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

  • Chapter
Root Physiology: from Gene to Function

Part of the book series: Plant Ecophysiology ((KLEC,volume 4))

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.

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References

  • 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 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Baker 1992 Actinorhizal symbiosis. In Biological Nitrogen Fixation. Eds. G Stacey., H Evans. and R Burris. pp. 259–292. Chapman & Hall, New York.

    Google Scholar 

  • Becana M and Klucas R V 1992 Oxidation and reduction of leghemoglobin in root nodules of leguminous plants. Plant Physiol. 98, 1217–1221.

    CAS  Google Scholar 

  • Becking J H 1979 Root-nodule symbiosis between Rhizobium and Parasponia parviflora (Ulmaceae). Plant Soil 51, 289–296.

    Article  Google Scholar 

  • Becking J H 1983a The Parasponia parviflora—Rhizobium symbiosis. Host specificity, growth and nitrogen fixation under various conditions. Plant Soil 75, 309–342.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 & Hall, New York.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Benson D R and Silvester W B 1993 Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol. Rev. 57, 293–319.

    PubMed  CAS  Google Scholar 

  • Berg R H 1999 Frankia forms infection threads. Can. J. Bot. 77, 1327–1333.

    Google Scholar 

  • Berg R H and McDowell L 1987a Endophyte differentiation in Casuarina actinorhizae. Protoplasma 136, 104–117.

    Article  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • Bergman B, Matveyev A and Rasmussen U 1996 Chemical signalling in cyanobacterial-plant symbioses. Trends Plant Sci. 1, 191–197.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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 

  • Bond G 1952 Some features of the root growth in nodulated plants of Myrica gale L. Ann. Bot. 16, 467–475.

    Google Scholar 

  • 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, 446–452.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Buikema W J and Haselkorn R 1993 Molecular genetics of cyanobacterial development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44, 33–52.

    Article  CAS  Google Scholar 

  • 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 

  • Burris R H 1991 Nitrogenases. J. Biol. Chem. 266, 9339–9342.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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, 43–59.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Colebatch G, Trevaskis B and Udvardi M 2002b Symbiotic nitrogen fixation research in the postgenomics era. New Phytol. 153, 37–42.

    CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Day A A and Udvardi M K 1993 Metabolite exchange across symbiosome membranes. Symbiosis 14, 175–189.

    CAS  Google Scholar 

  • Denison R F 1992 Mathematical modeling of oxygen diffusion and respiration in legume root nodules. Plant Physiol. 98, 901–907.

    CAS  Google Scholar 

  • Denison R F 2000 Legume sanctions and the evolution of symbiotic cooperation by rhizobia. Am. Nat. 156, 567–576.

    Article  Google Scholar 

  • Denison R F and Okano Y 2003 Leghaemoglobin oxygenation gradients in alfalfa and yellow sweetclover nodules. J. Exp. Bot. 54, 1085–1091.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Dommergues Y R 1995 Nitrogen fixation by trees in relation to soil nitrogen economy. Fertil. Res. 42, 215–230.

    Article  CAS  Google Scholar 

  • Doyle J J 1998 Phylogenetic perspectives on nodulation: Evolving views of plants and symbiotic bacteria. Trends Plant Sci. 3, 473–478.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Gallon J R 1992 Tansley Review No. 44: Reconciling the incompatible N2 fixation and O2. New Phytol. 122, 571–609.

    CAS  Google Scholar 

  • Gallon J R 2001 N2 fixation in phototrophs: Adaptation to a specialized way of life. Plant Soil 230, 39–48.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Grobbelaar N, Hattingh W and Marshall J 1986 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.

    CAS  Google Scholar 

  • 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 

  • 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. Bot. 28, 271–281.

    Article  CAS  Google Scholar 

  • Gualtieri G and Bisseling T 2000 The evolution of nodulation. Plant Mol. Biol. 42, 181–194.

    Article  PubMed  CAS  Google Scholar 

  • Guan C H, Ribeiro A, Akkermans A D L, Jing Y X, van Kammen A, 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • Hirsch A M, Fang Y, Asad S and Kapulnik Y 1997 The role of phytohormones in plant-microbe symbioses. Plant Soil 194, 171–184.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Huss-Danell K 1997 Tansley Review No. 93. Actinorhizal symbioses and their N2 fixation. New Phytol. 136, 375–405.

