Plant and Soil

, Volume 266, Issue 1–2, pp 205–230 | Cite as

Root-based N2-fixing symbioses: Legumes, actinorhizal plants, Parasponia sp. and cycads

  • J. Kevin Vessey
  • Katharina Pawlowski
  • Birgitta Bergman
Article

Abstract

In the mutualistic symbioses between legumes and rhizobia, actinorhizal plants and Frankia, Parasponia sp. and rhizobia, and cycads and cyanobacteria, the N2-fixing microsymbionts exist in specialized structures (nodules or cyanobacterial zones) within the roots of their host plants. Despite the phylogenetic diversity among both the hosts and the microsymbionts of these symbioses, certain developmental and physiological imperatives must be met for successful mutualisms. In this review, phylogenetic and ecological aspects of the four symbioses are first addressed, and then the symbioses are contrasted and compared in regard to infection and symbio-organ development, supply of carbon to the microsymbionts, regulation of O2 flux to the microsymbionts, and transfer of fixed-N to the hosts. Although similarities exist in the genetics, development, and functioning of the symbioses, it is evident that there is great diversity in many aspects of these root-based N2-fixing symbioses. Each symbiosis can be admired for the elegant means by which the host plant and microsymbiont integrate to form the mutualistic relationships so important to the functioning of the biosphere.

Key words

actinorhizal plants coralloid roots cyanobacteria cycads Frankia legume mutualism N2 fixation nod genes nif genes nodulation Nostoc Parasponia Rhizobium symbioses 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adams D G 2002 Cyanobacteria in symbiosis with hornworts and liverworts. In Cyanobacteria in Symbiosis, Eds. A N Rai, B Bergman and U Rasmussen. pp. 117–135. Kluwer Academic Publishers, Dordrecht.Google Scholar
  2. Ahern C P and Staff I A 1994 Symbiosis in cycads: the origin and development of corraloid roots in Macrozamia communis (Cycadaceae). Am. J. Bot. 81, 1559–1570.Google Scholar
  3. Akkermans A D L, Huss-Danell K and Roelofsen W 1981 Enzymes of the tricarboxylic acid cycle and the malate-aspartate shuttle in the N2 nitrogen-fixing endophyte of Alnus glutinosa. Physiol. Plant. 53, 289–294.Google Scholar
  4. Allaway D, Lodwig E M, Crompton L A, Wood M, Parsons R, Wheeler T R and Poole P S 2000 Identification of alanine dehydrogenase and its role in mixed secretion of ammonium and alanine by pea bacteroids. Mol. Microbiol. 36, 508–515.CrossRefPubMedGoogle Scholar
  5. Allen O N and Allen E K 1981 The Leguminosae: A Source Book of Characteristics, Uses and Nodulation. The University of Wisconsin Press, Madison. 812 pp.Google Scholar
  6. Allen G C and Elkan G H 1990 Growth, respiration, and polypeptide patterns of Bradyrhizobium sp. (Arachis) strain 3G4b20 from succinate- or oxygen-limited continuous cultures. Appl. Environ. Microbiol. 56, 1025–1032.PubMedGoogle Scholar
  7. Appleby C A, Tjepkema J D and Trinick M J 1983 Hemoglobin in a nonleguminous plant, Parasponia: possible genetic origin and function in nitrogen fixation. Science 220, 951–953.Google Scholar
  8. Baginsky C, Brito B, Imperial J, Palacios J M and Ruiz-Argueso T 2002 Diversity and evolution of hydrogenase systems in rhizobia. Appl. Environ. Microbiol. 68, 4915–4924.CrossRefPubMedGoogle Scholar
  9. Baker A, Dodd C D and Parsons R 1996 Identification of amino compounds synthesized and translocated in symbiotic Parasponia. Plant Cell Environ. 19, 1249–1260.Google Scholar
  10. Baker D D and Mullin B C 1992 Actinorhizal symbiosis. In Biological Nitrogen Fixation. Eds. G Stacey, H Evans and R Burris. pp. 259–292. Chapman and Hall, New York.Google Scholar
  11. Becana M and Klucas R V 1992 Oxidation and reduction of leghemoglobin in root nodules of leguminous plants. Plant Physiol. 98, 1217–1221.Google Scholar
  12. Becking J H 1979 Root-nodule symbiosis between Rhizobium and Parasponia parviflora (Ulmaceae). Plant Soil 51, 289–296.CrossRefGoogle Scholar
  13. Becking J H 1983a The Parasponia parviflora-Rhizobium symbiosis. Host specificity, growth and nitrogen fixation under various conditions. Plant Soil. 75, 309–342.Google Scholar
  14. Becking J H 1983b The Parasponia parviflora-Rhizobium symbiosis. Isotopic nitrogen fixation, hydrogen evolution and nitrogen-fixation, hydrogen evolution and nitrogen-fixation efficiency, and oxygen relations. Plant Soil 75, 343–360.Google Scholar
  15. Becking J H 1992 The Rhizobium symbiosis of the nonlegume Parasponia. In Biological Nitrogen Fixation: Achievements and Objectives. Eds. G. Stacey, R H Burris and H J Evans. pp. 497–559. Chapman and Hall, New York.Google Scholar
  16. Beckwith J, Tjepkema J D, Cashon R E, Schwintzer C R and Tisa L S 2002 Hemoglobin in five genetically diverse Frankia strains. Can. J. Microbiol. 48, 1048–1055.CrossRefPubMedGoogle Scholar
  17. Bender G L, Goydych W, Rolfe B G and Nayudu M 1987a The role of Rhizobium conserved and host specific nodulation genes in the infection of the non-legume Parasponia andersonii. Mol. Gen. Gen. 210, 299–306.Google Scholar
  18. Bender G L, Nayudu M, Goydych W and Rolfe B G 1987b Early infection events in nodulation of the non-legume Parasponia andersonii by Bradyrhizobium. Plant Sci. 51, 285–293.CrossRefGoogle Scholar
  19. Benoit L F and Berry A M 1990 Methods for production and use of actinorhizal plants in forestry, low maintenance landscapes and revegetation. In The Biology of Frankia and Actinorhizal Plants. Eds. C R Schwintzer and J D Tjepkema. pp. 281–297. Academic Press, New York.Google Scholar
  20. Benson D R, Arp D J and Burris R H 1980 Hydrogenase in actinorhizal root nodules and root nodule homgenates. J. Bacteriol. 142, 138–144.PubMedGoogle Scholar
  21. Benson D R and Hanna D 1983 Frankia diversity in an alder stand as estimated by sodium dodecyl sulfate-polyacrylamide gel electrophoresis of whole-cell proteins [Nitrogen-fixing symbiosis with actinomycetes]. Can. J. Bot. 61, 2919–2923.Google Scholar
  22. Benson D R and Silvester W B 1993 Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol. Rev. 57, 293–319.PubMedGoogle Scholar
  23. Berg R H 1999 Frankia forms infection threads. Can. J. Bot. 77, 1327–1333.Google Scholar
  24. Berg R H and McDowell L 1987a Endophyte differentiation in Casuarina actinorhizae. Protoplasma 136, 104–117.CrossRefGoogle Scholar
  25. Berg R H and McDowell L 1987b Cytochemistry of the wall of infected cells in Casuarina actinorhizae. Can. J. Bot. 66, 2038–2047.Google Scholar
