Bautista GHH, Valdés M

Language: Spanish
References: 134
Page: 90-102
PDF size: 105.05 Kb.

ABSTRACT

Nitrogen is the major factor limiting the growth of the living beings in the earth. In several instances the supply of this nutrient by plants is acquired by symbiosis. Symbiotic bacteria belong to 2 well established phylogenetic groups, the protobacteria Rhizobia and the actinobacteria Frankia. What do we know about Frankia the actinomycete associated to plants belonging to 8 different botanic families? Why there are not yet species in the genus? The 16S rDNA sequencing and the fingerprint techniques contribution to the bacterial phylogeny have dramatically changed our perception on the phylogeny and the taxonomy of all the living beings including Frankia. The polyphasic taxonomy intends to integrate different types of information: phenotypic methods, genotypic methods, and microbial phylogenies. These methods are used in the modern bacterial taxonomy for Frankia, although it is still difficult to formulate reliable and definitive classification of Frankia in species. However, this information provides much light on the genetic diversity and distribution of this nitrogen-fixing actinomycete.

REFERENCES

1. Acosta E., A. Cruz, M. Valdés & A. Medoza. 2005. Genome diversity of Frankia strains from different origins and host plants by AFLP analysis. Symbiosis 39:97-103.

2. Akimov V., S.V. Dobritsa & O. S. Stupar. 1991. Grouping of Frankia strains by DNA-DNA homology: How many genoespecies are in the genus Frankia? pp.635-636. In M Polsinelli, R Materassi & M Vincenzini (Eds). Nitrogen Fixation, Kluwer Academic Publisheres, Dordrecht, The Netherlands.

3. Alloisio N., S. Félix., J. Maréchal., P. Pujic., Z. Rouy., D. Vallenet., C. Medigue & P. Normand. 2007 Frankia alni proteome under nitrogen-fixing and nitrogen-replete conditions. Physiol Plant 130:440-453.

4. An, C. S., W. S. Riggsby & B. C. Mullin. 1985. Relationships of Frankia isolates based on deoxyribonucleic acid homology studies. Int J Syst Bacteriol 35:140-146.

5. Bagnarol E., J. Popovici., N. Alloisio., J. Maréchal., P. Pujic., P. Normand & M.P. Fernandez. 2007. Differential Frankia protein patterns induced by phenolic extracts from Myricaceae seeds. Physiol Plant 130:380-390.

6. Baker, D., W. L. Pengelly & G. J. Torrey. 1981. Immunological analysis of relationships among the isolated Frankia (Actinomycetales). Int J Syst Bacteriol 31:148-151.

7. Baker, D. D. 1987 Relationships among pure cultured strains of Frankia based on host specificity. Physiol Plant 70:245-248.

8. Becking, J. H. 1970. Frankiaceae fam. Nov. (Actinomicetales) with one new combination and six new species of the genus Frankia Brunchorst 1886. Int J System Bacteriol 20:201-220.

9. Benoist, P. & J. Schwencke. 1990. Native agarose-polyacrylamide gel electrophoresis allowing the detection of aminopeptidase, dehydrogenase and esterase activities at the nanogram level: enzymatic patterns in some Frankia strains. Ann Biochem 187:37-44.

10. Benson, D.R., D.J. Arp & R.H. Burris. 1980. Cell free nitrogenase and hydrogenase from actinorhizal root nodules. Science 205:688-689.

11. Benson, D.R., S.E. Buchholz & D. G. Hanna. 1984. Identification of Frankia strains by two dimentional polyacrylamide gel electrophoresis.

12. Benson, D.R., D.W. Stephens, M. L. Clawson & W.B. Silvester. 1996. Amplification of 16S rDNA genes from Frankia in root nodules of Ceanothus griseus, Coriaria arborea, Coriaria plumose, Discaria toumatou and Purshia tridentata. Appl Environ Microbiol 62:2904-2909.

13. Benson D. R., B.D. Vanden Heuvel & D. Potter. 2004 Actinorhizal symbioses: diversity and biogeography. BIOS Sc 15:99-130.

14. Benson D. R. & J. O. Dawson. 2007. Recent advances in the biogeography and genecology of symbiotic Frankia and its host plants. Physiol Plant130:318–330.

