Symbiosis

, Volume 51, Issue 3, pp 201–226 | Cite as

Life in soil by the actinorhizal root nodule endophyte Frankia. A review

  • Eugenia E. Chaia
  • Luis G. Wall
  • Kerstin Huss-Danell
Article

Abstract

Frankia is a genus of soil actinomycetes famous for its ability to form N2-fixing root nodule symbioses with actinorhizal plants. Although Frankia strains display a high diversity in terms of ecological niches in soil, current knowledge about Frankia is dominated by its life as an endophyte in root nodules. Increased use of molecular methods has refined and expanded insights into endophyte-host specificities and Frankia phylogeny. This review has focus on Frankia as a soil organism, including its part of microbial consortia, and how to study Frankia in soil. We highlight the use of nodulation tests and molecular methods to reveal population size and genetic diversity of Frankia in soil and discuss how autoregulation of nodulation and interactions with other soil microorganisms may influence the results. A comprehensive record of published interactions between Frankia and other soil microbes is summarized.

Keywords

Actinomycetes Frankia detection methods Frankia ecology N2 fixation Plant-microbe interaction Symbiosis 

Abbreviations

GU

genomic units

MPN

most probable number

NC

nodulation capacity

NT

nodulation test

NU

nodulating units

PCR

polymerase chain reaction

Notes

Acknowledgements

The tripartite collaboration between the authors was financially supported by STINT, the Swedish Foundation for International Cooperation in Research and Higher Education (grants to K Huss-Danell). Work by E Chaia was financially supported by Universidad Nacional del Comahue and by ANPCyT, the Agencia Nacional de Promoción Científica y Tecnológica. L G Wall is member of the CONICET, the Argentine National Research Council, and has received grants from Universidad Nacional de Quilmes, CONICET and ANPCyT. We thank Osei Ampomah and Claudio Valverde for valuable comments on the manuscript and Shari Gregory for improving the English text.

This paper is dedicated to the memory of Antoon D L Akkermans (1940–2006) for his pioneering and always creative and inspiring work on Frankia and actinorhizal plants, ranging from ecosystems worldwide to physiology and molecular biology of Frankia and its symbioses.