  26. Berger D and Altmann T 2000 A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana. Genes Dev. 14, 1119–1131.PubMedGoogle Scholar
  27. Bergersen F J 1996 Delivery of O2 to bacteroids in soybean nodule cells: Consideration of gradients of concentration of free, dissolved O2 in a near symbiosomes and beneath intercellular spaces. Protoplasma 191, 9–20.CrossRefGoogle Scholar
  28. Bergman B 2002 The Nostoc-Gunnera symbiosis. In Cyanobacteria in Symbiosis. Eds. A N Rai, B Bergman and U Rasmussen. pp. 207–232. Kluwer Academic Publishers, Dordrecht.Google Scholar
  29. Bergman B, Lindblad P and Rai A N 1986 Nitrogenase in free-living and symbiotic cyanobacteria: immunoelectron microscopic localization. FEMS Microbiol. Lett. 35, 75–78.CrossRefGoogle Scholar
  30. Bergman B, Matveyev A and Rasmussen U 1996 Chemical signalling in cyanobacterial-plant symbioses. Trends Plant Sci. 1, 191–197.CrossRefGoogle Scholar
  31. Bergman B, Rasmussen U and Rai A N 2004 Cyanobacterial Associations. In Associative Nitrogen-fixing Bacteria and Cyanobacterial Associations. Eds. C Elmerich and W E Newton. 41 pp. Kluwer Academic Publishers (in press).Google Scholar
  32. Berry A M, Harriott O T, Moreau R A, Osman S F, Benson D R and Jones A D 1993 Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc. Natl. Acad. Sci., USA 90, 6091–6094.PubMedGoogle Scholar
  33. Berry A M, Murphy T M, Okubara P A, Jacobsen K R, Swensen S M and Pawlowski K 2004 Novel expression pattern of cytosolic glutamine synthetase in nitrogen-fixing root nodules of the actinorhizal host, Datisca glomerata. Plant Physiol. (in review).Google Scholar
  34. Berry A M and Torrey J G 1983 Root hair deformation in the infection process of Alnus rubra [Actinomycete Frankia]. Can. J. Bot. 61, 2863–2876.Google Scholar
  35. Bogusz D, Llewellyn D J, Craig S, Dennis E S, Appleby C A and Peacock W J 1988 Nonlegume hemoglobin genes retain organ-specific expression in heterologous transgenic plants. Plant Cell 2, 633–641.Google Scholar
  36. Bond G 1952 Some features of the root growth in nodulated plants of Myrica gale L. Ann. Bot. 16, 467–475.Google Scholar
  37. Brenner E D, Stevenson D W and Twigg R W 2003 Cycads: Evolutionary innovations and the role of plant-derived neurotoxins. Trends Plant Sci. 8, 446–452CrossRefPubMedGoogle Scholar
  38. Bromfield E S P, Butler G and Barran L R 2001 Temporal effects on the composition of a population of Sinorhizobium meliloti associated with Medicago sativa and Melilotus alba. Can. J. Microbiol. 47, 567–573.CrossRefPubMedGoogle Scholar
  39. Brown P H and Hu H 1996 Phloem mobility of boron is species dependent: evidence for phloem mobility in sorbitol-rich species. Ann. Bot. 77, 497–505.Google Scholar
  40. Buikema W J and Haselkorn R 1993 Molecular genetics of cyanobacterial development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44, 33–52.CrossRefGoogle Scholar
  41. Burgess D and Peterson R L 1987 Development of Alnus japonica root nodules after inoculation with Frankia strain HFPArI3. Can. J. Bot. 65, 1647–1657.Google Scholar
  42. Burris R H 1991 Nitrogenases. J. Biol. Chem. 266, 9339–9342.PubMedGoogle Scholar
  43. Callaham D, Newcomb W, Torrey J G and Peterson R L 1979 Root hair infection in actinomycete-induced root nodule initiation in Casuarina cunninghamiana Myrica gale, Myrica cerifera and Comptonia peregrina. Bot. Gaz. 140, S1-S9.CrossRefGoogle Scholar
  44. Callaham D and Torrey J G 1977 Prenodule formation and primary nodule development in roots of Comptonia (Myricaceae). Can. J. Bot. 55, 2306–2318.Google Scholar
  45. Cérémonie H, Debelle F and Fernandez M P 1999 Structural and functional comparison of Frankia root hair deforming factor and rhizobia Nod factor. Can. J. Bot. 77, 1293–1301.CrossRefGoogle Scholar
  46. Chaudhuri H and Akhtar A R 1931 The coral-like roots of Cycas revoluta, Cycas circinalis and Zamia floridana and the alga inhabiting them. J. Ind. Bot. Soc. 10, 43–59Google Scholar
  47. Colebatch G, Kloska S, Trevaskis B, Freund S, Altmann T and Udvardi M K 2002a Novel aspects of symbiotic nitrogen fixation uncovered by transcript profiling with cDNA arrays. Mol. Plant-Microbe Interact. 15, 411–420.PubMedGoogle Scholar
  48. Colebatch G, Trevaskis B and Udvardi M 2002b Symbiotic nitrogen fixation research in the postgenomics era. New Phytol. 153, 37–42.Google Scholar
  49. Costa J-L and Lindblad P 2002 Cyanobacteria in symbiosis with cycads. In Cyanobacteria in Symbiosis, Eds. A N Rai, B Bergman and U Rasmussen. pp. 195–202. Kluwer Academic Publishers, Dordrecht.Google Scholar
  50. Christensen T, Dennis E S, Peacock J W, Landsmann J and Marcker K A 1991 Hemoglobin genes in non-legumes: cloning and characterization of a Casuarina glauca hemoglobin gene. Plant Mol. Biol. 16, 339–344.CrossRefPubMedGoogle Scholar
  51. Clawson M L and Benson D R 1999. Natural diversity of Frankia strains in actinorhizal root nodules from promiscuous hosts in the family Myricaceae. Appl. Environ. Microbiol. 65, 4521–4527.PubMedGoogle Scholar
  52. Cohen M F and Meeks J C 1997 A hormogonium regulating locus, hrmUA, of the cyanobacterium Nostoc punctiforme strain ATCC 29133 and its response to an extract of a symbiotic plant partner Anthoceros punctatus. Mol. Plant-Microbe Interact. 10, 280–289.PubMedGoogle Scholar
  53. Cullimore J V and Bennett M J 1992 Nitrogen assimilation in the legume root nodule: current status of the molecular biology of the plant enzymes. Can. J. Microbiol. 38, 461–466.Google Scholar
  54. Cvitanich C, Pallisgaard N, Nielsen K A, Hansen A C, Larsen K, Pihakaski-Maunsbach K, Marcker K A and Jensen E O 2000 CPP1, a DNA-binding protein involved in the expression of a soybean leghemoglobin c3 gene. Proc. Natl. Acad. Sci., USA 97, 8163–8168.CrossRefPubMedGoogle Scholar
  55. Day D A, Poole P S, Tyerman S D and Rosendahl L 2001 Ammonia and amino acid transport across symbiotic membranes in nitrogen-fixing legume nodules. Cell. Mol. Life Sci. 58, 61–71.PubMedGoogle Scholar
  56. Day A A and Udvardi M K 1993 Metabolite exchange across symbiosome membranes. Symbiosis 14, 175–189.Google Scholar
  57. Denison R F 1992 Mathematical modeling of oxygen diffusion and respiration in legume root nodules. Plant Physiol. 98, 901–907.Google Scholar
  58. Denison R F 2000 Legume sanctions and the evolution of symbiotic cooperation by rhizobia. Am. Nat. 156, 567–576.CrossRefGoogle Scholar