15. Berry, A. M., R. A. Moreau & A. D. Jones. 1991. Bacteriohopanetetrol: abundant lipid in Frankia cells and in nitrogen-fixing nodule tissue. Plant Physiol 95:111-115.

16. Berry A., O. Harriott., R. Moreau., S. Osman., D. Benson & A. Jones. 1993. Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc Nat Acad Sci 90:609–6094

17. Bosco M., M. P. Fernandez., P. Simonet., P. Materassi & P. Normand. 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.

18. Busse M. D. 2000. Ecological significance of nitrogen fixation by actinorhizal shrubs in interior forests of California and Oregon. USDA Forest Service Gen Tech Rep PSW-GTR-178.

19. Callaham D., P. Del Tredeci & J. G. Torrey. 1978. Isolation and cultivation in vitro of the actinomycete causing root nodulation in Comptonia. Science 199:899-902.

20. Clawson M. L., M. Carú & D. R. Benson. 1998. Diversity of Frankia strains in root nodules of plants from the families Elaeagnaceae and Rhamnaceae. Appl Environ Microbiol 64:3539-3543.

21. Clawson M. L. & D. R. Benson. 1999. Natural diversity of Frankia strains in actinorhizal root nodules from promiscuous hosts in the family Myricaceae. Appl Environ Microbiol 65:4521-7.

22. Clawson M. L., A. Bourret & D. R. Benson. 2004. Assessing the phylogeny of Frankia-actinorhizal plant nitrogen-fixing root nodule symbioses with Frankia 16S rRNA and glutamine synthetase gene sequences. Mol Phylogen Evol 31:131-8.

23. Cournoyer, B. & P. Normand. 1994. Characterization of a spontaneous thiostrepton-resistant Frankia alni infective isolate using PCR-RFLP of nif and glnII genes. Soil Biol Biochem 26:553-559.

24. Cournoyer B. & C. Lavire. 1999. Analysis of Frankia evolutionary radiation using glnII sequences. FEMS Microbiol Lett 177:29-34.

25. Dawson, J. O. 1990. Interactions among actinorhizal and associated plant species. pp 299-316. In C R Schwintzer & J D Tjepkema (Eds). The Biology of Frankia and Actinorhizal Plants, Academic Press, San Diego, California.

26. Diem, H. G., & Y. R. Dommergues. 1990. Current and potential uses and management of Casuarinaceae in the tropics and subtropics. pp 317-342. In C R Schwintzer & J D Tjepkema (Eds). The biology of Frankia and Actinorhizal Plants, Academic Press, San Diego, California.

27. Dixon R., S. Austin., T. Eydmann., S. Hill., S.O. Kim., P. Macheroux., R. Poole., F. Reyes., Sobzcyk & E. Soderback. 1998. Regulation of nif gene expression in free living diazotrophs: Recent advances. pp. 87-91. In H. Bothe, F.J. DeBrujin & W.E. Newton (Eds). Nitrogen Fixation: hundred years after, Gustav Fischer, Stuttgart, New York.

28. Dommergues Y. R. 1997. Contribution of actinorhizal plants to tropical soil productivity and rehabilitation. Soil Biol Biochem 29:931-941

29. Dommergues Y. R. & N. S. Subba Rao. 2000. Introduction of N2-fixing trees in non-N2- fixing tropical plantations. pp 131-154. In N S Subba Rao & Y R Dommergues (Eds). Microbial interactions in agriculture and forestry, Science Publishers, Enfield, New Hampshire.

30. Edmands J., N. A. Noridge & D. R. Benson. 1987. The actinorhizal root-nodule symbiont Frankia sp strain Cpll has two glutamine synthetases. Proc Natl Acad Sci. 84:6126-6130.

31. Fernandez M. P., H. Meugnier., P. A. D. Grimont & R. Bardin. 1989. Deoxyribonucleic acid relatedness among members of the genus Frankia. Int J Syst Bacteriol 39:424-429.

32. Gardes M., J. Bousquet & M. Lalonde. 1987. Isozyme Variation among 40 Frankia strains. Appl Environ Microbiol 53:1596-1603.

33. Gauthier D., T. Jaffre & Y. Prin. 1999. Occurrence of both Casuarina-infective and Elaeagnus-infective Frankia strains within actinorhizae of Casuarina collina endemic to New Caledonia. Eur J Soil Biol 35:9-15.