References

  1. Alloisio N, Félix S, Maréchal J, Pujic P, Rouy Z, Vallenet D, Medigue C, Normand P (2007) Frankia alni proteome under nitrogen-fixing and nitrogen-replete conditions. Physiol Plant 130:440–453Google Scholar
  2. Alloisio N, Queiroux C, Fournier P, Pujic P, Normand P, Vallenet D, Médigue C, Yamaura M, Kakoi K, Kucho K (2010) The Frankia alni symbiotic transcriptome. Mol Plant Microbe Interact 23:593–607PubMedGoogle Scholar
  3. Akkermans ADL, Hirsch AM (1997) A reconsideration of terminology in Frankia research: a need for congruence. Physiol Plant 99:574–578Google Scholar
  4. Arveby AS, Huss-Danell K (1988) Presence and dispersal of infective Frankia in peat and meadow soils in Sweden. Biol Fertil Soils 6:39–44Google Scholar
  5. Bagnarol E, Popovici J, Alloisio N, Maréchal J, Pujic P, Normand P, Fernandez MP (2007) Differential Frankia protein patterns induced by phenolic extracts from Myricaceae seeds. Physiol Plant 130:380–390Google Scholar
  6. Baker DD, Mullin BC (1994) Diversity of Frankia nodule endophytes of the actinorhizal shrub Ceanothus as assesed by RFLP patterns from single nodule lobes. Soil Biol Biochem 26:547–552Google Scholar
  7. 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 78:23–28Google Scholar
  8. Baker D, Newcomb W, Torrey JG (1980) Characterization of an ineffective actinorhizal microsymbiont, Frankia sp. EuIl (Actinomycetales). Can J Microbiol 26:1072–1089PubMedGoogle Scholar
  9. Barea JM, Pozo JM, Azcon R, Azcon-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778PubMedGoogle Scholar
  10. Bassi CA, Benson DR (2007) Growth characteristics of the slow-growing Actinobacterium Frankia sp. strain CcI3 on solid media. Physiol Plant 130:391–399Google Scholar
  11. Becerra A, Nouhra E, Daniele G, Domínguez L, McKay D (2005a) Ectomycorrhizas of Cortinarius helodes and Gyrodon monticola with Alnus acuminata from Argentina. Mycorrhiza 15:7–15PubMedGoogle Scholar
  12. Becerra A, Zak MR, Horton T, Micolini J (2005b) Ectomycorrhizal and arbuscular mycorrhizal colonization of Alnus acuminata from Calilegua National Park (Argentina). Mycorrhiza 15:525–531PubMedGoogle Scholar
  13. Becking JH (1970) Frankiaceae fam. nov. (Actinomycetales) with one new combination and six new species of the genus Frankia Brunchorst 1886. Int J Syst Bacteriol 20:201–220Google Scholar
  14. Benoit LF, Berry AM (1997) Flavonoid-like compounds from seeds of red alder (Alnus rubra) influence host nodulation by Frankia (Actinomycetales). Physiol Plant 99:588–593Google Scholar
  15. Benson DR, Dawson JO (2007) Recent advances in the biogeography and genecology of symbiotic Frankia and its host plants. Physiol Plant 130:318–330Google Scholar
  16. Benson DR, Stephens DW, Clawson ML, Silvester WB (1996) Amplification of 16S rRNA genes from Frankia strains in root nodules of Ceanothus griseous, Coriaria arborea, Coraria plumosa, Discaria toumatou, and Purshia tridentata. Appl Environ Microbiol 62:2904–2909PubMedGoogle Scholar
  17. Berry A, Torrey JG (1979) Isolation and characterization in vivo and in vitro of an actimyceteous endophyte from Alnus rubra Bong. In: Gordon J, Wheeler C, Perry D (eds) Symbiotic nitrogen fixation in the management of temperate forest. Forest Reseach Laboratory, Oregon State University, Corvallis, pp 69–83Google Scholar
  18. Berry AM, Harriot OT, Moreau RA, Osman SF, Benson DR, Jones AD (1993) Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to dinitrogenase. Proc Natl Acad Sci USA 90:6091–6094PubMedGoogle Scholar
  19. Bertin PN, Medigue C, Normand P (2008) Advances in environmental genomics: towards an integrated view of micro-organisms and ecosystems. Microbiology 154:347–359PubMedGoogle Scholar
  20. Bond G (1957) The development and significance of the root nodules of Casuarina. Ann Bot 21:378–380Google Scholar
  21. Bond G (1976) The results of the IBP survey of root-nodule formation in non-leguminous angiosperms. In: Nutman PS (ed) Symbiotic nitrogen fixation in plants. Cambridge University Press, Cambridge, pp 443–474Google Scholar
  22. Brunchorst (1886–1888) Über einige Wurzelanschwellungen, besonders diejenigen von Alnus und den Elaeagnaceen. Unters Bot Inst Tübingen 2:150–177Google Scholar
  23. Burleigh SH, Dawson JO (1994a) Occurrence of Myrica-nodulating Frankia in Hawaiian volcanic soils. Plant Soil 164:283–289Google Scholar
  24. Burleigh SH, Dawson JO (1994b) Desiccation tolerance and trehalose production in Frankia hyphae. Soil Biol Biochem 25:593–598Google Scholar
  25. Burleigh SH, Dawson JO (1995) Spores of Frankia strain HFPCcI3 nodulate Casuarina equisetifolia after passage through the digestive tracts of captive parakeets (Melipsittacus undulatus). Can J Bot 73:1527–1530Google Scholar
  26. 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
  27. Cervantes E, Rodríguez-Barrueco C (1992) Relationships between the mycorrhizal and actinorhizal symbioses in non-legumes. In: Norris JR (ed) Techniques for mycorrhizal research, methods in microbiology. Academic Press, London, pp 877–892Google Scholar
  28. Chaia EE, Ribeiro Guevara S, Rizzo A, Arribére M (2005) Occurrence of Discaria trinervis nodulating Frankia in dated sediments of glacial Andean lakes. Symbiosis 39:67–75Google Scholar
  29. Chaia EE, Fontenla S, Vobis G, Wall LG (2006a) Infectivity of soilborne Frankia and mycorrhizae in Discaria trinervis along a vegetation gradient in Patagonian soil. J Basic Microbiol 46:263–274PubMedGoogle Scholar
  30. Chaia EE, Valverde C, Wall LG (2006b) Local adaptation of Frankia isolates to different Discaria (Rhamnaceae) host species growing in Patagonia. Curr Microbiol 53:523–528PubMedGoogle Scholar
