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An update on the taxonomy of the genus Frankia Brunchorst, 1886, 174AL

Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Since the recognition of the name Frankia in the Approved Lists of bacterial names (1980), few amendments have been given to the genus description. Successive editions of Bergey’s Manual of Systematics of Archaea and Bacteria have broadly conflicting suprageneric treatments of the genus without any advances for subgeneric classification. This review focuses on recent results from taxongenomics and phenoarray approaches to the positioning and the structuring of the genus Frankia. Based on phylogenomic analyses, Frankia should be considered the single member of the family Frankiaceae within the monophyletic order, Frankiales. A polyphasic strategy incorporating genome to genome data and omniLog® phenoarrays, together with classical approaches, has allowed the designation and an amended description of a type strain of the type species Frankia alni, and the recognition of at least 10 novel species covering symbiotic and non symbiotic taxa within the genus. Genome to phenome data will be shortly incorporated in the scheme for proposing novel species including those recalcitrant to isolation in axenic culture.

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References

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

    Article  CAS  Google Scholar 

  • Akimov VN, Dobritsa SV, Stupar OS (1991) Grouping of Frankia strains by DNA: DNA homology: how many genospecies are in the genus Frankia? Nitrogen fixation. In: Polsinelli M, Materassi R, Vincenzini M (eds) Developments in plant and soil sciences. Kluwer Academic Publisher, Dordrecht, pp 635–636

    Google Scholar 

  • Auch AF, Jan M, Klenk HP, Göker M (2010) Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2(1):117

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Baker D, Torrey JG (1979) The isolation and cultivation of actinomycetes root nodule endophytes. In: Gordon JC, Wheeler CT, Perry DA (eds) Symbiotic nitrogen fixation in the management of temperate forests. Oregon State University Press, Corvallis, pp 38–56

    Google Scholar 

  • Baker D, Torrey JG (1980) Characterization of an effective actinorhizal microsymbiont, Frankia sp. AvcI1 (Actinomycetales). Can J Microbiol 26:1066–1071

    Article  CAS  PubMed  Google Scholar 

  • Baker D, Torrey JG, Kidd GH (1979) Isolation by sucrose-density fractionation and cultivation in vitro of actinomycetes from nitrogen-fixing root nodules. Nature 281:76–78

    Article  Google Scholar 

  • Baker D, Newcomb W, Torrey JG (1980) Characterization of an ineffective actinorhizal microsymbiont, Frankia sp. EuI1 (Actinomycetales). Can J Microbiol 26:1072–1089

    Article  CAS  PubMed  Google Scholar 

  • 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 Evol Microbiol 20:201–220

    Google Scholar 

  • Benson DR, Brooks JM, Huang Y, Bickhart DM, Mastronunzio JE (2011) The biology of Frankia sp. strains in the post-genome era. Mol Plant Microbe Interact 24:1310–1316

    Article  CAS  PubMed  Google Scholar 

  • Berry A, Sunell L (1990) The infection process and nodule development. In: Schwintzer CR, Tjepkema JD (eds) The biology of Frankia and actinorhizal plants. Academic Press, San Diego

    Google Scholar 

  • 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 90:6091–6094

    Article  CAS  PubMed  Google Scholar 

  • Brunchorst J (1886) Über einige Wurzelanschwellungen, besonders diejenigen von Alnus und den Elaegnaceen. Botanische Institut Tubingen 2:151–177

    Google Scholar 

  • Callaham D, Deltredici P, Torrey JG (1978) Isolation and cultivation in vitro of the actinomycete causing root nodulation in Comptonia. Science 199:899–902

    Article  CAS  PubMed  Google Scholar 

  • Chaia E (1998) Isolation of an effective strain of Frankia from nodules of Discaria trinervis (Rhamnaceae). Plant Soil 205(2):99–102

    Article  CAS  Google Scholar 

  • D’Angelo T, Oshone R, Abebe-Akele F, Simpson S, Morris K, Thomas WK et al (2016) Permanent draft genome sequence of Frankia sp. strain BR, a nitrogen-fixing actinobacterium isolated from the root nodules of Casuarina equisetifolia. Genome Announc 4(5):e01000-16