34. Gauthier, D., T. Jaffre & Y. Prin. 2000 Abundance of Frankia from Gymnostoma spp in the rhizosphere of Alphitonia neocaledonica, a non-nodulated Rhamnaceae endemic to New Caledonia. Eur J Soil Biol 36:169-175

35. Gevers D., F. M. Cohan., J. G. Lawrence., B. G. Spratt., T. Coenye., E. J. Feil., E. Stackebrandt., Y. Van de Peer., P. Vandamme., F. L. Thompson & J. Swigs. 2005 Re-evaluating bacterial species. Nat Microbiol. Rev 3:733-739.

36. Girgis, M. G. Z. & J. Schwencke. 1993. Differentiation of Frankia strains by their electrophoretic patterns of intracellular estearases and aminopeptidases. J Gen Microbiol 139:2225-2232.

37. Gtari M., D. Daffonchio & A. Boudabous. 2007. Occurrence and diversity of Frankia in Tunisian Soil. Physiol Plant 130:372-379.

38. Gualteri G. & T. Bisseling. 2000. The evolution of nodulation. Plant Mol Biol 42:181-194.

39. Gurtler, V. 1999.The role of recombination and mutation in 16S–23S rDNA spacer. Gene 238:241-252.

40. Hahn D. 2008. Polyphasic taxonomy of the genus Frankia. In K Pawlowsky & W E Newton (Eds). Nitrogen-fixing Actinorhizal Symbiosis, Kluwer Academic Publishers.

41. Hahn D., M. P. Lechevalier., A. Fischer & E. Stackebrandt. 1989. Evidence for a close phylogenetic relationship between members of the genera Frankia, Geodermatophilus, “Blastococcus” and emendation of the family Frankiaceae. Syst Applied Microbio 11:236-242.

42. Hahn D., A. Níkel & J. Dawson. 1999. Assessing Frankia populations in plants and soil using molecular methods. FEMS Microbiol Ecol 29:215-227.

43. Hanage W. P., C. Fraser & B. Spratt. 2006. Sequences, sequence clusters and bacterial species. Phil Trans R Soc B 361:1917-1927.

44. Harry D. E., D. C. Yang & J. O. Dawson. 1991. Nucleotide sequence and diversity in 16S ribosomal RNA from Frankia. Plant and Soil 131:143-146.

45. Horrière F. 1984. In vitro physiological approach to classification of Frankia isolates of ‘the Alnus group’, based on urease, protease and b-glucosidase activities. Plant Soil 74:7-13.

46. Huguet V., J. McCray Batzli., J. F. Zimpfer., P. Normand., J. O. Dawson & M. P. Fernandez. 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.

47. Huss Danell, K. 1997. Actinorhizal symbioses and their N2 fixation. New Phytol 136:375-405.

48. Jae O. C. & K. C. S. An Ho Bang. 2003. Molecular cloning and complementation analysis of nifV gene from Frankia EuIK1 strain. Mol Cells 15:27-33.

49. Jamann, S., M. P. Fernandez & P. Normand. 1993. Typing method for N2-fixing bacteria based on PCR-RFLP-application to the characterization of Frankia strains. Mol Ecol 2:17-26.

50. Jeong, S.-C. & D. D. Myrold. 1999. Genomic fingerprinting of Frankia microsymbionts from Ceanothus copopulations using repetitive sequences and polymerase chain reactions. Can J Bot 77:1220-1230.

51. Jeong, S. C., N. J. Ritchie & D. D. Myrold. 1999. Molecular phylogenies of plants and Frankia support multiple origins of actinorhizal symbioses. Mol Phylogen Evol 13:493-503.

52. Jeong, S. C. & D. D. Myrold. 2001. Population size and diversity of Frankia in soils of Ceanothus velutinus and Douglas-fir stands. Soil Biol Biochem 33:931-941.

53. John, T.R., J. M. Rice & J. D. Johnson. 2001 Analysis of pFQ12, a 22.4-kb Frankia plasmid. Can J Microbiol 47:608-617.

54. John T. R., J. Wiggington., J. Bock., R. Klemt & J. D. Johnson. 2004. An insertion sequence unique to Frankia ArI5. Plant Soil 254:107-113.

55. Kazazian H. H. 2004. Mobile elements drivers of genome evolution. Science 303:1626-1632.

56. Kim, H.B. & C. S. An. 1997. Nucleotide sequence and expression of nifHD from Frankia strain EuIK1, a symbiont of Elaeagnus umbellata. Physiol Plant 99:690-695.