  59. Denison R F and Okano Y 2003 Leghaemoglobin oxygenation gradients in alfalfa and yellow sweetclover nodules. J. Exp. Bot. 54, 1085–1091.CrossRefPubMedGoogle Scholar
  60. Diem H G and Dommergues Y R 1990. Current and potential uses and management of Casuarinaceae in the tropics and subtropics. In The Biology of Frankia and Actinorhizal Plants. Eds. C R Schwintzer and J D Tjepkema. pp. 317–342. Academic Press, New York.Google Scholar
  61. Dommergues Y R 1995 Nitrogen fixation by trees in relation to soil nitrogen economy. Fertil. Res. 42, 215–230.CrossRefGoogle Scholar
  62. Doyle J J 1998 Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria. Trends Plant Sci. 3, 473–478.CrossRefGoogle Scholar
  63. Franche C, Laplaze L, Duhoux E and Bogusz D 1998 Actinorhizal symbioses: Recent advances in plant molecular and genetic transformation Studies. Crit. Rev. Plant Sci. 17, 1–28.Google Scholar
  64. Galibert F, Finan T M, Long S R, Puhler A, Abola P, Ampe F, Barloy-Hubler F, Barnett M J, Becker A, Boistard P, Bothe G, Boutry M, Bowser L, Buhrmester J, Cadieu E, Capela D, Chain P, Cowie A, Davis R W, Dreano S, Federspiel N A, Fisher R F, Gloux S, Godrie T, Goffeau A, Golding B, Gouzy J, Gurjal M, Hernandez-Lucas I, Hong A, Huizar L, Hyman R W, Jones T, Kahn D, Kahn M L, Kalman S, Keating D H, Kiss E, Komp C, Lalaure V, Masuy D, Palm C, Peck M C, Pohl T M, Portetelle D, Purnelle B, Ramsperger U, Surzycki R, Thebault P, Vandenbol M, Vorholter F J, Weidner S, Wells D H, Wong K, Yeh K C and Batut J 2001 The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293, 668–672.PubMedGoogle Scholar
  65. Gallon J R 1992 Tansley Review No. 44: Reconciling the incompatible: N2 fixation and O2. New Phytol. 122, 571–609.Google Scholar
  66. Gallon J R 2001 N2 fixation in phototrophs: Adaptation to a specialized way of life. Plant Soil 230, 39–48.CrossRefGoogle Scholar
  67. Gantar M and Elhai J 1999 Colonization of wheat para-nodules by the N2-fixing cyanobacterium Nostoc sp. strain 2S9B. New Phytol. 141, 373–379.CrossRefGoogle Scholar
  68. Gauthier D, Jaffre T and 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, 169–175.CrossRefGoogle Scholar
  69. Gherbi H, Duhoux E, Franche C, Pawlowski K, Berry A M and Bogusz D 1997 Cloning of a full-length symbiotic hemoglobin cDNA and in situ localization of the corresponding mRNA in Casuarina glauca root nodule. Physiol. Plant. 99, 608–616.CrossRefGoogle Scholar
  70. Grobbelaar N, Hattingh W and Marshall J 19876 The occurrence of coralloid roots on the South African species of the Cycadales and their ability to fix nitrogen symbiotically. S. Afr. J. Bot. 52, 467–471.Google Scholar
  71. Grobbelaar N, Scott W E, Hattingh W and Marshall J 1987 The identification of the coralloid root endophytes of the southern African cycads and the ability of the isolates to fix dinitrogen. S. Afr. J. Bot. 53, 111–118.Google Scholar
  72. Grove T S, O’Connell A M and Malajczuk N 1980 Effects of fire on the growth, nutrient content and rate of nitrogen fixation on the cycad Macrozamia riedlei. Aust. J. Botany 28, 271–281.Google Scholar
  73. Gualtieri G and Bisseling T 2000 The evolution of nodulation. Plant Mol. Biol. 42, 181–194.CrossRefPubMedGoogle Scholar
  74. Guan C H, Ribeiro A, Akkermans A D L, Jing Y X, van Kammen, Bisseling T and Pawlowski K 1996 Nitrogen metabolism in actinorhizal nodules of Alnus glutinosa: Expression of glutamine synthetase and acetylornithine transaminase. Plant Mol. Biol. 32, 1177–1184.CrossRefPubMedGoogle Scholar
  75. Guinel F C and Geil R D 2002 A model for the development of the rhizobial and arbuscular mycorrhizal symbioses in legume and its use to understand the roles of ethylene in the establishment of these two symbioses. Can. J. Bot. 80, 695–720.CrossRefGoogle Scholar
  76. Hafeez F, Akkermans A D L and Chaudhary A H 1984 Observations on the ultrastructure of Frankia sp. in root nodules of Datisca cannabina L. Plant Soil 79, 383–402.CrossRefGoogle Scholar
  77. Halliday J and Pate J S 1976 Symbiotic nitrogen fixation by coralloid roots of the cycad Macrozamia riedlei: physiological characteristics and ecological significance. Aust. J. Plant Physiol. 3, 349–358.Google Scholar
  78. Haselkorn R, Schlictman D, Jones K and Buikema W J 1997 Heterocyst differentiation and nitrogen fixation in cyanobacteria. In Biological Nitrogen Fixation for the 21st Century. Eds. C Elmerich, A Kondorosi and W E Newton. pp. 93–96. Kluwer, Dordrecht.Google Scholar
  79. Heidstra R, Nilsen G, Martinez-Abarca F, van Kammen A and Bisseling T 1997 Nod factor-induced expression of leghemoglobin to study the mechanism of NH4NO3 inhibition on root hair deformation. Mol. Plant-Microbe Interact. 10, 215–220.PubMedGoogle Scholar
  80. Hirsch A M, Fang Y, Asad S and Kapulnik Y 1997 The role of phytohormones in plant-microbe symbioses. Plant Soil 194, 171–184.CrossRefGoogle Scholar
  81. Hughes M, Donnelly C, Crozier A and Wheeler C T 1999 Effects of the exposure of roots of Alnus glutinosa to light on flavonoids and nodulation. Can. J. Bot. 77, 1311–1315.CrossRefGoogle Scholar
  82. Hunt S and Layzell D B 1993 Gas exchange of legume nodules and the regulation of nitrogenase activity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44, 483–511.CrossRefGoogle Scholar
  83. Hunt P W, Klok E J, Trevaskis B, Watts R A, Ellis M H, Peacock W J and Dennis E S 2002 Increased level of hemoglobin 1 enhances survival of hypoxic stress and promotes early growth in Arabidopsis thaliana. Proc. Natl. Acad. Sci., USA 99, 17197–17202.PubMedGoogle Scholar
  84. Hunt P W, Watts R A, Trevaskis B, Llewelyn D J, Burnell J, Dennis E S and Peacock W J 2001 Expression and evolution of functionally distinct haemoglobin genes in plants. Plant Mol. Biol. 47, 677–692.CrossRefPubMedGoogle Scholar
  85. Huss-Danell K 1990 The physiology of actinorhizal nodules. In The Biology of Frankia and Actinorhizal Plants. Eds. C R Schwintzer and J D Tjepkema. pp. 129–156. Academic Press, New York.Google Scholar
  86. Huss-Danell K 1997 Tansley Review No. 93. Actinorhizal symbioses and their N2 fixation. New Phytol. 136, 375–405.CrossRefGoogle Scholar
  87. Huss-Danell K and Bergman B 1990 Nitrogenase in Frankia from root nodules of Alnus incana (L.) Moench: immunolocalization of the Fe- and MoFe-proteins during vesicle differentiation. New Phytol. 116, 443–455.Google Scholar