    Article  PubMed  PubMed Central  Google Scholar 

  • Diem HG, Gauthier D, Dommergues YR (1982) Isolation of Frankia from nodules of Casuarina equisetifolia. Can J Microbiol 28:526–530

    Article  Google Scholar 

  • Dobritsa SV (1998) Grouping of Frankia strains on the basis of susceptibility to antibiotics, pigment production and host specificity. Int J Syst Evol Microbiol 48:1265–1275

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 60:487–495

    Article  CAS  PubMed  Google Scholar 

  • Ghodhbane-Gtari F, Beauchemin N, Bruce D, Chain P, Chen A, Davenport KW et al (2013) Draft genome sequence of Frankia sp. strain CN3, an atypical, noninfective (Nod–) ineffective (Fix–) isolate from Coriaria nepalensis. Genome Announc 1(2):e00085-13

    Article  PubMed Central  Google Scholar 

  • Ghodhbane-Gtari F, Hurst SG, Oshone R, Morris K, Abebe-Akele F, Thomas WK et al (2014) Draft genome sequence of Frankia sp. strain BMG5. 23, a salt-tolerant nitrogen-fixing actinobacterium isolated from the root nodules of Casuarina glauca grown in Tunisia. Genome Announc 2(3):e00520-14

    Article  PubMed  PubMed Central  Google Scholar 

  • Girgis MG, Schwencke J (1993) Differentiation of Frankia strains by their electrophoretic patterns of intracellular esterases and aminopeptidases. J Gen Microbiol 139:2225–2232

    Article  CAS  Google Scholar 

  • 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(2):349–355

    Article  CAS  PubMed  Google Scholar 

  • Gtari M, Tisa LS, Normand P (2013) Diversity of Frankia strains, actinobacterial symbionts of actinorhizal plants. In: Aroca R (ed) Symbiotic Endophytes. Springer, Berlin, pp 123–148

    Chapter  Google Scholar 

  • Gtari M, Ghodhbane-Gtari F, Nouioui I, Ktari A, Hezbri K, Mimouni W, Sbissi I et al (2015) Cultivating the uncultured: growing the recalcitrant cluster-2 Frankia strains. Sci Rep 5:13112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gueddou A, Swanson E, Ktari A, Nouioui I, Hezbri K, Ghodhbane-Gtari F et al (2017) Permanent draft genome sequences of three Frankia sp. strains that are atypical, noninfective, ineffective isolates. Genome Announc 5(15):e00174-17

    Article  PubMed  PubMed Central  Google Scholar 

  • Gueddou A, Swanson E, Hezbri K, Nouioui I, Ktari I, Simpson S, Morris K, Thomas WK, Ghodhbane-Gtari F, Gtari M, Tisa LS (2018) Draft genome sequence of the symbiotic Frankia sp. strain BMG5.30 isolated from root nodules of Coriaria myrtifolia in Tunisia. Antonie Van Leeuwenhoek. https://doi.org/10.1007/s10482-018-1138-1

    Article  PubMed  Google Scholar 

  • Hahn D, Lechevalier MP, Fische 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 11:236–242

    Article  CAS  Google Scholar 

  • Hahn D, Nickel A, Dawson J (1999) Assessing Frankia populations in plants and soil using molecular methods. FEMS Microbiol Ecol 29:215–227

    Article  CAS  Google Scholar 

  • Hurst SG, Oshone R, Ghodhbane-Gtari F, Morris K, Abebe-Akele F, Thomas WK et al (2014) Draft genome sequence of Frankia sp. strain Thr, a nitrogen-fixing actinobacterium isolated from the root nodules of Casuarina cunninghamiana grown in Egypt. Genome Announc 2(3):e00493-14