  31. Chaia EE, Solans M, Vobis G, Wall LG (2007) Infectivity variation of Discaria trinervis-nodulating Frankia in Patagonian soil according to season and storage conditions. Physiol Plant 130:357–363Google Scholar
  32. Chapin FS III, Walker RL, Fastie CL, Sharman LC (1994) Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska. Ecol Monogr 64:149–175Google Scholar
  33. Chatarpaul L, Chakravarty P, Subramaniam P (1989) Studies in tetrapartite symbioses. Plant Soil 118:145–150Google Scholar
  34. Chaudhary AH, Hafeez F, Akkermans ADL, Chaudhary MF, Mirza MS (1985) Morphology, physiology and potential in agroforestry of Datisca, Coriaria and Alnus species from Pakistan. In: Malik KA, Naqvi SHM, Aleem MIH (eds) Proceedings International Symposium on Nitrogen and the Environment, 1984. Lahore, Publ. NIAB Faisalabad, pp 213–224Google Scholar
  35. 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
  36. Clawson ML, Benson DR, Resch SC (1997) Typical Frankia infect actinorhizal plants exotic to New Zealand. NZ J Bot 35:361–367Google Scholar
  37. 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
  38. Clawson ML, Gawronski J, Benson DR (1999) Dominance of Frankia strains in stands of Alnus incana subsp. rugosa and Myrica pensylvanica. Can J Bot 77:1203–1207Google Scholar
  39. 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
  40. Cruz-Cisneros R, Valdés M (1990) Ecological aspects of the actinorhizal plants growing in the basin of Mexico. Nitrogen-Fixing Tree Research Report 8:42–47Google Scholar
  41. Cruz-Cisneros R, Valdés M (1991) Actinorhizal root nodules on Adolphia infesta (H.B.K.) Meissner (Rhamanceae). Nitrogen-Fixing Tree Research Report 9:87–89Google Scholar
  42. Cusato MS, Tortosa RD (1990) Effective nodulation of rhamnaceous actinorhizal plants induced by air dry soils. Plant Soil 131:229–233Google Scholar
  43. Cusato MS, Tortosa RD (1998) Host specificity of Frankia from actinorhizal plant soils of South America. Φyton 62:231–236Google Scholar
  44. Cusato MS, Tortosa RD, Valiente L, Barneix AJ, Puelles MM (2007) Effects of Zn2+ on nodulation and growth of a South American actinorhizal plant, Discaria americana (Rhamnaceae). World J Microbiol Biotechnol 23:771–777Google Scholar
  45. Dawson JO (2008) Ecology of actinorhizal plants. In: Pawloski K, Newton WE (eds) Nitrogen fixation: origins, applications, and researh progress, vol. 6. Nitrogen-fixing actinorhizal symbioses. Springer, Dordrecht, pp 199–234Google Scholar
  46. Dawson JO, Kowalski DG, Dart PJ (1989) Variation with soil depth, topographic position and host species in the capacity of soils from an Australian locale to nodulate Casuarina and Allocasuarina seedlings. Plant Soil 118:1–11Google Scholar
  47. Densmore RV (2005) Succession on subalpine glacier mine spoil: effects of revegetation with Alnus viridis, Alaska, U.S.A. Arctic Antarct Alpine Res 37:297–303Google Scholar
  48. Diem HG, Gauthier D, Dommergues YR (1982) Extranodular growth of Frankia on Casuarina equisetifolia. FEMS Microbiol Lett 15:181–184Google Scholar
  49. Elo S, Maunuksela L, Salkinoja-Salonen M, Smolander A, Haahtela K (2000) Humus bacteria of Norway spruce stands: plant growth promoting properties and birch, red fescue and alder colonizing capacity. FEMS Microbiol Ecol 31:143–152PubMedGoogle Scholar
  50. Fessenden RJ, Sutherland BJ (1979) The effect of excess soil copper on the growth of black spruce and green alder seedlings. Bot Gaz 140:S82–S87Google Scholar
  51. Fontenla S, Godoy R, Rosso P, Havrylenko M (1998) Root associations in Austrocedrus forests and seasonal dynamics of arbuscular mycorrhizas. Mycorrhiza 8:29–33Google Scholar
  52. Fontenla S, Puntieri J, Ocampo JA (2001) Mycorrhizal associations in the Patagonian steppe, Argentina. Plant Soil 233:13–29Google Scholar
  53. Fraga-Beddiar A, Le Tacon F (1990) Interaction between a VA mycorrhizal fungus and Frankia associated with alder (Alnus glutinosa (L.) Gaertn.). Symbiosis 9:247–258Google Scholar
  54. Gabbarini LA, Wall LG (2008) Analysis of nodulation kinetics in Frankia—Discaria trinervis symbiosis reveals different factors involved in the nodulation process. Physiol Plant 133:776–875PubMedGoogle Scholar
  55. Gauthier D, Jaffré T, Prin Y (1999) Occurrence of both Casuarina-infective and Elaeagnus-infective Frankia strains within actinorhizae of Casuarina collina, endemic to New Caledonia. Eur J Soil Biol 35:9–15Google Scholar
  56. Gauthier D, Jaffre T, Prin Y (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 36:169–175Google Scholar
  57. Gentili F, Huss-Danell K (2002) Phosphorus modifies the effects of nitrogen on nodulation in split-root systems of Hippophaë rhamnoides. New Phytol 153:53–61Google Scholar
  58. Gentili F, Huss-Danell K (2003) Local and systemic effects of phosphorus and nitrogen on nodulation and nodule function in Alnus incana. J Exp Bot 54:2757–2767PubMedGoogle Scholar
  59. Gentili F, Wall LG, Huss-Danell K (2006) Effects of phosphorus and nitrogen on nodulation are seen already at the stage of early cortical cell divisions in Alnus incana. Ann Bot 98:309–315PubMedGoogle Scholar
  60. Gherbi H, Markman K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Péret B, Laplaze L, Franche C, Parniske M, Bogusz D (2008) SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proc Natl Acad Sci USA 105:4928–4932PubMedGoogle Scholar
  61. Ghodhbane-Gtari F, Essoussi I, Chattaoui M, Chouaia B, Jaouani A, Daffonchio D, Boudabous A, Gtari M (2010) Isolation and characterization of non-Frankia actinobacteria from root nodules of Alnus glutinosa, Casuarina glauca and Elaeagnus angustifolia. Symbiosis 50:51–57Google Scholar