  88. Jacobson-Lyon K, Jensen E O, Jorgensen J E, Marcker K A, Peacock W J and Dennis E S 1995 Symbiotic and nonsymbiotic hemoglobulin genes of Casuarina glauca. Plant Cell 7, 213–223.Google Scholar
  89. James E K, Iannetta P P M, Naisbitt T, Goi S R, Sutherland J M, Sprent J I, Minchin F R and Brewin N J 1994 A survey of N2-fixing nodules in the Leguminosae with particular reference to intercellular glycoprotein in the control of oxygen diffusion. Proc. Royal Soc. Edinburgh 102B, 429–432.Google Scholar
  90. James E K, Iannetta P P M, Deeks L, Sprent J I and Minchin F R 2000 Detopping causes production of intercellular space occlusions in both the cortex and infected region of soybean nodules. Plant Cell Environ. 23, 377–386.CrossRefGoogle Scholar
  91. Johansson C and Bergman B 1992 Early events during the establishment of the Gunnera/Nostoc symbiosis. Planta 188, 403–413.CrossRefGoogle Scholar
  92. John T R, Wiggington J, Bock J V, Klemt R and Johnson J D 2003 An insertion sequence unique to Frankia strain ArI5. Plant Soil 254, 107–113.CrossRefGoogle Scholar
  93. Kaneko T, Nakamura Y, Sato S, Asamizu E, Kato T, Sasamoto S, Watanabe A, Idesawa K, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Mochizuki Y, Nakayama S, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M and Tabata S 2000 Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res. 7, 331–338.PubMedGoogle Scholar
  94. Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T, Sasamoto S, Watanabe A, Idesawa K, Iriguchi M, Kawashima K, Kohara M, Matsumoto M, Shimpo S, Tsuruoka H, Wada T, Yamada M, Tabata S 2002 Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res. 9, 189–197.PubMedGoogle Scholar
  95. Kapranov P, Routt S M, Bankaitis V A, de Bruijn F J and Szczyglowski K 2001 Nodule-specific regulation of phosphatidylinositol transfer protein expression in Lotus japonicus. Plant Cell 13, 1369–1382.CrossRefPubMedGoogle Scholar
  96. Karr D B, Oehrle N W and Emerich D W 2003 Recovery of nitrogenase from aerobically isolated soybean nodule bacteroids. Plant Soil 257, 27–33.CrossRefGoogle Scholar
  97. Kelner D J, Vessey J K and Entz M H 1997 The nitrogen dynamics of one, two and three year stands of alfalfa in a cropping system. Agric. Ecosyst. Environ. 64, 1–10.Google Scholar
  98. Klint J, Ran R, Rasmussen, U and Bergman B 2003 Proteomics of the symbiotic cyanobacterium Nostoc punctiforme: identification of developmentally regulated proteins in hormogonia. Mol. Plant-Microbe Interact. (submitted)Google Scholar
  99. Knight C D and Adams D G 1996 A method for studying chemotaxis in nitrogen-fixing cyano-bacterium-plant symbioses. Physiol. Mol. Plant Pathol. 49, 73–77.CrossRefGoogle Scholar
  100. Knowlton S, Berry A and Torrey J G 1980 Evidence that associated soil bacteria may influence root hair infection of actinorhizal plants by Frankia. Can. J. Microbiol. 26, 971–977.PubMedGoogle Scholar
  101. Kuzma M M and Layzell D B 1994 Acclimation of soybean nodules to changes in temperature. Plant Physiol. 106, 263–270.PubMedGoogle Scholar
  102. Lancelle S A and Torrey J G 1984 Early development of Rhizobiuminduced root nodules of Parasponia rigida. I. Infection and early nodule initiation. Protoplasma 123, 26–37.CrossRefGoogle Scholar
  103. Lancelle S A and Torrey J G 1985 Early development of Rhizobiuminduced root nodules of Parasponia rigida. II. Nodule morphogenesis and symbiotic development. Can. J. Bot. 63, 25–35.Google Scholar
  104. Lavire C and Cournoyer B 2003 Progress on the genetics of the N2-fixing actinorhizal symbiont Frankia. Plant Soil 254, 125–137.CrossRefGoogle Scholar
  105. Lavire C, Louis D, Perriere G, Briolay J, Normand P and Cournoyer B 2001 Analysis of pFQ31, a 8551-bp cryptic plasmid from the symbiotic nitrogen-fixing actinomycete Frankia. FEMS Microbiol. Lett. 197, 111–116.PubMedGoogle Scholar
  106. Layzell D B 1990 N2 fixation, NO3 reduction and NH4+ assimilation. In Plant Physiology, Biochemistry and Molecular Biology. Eds. D T Dennis and D H Turpin. pp. 389–406. Longman Group, Essex.Google Scholar
  107. Lee H, Sung S B, Kim H B and An C S 2001 Sequence analysis and expression patterns of two nifA genes from Frankia EuIK1. Austral. J. Plant Physiol. 28, 939–949.Google Scholar
  108. Lhuissier F G P, De Ruijter N C A, Sieberer B J, Esseling J J, Emons A M C 2001 Time course of cell biological events evoked in legume root hairs by Rhizobium Nod factors: State of the art. Ann. Bot. 87, 289–302.CrossRefGoogle Scholar
  109. Li Y Z, Parsons R, Day D A and Bergersen F J 2002 Reassessment of major products of N2 fixation by bacteroids from soybean root nodules. Microbiology-SGM 148, 1959–1966.Google Scholar
  110. Lindblad P 1992 Ornithine cycle in Nostoc PCC 73102. Occurrence and localization of ornithine carbamoyl transferase and the effect of external carbon and ornithine on nitrogenase activity and citrulline synthesis. Protoplasma 152, 87–95.Google Scholar
  111. Lindblad P, Atkins C A and Pate J S 1991 N2 fixation by freshly isolated Nostoc from coralloid roots of the cycad Macrozamia riedlei (Fisch. ex Gaud.) Gardn. Plant Physiol. 95, 753–759.Google Scholar
  112. Lindblad P and Bergman B 1986 Glutamine synthetases: activity and localization in cyanobacteria of the cycads Cycas revoluta and Zamia skinneri. Planta 169, 1–7.CrossRefGoogle Scholar
  113. Lindblad P and Bergman B 1990 The cycad-cyanobacterial symbiosis. In Handbook of Symbiotic Cyanobacteria. Ed. A N Rai. pp. 137–159. CRC Press, Boca Raton.Google Scholar
  114. Lindbald P, Bergman B, Hofsten A, Hällblom L and Nylund J-E 1985a The cyanobacterium-Zamia symbiosis: an ultrastructural study. New Phytol. 101, 707–716.Google Scholar
  115. Lindblad P, Hällblom L and Lindblad P 1985b The cyanobacterium-Zamia symbiosis: C2H2 reduction and heterocyst frequency. Symbiosis 1, 19–28.Google Scholar
  116. Liu Q and Berry A M 1991 The infection process and nodule initiation in the Frankia-Ceanothus root nodule symbiosis: A structural and histochemical study. Protoplasma 163, 82–92.Google Scholar
  117. Lodwig E and Poole P 2003 Metabolism of Rhizobium bacteroids. Crit. Rev. Plant Sci. 22, 37–78.Google Scholar
  118. Lopez M F, Fontaine M S and Torrey J G 1984 Levels of trehalose and glycogen in Frankia sp. HFPArI3 (Actinomycetales) [Nitrogen-fixing bacteria]. Can. J. Microbiol. 30, 746–752.Google Scholar
  119. Lopez M F, Young P and Torrey J G 1986 A comparison of carbon source utilization for growth and nitrogenase activity in two Frankia isolates. Can. J. Microbiol. 32, 353–358.Google Scholar