57. Kumada Y., D. R. Benson., D. Hillemann., T. J. Hosted., D. A. Rochefort., C. Thompson., W. Wohlleben & Y. Tateno. 1993. Evolution of the glutamine synthetase gene: one of the oldest genes ever studied. Proc Nat Acad Sci. 90:3009-3013.

58. Lalonde M., L. Simon., J. Bousquet & A. Seguin. 1988. Advances in the taxonomy of Frankia: recognition of species Alni, elaeagnii and novel subspecies pommeri and vandijkii. pp 671-680. In H. Bothe, F.J. DeBrujin & W.E. Newton (Eds). Nitrogen Fixation: hundred years after, Gustav Fischer, Stuttgart, New York.

59. Lavire C., D. Louis., G. Perriere., J. Briolay., P. Normand & B. Cournoyer. 2001. Analysis of pFQ31, a 8551-bp cryptic plasmid from three symbiotic nitrogen-fixing actinomycete Frankia. FEMS Microbiol Lett 197:111-116.

60. Lavire C. & B. Cournoyer. 2003. Progress on the genetics of the N2 fixing actinorhizal symbiont Frankia. pp 125-137. In P. Normand, K. Pawlowsky & J. O. Dawson. Frankia Symbiosis: Proc 12th International Meeting on Frankia and Actinorhizal Plants, Kluwer Academic Publishers.

61. Lechevalier, M.P. 1983. Cataloging Frankia strains. Can J Microbiol 61: 2964-2967.

62. Lechevalier, M.P. 1984. The taxonomy of the genus Frankia. Plant and soil 78:1-6.

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

64. Lechevalier, M.P. & H. A. Lechevalier. 1984. Taxonomy of Frankia. pp. 2410-2417. In S T Williams, M E Sharpe and J G: Holt (Eds). Bergey’s manual of systematic bacteriology vol 4, The Williams and Wilkins Co, Baltimore.

65. Lee H., S. B. Sung., H.B. Kim & C. S. An. 2001. Sequence analysis and expression patterns of two nifA genes from Frankia EuIK1. Aust J Plant Physiol 28: 939-949.

66. Leul M., P. Normand & A. Sellstedt. 2007. The organization, regulation and phylogeny of uptake hydrogenase genes in Frankia. Physiol Plant 130:464-470.

67. Ligon M. J & James P. Nakas. 1987. Isolation and characterization of Frankia sp strain FaCl genes Involved in nitrogen fixation. Appl Environ Microbiol 53:2321-2327.

68. Lumini E. & M. Bosco. 1996. PCR-restriction fragment length polymorphism identification and host range of single-spore isolates of the flexible Frankia sp strain UFI 132715. Appl Environ Microbiol 62:3026-3029.

69. Maggia L. & J. Bousquet. 1994. Molecular phylogeny of the actinorhizal Hamamelidae and relationships with host promiscuity towards Frankia. Mol Ecol 3:459-467.

70. Maréchal J., B. Clement., R. Nalin., G. Corinne., S. Orso., J. Cvejic., M. Bruneteau., A. Berry & Philippe Normand. 2000. A recA gene phylogenetic analysis confirms the close proximity of Frankia to Acidothermus. Int J Syst Bacteriol 50: 781–785.

71. Martinez-Argudo I., R. Little., N. Shearer., P. Johnson & R. Dixon. 2004. The nifL-nifA System: a multidomain transcriptional regulatory complex that integrates environmental signals. J Bacteriol 186:601-610.

72. Mattsson U. & Anita Sellstedt. 2000. Hydrogenase in Frankia KB5: expression of and relation. Rev Canad Microbiol 46:91-95.

73. Mirza S., D. Hahn & A. D. L. Akkermans. 1992. Isolation and characterization of Frankia strains from Coriaria nepalensis. Syst Appl Microbiol 15:289-295.

74. Mirza S. M., S. Hammed & Antoon D. L Akkermans. 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.

75. Mort A., P. Normand & M. Lalonde. 1983. 2-O-Methyl-D-Mannose, a key sugar in the taxonomy of Frankia. Can J Microbiol 29:993-1002.

