Early Interactions, Infection And Nodulation In Actinorhizal Symbiosis

  • L. G. Wall
  • A. M. Berry
Part of the Nitrogen Fixation: Origins, Applications, and Research Progress book series (NITR, volume 6)


Nitrogen Fixation Root Hair Nodule Development Frankia Strain Early Interaction 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Angulo Carmona, A. F. (1974). La formation des nodules fixateurs d’azote chez Alnus glutinosa (L.) Vill. Acta Bot. Neerl., 23, 257-303.Google Scholar
  2. Arnone, J. A., Kohls, S. J., and Baker, D. D. (1994). Nitrate effects on nodulation and nitrogenase activity of actinorhizal Casuarina studied in split root systems. Soil Biol. Biochem., 26, 599-606.CrossRefGoogle Scholar
  3. Baker, A., Hill, G. F., and Parsons, R. (1997). Alteration of N nutrition in Myrica gale induces changes in nodule growth, nodule activity and amino acid composition. Physiol. Plant., 99, 632-639.CrossRefGoogle Scholar
  4. Baker, A., and Parsons, R. (1997). Evidence for N feedback regulation of N2 fixation in Alnus glutinosa L. J. Exp. Bot., 48, 67-73.CrossRefGoogle Scholar
  5. Baker, D. D. (1987). Relationships among pure culture strains of Frankia based on host specificity. Physiol. Plant., 70, 245-248.CrossRefGoogle Scholar
  6. Benoit, L. F., and Berry, A. M. (1997). Flavonoid-like compounds from seeds of red alder (Alnus rubra) influence host nodulation by Frankia (Actinomycetales). Physiol. Plant., 99, 588-593.CrossRefGoogle Scholar
  7. Benson, D. R., and Clawson, M. L. (2000). Evolution of the actinorhizal plant symbiosis. In E. W. Triplett (Ed.), Prokaryotic nitrogen fixation: A model system for analysis of a biological process (pp. 207-224). Wymondham, UK: Horizon Scientific Press.Google Scholar
  8. Benson, D. R., Stephens, D. W., Clawson, M. L., and Silvester, W. B. (1996). Amplification of 16S rRNA genes from Frankia strains in root nodules of Ceanothus griseus, Coriaria arborea, Coriaria plumosa, Discaria toumatou, and Purshia tridentata. Appl. Environ. Microbiol., 62, 2904-2909.PubMedGoogle Scholar
  9. Berg, R. H. (1999a). Frankia forms infection threads. Can. J. Bot., 77, 1327-1333.CrossRefGoogle Scholar
  10. Berg, R. H. (1999b). Cytoplasmic bridge formation in the nodule apex of actinorhizal root nodules. Can. J. Bot., 77, 1351-1357.CrossRefGoogle Scholar
  11. Berry, A. M. (1984). The actinorhizal infection process: Review of recent research. In M. J. Klug and C. A. Reddy (Eds.), Current perspectives in microbial ecology (pp. 222-229). Washington, DC: ASM.Google Scholar
  12. Berry, A. M., and Torrey, J. G. (1983). Root hair deformation in the infection process of Alnus rubra. Can. J. Bot., 66, 2863-2876.Google Scholar
  13. Berry, A. M., Torrey J. G., and McCully, M. E. (1983). The fine structure of root hair wall and surface mucilage in the actinorhizal host Alnus rubra. In R. Goldberg (Ed.), Plant molecular biology (pp. 319-327). New York: Liss.Google Scholar
  14. Berry, A. M., McIntyre, M., and McCully M. E. (1986). Fine structure of root hair infection leading to nodulation in the Frankia-Alnussymbiosis. Can. J. Bot., 64, 292-305.Google Scholar
  15. Berry, A. M., and McCully, M. E. (1990). Callose-containing deposits in relation to root hair infections of Alnus rubra Bong. by Frankia. Can. J. Bot., 68, 798-802CrossRefGoogle Scholar
  16. Berry, A. M., Rasmussen, U., Bateman, K., Huss-Danell, K., Lindwall, S., and Bergman, B. (2002). Arabinogalactan proteins are expressed at the symbiotic interface in root nodules of Alnus spp. New Phytol., 155, 469-479.CrossRefGoogle Scholar
  17. Berry, A. M., Kahn, R. K. S., and Booth, M. C. (1989). Identification of indole compounds secreted by Frankia HFPArI3 in defined culture medium Plant Soil, 118, 205-209.CrossRefGoogle Scholar
  18. Berry, A. M., and Sunell, L. A. (1990). The infection process and nodule development. In C. R. Schwintzer and J. D. Tjepkma (Eds.), The biology ofFrankia and actinorhizal plants (pp. 61-81). San Diego, CA: Academic Press.Google Scholar
  19. Bolaños, L., Brewin, N. J., and Bonilla, I. (1996). Effects of boron on Rhizobium-legume cell-surface interactions and nodule development. Plant Physiol., 110, 1249-1256PubMedGoogle Scholar
  20. Bolaños, L., Redondo-Nieto, M., Bonilla, I., and Wall, L. G. (2002). Boron requirement for growth, nitrogen fixation and nodulation of Frankia BCU110501. Physiol. Plant, 115, 563-570.PubMedCrossRefGoogle Scholar
