1887

Abstract

The genus comprises a group of nitrogen-fixing actinobacteria that form root-nodule symbioses with perennial dicotyledonous plants in the nitrogen-fixing clade. These bacteria have been characterized phylogenetically and grouped into four clusters (clusters 1–4). Cluster 2 contains mostly uncultured strains that induce nodules on species of the genera (Datiscaceae), (Coriariaceae), (Rhamnaceae) and several genera in the family Rosaceae (, ), all of which except members of the genus are present within the California Floristic Province (CFP) or neighbouring areas of western North America. Those strains occurring in western North America are genetically very closely related to one another, and genetically distinct from strains characterized from other locales. We hereby propose to create a ' Frankia californiensis' species for those cluster 2 strains of the genus with both high genetic similarity and a geographical distribution in or near the CFP.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.002147
2017-10-01
2024-12-06
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/67/10/3706.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.002147&mimeType=html&fmt=ahah

References

  1. Benson DR, Silvester WB. Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 1993; 57:293–319[PubMed]
    [Google Scholar]
  2. Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullin BC et al. Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc Natl Acad Sci USA 1995; 92:2647–2651 [View Article][PubMed]
    [Google Scholar]
  3. Normand P, Orso S, Cournoyer B, Jeannin P, Chapelon C et al. Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae . Int J Syst Bacteriol 1996; 46:1–9 [View Article][PubMed]
    [Google Scholar]
  4. Callaham D, Deltredici P, Torrey JG. Isolation and cultivation in vitro of the actinomycete causing root nodulation in Comptonia . Science 1978; 199:899–902 [View Article][PubMed]
    [Google Scholar]
  5. Pommer E. Über die Isolierung des Endophyten aus den Wurzelknöllchen Alnus glutinosa Gaertn. und uber erfolgreiche Re-Infektionsversuche. Ber Deutsch Botan Gesell 1959; 72:138–150
    [Google Scholar]
  6. Normand P, Benson DR. Genus I Frankia Brunchorst 1886, 174AL . In Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Ludwig W, Suzuki KI, Parte A. et al. (editors) Bergey's Manual of Systematic Bacteriology, The Actinobacteria vol. 5 New York: Bergey's Manual Trust, Springer; 2012 pp. 512–520
    [Google Scholar]
  7. Gtari M, Ghodhbane-Gtari F, Nouioui I, Ktari A, Hezbri K et al. Cultivating the uncultured: growing the recalcitrant cluster-2 Frankia strains. Sci Rep 2015; 5:13112 [View Article][PubMed]
    [Google Scholar]
  8. Woronin MS. Über die bei der Schwarzerle (Alnus glutinosa) und bei der gewöhnlichen Garten-Lupine (Lupinus mutabilis) auftretenden Wurzelanschwellungen. In Mémoires De l'Academie Impériale Des Sciences De St. Pétersbourg, VII Series 1866 pp. 1–13
    [Google Scholar]
  9. Brunchorst J. ber einige wurzelanschwellungen, besonders die jenigen von Alnus, und den elaeagnaceen. Unters Bot Inst Tübingen 1886; 2:151–177
    [Google Scholar]
  10. Becking JH. Frankiaceae fam. nov. (Actinomycetales) with one new combination and six new species of the genus Frankia brunchorst 1886, 174. Int J Syst Bacteriol 1970; 20:201–220 [View Article]
    [Google Scholar]
  11. Fernandez MP, Meugnier H, Grimont PAD, Bardin R. Deoxyribonucleic acid relatedness among members of the Genus Frankia . Int J Syst Bacteriol 1989; 39:424–429 [View Article]
    [Google Scholar]
  12. Nouioui I, Ghodhbane-Gtari F, Montero-Calasanz MD, Göker M, Meier-Kolthoff JP et al. 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 2016; 66:5201–5210 [View Article][PubMed]
    [Google Scholar]
  13. Nouioui I, Ghodhbane-Gtari F, del Carmen Montero-Calasanz M, Rohde M, Tisa LS et al. Frankia inefficax sp. nov., an actinobacterial endophyte inducing ineffective, non nitrogen-fixing, root nodules on its actinorhizal host plants. Antonie van Leeuwenhoek 2017; 110:313–320 [View Article][PubMed]
    [Google Scholar]
  14. Nouioui I, del Carmen Montero-Calasanz M, Ghodhbane-Gtari F, Rohde M, Tisa LS et al. Frankia discariae sp. nov.: an infective and effective microsymbiont isolated from the root nodule of Discaria trinervis . Arch Microbiol 2017; 199:641–647 [View Article][PubMed]
    [Google Scholar]
  15. Nouioui I, Ghodhbane-Gtari F, Rohde M, Klenk HP, Gtari M. Frankia coriariae sp. nov., an infective and effective microsymbiont isolated from Coriaria japonica . Int J Syst Evol Microbiol 2017; 67: [View Article][PubMed]