76. Murry, M. A., A. S. Konopka, S. D. Pratt, & T. L. Vandergon. 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.

77. Murry M. A., D. Zhang., M. Schneider & F. J. de Bruijn. 1995. Use of repetitive sequences and the polymerase chain reaction (rep-PCR) to fingerprint the genomes of Frankia isolates. Symbiosis 19:223-240.

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

79. Nalin R., A. M. Domenach & P. Normand. 1995. Molecular structure of the Frankia sp nifD-K intergenic spacer and design of Frankia genus compatible primer. Mol Ecol 4:483-91.

80. Nasr H., A. M. Domenach., M. H. Ghorbel & D. R. Benson. 2007. Divergence in symbiotic interactions between same genotypic PCR-RFLP Frankia strains and different Casuarinaceae species under natural conditions. Physiol Plant 130:400-408.

81. Navarro E., T. Jaffre., D. Gauthier., F. Gourbière., G. Rinaudo., P. Simonet & P. Normand. 1999. Distribution of Gymnostoma sp microsymbiotic Frankia strains in New Caledonia is related to soil type and to host-plant species. Mol Ecol 8:1781-1788.

82. Navarro E., R. Nalin., D. Gauthier & P. Normand. 1997. The nodular microsymbionts of Gymnostoma sp are Elaeagnus-Infective Frankia strains. Appl Environ Microbiol 63:1610-1616.

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

84. Newcomb W., D. Callaham., J. G. Torrey & R. L. Peterson. 1979. Morphogenesis and fine structure of the actinomycetous endophyte of nitrogen-fixing root nodules of Comptonia peregrina. Bot Gaz 140,S22-S34.

85. Nikel A., O. Pelz., D. Hahn., M. Saurer., R. Siegwolf & J. Zeyer. 2001. Effect of inoculation and leaf litter amendment on establishment of nodule-forming Frankia populations in soil. Appl Environ Microbiol 67:2603-2609.

86. Normand P., P. Simonet., J. L. Butour., C. H. Rosenberg., A. Moiroud & M. Lalonde. 1983. Plasmids in Frankia sp. J Bacteriol 155:32-35.

87. Normand P & J. Bousquet. 1989. Phylogeny of nitrogenase sequences in Frankia and other nitrogen-fixing microorganisms. J Mol Evol 29:436-447.

88. Normand P., M. Gouy., B. Cournoyer & P. Simonet. 1992. Nucleotide sequence of nifD from Frankia alni strain ArI3: Phylogenetic inferences. Mol Biol Evol 9:495-506.

89. Normand P., S. Orso., B. Cournoyer., P. Jeannin., C. Chapelon., J. Dawson., L. Evtushenko & A. K. Misra. 1996. Molecular phylogeny of the genus Frankia and related genera and emendation of family Frankiaceae. Int J Syst Bacteriol 46:1-9.

90. Normand P., P. Lapierre., L. S. Tisa., J. P. Gogarten., N. Alloisio., E. Bagnarol., C. A. Bassi., A. M. Berry., D. M. Bickhart., N. Choisne., A. Couloux., B. Cournoyer., S. Cruveiller., V. Daubin., N. Demange., M. P. Francino., E. Goltsman., Y. Huang., O. R. Kopp., L. Labarre., A. Lapidus., C. Lavire., J. Maréchal., M. Martinez., J. E. Mastronunzio., B. C. Mullin., J. Niemann., P. Pujic., T. Rawnsley., Z. Rouy., C. Schenowitz., A. Sellstedt., F. Tavares., J. Tomkins., D. Vallenet., C. Valverde., L. G. Wall., Y. Wang., C. Médigue & D. R. Benson. 2007a. Genome characteristics of facultatively symbiotic Frankia sp strains reflect host range and host plant biogeography. Genome Res 17: 7–15.

91. Normand P., C. Queiroux., L. S. Tisa., D. R. Benson., Z. Rouy., S. Cruvellier & C. Médigue. 2007b. Exploring the genomes of Frankia. Physiol Plant 130:331-343.

92. Paschke M., J. O. Dawson & M.B. David. 1989. Soil nitrogen mineralization in plantations of Juglans nigra interplanted with Elaeganus umbellata or Alnus glutinosa. Plant Soil 118:33-42.

93. Paschke M. & J. Dawson. 1992. Frankia abundance in soils beneath Betula nigra and other non-actinorhizal woody plants. Acta Oecol 13:407-415.