  120. Madsen E B, Madsen L H, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N and Stougaard J 2003 A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425, 637–640.CrossRefPubMedGoogle Scholar
  121. Marie C, Deakin W J, Viprey V, Kopcinska J, Golinowski W, Krishnan H B, Perret X and Broughton W J 2003 Characterization of Nops, nodulation outer proteins, secreted via the type III secretion system of NGR234. Mol. Plant-Microbe Interact. 16, 743–751.PubMedGoogle Scholar
  122. Mariotti A, Sougoufara B and Dommergues Y R 1992. Estimation of nitrogen fixation using the natural abundance method in a plantation of Casuarina equisetifolia (Forst). Soil Biol. Biochem. 24, 647–653.CrossRefGoogle Scholar
  123. Martel A, Jansson E, Garcia-Reina G and Lindblad P 1993 Ornithine cycle in Nostoc 73102. Arginase, OCT and arginine deaminase, and the effects of addition of external srginine, ornithine and citrulline. Arch. Microbiol. 59, 506–511.Google Scholar
  124. Martinez-Romero E 2003 Diversity of Rhizobium-Phaseolus vulgaris symbiosis: Overview and perspectives. Plant Soil 252, 11–23.Google Scholar
  125. Marvel D J, Torrey J G and Ausubel F M 1987 Rhizobium symbiotic genes required for nodulation of legume and nonlegume hosts. Proc. Natl. Acad. Sci., USA 84, 1319–1323.Google Scholar
  126. Mattsson U, Johansson L, Sandström G and Sellstedt A 2001 Frankia KB5 possesses a hydrogenase immunologically related to membrane-bound [NiFe]-hydrogenases. Curr. Microbiol. 42, 438–441.CrossRefPubMedGoogle Scholar
  127. Mattsson U and Sellstedt A 2002 Nickel affects activity more than expression of hydrogenase protein in Frankia. Curr. Microbiol. 44, 88–93.CrossRefPubMedGoogle Scholar
  128. McClure P R, Coker III G T and Schubert K R 1983 Carbon dioxide fixation in roots and nodules of Alnus glutinosa. Plant Physiol. 71, 652–657.Google Scholar
  129. McEwan N R, Green D C and Wheeler C T 1992 Utilisation of the root hair curling reaction in Alnus glutinosa for the assay of nodulation signal compounds. Acta Oecologica 13, 509–510.Google Scholar
  130. Meeks J C, Campbell E, Hagen K, Hanson T, Hitzeman N and Wong F 1999 Developmental alternatives of symbiotic Nostoc punctiforme in response to its symbiotic partner Anthoceros punctatus. In The Phototrophic Prokaryotes, Eds. G A Peschek, W Löffelhardt and G Schmetterer. pp. 665–678, Kluwer Academic Publisher, New York.Google Scholar
  131. Meesters T M 1987 Localization of nitrogenase in vesicles of Frankia sp. Cc1.17 by immunogoldlabelling on ultrathin cryosections. Arch. Microbiol. 146, 327–331CrossRefGoogle Scholar
  132. Miklashevichs E, Rohrig H, Schell J and Schmidt J 2001 Perception and signal transduction of rhizobial NOD factors. Crit. Rev. Plant Sci. 20, 373–394.Google Scholar
  133. Miller I M and Baker D D 1985 The initiation, development and structure of root nodules in Elaeagnus angustifolia L. (Elaeagnaceae). Protoplasma 128, 107–119.CrossRefGoogle Scholar
  134. Miller I M and Baker D D 1986 Nodulation of actinorhizal plants by Frankia strains capable of both root hair infection and intercellular penetration. Protoplasma 131, 82–91.CrossRefGoogle Scholar
  135. Mohapatra S S and Gresshoff P M 1984 Carbon-nitrogen requirements for the expression of nitrogenase activity in cultured Parasponia-Rhizobium strain ANU 289 [Nitrogen-fixing bacteria]. Arch. Microbiol. 137, 58–62.CrossRefGoogle Scholar
  136. Newcomb W and Pankhurst C E 1982 Fine structure of actinorhizal nodules of Coriaria arborea (Coriariaceae). New Zealand J. Bot. 20, 93–103.Google Scholar
  137. Nilsson M, Bhattacharya J, Rai A N and Bergman B 2002 Colonization of roots of rice (Oryza sativa) by symbiotic Nostoc strains. New Phytol. 156, 517–525.CrossRefGoogle Scholar
  138. Obukowicz M, Schaller M and Kennedy G S 1981 Ultrastructure and phenolic histochemistry of the Cycas revoluta-Anabaena symbiosis. New Phytol. 87, 751–759.Google Scholar
  139. Oh C J, Kim H B and An C S 2003 Molecular cloning and complementation analysis of nifV gene from Frankia EuIK1 strain. Mol. Cells 15, 27–33.PubMedGoogle Scholar
  140. Oke V and Long S R 1999 Bacteroid formation in the Rhizobium-legume symbiosis. Curr. Opin. Microbiol. 2, 641–646.CrossRefPubMedGoogle Scholar
  141. Okubara P A, Fujishige N A, Hirsch A M and Berry A M 2000 Dg93, a nodule-abundant mRNA of Datisca glomerata with homology to a soybean early nodulin. Plant Physiol. 122, 1073–1079.CrossRefPubMedGoogle Scholar
  142. Ow M C, Gantar M and Elhai J 1999 Reconstitution of a cycadcyanobacterial association. Symbiosis 27, 125–134.Google Scholar
  143. Pandya S, Iyer P, Gaitonde V, Parekh T and Desai A 1999 Chemotaxis of rhizobium SP.S2 towards Cajanus cajan root exudate and its major components. Curr. Microbiol. 38, 205–209.PubMedGoogle Scholar
  144. Parker M A, Lafay B, Burdon J J and van Berkum P 2002 Conflicting phylogeographic patterns in rRNA and nifD indicate regionally restricted gene transfer in Bradyrhizobium. Microbiology-SGM 148, 2557–2565.Google Scholar
  145. Parsons R, Silvester W B, Harris S, Gruijters W T M and Bullivant S 1987 Frankia vesicles provide inducible and absolute oxygen protection for nitrogenase. Plant Physiol. 83, 728–731.Google Scholar
  146. Parsons R and Sunley R J 2001 Nitrogen nutrition and the role of root-shoot nitrogen signalling particularly in symbiotic systems. J. Exp. Bot. 52, 435–443.PubMedGoogle Scholar
  147. Pate J S, Lindblad P, and Atkins C A 1988 Pathways of assimilation and transfer of the fixed nitrogen in coralloid roots of cycad-Nostoc symbioses. Planta 176, 461–471.CrossRefGoogle Scholar
  148. Pate J S 1989 Synthesis, transport, and utilization of products of symbiotic nitrogen fixation. Recent Adv. Phytochem. 23, 65–115.Google Scholar
  149. Pathirana S M and Tjepkema J D 1995 Purification of hemoglobin from the actinorhizal root nodules of Myrica gale L. Plant Physiol. 107, 827–831.PubMedGoogle Scholar
  150. Pawlowski K, Swensen S, Guan C H, Hadri A E, Berry A M and Bisseling T 2003 Distinct patterns of symbiosis-related gene expression in actinorhizal nodules from different plant families. Mol. Plant-Microbe Interact. 16, 796–807.PubMedGoogle Scholar
  151. Pawlowski K, Twigg P, Dobritsa S, Guan C and Mullin B C 1997 A nodule-specific gene family from Alnus glutinosa encodes glycine- and histidine-rich proteins expressed in the early stages of actinorhizal nodule development. Mol. Plant-Microbe Interact. 10, 656–664.PubMedGoogle Scholar