    Article  PubMed  PubMed Central  Google Scholar 

  • Konstantinidis KT, Tiedje JM (2005) Towards a genome-based taxonomy for prokaryotes. J Bacteriol 187:6258–6264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lalonde M, Calvert HE, Pine S (1981) Isolation and use of Frankia strains in actinorhizae formation. In: Gibson AH, Newton WE (eds) Current perspectives in nitrogen fixation. Australian Academy of Sciences, Canberra, pp 296–299

  • Lechevalier MP (1986) Catalog of Frankia strains. Actinomycete 19:131–162

    Google Scholar 

  • Lechevalier MP (1994) Taxonomy of the genus Frankia (Actinomycetales). Int J Syst Evolution Microbiol 44:1–8

    Google Scholar 

  • Lechevalier MP, Lechevalier HA (1979) The taxonomic position of the actinomycetic endophytes. In: Gordon JC, Wheeler CT, Perry DA (eds) Symbiotic nitrogen fixation in the management of temperate forests. Oregon State University, Corvallis, pp 111–121

    Google Scholar 

  • Lechevalier M, Lechevalier H (1989) Genus Frankia Brunchorst, 1886, 174AL. In: Williams ST, Sharpe ME, Holt C (eds) Bergey’s manual of systematicbacteriology, vol 4. Williams and Wilkins, Baltimore, pp 2410–2417

    Google Scholar 

  • Lechevalier MP, Lechevalier HA (1990) Systematics, isolation and culture of Frankia. In: Schwintzer CR, Tjepkema JD (eds) The biology of Frankia and actinorhizal plants. Academic Press, San Diego, pp 35–60

    Chapter  Google Scholar 

  • 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 78:15–22

    Article  CAS  Google Scholar 

  • Lechevalier MP, Horriere F, Lechevalier HA (1982) The biology of Frankia and related organisms. Dev Ind Microbiol 23:51–60

    Google Scholar 

  • Lechevalier MP, Baker D, Horrière F (1983) Physiology, chemistry, serology, and infectivity of two Frankia isolates from Alnus incana subsp. rugosa. Can J Bot 61:2826–2833

    Article  CAS  Google Scholar 

  • 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 21:303–311

    Article  CAS  Google Scholar 

  • Mansour SR, Moussa LAA (2005) Role of Gamma-radiation on spore germination and infectivity of Frankia strains CeI523 and CcI6 isolated from Egyptian Casuarina. Isot Radiat Res 37:1023–1038

    Google Scholar 

  • Mansour SR, Oshone R, Hurst SG, Morris K, Thomas WK, Tisa LS (2014) Draft genome sequence of Frankia sp. strain CcI6, a salt-tolerant nitrogen-fixing actinobacterium isolated from the root nodule of Casuarina cunninghamiana. Genome Announc 2(1):e01205-13

    Article  PubMed  PubMed Central  Google Scholar 

  • Meier-Kolthoff JP, Göker M, Spröer C, Klenk HP (2013) When should a DDH experiment be mandatory in microbial taxonomy? Arch Microbiol 195:413–418

    Article  CAS  PubMed  Google Scholar 

  • Miller JM, Rhoden DL (1991) Preliminary evaluation of Biolog, a carbon source utilization method for bacterial identification. J Clin Microbiol 29:1143–1147

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mirza MS, Hameed S, Akkermans AD (1994) 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ngom M, Oshone R, Hurst SG, Abebe-Akele F, Simpson S, Morris K et al (2016) Permanent draft genome sequence for Frankia sp. strain CeD, a nitrogen-fixing actinobacterium isolated from the root nodules of Casuarina equistifolia grown in Senegal. Genome Announc 4(2):e00265-16

    Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen TV, Wibberg D, Battenberg K, Blom J, Heuvel BV, Berry AM, Kalinowski J et al (2016) An assemblage of Frankia Cluster II strains from California contains the canonical nod genes and also the sulfotransferase gene nodH. BMC Genom 17:796

    Article  CAS  Google Scholar 

  • Normand P, Benson DR (2015) Frankia Brunchorst 1886, 174AL. In: Whitman WB, Rainey F, Kämpfer P, Trujillo M, Chun J, De Vos P, Hedlund B, Dedysh S (eds) Bergey’s manual of systematics of archaea and bacteria. Wiley, Hoboken. https://doi.org/10.1002/9781118960608.gbm00042