94. Pawlowski K & T. Bisseling. 1996. Rhizobial and actinorhizal symbioses: what are the shared features?. Plant Cell 8:1899-1913.

95. Pérez N. O., H. Olivera & M. Valdés. 1999. Genetic characterization of Mexican Frankia strains nodulating Casuarina equisetifolia. Can J Botany 77:1214-1219.

96. Ramirez-Saad H., J. D. Janse & A. D. L. Akkermans. 1998. Root nodules of Ceanothus caeruleus contain both the N2-fixing Frankia endophyte and a phylogenetically related Nod-/Fix- actinomycete. Can J Microbiol 44:140-148.

97. Rawnsley T. & L.S. Tisa. 2007. Development of a physical map for three Frankia strains and a partial map for Frankia EuI1c. Physiol Plant 130:427-439.

98. Rees D. C., C. Shindelin., J. Kisker., J. W. Schlessman., L. C. Peters., Seefeldt & J. B. Howard. 1998. Complex Structures of Nitrogenase p: 11-16 In Biological Nitrogen Fixation for the 21Century, Kluwer Academic Publishers.

99. Ritchie N. J. & D. D. Myrold. 1999. Geographic distribution and genetic diversity of Ceanothus-infective Frankia strains. Appl Environ Microbiol 65:1378-1383.

100. Robertson D.L. & A. Tartar. 2006. Evolution of glutamine synthetase in heterokonts: Evidence for endosymbiotic gene transfer and the early evolution of photosynthesis. Mol Biol Evol 23:1048-1055.

101. Rosa-Putra S., R. Nalin., A. M. Domenach & M. Rorhner. 2001. Novel hopanoids from Frankia and related soil bacteria. Eu J Biochem 268: 4300-4306.

102. Rouvier C., S. Nazaret., M. P. Fernandez., B. Picard., P. Simonet & P. Normand. 1992. rrn and nif intergenic spacers, and isoenzyme patterns as tools to characterize Casuarina-infective Frankia strains. Acta Oecol 13:487-495.

103. Rouvier C., Y. Prin., P. Reddell., P. Normand & P. Simonet. 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 62:979-985.

104. Roy A. & J. Bousquet. 1996. The evolution of the actinorhizal symbiosis through phylogenetic analysis of host plants. Acta Bot Gallica 143:635-650.

105. Ruvkun G. B. & F. M. Ausbel. 1980. Interspecies homology of nitrogenase genes. Proc Natl Acad Sci 77:191-195.

106. Sayed W. F. 2003. Effects of land irrigation with partially-treated wastewater on Frankia survival and infectivity. pp 19-26. In P Normand, K Pawlowsky & J O Dawson (Eds). Frankia Symbiosis: Proc 12th International Meeting on Frankia and Actinorhizal Plants, Kluwer Academic Publishers.

107. Schwencke J. & M. Carú. 2001. Advances in Actinorhizal Symbiosis: host plant- Frankia interactions, Biology and Applications in Arid Land Reclamation. A review. Arid Land Res Manage15:285 – 327.

108. Sellstedt A. & P. Lindbland. 1990. Activities, occurrence, and localization of hydrogenase in free-living and symbiotic Frankia. Plant Physiol 92:809-815.

109. Silvester W.B., J.K. Silvester & J. G. Torrey. 1988.Adaptation of nitrogenase to varying oxygen tension and the role of the vesicle in the root nodules of Alnus incana ssp. rugosa. Can J Bot 66:1772-1779.

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

111. Simonet P., P. Normand., A. Moiroud & M. Lalonde. 1985. Restriction enzyme digestion patterns of Frankia plasmids. Plant Soil 87:49-60.

112. Simonet P., J. Haurat., P. Normand., R. Bardin & A. Moiroud. 1986. Localization of nif genes on a large plasmid in Frankia sp strain ULQ0132105009. Mol Gen Genetics 204: 492-495.

113. Simonet P., P. Normand & R. Bardin. 1988. Heterologous hybridization of Frankia DNA to Rhizobium meliloti and Klebsiella pneumoniae nif genes. FEMS Microbiol Lett 55 :141-146.

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

115. Smolander, A. & V. Sundman. 1987. Frankia in acid soils of forest devoid of actinorhizal plants. Physiol Plantarum 70:297-303.