  152. Peoples M B, Giller K E, Herridge D F and Vessey J K 2002 Limitations to biological nitrogen fixation as a renewable source of nitrogen for agriculture. In Nitrogen Fixation - Global Perspectives. Eds. T M Finan, M R O’Brian, D B Layzell, J K Vessey and W Newton. pp. 356–360. CABI Publishing, New York.Google Scholar
  153. Phillips D A, Wery J, Joseph C M, Jones A D and Teuber L R 1995 Release of flavonoids and betaines from seeds of seven Medicago species. Crop Sci. 35, 805–808.Google Scholar
  154. Plazinski J, Croft L, Taylor R, Zheng Q, Rolfe B G and Gunning B E S 1991 Indigenous plasmids in Anabaena azollae: their taxonomic distribution and existense of regions of homology of symbiotic genes of Rhizobium. Can. J. Microbiol. 37, 171–181.Google Scholar
  155. Poza-Carrion C, Fernandez-Valiente E, Pinas F F and Leganes F 2001 Acclimation of photosynthetic pigments and photosynthesis of the cyanobacterium Nostoc sp strain UAM 206 to combined fluctuations of irradiance, pH, and inorganic carbon availability J. Plant Physiol. 158, 1455–1461.Google Scholar
  156. Price G D, Mohapatra S S and Gresshoff P M 1984 Structure of nodules formed by Rhizobium strain ANU289 in the nonlegume Parasponia and the legume Siratro (Macroptilium atropurpureum). Bot. Gaz. 145, 444–451.Google Scholar
  157. Price N P J 1999 Carbohydrate determinants of Rhizobium-legume symbioses. Carbohydr. Res. 317, 1–9.CrossRefPubMedGoogle Scholar
  158. Qian J H, Kwon S W and Parker M A 2003 rRNA and nifD phylogeny of Bradyrhizobium from sites across the Pacific Basin. FEMS Microbiol. Lett. 219, 159–165.CrossRefPubMedGoogle Scholar
  159. Racette S and Torrey J G 1989 Root nodule initiation in Gymnostoma (Casuarinaceae) and Shepherdia (Elaeagnaceae) induced by Frankia strain HFPGpI1. Can. J. Bot. 67, 2873–2879.Google Scholar
  160. Radutoiu S, Madsen L H, Madsen E B, Felle H H, Umehara Y, Gronlund M, Sato S, Nakamura Y, Tabata S, Sandal N and Stougaard J 2003 Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585–592.CrossRefPubMedGoogle Scholar
  161. Rai A N, Bergman B and Rasmussen U 2002 Cyanobacteria in Symbiosis. Kluwer Academic Publishers, Dordrecht. 368 pp.Google Scholar
  162. Rai A N, Söderbäck E and Bergman B 2000 Tansley Review No. 116: Cyanobacterium-plant symbioses. New Phytol. 147, 449–481.CrossRefGoogle Scholar
  163. Ramirez-Saad H, Janse J D and Akkermans A D L 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.Google Scholar
  164. Rasmussen U, Johansson C, Renglin A, Pettersson C and Bergman B 1996 A molecular characterization of the Gunnera-Nostoc symbiosis: Comparison with Rhizobium- and Agrobacterium-plant interactions. New Phytol. 133, 391–398.Google Scholar
  165. Rasmussen U and Nilsson M 2002 Cyanobacterial diversity and specificity in plant symbioses. In Cyanobacteria in Symbiosis, Eds. A N Rai, B Bergman and U Rasmussen. pp. 313–328. Kluwer Academic Publishers, Dordrecht.Google Scholar
  166. Reinhold-Hurek B and Hurek T 1997 Interaction between diazotrophs and grasses. In Biological Fixation of Nitrogen for Ecology and Sustainable Agriculture. Eds. A Legocki, H Bothe and A Puhler. pp. 317–324. Springer-Verlag, Berlin.Google Scholar
  167. Ribbe M, Gadkari D and Meyer O 1997 N2 fixation by Streptomyces thermoautotrophicus involves a molybdenum-dinitrogenase and a manganese-superoxide oxidoreductase that couple N2 reduction to the oxidation of superoxide produced from O2 by a molybdenum-CO dehydrogenase. J. Biol. Chem. 272, 26627–26633.CrossRefPubMedGoogle Scholar
  168. Rippka R, Deruelles J, Waterbury J B, Herdman M and Stainer R Y 1979 Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111, 1–61.Google Scholar
  169. Robinson J B and Bauer W D 1993 Relationships between C4 dicarboxylic acid transport and chemotaxis in Rhizobium meliloti. J. Bacteriol. 175, 2284–2291.PubMedGoogle Scholar
  170. Rodriguez-Barrueco C and de Castro F B 1973 Cytokinin-induced pseudonodules on Alnus glutinosa. Physiol. Plant. 29, 227–280.Google Scholar
  171. Roelofsen W and Akkermann A D L 1979 Uptake and evolution of H2 and reduction of C2H2 by root nodules and homogenates of Alnus glutinosa L. Plant Soil 110, 167–176.Google Scholar
  172. Santi C, Svistoonoff S, Constans L, Auguy F, Duhoux E, Bogusz D and Franche C 2003a Choosing a reporter for gene expression studies in transgenic actinorhizal plants of the Casuarinaceae family. Plant Soil 254, 229–237.CrossRefGoogle Scholar
  173. Santi C, von Groll U, Ribeiro A, Chiurazzi M, Auguy F, Bogusz D, Franche C and Pawlowski K 2003b Comparison of nodule induction in legume and actinorhizal symbioses: The induction of actinorhizal nodules does not involve ENOD40. Mol. Plant-Microbe Interact. 16, 808–816PubMedGoogle Scholar
  174. Schneider D, Wink M, Sporer F and Lounibos P 2002 Cycads: Their evolution, toxins, herbivores and insect pollinators. Naturwissenschaften 89, 281–294.CrossRefPubMedGoogle Scholar
  175. Schopf J W, Kudryavtsev A B, Agresti D G, Wdowlak T J and Czaja A D 2002 Laser-Raman imagery of Earth’s earliest fossils. Nature 416, 73–76.CrossRefPubMedGoogle Scholar
  176. Schubert K R 1986 Products of biological nitrogen fixation in higher plants: synthesis, transport, and metabolism. Annu. Rev. Plant Physiol. 37, 539–574.CrossRefGoogle Scholar
  177. Schultze M and Kondorosi A 1998 Regulation of symbiotic root nodule development. Annu. Rev. Genet. 32, 33–57.CrossRefPubMedGoogle Scholar
  178. Schwencke J and Caru M 2001 Advances in actinorhizal symbiosis: Host plant-Frankia interactions, biology, and applications in arid land reclamation. A Review. Arid Land Res. Man. 15, 285–327.Google Scholar
  179. Schwintzer C R, Berry A M and Disney L D 1982 Seasonal patterns of root nodule growth, endophyte morphology, nitrogenase activity and shoot development in Myrica gale. Can. J. Bot. 60, 746–757.Google Scholar
  180. Scott K F, Saad M, Price G D, Gresshoff P M, Kane H and Chua K Y 1987 Conserved nodulation genes are obligatory for nonlegume nodulation. In Molecular Genetics and Plant-Microbe Interactions. Eds. D-P S Verma and N Brisson. Kluwer Academic Publishers, Dordrecht.Google Scholar
  181. Sellstedt A and Atkins C A 1991 Composition of amino compounds transported in xylem of Casuarina sp. J. Exp. Bot. 42, 1493–1497.Google Scholar
  182. Sergeeva E, Liaimer A and Bergman B 2002 Evidence for production of the phytohormone indole-3-acetic acid by cyanobacteria. Planta 215, 229–238.CrossRefPubMedGoogle Scholar