    [Google Scholar]
  16. Persson T, Battenberg K, Demina IV, Vigil-Stenman T, vanden Heuvel B et al. Candidatus Frankia datiscae Dg1, the actinobacterial microsymbiont of Datisca glomerata, expresses the canonical nod genes nodABC in symbiosis with its Host Plant. PLoS One 2015; 10:e0127630 [View Article][PubMed]
    [Google Scholar]
  17. Hickman JC. The Jepson Manual: Vascular Plants of California Berkeley and Los Angeles, CA: University of California Press; 2012
    [Google Scholar]
  18. Henrickson J. Notes on rosaceae. Phytologia 1986; 60:468
    [Google Scholar]
  19. Mabberley DJ. The Plant Book. A Portable Dictionary of the Higher Plants Cambridge: Cambridge University Press; 1987
    [Google Scholar]
  20. Samant S, Huo T, Dawson JO, Hahn D. Abundance and relative distribution of Frankia host infection groups under actinorhizal Alnus glutinosa and non-actinorhizal Betula nigra trees. Microb Ecol 2016; 71:473–481 [View Article][PubMed]
    [Google Scholar]
  21. Battenberg K, Wren JA, Hillman J, Edwards J, Huang L et al. The influence of the host plant is the major ecological determinant of the presence of the nitrogen-fixing root nodule symbiont, Cluster II Frankia species in Soil. Appl Environ Microbiol 2017; 83:e0266102616 [View Article][PubMed]
    [Google Scholar]
  22. Nguyen TV, Wibberg D, Battenberg K, Blom J, vanden Heuvel B et al. An assemblage of Frankia Cluster II strains from California contains the canonical nod genes and also the sulfotransferase gene nodH . BMC Genomics 2016; 17:796 [View Article][PubMed]
    [Google Scholar]
  23. Auch AF, Henz SR, Holland BR, Göker M. Genome BLAST distance phylogenies inferred from whole plastid and whole mitochondrion genome sequences. BMC Bioinformatics 2006; 7:350 [View Article][PubMed]
    [Google Scholar]
  24. Blom J, Albaum SP, Doppmeier D, Pühler A, Vorhölter FJ et al. EDGAR: a software framework for the comparative analysis of prokaryotic genomes. BMC Bioinformatics 2009; 10:154 [View Article][PubMed]
    [Google Scholar]
  25. Ritchie NJ, Myrold DD. Geographic distribution and genetic diversity of Ceanothus-infective Frankia strains. Appl Environ Microbiol 1999; 65:1378–1383[PubMed]
    [Google Scholar]
  26. Oakley B, North M, Franklin JF, Hedlund BP, Staley JT. Diversity and distribution of Frankia strains symbiotic with Ceanothus in California. Appl Environ Microbiol 2004; 70:6444–6452 [View Article][PubMed]
    [Google Scholar]
  27. vanden Heuvel BD, Benson DR, Bortiri E, Potter D. 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 2004; 50:989–1000 [View Article][PubMed]
    [Google Scholar]
  28. Nouioui I, Ghodhbane-Gtari F, Fernandez MP, Boudabous A, Normand P et al. Absence of cospeciation between the uncultured Frankia microsymbionts and the disjunct actinorhizal Coriaria species. Biomed Res Int 2014; 2014:1–9 [View Article][PubMed]
    [Google Scholar]
  29. Persson T, Benson DR, Normand P, vanden Heuvel B, Pujic P et al. Genome sequence of "Candidatus Frankia datiscae" Dg1, the uncultured microsymbiont from nitrogen-fixing root nodules of the dicot Datisca glomerata. J Bacteriol 2011; 193:7017–7018 [View Article][PubMed]
    [Google Scholar]
  30. Gtari M, Ghodhbane-Gtari F, Nouioui I, Ktari A, Hezbri K et al. Cultivating the uncultured: growing the recalcitrant cluster-2 Frankia strains. Sci Rep 2015; 5:13112 [View Article][PubMed]
    [Google Scholar]
  31. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004; 5:113 [View Article][PubMed]
    [Google Scholar]
  32. Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010; 27:221–224 [View Article][PubMed]
    [Google Scholar]
  33. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003; 52:696–704 [View Article][PubMed]
    [Google Scholar]
  34. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [View Article][PubMed]
    [Google Scholar]
  35. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article][PubMed]
    [Google Scholar]
  36. Perrière G, Gouy M. WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 1996; 78:364–369 [View Article][PubMed]
    [Google Scholar]
  37. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article][PubMed]
    [Google Scholar]
  38. Liu Q-Q, Berry A. The infection process and nodule initiation in the Frankia-Ceanothus root nodule symbiosis: a structural and histochemical study. Protoplasma 1991; 163:82–92 [Crossref]
    [Google Scholar]
  39. Karnovsky MJ. A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 1965; 27:137–138