  62. Gogarten JP, Townsend JP (2005) Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 3:679–687PubMedGoogle Scholar
  63. 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
  64. 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 by nifH sequence analysis. Soil Biol Biochem 39:372–377Google Scholar
  65. Gtari M, Daffonchio D, Boudabous A (2007b) Occurrence and diversity of Frankia in Tunisian soil. Physiol Plant 130:372–379Google Scholar
  66. Hahn D (2008) Polyphasic taxonomy of the genus Frankia. In: Pawloski K, Newton WE (eds) Nitrogen fixation: origins, applications, and researh progress, vol. 6. Nitrogen-fixing actinorhizal symbioses. Springer, Dordrecht, pp 25–47Google Scholar
  67. Hahn D, Starrenburg MJC, Akkermans ADL (1988) Variable compatibilitiy of cloned Alnus glutinosa ecotypes against ineffective Frankia strains. Plant Soil 107:233–243Google Scholar
  68. Hahn D, Kester R, Starrenburg MJC, Akkermans ADL (1990) Extraction of ribosomal RNA from soil for detection of Frankia with oligonucleotide probes. Arch Microbiol 154:329–335PubMedGoogle Scholar
  69. Hahn D, Zepp K, Zeyer J (1997) Whole cell hybridization as a tool to study Frankia populations in root nodules. Physiol Plant 99:696–706Google Scholar
  70. Hahn D, Nickel A, Dawson J (1999) Assessing Frankia populations in plants and soil using molecular methods. FEMS Microbiol Ecol 29:215–227Google Scholar
  71. Hilger AB, Myrold DD (1991) Method for extraction of Frankia DNA from soil. Agr Ecosyst Environ 34:107–113Google Scholar
  72. Hilger AB, Myrold DD (1992) Quantitation of soil Frankia by bioassay and gene probe methods: response to host and non-host rhizospheres and liming. Acta Ecol 13:505–506Google Scholar
  73. Hiltner L (1895) Über die Bedeutung der Wurzelknöllchen von Alnus glutinosa für die Stickstoffernährung dieser Pflanze. Landwirtschaftlichen Versuchs-Stationen 46:153-161Google Scholar
  74. Houwers A, Akkermans ADL (1981) Influence of inoculation on yield of Alnus glutinosa in the Netherlands. Plant Soil 61:189–202Google Scholar
  75. Huguet V, McCray Batzli JM, Zimpfer JF, Normand P, Dawson JO, Fernandez MP (2001) Diversity and specificity of Frankia strains in nodules of sympatric Myrica gale, Alnus incana, and Shepherdia canadensis determined by rrs gene polymorphism. Appl Environ Microbiol 67:2116–2122PubMedGoogle Scholar
  76. Huguet V, Batzli JM, Zimpfer JF, Gourbière JO, Dawson JO, Fernandez MP (2004) Nodular symbionts of Shepherdia, Alnus, and Myrica from a sand dune ecosystem: trends in occurrence of soilborne Frankia genotypes. Can J Bot 82:691–699Google Scholar
  77. Huss-Danell K (1997) Transley review No. 93. Actinorhizal symbioses and their N2 fixation. New Phytol 136:375–405Google Scholar
  78. Huss-Danell K, Bergman B (1990) Dinitrogenase in Frankia from root nodules of Alnus incana (L.) Moench: immunolocalization of the Fe- and MoFe-proteins during vesicle differentiation. New Phytol 116:443–455Google Scholar
  79. Huss-Danell K, Myrold DD (1994) Intrageneric variation in nodulation of Alnus: consequences for quantifying Frankia nodulation units in soil. Soil Biol Biochem 26:525–531Google Scholar
  80. Huss-Danell K, Uliassi D, Renberg I (1997) River and lake sediments as sources of infective Frankia (Alnus). Plant Soil 197:35–39Google Scholar
  81. Huss-Danell K, Sverrisson H, Hahlin AS, Danell K (1999) Occurrence of Alnus-infective Frankia and Trifolium infective Rhizobium in circumpolar soils. Arctic Antarct Alpine Res 31:400–406Google Scholar
  82. Jeong SC, Myrold DD (2001) Population size and diversity of Frankia in soils of Ceanothus velutinus and Douglas-fir stands. Soil Biol Biochem 33:931–941Google Scholar
  83. Kellermann J, Medan D, Aagesen L, Hilger HH (2005) Rehabilitation of the South American genus Ochetophila Poepp. ex Endl. (Rhamnaceae, Colletiae). NZ J Bot 43:865–869Google Scholar
  84. 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
  85. 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 130:315–470Google Scholar
  86. Knowlton S, Berry A, Torrey JG (1980) Evidence that associated soil bacteria may influence root hair infection of actinorhizal plants by Frankia. Can J Microbiol 26:971–977PubMedGoogle Scholar
  87. Knowlton S, Dawson JO (1983) Effects of Pseudomonas cepacia and cultural factors on the nodulation of Alnus roots by Frankia. Can J Bot 61:2877–2882Google Scholar
  88. Kohls SJ, Van Kessel C, Baker DD, Grigal D, Lawrence DB (1994) Assessment of N2 fixation and N cycling by Dryas along a chronosequence within the forelands of the Athabasca glacier, Canada. Soil Biol Biochem 26:623–632Google Scholar
  89. Laplaze L, Duhoux E, Franche C, Frutz T, Svistoonoff S, Bisseling T, Bogusz D, Pawlowski K (2000) Casuarina glauca prenodule cells display the same differentiation as the corresponding nodule cells. Mol Plant Microbe Interact 13:107–112PubMedGoogle Scholar
  90. Lechevalier MP (1983) Cataloguing Frankia strains. Can J Bot 61:2964–2967Google Scholar
  91. Lechevalier MP, Lechevalier HA (1984) Actinomycetes with multilocular sporangia. In: Williams ST, Sharpe ME, Holt JG (eds) Bergey’s manual of determinative bacteriology, vol 4, 1. William and Wilkins, Baltimore, pp 2410–2417Google Scholar
  92. 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, New York, pp 35–60Google Scholar
  93. Lie TA (1974) Environmental effects on nodulation and symbiotic nitrogen fixation. In: Quispel A (ed) The biology of nitrogen fixation frontiers of biology, vol 33. North-Holland Research Publishing Company, Amsterdam, pp 555–582Google Scholar