    Chapter  Google Scholar 

  • Normand P, Lalonde M (1982) Evaluation of Frankia strains isolated from provenances of two Alnus species. Can J Microbiol 28:1133–1142

    Article  Google Scholar 

  • 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 the family Frankiaceae. Int J Syst Evol Microbiol 46:1–9

    CAS  Google Scholar 

  • Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E et al (2007) Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res 17:7–15

    Article  PubMed  PubMed Central  Google Scholar 

  • Normand P, Nguyen TV, Battenberg K, Berry AM, Heuvel BV, Fernandez MP, Pawlowski K (2017) Proposal of ‘Candidatus Frankia californiensis’, the uncultured symbiont in nitrogen-fixing root nodules of a phylogenetically broad group of hosts endemic to western North America. Int J Syst Evol Microbiol 67:3706–3715

    Article  CAS  PubMed  Google Scholar 

  • Normand N, Nouioui I, Pujic P, Fournier P, Dubost A, Klenk H-P, Nguyen A et al (2018) Frankia canadensis sp. nov., isolated from root nodules of Alnus incana ssp rugosa growing in Canada. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijsem.0.002939

    Article  PubMed  Google Scholar 

  • 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 100:579–587

    Article  PubMed  Google Scholar 

  • Nouioui I, Beauchemin N, Cantor MN, Chen A, Detter JC, Furnholm T et al (2013) Draft genome sequence of Frankia sp. strain BMG5. 12, a nitrogen-fixing actinobacterium isolated from Tunisian soils. Genome Announc 1(4):e00468-13

    Article  PubMed  PubMed Central  Google Scholar 

  • Nouioui I, Ghodhbane-Gtari F, Montero-Calasanz MD, Göker M, Meier-Kolthoff JP, Schumann P, Rohde M et al (2016a) Proposal of a type strain for Frankia alni (Woronin 1866) Von Tubeuf 1895, emended description of Frankia alni, and recognition of Frankia casuarinae sp. nov. and Frankia elaeagni sp. nov. Int J Syst Evol Microbiol 66:5201–5210

    Article  CAS  PubMed  Google Scholar 

  • Nouioui I, Gtari M, Göker M, Ghodhbane-Gtari F, Tisa LS, Fernandez MP et al (2016b) Draft genome sequence of Frankia strain G2, a nitrogen-fixing actinobacterium isolated from Casuarina equisetifolia and able to nodulate actinorhizal plants of the order Rhamnales. Genome Announc 4(3):e00437-16

    Article  PubMed  PubMed Central  Google Scholar 

  • Nouioui I, Ghodhbane-Gtari F, Montero-Calasanz MDC, Rohde M, Tisa LS, Gtari M, Klenk HP (2017a) Frankia inefficax sp. nov., an actinobacterial endophyte inducing ineffective, non nitrogen-fixing, root nodules on its actinorhizal host plants. Antonie Van Leeuwenhoek 110:313–320

    Article  CAS  PubMed  Google Scholar 

  • Nouioui I, Ghodhbane-Gtari F, Rohde M, Klenk HP, Gtari M (2017b) Frankia coriariae sp. nov., an infective and effective microsymbiont isolated from Coriaria japonica. Int J Syst Evol Microbiol 67:1266–1270

    Article  CAS  PubMed  Google Scholar 

  • Nouioui I, Gueddou A, Ghodhbane-Gtari F, Rhode M, Gtari M, Klenk H-P (2017c) Frankia asymbiotica sp. nov., a non infective actinobacterium isolated from Morella californica root nodule. Int J Syst Evol Microbiol 67:4897–4901

    Article  CAS  PubMed  Google Scholar 

  • Nouioui I, Montero-Calasanz MDC, Ghodhbane-Gtari F, Rohde M, Tisa LS, Klenk HP, Gtari M (2017d) Frankia discariae sp. nov.: an infective and effective microsymbiont isolated from the root nodule of Discaria trinervis. Arch Microbiol 199:641–647

