedGoogle Scholar
  107. Pokharel A, Mirza BS, Dawson JO, Hahn D (2010) Frankia populations in soil and root nodules of sympatrically grown Alnus taxa. Microb Ecol 61:92–100PubMedGoogle Scholar
  108. Portier P, Fischer-LeSaux M, Mougel C, Lerondelle C, Chapulliot D, Thioulouse J, Nesme X (2006) Identification of genomic species in Agrobacterium Biovar 1 by AFLP genomic markers. Appl Environ Microbiol 72:7123–7131PubMedGoogle Scholar
  109. Quispel A (1990) Discoveries, discussions, and trends in research on actinorhizal root nodule symbioses before 1978. In: Schwintzer CR, Tjepkema JD (eds) The biology of Frankia and actinorhizal plants. Academic, New York, NY, pp 15–33Google Scholar
  110. Rademaker JLW, Hoste B, Louws FJ, Kersters K, Swings J, Vauterin L, Vauterin P, DeBruijn FJ (2000) Comparison of AFLP and rep-PCR genomic fingerprinting with DNA-DNA homology studies: Xanthomonas as a model system. Int J Syst Evol Microbiol 50:665–677PubMedGoogle Scholar
  111. Ridgway KP, Marland LA, Harrison AF, Wright J, Young JPW, Fitter AH (2004) Molecular diversity of Frankia in root nodules of Alnus incana grown with inoculum from polluted urban soils. FEMS Microbiol Ecol 50:255–263PubMedGoogle Scholar
  112. Ritchie NJ, Myrold DD (1999a) Phylogenetic placement of uncultured Ceanothus microsymbionts using 16S rRNA gene sequences. Can J Bot 77:1208–1213Google Scholar
  113. Ritchie NJ, Myrold DD (1999b) Geographic distribution and genetic diversity of Ceanothus-infective Frankia strains. Appl Environ Microbiol 65:1378–1383PubMedGoogle Scholar
  114. Rouvier C, Prin Y, Reddell P, Normand P, Simonet P (1996) Genetic diversity among Frankia strains nodulating members of the family Casuarinaceae in Australia revealed by PCR and restriction fragment length polymorphism analysis with crushed root nodules. Appl Environ Microbiol 62:979–985PubMedGoogle Scholar
  115. Schwintzer CR (1990) Spore-positive and spore-negative nodules. In: Schwintzer CR, Tjepkema JD (eds) The biology of Frankia and actinorhizal plants. Academic, New York, NY, pp 177–193Google Scholar
  116. Sellstedt A, Winship LJ (1990) Acetylene, not ethylene, inactivates the uptake hydrogenase of actinorhizal nodules during acetylene reduction assays. Plant Physiol 94:91–94PubMedGoogle Scholar
  117. 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 1:525–533PubMedGoogle Scholar
  118. Snel B, Bork P, Huynen MA (2002) Genomes in flux: the evolution of archaeal and proteobacterial gene content. Genome Res 12:17–25PubMedGoogle Scholar
  119. Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullin BC, Dowd JM, Martin PG (1995) Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc Natl Acad Sci USA 92:2647–2651PubMedGoogle Scholar
  120. St-Laurent L, Lalonde M (1986) Isolation and characterization of Frankia strains isolated from Myrica gale. Can J Bot 65:1356–1363Google Scholar
  121. Tisa L, McBride M, Ensign J (1983) Studies of growth and morphology of Frankia strains EAN1pec, EuI1c, CpI1 and ACN1AG. Can J Bot 61:2768–2773Google Scholar
  122. Torrey JG (1987) Endophyte sporulation in root nodules of actinorhizal plants. Physiol Plant 70:279–288Google Scholar
  123. Torrey JG (1990) Cross-inoculation groups within Frankia. In: Schwintzer CR, Tjepkema JD (eds) The biology of Frankia and actinorhizal plants. Academic, New York, NY, pp 83–106Google Scholar
  124. Torrey JG, Racette S (1988) Specificity among the Casuarinaceae in root nodulation by Frankia. Plant Soil 118:157–164Google Scholar