  94. Mansour SR, Baker DD (1994) Selection trials for effective N2-fixing Casuarina-Frankia combinations in Egypt. Soil Biol Biochem 26:655–658Google Scholar
  95. Markham JH (2005) The effect of Frankia and Paxillus involutus on the perfomance of Alnus incana subsp. rugosa in mine tailings. Can J Bot 83:1384–1390Google Scholar
  96. Markham JH, Chanway CP (1996) Alnus rubra nodulation capacity of soil under five species from harvested forest sites in coastal British Columbia. Plant Soil 178:283–286Google Scholar
  97. Martin KJ, Posvatz NJ, Myrold DD (2003) Nodulation potential of red alder stands covering a wide age range. Plant Soil 254:187–192Google Scholar
  98. Mastronunzio JE, Benson DR (2010) Wild nodules can be broken: Proteomics of Frankia in field-collected root nodules. Symbiosis 50:13–26Google Scholar
  99. Mastronunzio JE, Tisa LS, Normand P, Benson DR (2008) Comparative secretome analysis suggests low plant cell wall degrading capacity in Frankia symbionts. BMC Genomics 9:47–62PubMedGoogle Scholar
  100. 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
  101. Maunuksela L, Hahn D, Haahtela K (2000) Effect of freezing soils on nodulation capacities of total and specific Frankia populations. Symbiosis 29:107–119Google Scholar
  102. McCray Batzli J, Zimpfer JF, Huguet V, Smyth CA, Fernandez M, Dawson JO (2004) Distribution and abundance of infective, soilborne Frankia and host symbionts Shepherdia, Alnus and Myrica in a sand dune ecosystem. Can J Bot 82:700–709Google Scholar
  103. Medan D, Tortosa RD (1981) Nódulos actinomicorrícicos en especies argentinas de los géneros Kentrothamnus, Trevoa (Rhamnaceae) y Coriaria (Coriariaceae). Bol Soc Argent Bot 20:71–81Google Scholar
  104. Meesters TM (1987) Localization of nitrogenase in vesicles of Frankia sp. Cc1.17 by immunogold labelling on ultrathin cryosections. Arch Microbiol 146:327–331Google Scholar
  105. Mirza MS, Hahn D, Akkermans ADL (1992) Isolation and characterization of Frankia strains from Coriaria nepalensis. Syst Appl Microbiol 15:289–295Google Scholar
  106. Mirza MS, Hameed S, Akkermans ADL (1994) Genetic diversity of Datisca cannabina-compatible Frankia strains as determined by sequence analyses of the PCR-amplified 16S rRNA gene. Appl Environ Microbiol 62:3034–3036Google Scholar
  107. Mirza BS, Welsh A, Hahn D (2007) Saprophytic growth of inoculated Frankia sp. in soil microcosms. FEMS Microbiol Ecol 62:280–289PubMedGoogle Scholar
  108. Mirza BS, Welsh A, Rieder JP, Paschke MW, Hahn D (2009) Diversity of frankiae in soils from five continents. Syst Appl Microbiol 32:558–570PubMedGoogle Scholar
  109. Murry MA, Konopka AS, Pratt SD, Vandergon TL (1997) The use of PCR-based typing methods to asses the diversity of Frankia nodule endophytes of the actinorhizal shrub Ceanothus. Physiol Plant 99:714–721Google Scholar
  110. Myrold DD, Huss-Danell K (1994) Population dynamics of Alnus-infective Frankia in a forest soil with and without host trees. Soil Biol Biochem 26:533–540Google Scholar
  111. Myrold DD, Hilger AB, Strauss SH (1990) Detecting Frankia in soils using PCR. In: Gresshoff PM, Roth LR, Stacey G, Newton WE (eds) Nitrogen fixation: achievements and objectives. Chapman and Hall, New York, pp 429–430Google Scholar
  112. Myrold DD, Hilger AB, Huss-Danell K, Martin KJ (1994) Use of molecular methods to enumerate Frankia in soil. In: Ritz K, Dighton J, Giller KE (eds) Beyond the biomass. Wiley-Sayce, Chichester, UK, pp 127–136Google Scholar
  113. Nalin R, Normand P, Domenach AM (1997) Distribution and N2-fixing activity of Frankia strains in relation to soil depth. Physiol Plant 99:732–738Google Scholar
  114. Nalin R, Normand P, Simonet P, Domenach AM (1999) Polymerase chain reaction and hybridization on DNA extracted from soils as a tool for Frankia spp. population distribution studies in soil. Can J Bot 77:1239–1247Google Scholar
  115. Navarro E, Nanlin R, Gauthier D, Normand P (1997) The nodular microsymbionts of Gymnostoma spp. are Elaeagnus infective Frankia strains. Appl Environ Microbiol 63:1610–1616PubMedGoogle Scholar
  116. Navarro E, Rouvier C, Normand P, Domenach A-M, Simonet P, Prin Y (1998) Evolution of Frankia—Casuarinaceae interactions. Genet Select Evol 30:S357–S372Google Scholar
  117. 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
  118. Newcomb W, Pankhurst CE (1982) Ultrastructure of actinorhizal root nodules of Discaria toumatou Raoul (Rhamnaceae). NZ J Bot 20:105–113Google Scholar
  119. Newcomb W, Wood SM (1987) Morphogenesis and fine structure of Frankia (Actinomycetales): the microsymbiont of nitrogen-fixing actinorhizal nodules. Int Rev Cytol 109:1–88PubMedGoogle Scholar
  120. Niner BM, Brandt JP, Villegas M, Marshall CR, Hirsch AM, Valdés M (1996) Analysis of partial sequences of genes coding for 16S rRNA of actinomycetes isolated from Causarina equisetifolia nodules in Mexico. Appl Environ Microbiol 62:3034–3036PubMedGoogle Scholar
  121. 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 Bacteriol 46:1–9PubMedGoogle Scholar
  122. 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, Tompkins JP, Vallenet D, Valverde C, Wall LG, Wang Y, Medigue C, Benson DR (2007a) Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res 17:7–15PubMedGoogle Scholar
  123. Normand P, Queiroux C, Tisa LS, Benson DR, Rouy Z, Cruveiller S, Médigue C (2007b) Exploring the genome of Frankia. Physiol Plant 130:331–343Google Scholar
  124. 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