116. Soltis,D.E., Soltis, P.S., M.W. Chase, M.E. Mort, D.C. Albach, M. Zanis, V. Savolainen, W.H. Hahn, S.B. Hoot, M.F. Fay, M. Axtell, S.M. Swensen, L.M. Princel, W.J.O.H.N. Kress, K.C. Nixon, J.S. Farris. 2000. Angiosperm phynology inferred from 18S rDNA, rbcL, and atpB sequences. Bot J Linn Soc 133:381-461.

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

118. St. Laurent L., J. Bousquet., L. Simon & M. Lalonde. 1987. Separation of various Frankia strains in the Alnus and Elaeagnus host specificity groups using sugar analysis. Can J Microbiol 33:764-772.

119. Stackebrandt E., W. Frederiksen., G. M. Garrity., PAD Grimont., P. Kampfer., MCJ. Maiden., X. Nesme., Rossello-Mora R., J. Swings., H. G. Truper., L. Vauterin., A. C. Ward & W. B. Whitman. 2002. Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J of Syst Evol Microbiol 52:1043-1047.

120. Swensen, S. M. 1996 The evolution of actinorhizal symbioses: Evidence for multiple origins of the symbiotic association. Am J Bot 83:1503-1512.

121. Swensen S. M., B. C. Mullin & M. W. Chase. 1994. Phylogenetic affinities of the Datiscaceae based on an analysis of nucleotide sequences from the plastid rbcL gene. Syst Bot 19:157-168.

122. Swensen S. M. & David R. Benson. 2008. Evolution of actinorhizal host plants and Frankia endosymbionts. pp 2-33. In K Pawlowsky & W E Newton (Eds). Nitrogen-fixing Actinorhizal Symbiosis, Kluwer Academic Publishers.

123. Tjepkema, J. D., & J. G. Torrey. 1979. Symbiotic nitrogen fixation in actinomycete-nodulated plants. Bot Gazette 140:i-ii.

124. Tjepkema, J. D., W. Ormerod & J.G. Torrey. 1981. Factors affecting vesicle formation and acetylene reduction (nitrogenase activity) in Frankia CpI4. Can J Microbiol 27:815-823.

125. Torrey, J. G. 1978. Nitrogen fixation by actinomycete-nodulated angiosperms. BioScience 28:586-592.

126. Torrey, J. G. 1985. The site of nitrogenase in Frankia in free-living culture and in symbiosis. In pp. 293-299. H J Evans, P J Bottomley & W E Newton (Eds). Nitrogen fixation research progress. Martinus Nijhof , Dordrecht The Netherlands.

127. Trujillo Cabrera, Y. 2007. Diversidad genética de Frankia en el interior de los nódulos de Casuarina en México. Tesis de Maestría, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, México.

128. Tsai Y. L. & D. R. Benson. 1989. Physiological characteristics of glutamine synthetases I and II of Frankia sp strain CpI1. Arch Microbiol 152:382-386.

129. Valdés M. 2008. Frankia Ecology. pp . In K Pawlowsky & W E Newton (Eds). Nitrogen-fixing Actinorhizal Symbiosis, Kluwer Academic Publishers.

130. Valdés, M., L. Vásquez, N.O. Pérez. 2001.Genetic markers (RAPDs and repPCR) for ecological studies of the nitrogen-fixing symbiosis Frankia-Casuarina. European Trop For Res Network 341:27-29.

131. Vanden Heuvel B. D., R. D. Benson., E. Bortiri., M. Valdés M. & Daniel Potter. 2004. Low genetic diversity among Frankia sp Strains nodulating sympatric populations of actinorhizal species of Rosaceae, Ceanothus (Rhamnaceae) and Datisca glomerata (Datiscaceae) west of the Sierra Nevada (California). Can J Microbiol 50:989-1000.

132. Verghese & A. K. Misra. 2002. Frankia-actinorhizal symbiosis with special reference to host-microsymbiont relationship. Current Science 83: 404-407

133. Wall L. G. 2000. The actinorhizal symbiosis. J Plant Growth Regul 19: 167-182.

134. Xu X. D., R. Q. Kong., de Bruijn F.J., S. Y. He., M. A. Murry., T. Newman & P. Wolk. 2002. DNA sequence and genetic characterization of plasmid pFQ11 from Frankia alni strain CpI1. FEMS Microbiol. Lett. 207:103107.