    Article  CAS  PubMed  Google Scholar 

  • Nouioui I, Ghodhbane-Gtari F, Jando M, Rhode M, Klenk H-P, Gtari M (2018a) Frankia torreyi sp. nov., Frankia torreyi sp. nov., the first actinobacterium of the genus Frankia Brunchorst 1886, 174AL isolated in axenic culture. Antonie Van Leeuwenhoek. https://doi.org/10.1007/s10482-018-1131-8

    Article  PubMed  Google Scholar 

  • Nouioui I, Ghodhbane-Gtari F, Klenk HP, Gtari M (2018b) Frankia saprophytica sp. nov. an atypical non-infective (Nod–) and non-nitrogen fixing (Fix–) actinobacterium isolated from Coriaria nepalensis root nodules. Int J Syst Evol Microbiol 68:1090–1095

    Article  CAS  PubMed  Google Scholar 

  • Nouioui I, Ghodhbane-Gtari F, Rhode M, Sangal V, Klenk HP, Gtari M (2018c) Frankia irregularis sp. nov., an actinobacterium unable to nodulate its original host, Casuarina equisetifolia, but effectively nodulate members of the actinorhizal Rhamnales. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijsem.0.002914

    Article  PubMed  Google Scholar 

  • Nouioui I, Carro L, García-López M, Meier-Kolthoff J, Woyke T, Kyrpides N et al (2018d) Genome-based taxonomic classification of the phylum Actinobacteria. Front Microbiol 9:2007

    Article  PubMed  PubMed Central  Google Scholar 

  • Oshone R, Hurst SG, Abebe-Akele F, Simpson S, Morris K, Thomas WK, Tisa LS (2016) Permanent draft genome sequences for two variants of Frankia sp. strain CpI1, the first Frankia strain isolated from root nodules of Comptonia peregrina. Genome Announc 4(1):e01588-15

    Article  PubMed  PubMed Central  Google Scholar 

  • Persson T, Benson DR, Normand P, van den Heuvel B, Pujic P, Chertkov O et al (2011) Genome sequence of “Candidatus Frankia datiscae” Dg1, the uncultured microsymbiont from nitrogen-fixing root nodules of the dicot Datisca glomerata. J Bacteriol 193:7017–7018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pesce C, Swanson E, Simpson S, Morris K, Thomas WK, Tisa LS, Sellstedt A (2017) Draft Genome Sequence of the Symbiotic Frankia sp. Strain KB5 Isolated from Root Nodules of Casuarina equisetifolia. J Genomics 5:64

    Article  PubMed  PubMed Central  Google Scholar 

  • Pujalte MJ, Lucena T, Rodrigo-Torres L, Arahal (2018) Comparative genomics of Thalassobius including the description of Thalassobius activus sp. nov., and Thalassobius autumnalis sp. nov. Front Microbiol 8:2645

    Article  PubMed  PubMed Central  Google Scholar 

  • Riesco R, Carro L, Román-Ponce B, Prieto C, Blom J, Klenk H-P, Normand P, Trujillo ME (2018) Defining the species Micromonospora saelicesensis and Micromonospora noduli under the framework of genomics. Front Microbiol 9:1360

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosbrook PA, Burggraaf AJP, Reddell P (1989) A Comparison of 2 Methods and Different Media for Isolating Frankia from Casuarina Root-Nodules. Plant Soil 120:187–193

    Article  Google Scholar 

  • Sen A, Daubin V, Abrouk D, Gifford I, Berry AM, Normand P (2014) The phylogeny of actinobacteria revisited in the light of complete genomes, the orders Frankiales and Micrococcales should be split into coherent entities. Proposal of Frankiales ord. nov., Geodermatophilales ord. nov., Acidothermales ord. nov. and Nakamurellales ord. nov. Int J Syst Evol Microbiol 64:3821–3832