  125. Valdés La Hens (2007) Aislamiento y caracterización de actinomycetes simbióticos de nódulos de Alnus acuminata. PhD thesis. University of Quilmes, Argentina, p 312Google Scholar
  126. Van Dijk C (1978) Spore formation and endophyte diversity in root nodules of Alnus glutinosa (L.) Vill. New Phytol 81:601–615Google Scholar
  127. Van Dijk C (1984) Ecological aspects of spore formation in the Frankia-Alnus symbiosis. PhD thesis, State University, Leiden, The NetherlandsGoogle Scholar
  128. Van Dijk C, Merkus E (1976) A microscopic study of the development of a spore-like stage in the life cycle of the root nodule endophyte of Alnus glutinosa (L.) Vill. New Phytol 77:73–90Google Scholar
  129. Vanden Heuvel BD, Benson DR, Bortiri E, Potter D (2004) Low genetic diversity among Frankia spp. strains nodulating sympatric populations of actinorhizal species of Rosaceae, Ceanothus (Rhamnaceae) and Datisca glomerata (Datiscaceae) west of the Sierra Nevada (California). Can J Microbiol 50:989–1000PubMedGoogle Scholar
  130. VandenBosch KA, Torrey JG (1984) Consequences of sporangial development for nodule function in root nodules of Comptonia peregrina and Myrica gale. Plant Physiol 76:556–560PubMedGoogle Scholar
  131. VandenBosch KA, Torrey JG (1985) Development of endophytic Frankia sporangia in field- and laboratory-grown nodules of Comptonia peregrina and Myrica gale. Am J Bot 72:99–108Google Scholar
  132. Welsh A, Mirza BS, Rieder JP, Paschke M, Hahn D (2009a) Diversity of frankiae in root nodules of Morella pensylvanica grown in soils from five continents. Syst Appl Microbiol 32:201–210PubMedGoogle Scholar
  133. Welsh AK, Dawson JO, Gottfried GJ, Hahn D (2009b) Diversity of Frankia populations in root nodules of geographically isolated Arizona alder trees in central Arizona (United States). Appl Environ Microbiol 75:6913–6918PubMedGoogle Scholar
  134. Wheeler CT, Akkermans ADL, Berry AB (2008) Frankia and actinorhizal plants: a historical perspective. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing actinorhizal symbioses. Springer, Berlin, pp 1–24Google Scholar
  135. Wolters DJ, Van Dijk C, Zoetendal EG, Akkermans ADL (1997) Phylogenetic characterization of ineffective Frankia in Alnus glutinosa (L.) Gaertn. nodules from wetland soil inoculants. Mol Ecol 6:971–981PubMedGoogle Scholar
  136. Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M, Tindall BJ, Hooper SD, Pati A, Lykidis A, Spring S, Anderson IJ, D’haeseleer P, Zemla A, Singer M, Lapidus A, Nolan M, Copeland A, Han C, Chen F, Cheng JF, Lucas S, Kerfeld C, Lang E, Gronow S, Chain P, Bruce D, Rubin EM, Kyrpides NC, Klenk HP, Eisen JA (2009) A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462:1056–1060PubMedGoogle Scholar
  137. Zhi XY, Li WJ, Stackebrandt E (2009) An update of the structure and 16S rRNA gene sequence-based definition of higher ranks of the class Actinobacteria, with the proposal of two new suborders and four new families and emended descriptions of the existing higher taxa. Int J Syst Evol Microbiol 59:589–608PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Laboratoire Microorganismes et Biomolécules ActivesUniversité de Tunis El-Manar (FST) et Université de Carthage (INSAT)TunisTunisia
  2. 2.Department of Molecular, Cellular, and Biomedical SciencesUniversity of New HampshireDurhamUSA
  3. 3.Ecologie Microbienne, Centre National de la Recherche Scientifique UMR 5557Université Lyon IVilleurbanne cedexFrance

Personalised recommendations