    Article  CAS  Google Scholar 

  • 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 

  • 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 

  • 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. Roy. Soc. Edinburgh 102B, 429–432.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Johansson C and Bergman B 1992 Early events during the establishment of the Gunnera/Nostoc symbiosis. Planta 188, 403–413.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 and Tabata S 2002 Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res. 9, 189–197.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 for publication.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Kuzma M M and Layzell D B 1994 Acclimation of soybean nodules to changes in temperature. Plant Physiol. 106, 263–270.

    PubMed  CAS  Google Scholar 

  • Lancelle S A and Torrey J G 1984 Early development of Rhizobium-induced root nodules of Parasponia rigida. I. Infection and early nodule initiation. Protoplasma 123, 26–37.

    Article  Google Scholar 

  • Lancelle S A and Torrey J G 1985 Early development of Rhizobium-induced root nodules of Parasponia rigida. II. Nodule morphogenesis and symbiotic development. Can. J. Bot. 63, 25–35.

    Google Scholar 

  • Lavire C and Cournoyer B 2003 Progress on the genetics of the N2-fixing actinorhizal symbiont Frankia. Plant Soil 254, 125–137.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • Lhuissier F G P, De Ruijter N C A, Sieberer BJ, Esseling J J and 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Lindblad P and Bergman B 1990 The cycad-cyanobacterial symbiosis. In Handbook of Symbiotic Cyanobacteria. Eds. A N Rai. pp. 137–159. CRC Press, Boca Raton.

    Google Scholar 

  • 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 

  • Lindblad P, Hällblom L and Lindblad P 1985b The cyanobacterium-Zamia symbiosis: C2H2 reduction and heterocyst frequency. Symbiosis 1, 19–28.

    CAS  Google Scholar 

  • 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 

  • Lodwig E and Poole P 2003 Metabolism of Rhizobium bacteroids. Crit. Rev. Plant Sci. 22, 37–78.

    CAS  Google Scholar 

  • Lopez M F, Fontaine M S and Torrey J G 1984 Levels of trehalose and glycogen in Frankia sp. HFPArI3 (Actinomy-cetales) [Nitrogen-fixing bacteria]. Can. J. Microbiol. 30, 746–752.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 sarginine, ornithine and citrulline. Arch. Microbiol. 59, 506–511.

    Google Scholar 

  • Martinez-Romero E 2003 Diversity of Rhizobium-Phaseolus vulgaris symbiosis: Overview and perspectives. Plant Soil 252, 11–23.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Mattsson U and Sellstedt A 2002 Nickel affects activity more than expression of hydrogenase protein in Frankia. Curr. Microbiol. 44, 88–93.

    Article  PubMed  CAS  Google Scholar 

  • McClure P R, Coker G T III and Schubert K R 1983 Carbon dioxide fixation in roots and nodules of Alnus glutinosa. Plant Physiol. 71, 652–657.

    CAS  Google Scholar 

  • 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 Oecol. 13, 509–510.

    Google Scholar 

  • 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 

  • Meesters T M 1987 Localization of nitrogenase in vesicles of Frankia sp. Cc1.17 by immunogoldlabelling on ultrathin cryosections. Arch. Microbiol. 146, 327–331.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Newcomb W and Pankhurst C E 1982 Fine structure of actinorhizal nodules of Coriaria arborea (Coriariaceae). N. Z. J. Bot. 20, 93–103.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • Oke V and Long S R 1999 Bacteroid formation in the Rhizobium-legume symbiosis. Curr. Opin. Microbiol. 2, 641–646.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ow M C, Gantar M and Elhai J 1999 Reconstitution of a cycad-cyanobacterial association. Symbiosis 27, 125–134.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Pate J S 1989 Synthesis, transport, and utilization of products of symbiotic nitrogen fixation. Rec. Adv. Phytochem. 23, 65–115.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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 existence of regions of homology of symbiotic genes of Rhizobium. Can. J. Microbiol. 37, 171–181.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • Price N P J 1999 Carbohydrate determinants of Rhizobium-legume symbioses. Carbohydr. Res. 317, 1–9.

    Article  PubMed  CAS  Google Scholar 

  • Qian J H, Kwon S W and Parker M A 2003 rRNA, nifD phylogeny of Bradyrhizobium from sites across the Pacific Basin. FEMS Microbiol. Lett. 219, 159–165.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 Lys M receptor-like kinases. Nature 425, 585–592.

    Article  PubMed  CAS  Google Scholar 

  • Rai A N, Bergman B and Rasmussen U 2002 Cyanobacteria in Symbiosis. Kluwer Academic, Dordrecht. 368 pp.

    Google Scholar 

  • Rai A N, Söderbäck E and Bergman B 2000 Tansley Review No. 116: Cyanobacterium-plant symbioses. New Phytol. 147, 449–481.