    Article  CAS  PubMed  Google Scholar 

  • Simon L, Jabaji-Hare S, Bousquet J, Lalonde M (1989) Confirmation of Frankia species using cellular fatty acids analysis. Syst Appl Microbiol 11:229–235

    Article  Google Scholar 

  • Skerman VBD, McGowan V, Sneath PHA (1980) Approved lists of bacterial names. Int J Syst Evol Microbiol 30:225–420

    Article  Google Scholar 

  • Stackebrandt E, Rainey FA, Ward-Rainey NL (1997) Proposal for a new hierarchic classification system, Actinobacteria classis nov. Int J Syst Evol Microbiol 47:479–491

    Google Scholar 

  • Swanson E, Oshone R, Simpson S, Morris K, Abebe-Akele F, Thomas WK, Tisa LS (2015a) Permanent draft genome sequence of Frankia sp. strain ACN1ag, a nitrogen-fixing actinobacterium isolated from the root nodules of Alnus glutinosa. Genome Announc 3(6):e01483-15

    Article  PubMed  PubMed Central  Google Scholar 

  • Swanson E, Oshone R, Simpson S, Morris K, Abebe-Akele F, Thomas WK, Tisa LS (2015b) Permanent draft genome sequence of Frankia sp. strain AvcI1, a nitrogen-fixing actinobacterium isolated from the root nodules of Alnus viridis subsp. crispa grown in Canada. Genome Announc 3(6):e01511-15

    Article  PubMed  PubMed Central  Google Scholar 

  • Tisa LS, Ensign JC (1987) Comparative physiology of nitrogenase activity and vesicle development for Frankia strains CpI1, ACN1ag, EAN1pec and EUN1f. Arch Microbiol 147:383–388

    Article  CAS  Google Scholar 

  • Tisa L, McBride M, Ensign JC (1983) Studies of growth and morphology of Frankia strains EAN1pec, EuI1c, CpI1 and ACN1AG. Can J Bot 61:2768–2773

    Article  CAS  Google Scholar 

  • Tisa LS, Oshone R, Sarkar I, Ktari A, Sen A, Gtari M (2016) Genomic approaches toward understanding the actinorhizal symbiosis: an update on the status of the Frankia genomes. Symbiosis 70:5–16

    Article  CAS  Google Scholar 

  • Torrey JG (1987) Endophyte sporulation in root nodules of actinorhizal plants. Physiol Plant 70:279–288

    Article  Google Scholar 

  • Von Tubeuf K (1895) In Pflanzenkrankheiten durch Kryptogame Parasiten verursacht. Springer, Berlin, pp 1–599

    Google Scholar 

  • Wall LG, Beauchemin N, Cantor MN, Chaia E, Chen A, Detter JC et al (2013) Draft genome sequence of Frankia sp. strain BCU110501, a nitrogen-fixing actinobacterium isolated from nodules of Discaria trinevis. Genome Announc 1(4):e00503-13

    Article  PubMed  PubMed Central  Google Scholar 

  • Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH et al (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464

    Article  Google Scholar 

  • Woronin MS (1866) Über die bei der Schwarzerle (Alnus glutinosa) und bei der gewöhnlichen Garten-Lupine (Lupinus mutabilis) auftretenden Wurzelanschwellungen. Mem Acad Imp Sci St Petersbourg VII Ser 10:1–13

    Google Scholar 

  • Zhang Z, Lopez MF, Torrey JG (1984) A comparison of cultural characteristics and infectivity of Frankia isolates from root nodules of Casuarina species. Plant Soil 78:79–90

    Article  Google Scholar 

  • 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 59:589–608

    Article  CAS  PubMed  Google Scholar 

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MG conceived the study. MG, IN, IS, FGG, LST, AS and HPK wrote the manuscript.

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Correspondence to Maher Gtari.

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Gtari, M., Nouioui, I., Sarkar, I. et al. An update on the taxonomy of the genus Frankia Brunchorst, 1886, 174AL. Antonie van Leeuwenhoek 112, 5–21 (2019). https://doi.org/10.1007/s10482-018-1165-y

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