  125. Obertello M (2001) Simbiosis tripartita Discaria trinervis- Frankia (BCU110501)-AMF: Estudio de posibles interacciones en los mecanismos de regulación. Licenciature Thesis, University of Buenos Aires, Argentina, pp 75Google Scholar
  126. Oremus PAI (1980) Occurrence and infective potential of the endophyte of Hippophae rhamnoides L. ssp. rhamnoides in coastal sand-dune areas. Plant Soil 56:123–139Google Scholar
  127. Paschke MW (1993) Distribution and dispersal of Frankia. Ph.D. Thesis. University of Illinois at Urbana-Champaign. Illinois, USA, pp 83Google Scholar
  128. Paschke MW, Dawson JO (1992) The occurrence of Frankia in tropical forest soil of Costa Rica. Plant Soil 142:63–67Google Scholar
  129. Paschke MW, Dawson JO (1993) Avian dispersal of Frankia. Can J Bot 71:1128–1131Google Scholar
  130. Paschke MW, Dawson JO, Condon BM (1994) Frankia in prairie, forest, and cultivated soils of Central Illinois, USA. Pedobiologia 38:546–551Google Scholar
  131. Picard C, Ponsonnet C, Paget E, Nesme X, Simonet P (1992) Detection and enumeration of bacteria in soil by direct DNA extraction and polymerase chain reaction. Appl Environ Microbiol 58:2717–2722PubMedGoogle Scholar
  132. Pommer EH (1959) Beiträge zur Anatomie und Biologie der Wurzelknöllchen von Alnus glutinosa Gaertn. Flora (Jena) 143:603–634Google Scholar
  133. Pratt SD, Konopka AS, Murry MA, Ewers FW, Davis SD (1997) Influence of soil moisture on the nodulation of post-fire seedlings of Ceanothus spp. growing in the Santa Monica mountains of Southern California. Physiol Plant 99:673–679Google Scholar
  134. Probanza A, Lucas JA, Acero N, Gutierrez Mañero FJ (1996) The influence of native rhizobacteria on european alder (Alnus glutinosa (L.) Gaertn.) growth. Plant Soil 182:59–66Google Scholar
  135. Probanza A, Acero N, Ramos B, Gutierrez Mañero FJ (1997) Effects of european alder (Alnus glutinosa (L.) Gaertn) rhizobacteria on nodular metabolism and root development. Plant Growth Regul 22:145–149Google Scholar
  136. Quispel A (1954) Symbiotic nitrogen fixation in non-leguminous plants. II The influence of the inoculation density and external factors on the nodulation of Alnus glutinosa and its importance to our understanding of the mechanisms of infection. Acta Bot Neerl 3:512–532Google Scholar
  137. Quispel A (1958) Symbiotic nitrogen fixation in non-leguminous plants. IV. The influence of some environmental conditions on different phases of the nodulation process in Alnus glutinosa. Acta Bot Neerl 7:191–204Google Scholar
  138. 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, San Diego, pp 15–33Google Scholar
  139. Quispel A, Burggraaf AJP, Borsje H, Tak T (1983) The role of lipids in the growth of Frankia isolates. Can J Bot 61:2801–2806Google Scholar
  140. Quispel A, Svendsen AB, Schripsema J, Baas WJ, Erkelens C, Lugtenburg J (1989) Identification of dipterocarpol as isolation factor for the induction of primary isolation of Frankia from root nodules of Alnus glutinosa (L.) Gaertner. Mol Plant Microbe Interact 2:107–112Google Scholar
  141. Ramirez-Saad HC (1999) Molecular ecology of Frankia and other soil bacteria under natural and chlorobenzoate-stressed conditions. PhD Thesis, Wageningen Agricultural University, The Netherlands. pp 119Google Scholar
  142. Ramirez-Saad HC, Janse JD, Akkermans ADL (1988) Root nodules of Ceanothus caeruleus contain both the N2-fixing Frankia endophyte and a phylogenetically related Nod/Fix actinomycete. Can J Microbiol 44:140–148Google Scholar
  143. Reddell P, Spain AV (1991) Transmission of infective Frankia (actinomycetales) propagules in casts of the endogeic earth-worm Pontoscolex corethurus (Oligochaeta, Glossoscolecidae). Soil Biol Biochem 23:775–778Google Scholar
  144. Reddell P, Bowen GD, Robson AD (1986) Nodulation of Casuarinaceae in relation to host species and soil properties. Aust J Bot 34:435–444Google Scholar
  145. Reddell P, Diem HG, Dommergues YR (1991) Use of actinorhizal plants in arid and semiarid environments. In: Skujins J (ed) Semi-arid lands and deserts, soil resources and reclamation. Marcel Dekker Inc., New York, pp 469–485Google Scholar
  146. 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 50:255PubMedGoogle Scholar
  147. Righetti TL, Chard CH, Backkhaus RA (1986) Soil and environmental factors related to nodulation in Cowania and Purshia. Plant Soil 91:147–160Google Scholar
  148. Ringø E, Clausen E, Løvaas E, Van Ghelue M, Solheim B (1995) Effects of extracts of Alnus glutinosa seeds on growth of Frankia strain ArI3 under static and fermentor culture conditions. Plant Soil 176:283–288Google Scholar
  149. Ritchie NJ, Myrold D (1999) Geographic distribution and genetic diversity of Ceanothus -infective Frankia strains. Appl Environ Microbiol 65:1378–1383PubMedGoogle Scholar
  150. Rönkkö R, Smolander A, Nurmiaho-Lassila E-L, Haahtela K (1993) Frankia in the rhizosphere of nonhost plants: a comparison with root-associated nitrogen fixing Enterobacter, Klebsiella and Pseudomonas. Plant Soil 153:85–95Google Scholar
  151. 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
  152. Roy S, Khasa DP, Greer CW (2007) Combining alders, frankiae, and mycorrhizae for the revegetation and remediation of contamined ecosystems. Can J Bot 85:237–251Google Scholar
  153. Russo RO (1989) Evaluating alder-endophyte (Alnus-acuminata-Frankia-Mycorrhizae) interactions. Plant Soil 118:151–155Google Scholar
  154. Sayed WF (2003) Effects of land irrigation with partially-treated wastewater on Frankia survival and infectivity. Plant Soil 254:19–25Google Scholar
  155. Sayed WF, Wheeler CT (1999) Effect of the flavonoid quercetin on culture and isolation of Frankia from Casuarina root nodules. Folia Microbiol 44:59–62Google Scholar