  21. Bonilla, I., García-González, M., and Mateo, P. (1990). Boron requirement in cyanobacteria. Its possible role in the early evolution of photosynthetic organisms. Plant Physiol., 94, 1554-1560.PubMedGoogle Scholar
  22. Burggraaf, A. J. P., van der Linden, J., and Tak, T. (1983). Studies on the localization of infectible cells on Alnus glutinosa roots. Plant Soil, 74, 175-188.CrossRefGoogle Scholar
  23. Caetano-Anollés, G., and Gresshoff, P.M. (1991). Plant genetic control of nodulation. Ann. Rev. Microbiol., 45, 345-382.CrossRefGoogle Scholar
  24. 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
  25. Callaham, D., Newcomb, W., Torrey, J. G., and Peterson, R. L. (1979). Root hair infection in actinomycete-induced root nodule initiation in Casuarina, Myrica and Comptonia. Bot. Gaz. (Chicago), 140 (Suppl.), S1-S9.Google Scholar
  26. Cérémonie, H., Debellé, 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
  27. Chaboud, A., and Lalonde, M. (1982). Lectin binding on surfaces of Frankia strains. Can. J. Bot., 61, 2889-2897.CrossRefGoogle Scholar
  28. Chaia, E., Valverde, C., and Wall, L. G. (2006). Local adaptation of Frankiato different Discaria (Rhamnaceae) host species growing in Patagonia. Curr. Microbiol., 53,523-528.Google Scholar
  29. Chaia, E., and Raffaele, E. (2000). Spatial patterns of root branching and actinorhizal nodulation in Discaria trinervis seedlings. Symbiosis, 29, 329-341.Google Scholar
  30. Cusato, M. S., and Tortosa, R. D. (2000). Interactions between Frankiaand crops. Phyton, 68, 47-53.Google Scholar
  31. Dénarié, J., Debellé, F., and Promé, J. C. (1996). Rhizobium lipochitooligosaccharide nodulation factors: Signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem., 65, 503-535.PubMedCrossRefGoogle Scholar
  32. Dobritsa, S. V., and Novik, S. N. (1992). Feedback regulation of nodule formation in Hippophaë rhamnoides. Plant Soil, 144, 45-50.CrossRefGoogle Scholar
  33. 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.CrossRefGoogle Scholar
  34. Gabbarini, L., and Wall, L. G. (2002). Novel interactions in actinorhizal symbiosis. 8th New Phytologist Symposium, Soil microbes and plant productivity, 9-14 June 2002, Helsinki, Finland. Book of Abstracts.Google Scholar
  35. Gentili, F. (2003). Nutrient effects on nodulation and N 2 fixation in actinorhizal symbioses.Ph.D. thesis. Swedish University of Agricultural Sciences, Agragria 392, Umeå, Sweden.Google Scholar
  36. Gentili, F., and Huss-Danell, K. (2002). Phosphorus modifies the effects of nitrogen on nodulation in split-root systems of Hippophaë rhamnoides. New Phytol, 153, 53-61.CrossRefGoogle Scholar
  37. Gentili, F., and Huss-Danell, K. (2003). Local and systemic effects of phosphorous and nitrogen on nodulation and nodule function in Alnus incana. J. Exp. Bot., 54, 2757-2767.PubMedCrossRefGoogle Scholar
  38. Glick, B. R. (1999). Biochemical and genetic mechanisms used by plant growth promoting bacteria. New York, NY: Imperial College Press.Google Scholar
  39. Hammad, Y., Maréchal, J., Cournoyer, B., Norman, P., and Domenach, A.-M. (2001). Modification of the protein expression pattern induced in the nitrogen-fixing actinomycete Frankiasp. strain ACN14a-tsr by root exudates of its symbiotic host Alnus glutinosaand cloning of the sodFgene. Can. J. Microbiol., 47, 541-547.PubMedCrossRefGoogle Scholar
  40. Hammad, Y., Nalin, R., Maréchal, J., Fiasson, K., Pepin, R., et al. (2003). A possible role for phenyl acetic acid (PAA) on Alnus glutinosanodulation by Frankia. Plant Soil, 254,193-205.Google Scholar
  41. Heidstra, R., Geurts, R., Franssen, H., Spaink, H. P., van Kammen, A., and Bisseling, T. (1994). Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiol., 105, 787-797.PubMedGoogle Scholar
  42. Hirsch, A. M., and La Rue, T. A. (1997). Is the legume nodule a modified root or stem or an organ sui generis? Crit. Rev. Plant. Sci., 16, 361-392.CrossRefGoogle Scholar
  43. 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, 1-5.CrossRefGoogle Scholar
  44. Huss-Danell, K. (1997). Actinorhizal symbioses and their N2fixation. New Phytol., 136, 375-405.CrossRefGoogle Scholar
  45. Israel, D. W. (1993). Symbiotic dinitrogen fixation and host-plant growth during development of and recovery from phosphorus deficiency. Physiol. Plant., 88, 294-300.CrossRefGoogle Scholar