  183. Serraj R, Sinclair T R and Purcell L C 1999 Symbiotic N2 fixation response to drought. J. Exp. Bot. 50, 143–155.CrossRefGoogle Scholar
  184. Silvente S, Camas A and Lara M 2003 Heterogeneity of sucrose synthase genes in bean (Phaseolus vulgaris L.): Evidence for a nodule-enhanced sucrose synthase gene. J. Exp. Bot. 54, 749–755.PubMedGoogle Scholar
  185. Silvester W B and Harris S L 1989 Nodule structure and nitrogenase activity of Coriaria arborea in response to varying oxygen partial pressure. Plant Soil 118, 97–110.CrossRefGoogle Scholar
  186. Silvester W B, Harris S L, Tjepkema J D 1990 Oxygen regulation and hemoglobin. In The Biology of Frankia and Actinorhizal Plants. Eds. C R Schwintzer and J D Tjepkema. pp. 157–176. Academic Press, New York.Google Scholar
  187. Silvester W B, Langenstein B and Berg R H 1999 Do mitochondria provide the oxygen diffusion barrier in root nodules of Coriaria and Datisca? Can. J. Bot. 77, 1358–1366.CrossRefGoogle Scholar
  188. Silvester W B, Parsons R and Watt P W 1996 Direct measurement of release and assimilation of ammonia in the Gunnera-Nostoc symbiosis. New Phytol. 132, 617–625.Google Scholar
  189. Silvester W B, Whitbeck J, Silvester J K and Torrey J G 1988. Growth, nodule morphology, and nitrogenase activity of Myrica gale with roots grown at various oxygen levels. Can. J. Bot. 66, 1762–1771.Google Scholar
  190. Simms E L and Taylor D L 2002 Partner choice in nitrogen-fixation mutualisms of legumes and rhizobia. Integ. Comp. Biol. 42, 369–380.Google Scholar
  191. Smith C A, Skvirsky R C and Hirsch A M 1986 Histochemical evidence for the presence of a suberinlike compound in Rhizobium-induced nodules of the nonlegume Parasponia rigida. Can. J. Bot. 64, 1474–1483.Google Scholar
  192. Soedarjo M and Borthakur D 1998 Mimosine, a toxin produced by the tree-legume Leucaena provides a nodulation competition advantage to mimosine-degrading Rhizobium strains. Soil Biol. Biochem. 30, 1605–1613.CrossRefGoogle Scholar
  193. Soltis D E, Soltis P S, Morgan D R, Swensen S M, Mullin B C, Dowd J M and Martin P G 1995 Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc. Natl. Acad. Sci., USA 92, 2647–2651.PubMedGoogle Scholar
  194. Soltis P S, Soltis D E, Zanis M J and Kim S 2000 Basal lineages of angiosperms: relationships and implications for floral evolution. Int. J. Plant Sci. 161, S97-S107.CrossRefGoogle Scholar
  195. Smolander A, Ronkko R, Nurmiaho-Lassila E L and Haahtela K 1990 Growth of Frankia in the rhizosphere of Betula pendula, a nonhost tree species. Can. J. Microbiol. 36, 649–656.Google Scholar
  196. Sprent J I and Raven J A 1992 Evolution of nitrogen-fixing root nodules symbioses. In Biological Nitrogen Fixation: Achievements and Objectives. Eds. G Stacey, R H Burris and H J Evans. pp. 461–196. Chapman and Hall, New York.Google Scholar
  197. Sprent J I and Scott R 1979 The nitrogen economy of Myrica gale and its possible significance for the afforestation of peat soils. In Symbiotic Nitrogen Fixation in the Management of Temperate Forests. Eds. J C Gordon, C T Wheeler and A Perry. pp. 234–242. Forest Research Laboratory, State University, Corvallis.Google Scholar
  198. Stevens G A Jr and Berry A M 1988 Cytokinin secretion by Frankia sp. HFPArI3 in defined medium. Plant Physiol. 87, 15–16.Google Scholar
  199. Suganuma N, Nakamura Y, Yamamoto M, Ohta T, Koiwa H, Akao S and Kawaguchi M 2003 The Lotus japonicus Senl gene controls rhizobial differentiation into nitrogen-fixing bacteroids in nodules. Mol. Gen. Genomics 269, 312–320.CrossRefGoogle Scholar
  200. Suominen L, Roos C, Lortet G, Paulin L and Lindstrom K 2001 Identification and structure of the Rhizobium galegae common nodulation genes: Evidence for horizontal gene transfer. Mol. Biol. Evol. 18. 907–916.PubMedGoogle Scholar
  201. Svistoonoff S, Laplaze L, Auguy F, Santi C, Fontanillas E, Duhoux E, Franche C and Bogusz D 2003 Expression pattern of ara12*, an Arabidopsis homologue of the nodule-specific actinorhizal subtilases cg12/ag12. Plant Soil 254, 239–244.CrossRefGoogle Scholar
  202. Swensen S M 1996 The evolution of actinorhizal symbioses - evidence for multiple origins of the symbiotic association. Amer. J. Bot. 83, 1503–1512.Google Scholar
  203. Szczyglowski K, Kapranov P, Hamburger D and de Bruijn F J 1998 The Lotus japonicus LjNOD70 nodulin gene encodes a protein with similarities to transporters. Plant Mol. Biol. 37, 651–661.CrossRefPubMedGoogle Scholar
  204. Tamagnini P, Axelsson R, Lindberg P, Oxelfelt F, Wunschiers R and Lindblad P 2002 Hydrogenases and hydrogen metabolism of cyanobacteria. Microbiol. Mol. Biol. Rev. 66, 1–20.PubMedGoogle Scholar
  205. Tjepkema J D and Cartica R J 1982 Diffusion limitation of oxygen uptake and nitrogenase activity in the root nodules of Parasponia rigida Merr. and Perry. Plant Physiol. 69, 728–733.Google Scholar
  206. Torrey J G and Callaham D 1979 Early nodule development in Myrica gale. Soil actinomycete causing nodulation. Bot. Gaz. 140, S10-S14.Google Scholar
  207. Treutlein J and Wink M 2002 Molecular phylogeny of cycads inferred from rbcL sequences. Naturwissenschaften 89, 221–225.CrossRefPubMedGoogle Scholar
  208. Trevaskis B, Colebatch G, Desbrosses G, Wandrey M, Wienkoop S, Saalbach G and Udvardi M 2002 Differentiation of plant cells during symbiotic nitrogen fixation. Comp. Func. Gen. 3, 151–157.Google Scholar
  209. Trinick M J 1973 Symbiosis between Rhizobium and the nonlegume, Trema aspera. Nature (Lond.) 244, 459–460.CrossRefGoogle Scholar
  210. Trinick M J 1979 Structure of nitrogen-fixing nodules formed by Rhizobium on roots of Parasponia andersonii Planch. Can. J. Microbiol. 25, 565–578.PubMedGoogle Scholar
  211. Trinick M J 1981 The effective Rhizobium symbiosis with the non-legume Parasponia andersonii. In Current Perspectives in Nitrogen Fixation. Eds. A H Gibson and W E Newton. pp. 480. Elsevier/North-Holland Biomedical Press, Amsterdam.Google Scholar
  212. Trinick M J and Galbraith J 1980 The Rhizobium requirements of the non-legume Parasponia andersonii in relationship to the cross-inoculation group concept of legumes nitrogen fixation. New Phytol. 86, 17–26.Google Scholar
  213. Tyerman S D, Whitehead L F and Day D A 1995 A channel-like transporter for NH4+ on the symbiotic interface of N2-fixing plants. Nature 378, 629–632.CrossRefGoogle Scholar
  214. Udvardi M K and Day D A 1990 Ammonia (14C-methylamine) transport across the bacteroid and peribacteroid membranes of soybean root nodules. Plant Physiol. 94, 71–76.Google Scholar