    [Google Scholar]
  40. Benson DR, Stephens DW, Clawson ML, Silvester WB. 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 1996; 62:2904–2909[PubMed]
    [Google Scholar]
  41. Murry MA, Konopka AS, Pratt SD, Vandergon TL. The use of PCR-based typing methods to assess the diversity of Frankia nodule endophytes of the actinorhizal shrub Ceanothus . Physiol Plant 1997; 99:714–721 [View Article]
    [Google Scholar]
  42. Clawson ML, Bourret A, Benson DR. Assessing the phylogeny of Frankia-actinorhizal plant nitrogen-fixing root nodule symbioses with Frankia 16S rRNA and glutamine synthetase gene sequences. Mol Phylogenet Evol 2004; 31:131–138 [View Article][PubMed]
    [Google Scholar]
  43. Berry AM, Murphy TM, Okubara PA, Jacobsen KR, Swensen SM et al. Novel expression pattern of cytosolic Gln synthetase in nitrogen-fixing root nodules of the actinorhizal host, Datisca glomerata . Plant Physiol 2004; 135:1849–1862 [View Article][PubMed]
    [Google Scholar]
  44. Okubara PA, Pawlowski K, Murphy TM, Berry AM. Symbiotic root nodules of the actinorhizal plant Datisca glomerata express rubisco activase mRNA. Plant Physiol 1999; 120:411–420 [View Article][PubMed]
    [Google Scholar]
  45. Kohls SJ, Thimmapuram J, Buschena CA, Paschke MW, Dawson JO. Nodulation patterns of actinorhizal plants in the family Rosaceae . Plant Soil 1994; 162:229–239 [View Article]
    [Google Scholar]
  46. Silvester WB, Langenstein B, Berg RH. Do mitochondria provide the oxygen diffusion barrier in root nodules of Coriaria and Datisca ?. Can. J. Bot 1999; 77:1358–1366 [View Article]
    [Google Scholar]
  47. Zhang LB, Simmons MP, Kocyan A, Renner SS. Phylogeny of the Cucurbitales based on DNA sequences of nine loci from three genomes: implications for morphological and sexual system evolution. Mol Phylogenet Evol 2006; 39:305–322 [View Article][PubMed]
    [Google Scholar]
  48. Lalonde M. 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 1979; 140:S35–S43 [View Article]
    [Google Scholar]
  49. Pozzi AC, Bautista-Guerrero HH, Nouioui I, Cotin-Galvan L, Pepin R et al. In-planta sporulation phenotype: a major life history trait to understand the evolution of Alnus-infective Frankia strains. Environ Microbiol 2015; 17: [View Article][PubMed]
    [Google Scholar]
  50. Takhtajan AL, Crovello TJ, Cronquist A. Floristic Regions of the World Berkeley, CA: University of California Press; 1986
    [Google Scholar]
  51. Newcomb W, Pankhurst CE. Fine structure of actinorhizal root nodules of Coriaria arborea (Coriariaceae). New Zealand Journal of Botany 1982; 20:93–103 [View Article]
    [Google Scholar]
  52. Berg RH, Langenstein B, Silvester WB. Development in the Datisca-Coriaria nodule type. Can J Bot 1999; 77:1334–1350
    [Google Scholar]
  53. Hafeez F, Akkermans ADL, Chaudhary AH. Observations on the ultrastructure of Frankia sp. in root nodules of Datisca cannabina L. Plant Soil 1984; 79:383–402 [View Article]
    [Google Scholar]
  54. Kummerow J, Alexander JV, Neel JW, Fishbeck K. Symbiotic nitrogen fixation in Ceanothus roots. Am J Bot 1978; 65:63–69 [View Article]
    [Google Scholar]
  55. Strand R, Laetsch W. Cell and endophyte structure of the nitrogen-fixing root nodules of Ceanothus integerrimus H. & A. I. Fine structure of the nodule and its endosymbiont. Protoplasma 1977; 93:165–178 [Crossref]
    [Google Scholar]
  56. Liu Q, Berry AM. Localization and characterization of pectic polysaccharides in roots and root nodules of Ceanothus spp. during intercellular infection by Frankia. Protoplasma 1991; 163:93–101 [View Article]
    [Google Scholar]
  57. Hoeppel RE, Wollum AG. Histological studies of ectomycorrhizae and root nodules from Cercocarpus montanus and Cercocarpus paucidentatus . Canadian Journal of Botany 1971; 49:1315–1318 [View Article]
    [Google Scholar]
  58. Berry A, Sunell L. The infection process and nodule development. In Schwintzer C, Tjepkema JD. (editors) The Biology of Frankia and Actinorhizal Plants San Diego: Academic Press, Inc; 1990 pp. 61–81 [Crossref]
    [Google Scholar]
  59. Newcomb W. Fine structure of the root nodules of Dryas Drummondii Richards (Rosaceae). Canadian Journal of Botany 1981; 59:2500–2514 [View Article]
    [Google Scholar]
  60. Bond G. Observations on the root nodules of Purshia tridentata . Proc Roy Soc London 1976 Ser B 193:127–135 [View Article]
    [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.002147
Loading
/content/journal/ijsem/10.1099/ijsem.0.002147
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error