  156. Sayed WF, Wheeler CT, Zahran HH, Shoreit AAM (1997) Effect of temperature and soil moisture on the survival and symbiotic effectiveness of Frankia spp. Biol Fertil Soils 25:349–353Google Scholar
  157. Schwintzer CR (1990) Spore-positive and spore-negative nodules. In: The biology of Frankia and actinorhizal plants. Academic Press, San Diego, pp 177-193Google Scholar
  158. Seeds JD, Bishop JG (2009) Low Frankia inoculation potentials in primary successional sites at Mount St. Helens, Washington, USA. Plant Soil 323:225–233Google Scholar
  159. Selim SH, Schwencke J (1995) Simple and reproducible nodulation test for Casurina-compatible Frankia strains: inhibition of nodulation and plant performance by some cations. Arid Soil Res Rehabil 9:25–37Google Scholar
  160. Sellstedt A, Huss Danell K (1986) Biomass production and nitrogen utilization by Alnus incana when grown on N2 or NH4+ made available at the same rate. Planta 167:387–394Google Scholar
  161. Semones SW, Young DR (1995) VAM association in the shrub Myrica cerifera on a Virginia, USA barrier island. Mycorrhiza 5:423–429Google Scholar
  162. Sempavalan BJ, Wheeler CT, Hooker JE (1995) Lack of competition between Frankia and Glomus for infection and colonization of roots of Casuarina equisetifolia (L.). New Phytol 130:429–436Google Scholar
  163. Silvester WB, Balboa O, Martinez JA (1985) Nodulation and nitrogen fixation in members of the Rhamnaceae (Colletia, Retanilla, Talguenea and Trevoa) growing in the Chilean matorral. Symbiosis 1:29–38Google Scholar
  164. Simonet P, Bosco M, Chapelon C, Moirud A, Normand P (1994) Molecular characterization of Frankia microsymbionts from spore-positive and spore-negative nodules in a natural alder stand. Appl Environ Microbiol 60:1335–1341PubMedGoogle Scholar
  165. Smolander A (1990) Frankia populations in soils under different tree species with special emphasis on soils under Betula pendula. Plant Soil 121:1–10Google Scholar
  166. Smolander A, Sundman V (1987) Frankia in acid soils devoid of actinorhizal plants. Physiol Plant 70:297–303Google Scholar
  167. Solans M (2007) Discaria trinervis-Frankia simbiosis promotion by saprophytic actinomycetes. J Basic Microbiol 47:243–250PubMedGoogle Scholar
  168. Solans M, Vobis G (2003) Actinomycetes saprofíticos asociados a la rizósfera y rizoplano de Discaria trinervis. Ecología Austral 13:97–107Google Scholar
  169. 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
  170. Tjepkema JD, Ormerod W, Torrey JG (1980) Vesicle formation and acetylene reduction activity in Frankia sp. CpI1 cultured in defined nutrient media. Nature 287:633–635Google Scholar
  171. Torrey JG (1987) Endophyte sporulation in root nodules of actinorhizal plants. Physiol Plant 70:279–288Google Scholar
  172. Tortosa RD, Cusato M (1991) Effective nodulation of rhamnaceous actinorhizal plants induced by air dried soils. Plant Soil 131:229–223Google Scholar
  173. Tortosa RD, Medan D (1989) Novedades sobre nódulos actinomicorrícicos en angiospermas sudamericanas. Rev Facultad de Agronomía, University of La Plata, La Plata, Argentina 10:79–86Google Scholar
  174. Trujillo ME, Kroppenstedt RM, Schumann P, Carro L, Martínez-Molina E (2006) Micromonospora coriariae sp. nov., isolated from root nodules of Coriaria myrtifolia. Int J Syst Evol Microbiol 56:2381–2385PubMedGoogle Scholar
  175. Valdés M (2008) Frankia ecology. In: Pawloski K, Newton WE (eds) Nitrogen fixation: origins, applications, and research progress, vol. 6. Nitrogen-Fixing Actinorhizal Symbioses. Springer, Dordrecht, pp 49–71Google Scholar
  176. Valdés M, Perez NO, Estrada de los Santos P, Caballero-Mellado J, Peña-Cabriales JJP, Normand P, Hirsch AM (2005) Non-Frankia Actinomycetes isolated from surface sterilized roots of Casuarina equisetifolia fix nitrogen. Appl Environ Microbiol 71:460–466PubMedGoogle Scholar
  177. Valdés La Hens (2007) Aislamiento y caracterización de actinomycetes simbióticos de nódulos de Alnus acuminata. PhD Thesis. University of Quilmes, Argentina, pp 312Google Scholar
  178. Valverde C, Wall LG (1999) The regulation of nodulation in Discaria trinervis (Rhamnaceae)—Frankia symbiosis. Can J Bot 77:1302–1310Google Scholar
  179. Valverde C, Ferrari A, Wall LG (2002) Phosphorus and the regulation of nodulation in the actinorhizal symbiosis between Discaria trinervis (Rhamnaceae) and Frankia BCU110501. New Phytol 153:43–52Google Scholar
  180. 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
  181. Van Dijk C (1978) Spore formation and endophyte diversity in root nodules of Alnus glutinosa (L.) Vill. New Phytol 81:601–615Google Scholar
  182. Van Dijk C (1979) Endophyte distribution in the soil. In: Gordon JC, Wheeler CT, Perry DA (eds) Proceedings workshop symbiotic nitrogen fixation in the management of temperate forests. Forest Research Laboratory, Oregon State University, Corvallis, pp 84–94Google Scholar
  183. Van Dijk C (1984) Ecological aspects of spore formation in the Frankia-Alnus symbiosis. PhD Thesis, Leiden State University, The Netherlands, pp 154Google Scholar
  184. Van Dijk C, Merkus (1976) A microscopical study of the development of a spore-like stage in the life cycle of the root nodule endophyte of Alnus glutinosa (L.) Gaertn. New Phytol 77:73–91Google Scholar
  185. Van Dijk C, Sluimer-Stolk A (1990) An ineffective strain type of Frankia in the soil of natural stands of Alnus glutinosa (L.) Gaertner. Plant Soil 127:107–121Google Scholar
  186. Van Dijk C, Sluimer A (1994) Resistance to an ineffective Frankia strain type in Alnus glutinosa (L.) Gaertn. New Phytol 128:497–504Google Scholar