    Article  CAS  Google Scholar 

  • 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-/Fixactinomycete. Can. J. Microbiol. 44, 140–148.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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 

  • Ribbe M, Gadkari D and Meyer O 1997 N2 fixation by Streptomyces thermoautotrophicus involves a molybdenumdinitrogenase 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Robinson J B and Bauer W D 1993 Relationships between C4 dicarboxylic acid transport and chemotaxis in Rhizobium meliloti. J. Bacteriol. 175, 2284–2291.

    PubMed  CAS  Google Scholar 

  • Rodriguez-Barrueco C and de Castro F B 1973 Cytokinin-induced pseudonodules on Alnus glutinosa. Physiol. Plant. 29, 227–280.

    Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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, 808–816.

    PubMed  CAS  Google Scholar 

  • Schneider D, Wink M, Sporer F and Lounibos P 2002 Cycads: Their evolution, toxins, herbivores and insect pollinators. Naturwissenschaften 89, 281–294.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Schubert K R 1986 Products of biological nitrogen fixation in higher plants: Synthesis, transport, and metabolism. Annu. Rev. Plant Physiol. 37, 539–574.

    Article  CAS  Google Scholar 

  • Schultze M and Kondorosi A 1998 Regulation of symbiotic root nodule development. Annu. Rev. Genet. 32, 33–57.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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 

  • Sellstedt A and Atkins C A 1991 Composition of amino compounds transported in xylem of Casuarina sp. J. Exp. Bot. 42, 1493–1497.

    CAS  Google Scholar 

  • Sergeeva E, Liaimer A and Bergman B 2002 Evidence for production of the phytohormone indole-3-acetic acid by cyanobacteria. Planta 215, 229–238.

    Article  PubMed  CAS  Google Scholar 

  • Serraj R, Sinclair T R and Purcell L C 1999 Symbiotic N2 fixation response to drought. J. Exp. Bot. 50, 143–155.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Silvester W B, Harris S L and 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 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • Simms E L and Taylor D L 2002 Partner choice in nitrogen-fixation mutualisms of legumes and rhizobia. Integrat. Comp. Biol. 42, 369–380.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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. Can. J. Microbiol. 36, 649–656.

    Google Scholar 

  • 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 & Hall, New York.

    Google Scholar 

  • 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 

  • Stevens G A Jr and Berry A M 1988 Cytokinin secretion by Frankia sp. HFPArI3 in defined medium. Plant Physiol. 87, 15–16.

    CAS  Google Scholar 

  • Suganuma 2003 The Lotus japonicus Sen1 gene controls rhizobial differentiation into nitrogen-fixing bacteroids in nodules. Mol. Gen. Genom. 269, 312–320.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 nodulespecific actinorhizal subtilases cg12/ag12. Plant Soil 254, 239–244.

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Torrey J G and Callaham D 1979 Early nodule development in Myrica gale. Soil actinomycete causing nodulation. Bot. Gaz. 140, S10–S14.

    Google Scholar 

  • Treutlein J and Wink M 2002 Molecular phylogeny of cycads inferred from rbcL sequences. Naturwissenschaften 89, 221–z225

    Article  PubMed  CAS  Google Scholar 

  • 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. Funct. Gen. 3, 151–157.

    CAS  Google Scholar 

  • Trinick M J 1973 Symbiosis between Rhizobium and the non-legume, Trema aspera. Nature (Lond.) 244, 459–460.

    Article  Google Scholar 

  • Trinick M J 1979 Structure of nitrogen-fixing nodules formed by Rhizobium on roots of Parasponia andersonii Planch. Can. J. Microbiol. 25, 565–578.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Valverde C and Wall L G 1999 Time course of nodule development in the Discaria trinervis (Rhamnaceae)-Frankia symbiosis. New Phytol. 141, 345–354.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • Vessey J K 2003 Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255, 571–586.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • Vikman P-A and Huss-Danell K 1987b Capacity for hexose respiration in symbiotic Frankia from Alnus incana. Physiol. Plant. 70, 349–354.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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 

  • Wheeler C T, Watts S H and 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.

    CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

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Correspondence to J. Kevin Vessey .

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Hans Lambers Timothy D. Colmer

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Kevin Vessey, J., Pawlowski, K., Bergman, B. (2005). Root-based N2-fixing symbioses: Legumes, actinorhizal plants, Parasponia sp. and cycads. In: Lambers, H., Colmer, T.D. (eds) Root Physiology: from Gene to Function. Plant Ecophysiology, vol 4. Springer, Dordrecht. https://doi.org/10.1007/1-4020-4099-7_3

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