  215. Udvardi M K, Lister D L and Day D A 1992 Isolation and characterization of a ntrC and mutant of Bradyrhizobium (Parasponia) sp. ANU289. J. Gen. Microbiol. 138, 1019–1025.PubMedGoogle Scholar
  216. Valverde C and Wall L G 1999 Time course of nodule development in the Discaria trinervis (Rhamnaceae)-Frankia symbiosis. New Phytol. 141, 345–354.CrossRefGoogle Scholar
  217. Valverde C and Wall L G 2003 Ammonium assimilation in root nodules of actinorhizal Discaria trinervis. Regulation of enzyme activities and protein levels by the availability of macronutrients (N, P and C). Plant Soil 254, 139–153.Google Scholar
  218. Van Ghelue M, Løvaas E, Ringø E and Solheim B 1997 Early interactions between Alnus glutinosa (L.) Gaertn. and Frankia strain ArI3. Production and specificity of root hair deformation factor(s). Physiol. Plant. 99, 579–587.Google Scholar
  219. Van Ghelue M, Ribeiro A, Solheim B, Akkermans A D L, Bisseling T and Pawlowski K 1996 Sucrose synthase and enolase expression in actinorhizal nodules of Alnus glutinosa: Comparison with legume nodules. Mol. Gen. Genet. 250, 437–446.CrossRefPubMedGoogle Scholar
  220. Van Straten J, Akkermans A D L and Roelofsen W 1977 Nitrogenase activity of endophyte suspensions derived from root nodules of Alnus, Hippophae, Shepherdia and Myrica spp. Nature 266, 257–258.Google Scholar
  221. Vessey J K 2003 Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255, 571–586.CrossRefGoogle Scholar
  222. Vessey J K and Pan B 2003 Living a grounded life: Growth and nitrogenase activity of Gluconacetobacter diazotrophicus on solid media in response to culture conditions. Symbiosis 35, 181–197.Google Scholar
  223. Vessey J K, Walsh K B and Layzell D B 1988 Oxygen limitation of N2 fixation in stem-girdled and nitrate-treated soybean. Physiol. Plant. 73, 113–121.Google Scholar
  224. Vikman P-A 1992 The symbiotic vesicle is a major site for respiration in Frankia from Alnus incana root nodules. Can. J. Microbiol. 38, 779–784.Google Scholar
  225. Vikman P-A and Huss-Danell K 1987a Purity of Frankia preparations from root nodules of Alnus incana. Physiol. Plant. 71, 489–494.Google Scholar
  226. Vikman P-A and Huss-Danell K 1987b Capacity for hexose respiration in symbiotic Frankia from Alnus incana. Physiol. Plant. 70, 349–354.Google Scholar
  227. Vikman P-A and Huss-Danell K 1991 Respiration of malate and glutamate in symbiotic Frankia prepared from Alnus incana. J. Exp. Bot. 42, 221–228.Google Scholar
  228. Vikman P-A and Vessey J K 1993 Ontogenetic changes in root nodule subpopulations of common bean (Phaeolus vulgaris L.). III. Nodule formation, growth and degradation. J. Exp. Bot. 44, 579–586.Google Scholar
  229. Viterbo A, Matveyev A, Rasmussen U and Bergman B 1999 Characterization of a nodM/glmS homologous gene in the symbiotic cyanobacterium Nostoc PCC 9229. Symbiosis 26, 237–246.Google Scholar
  230. Walsh K B, Vessey J K and Layzell D B 1987 Carbohydrate supply and N2 fixation in soybean. The effect of varied daylength and stem girdling. Plant Physiol. 85, 137–144.Google Scholar
  231. Wang C M, Ekman M and Bergman B 2004 Expression of cyanobacterial genes and proteins involved in heterocyst differentiation and dinitrogen fixation along a plant symbiosis development profile Mol. Plant-Microbe Interact. (in press).Google Scholar
  232. Waters J K, Hughes B L, Purcell L C, Gerhardt K O, Mawhinney T P and Emerich D W 1998 Alanine, not ammonia, is excreted from N2-fixing soybean nodule bacteroids. Proc. Natl. Acad. Sci., USA 95, 12038–12042.CrossRefPubMedGoogle Scholar
  233. Webster G, Davey M R and Cocking E C 1995a Parasponia with rhizobia: a neglected non-legume nitrogen-fixing symbiosis. AgBiotech News Info. 7, 119–124.Google Scholar
  234. Webster G, Poulton P R, Cocking E C and Davey M R 1995b The nodulation of micro-propagated plants of Parasponia andersonii by tropical legume rhizobia. J. Exp. Bot. 46, 1131–1137.Google Scholar
  235. Weisz P R and Sinclair T R 1987 Regulation of soybean nitrogen fixation in response to rhizosphere oxygen. I. Role of nodule respiration. Plant Physiol. 84, 900–905.Google Scholar
  236. Wheeler C T, Watts S H, Hillman J R 1983 Changes in carbohydrates and nitrogenase compounds in the root nodules of Alnus glutinosa in relation to dormancy. New Phytol 95, 209–218.Google Scholar
  237. Wittmann W, Bergersen F J and Kennedy G S 1965 The coralloid roots of Macrozamia communis L. Johnson. Aust. J. Biol. Sci. 18, 1129–1134.Google Scholar
  238. Wong F C Y and Meeks J C 1994 Establishment of a functional symbiosis between the cyanobacterium Nostoc punctiforme and the bryophyte Anthoceros punctatus requires genes involved in nitrogen control and initiation of heterocyst differentiation. Microbiology-SGM 148, 315–323.Google Scholar
  239. Wycoff K L, Hunt S, Gonzales M B, VandenBosch K A, Layzell D B and Hirsch A M 1998 Effects of oxygen on nodule physiology and expression of nodulins in alfalfa. Plant Physiol. 117, 385–395.CrossRefPubMedGoogle Scholar
  240. Zehr J P, Jenkins B D, Short S M and Steward G F 2003 Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ. Microbiol. 5, 539–554.CrossRefPubMedGoogle Scholar
  241. Zeng S and Tjepkema J D 1994 The wall of the infected cell may be the major diffusion barrier in nodules of Myrica gale L. Soil Biol Biochem. 26, 633–639.CrossRefGoogle Scholar
  242. Zepp K, Hahn D and Zeyer J 1997 Evaluation of a 23S rRNA insertion as target for the analysis of uncultured Frankia populations in root nodules of alders by whole cell hybridization. Syst. Appl. Microbiol. 20, 124–132.Google Scholar
  243. Zheng W, Song T, Bao X, Bergman B and Rasmussen U 2002 High cyanobacterial diversity in coralloid roots of cycads revealed by PCR fingerprinting. FEMS Microbiol. Ecol. 40, 215–222.Google Scholar
  244. Zhulin I B, Bespalov V A, Johnson M S and Taylor B L 1996 Oxygen taxis and proton motive force in Azospirillum brasilense. J. Bacteriol. 178, 5199–5204.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • J. Kevin Vessey
    • 1
  • Katharina Pawlowski
    • 2
  • Birgitta Bergman
    • 3
  1. 1.Department of Plant ScienceUniversity of ManitobaWinnipegCanada
  2. 2.Plant Biochemistry, Albrecht von Haller Institute for Plant SciencesGöttingen UniversityGöttingenGermany
  3. 3.Department of BotanyStockholm UniversityStockholmSweden

Personalised recommendations