  187. VanGuilder HD, Vrana KE, Freeman WM (2008) Twenty-five years of quantitative PCR for gene expression analysis. Biotechniques 44:619–626PubMedGoogle Scholar
  188. Visser S, Danielsson RM, Parkinson D (1991) Field perfomance of Elaeagnus commutata and Shepherdia canadensis (Elaeagnaceae) inoculated with soil containing Frankia and vesicular-arbuscular mycorrhizal fungi. Can J Bot 69:1321–1328Google Scholar
  189. Wall LG (2000) The actinorhizal symbiosis. J Plant Growth Regul 19:167–182PubMedGoogle Scholar
  190. Wall LG, Berry AM (2008) Early interactions, infection and nodulation in actinorhizal symbiosis. In: Pawlowski K, Newton WE (eds). Nitrogen fixation: origins, applications, and research progress, vol. 6 nitrogen-fixing actinorhizal symbioses. Springer, pp 147–166Google Scholar
  191. Wall LG, Huss-Danell K (1997) Regulation of nodulation in Alnus incana—Frankia symbiosis. Physiol Plant 99:594–600Google Scholar
  192. Wall LG, Hellsten A, Huss-Danell K (2000) Nitrogen, phosphorous, and the ratio between them affect nodulation in Alnus incana and Trifolium pratense. Symbiosis 29:91–105Google Scholar
  193. Wall LG, Valverde C, Huss-Danell K (2003) Regulation of nodulation in the absence of N2 is different in actinorhizal plants with different infection pathways. J Exp Bot 385:1253–1258Google Scholar
  194. Weber A (1986) Distribution of spore-positive and spore-negative nodules in stands of Alnus glutinosa and Alnus incana in Finland. Plant Soil 96:205–213Google Scholar
  195. Welsh A, Mirza BS, Rieder JP, Paschke M, Hahn D (2009) Diversity of frankiae in root nodules of Morella pensylvanica grown in soils from five continents. Syst Appl Microbiol 32:201–210PubMedGoogle Scholar
  196. Wijnholds AE, Young DR (2000) Interdependencies of Myrica cerifera seedlings and the nodule forming actinomycete, Frankia, in coastal environment. J Coast Res 16:139–144Google Scholar
  197. Wollum AG, Youngberg CT (1969) Effects of soil temperature on nodulation of Ceanothus velutinus Dougl. Soil Sci Soc Am J 33:801–803Google Scholar
  198. Wollum AG, Youngberg CT, Chichester FW (1968) Relation of previous timber stand age to nodulation of Ceanothus velutinus. Forest Sci 14:114–118Google Scholar
  199. Wolters DJ, Akkermans ADL, Van Dijk C (1997a) Ineffective Frankia strains in the wet stands of Alnus glutinosa L. Gaertn. in The Netherlands. Soil Biol Biochem 29:1707–1712Google Scholar
  200. Wolters DJ, Van Dijk C, Zoetendal EG, Akkermans ADL (1997b) Phylogenetic characterization of ineffective Frankia in Alnus glutinosa (L.) Gaertn. nodules from wetland soil inoculants. Mol Ecol 6:971–981PubMedGoogle Scholar
  201. Wolters DJ, Van Dijk C, Akkermans ADL, Woldendorp JW (1999) Ineffective Frankia and host resistance in natural populations of Alnus glutinosa (L.) Gaertn. Acta Ecol 20:1–79Google Scholar
  202. Woomer PL, Singleton PW, Bohlool BB (1988) Reliability of the most-probable-number technique for enumerating Rhizobia in tropical soils. Appl Environ Microbiol 54:1494–4197PubMedGoogle Scholar
  203. Young DR, Sande E, Peters G (1992) Spatial relationships of Frankia and Myrica cerifera on a Virginia, USA Barrier Island. Symbiosis 12:209–220Google Scholar
  204. Zepp K, Hahn D, Zeyer J (1997a) Evaluation of a 23S rRNA insertion as target for the analysis of uncultured Frankia populations in root nodules of alder by whole cell hybridization. Syst Appl Microbiol 20:124–132Google Scholar
  205. Zepp K, Hahn D, Zeyer J (1997b) In-situ analysis of introduced and indigenous Frankia populations in soil and root nodules obtaianed on Alnus glutinosa. Soil Biol Biochem 29:1595–1600Google Scholar
  206. Zhong C, Zhang Y, Chen Y, Jiang Q, Chen Z, Liang J, Pinyopusarerk K, Franche C, Bogusz D (2010) Casuarina research and applications in China. Symbiosis 50:107–114Google Scholar
  207. Zimpfer JC, Smyth CA, Dawson JO (1997) The capacity of Jamaican mine spoils, agricultural and forest soils to nodulate Myrica cerifera, Leucaena leucocephala and Casuarina cunninghamiana. Physiol Plant 99:664–672Google Scholar
  208. Zimpfer JF, Kennedy GJ, Smyth CA, Hamelin J, Navarro E, Dawson JO (1999) Localization of Casuarina-infective Frankia near Casuarina cunninghamiana trees in Jamaica. Can J Bot 77:1248–1256Google Scholar
  209. Zimpfer JF, McCarty E, Kaelke CM, Mulongwe L, Igual JM, Smyth CA, Dawson JO (2002) Casuarina cunninghamiana cladode extracts increase the Frankia infectious capacity of a tropical soil. Symbiosis 33:73–90Google Scholar
  210. Zimpfer JF, Kaelke CM, Smyth CA, Hahn D, Dawson JO (2003) Frankia inoculation, soil biota, and host tissue amendment influence Casuarina nodulation capacity of a tropical soil. Plant Soil 254:1–10Google Scholar
  211. Zitzer SF, Dawson JO (1992) Soil properties and actinorhizal vegetation influence nodulation of Alnus glutinosa and Elaeagnus angustifolia by Frankia. Plant Soil 140:197–204Google Scholar
  212. Zitzer SF, Archer SR, Boutton TW (1996) Spatial variability in the potential for symbiotic N2 fixation by woody plants in a subtropical savanna ecosystem. J Appl Ecol 33:1125–1136Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Eugenia E. Chaia
    • 1
  • Luis G. Wall
    • 2
  • Kerstin Huss-Danell
    • 3
  1. 1.Centro Regional Universitario BarilocheUniversidad Nacional del Comahue/INIBIOMABarilocheArgentina
  2. 2.Departamento de Ciencia y TecnologíaUniversidad Nacional de QuilmesBernalArgentina
  3. 3.Department of Agricultural Research for Northern SwedenSwedish University of Agricultural SciencesUmeåSweden

Personalised recommendations