  46. Jeong, S. C., Ritchie, N. J., and Myrold, D. D. (1999). Molecular phylogenies of plant and Frankiasupport multiple origins of actinorhizal symbioses. Mol. Phylogen. Evol., 13, 493-503.CrossRefGoogle Scholar
  47. Knowlton, S., Berry, A. M., and Torrey, J.G. (1980). Evidence that associated soil bacteria may influence root hair infection of actinorhizal plants by Frankia. Can. J. Microbiol., 26, 971-7.PubMedCrossRefGoogle Scholar
  48. Kohls, S. J., and Baker, D. D. (1989). Effects of substrate nitrate concentration on symbiotic nodule formation in actinorhizal plants. Plant Soil, 118, 171-179.CrossRefGoogle Scholar
  49. Krusell, L., Madsen, L. H., Sato, S., Aubert, G., Genua, A., et al. (2002). Shoot control of root development and nodulation is mediated by a receptor like kinase. Nature, 420, 422-426PubMedCrossRefGoogle Scholar
  50. Laplaze, L., Duhoux, E., Franche, C., Frutz, T., Svistoonoff, S., et al. (2000). Casuarina glauca prenodule cells display the same differentiation as the corresponding nodule cells. Mol. Plant-Microbe Interact., 13, 107-112.PubMedCrossRefGoogle Scholar
  51. Liu, Q., and Berry, A. M. (1991a). The infection process and nodule initiation in the Frankia-Ceanothus root nodule symbiosis. Protoplasma, 163, 82-92.CrossRefGoogle Scholar
  52. Liu, Q., and Berry, A. M. (1991b). Localization and characterization of pectic polysacharides in roots and root nodules of Ceanothus spp. during intercellular infection by Frankia. Protoplasma, 163, 93-101.CrossRefGoogle Scholar
  53. Loh, J., Lohar, D. P., Andersen, B., and Stacey, G. (2002). A two-component regulator mediates population-density-dependent expression of the Bradyrhizobium japonicum nodulation genes. J. Bacteriol., 184, 1759-1766.PubMedCrossRefGoogle Scholar
  54. Loh, J., Pierson, E. A., Pierson III, L. S., Stacey, G., and Chaterjee A. (2002b). Quorum sensing in plant-associated bacteria. Curr. Op. Plant Biol., 5, 285-290.CrossRefGoogle Scholar
  55. Lugtenberg B. J. J., Dekkers, L., and Bloemberg G. V. (2001). Molecular determinants of rhizosphere colonization by pseudomonads. Ann. Rev. Phytopathol., 39, 461-490.CrossRefGoogle Scholar
  56. MacConnell, J. T., and Bond, G. (1957). A comparison of the effect of combined nitrogen on nodulation in non-legumes and legumes. Plant Soil, 8, 378-388.CrossRefGoogle Scholar
  57. Mathesius, U. (2001). Flavonoids induced in cells undergoing nodule organogenesis in white clover are regulators of auxin breakdown by peroxidase. J. Exp. Bot., 52, 419-426.PubMedGoogle Scholar
  58. Mathesius, U., Weinman, J. J., Rolfe, B. G., and Djordjevic, M. A. (2000). Rhizobia can induce nodules in white clover by “hijacking” mature cortical cells activated during lateral root development. Mol. Plant-Microbe Interact., 13, 170-182.PubMedCrossRefGoogle Scholar
  59. Mathesius, U., Mulders, S., Gao, M., Teplitski, M., Caetano-Anollés, G., et al. (2003). Extensive and specific responses of a eucaryote to bacterial quorum-sensing signals. Proc. Natl. Acad. Sci. U.S.A., 100, 1444-1449.PubMedCrossRefGoogle Scholar
  60. Maunuksela, L., Zeep, K., Koivula, T., Zeyer, J., Haatela, K., and Hahn, D. (1999). Analysis of Frankia populations in three soils devoid of actinorhizal plants. FEMS Microbiol. Ecol., 28, 11-22CrossRefGoogle Scholar
  61. 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
  62. 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
  63. Miller, M. B., and Bassler, B. L. (2001). Quorum sensing in bacteria. Annu. Rev. Microbiol., 55, 165-99.PubMedCrossRefGoogle Scholar
  64. Nishimura, R., Hayashi, M., Wu, G., Kouchi, H., Imaizumi-Anraku, H., et al. (2002). HAR1 mediates systemic regulation of symbiotic organ development. Nature, 420, 426-430PubMedCrossRefGoogle Scholar
  65. Normand, P., Orso, S., Cournoyer, B., Jeannin, P., Chapelon, C., et al. (1996). Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae. Int. J. Syst. Bacteriol., 46, 1-9.PubMedCrossRefGoogle Scholar
  66. 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 gene. Plant Physiol., 122, 1073-1079.PubMedCrossRefGoogle Scholar
  67. Parsons, R., Stanforth, A., Raven, J. A., and Sprent, J. I. (1993). Nodule growth and activity may be regulated by a feedback mechanism involving phloem nitrogen. Plant Cell Env., 16, 125-136.CrossRefGoogle Scholar
  68. Pawlowski, K., and Bisseling, T. (1996). Rhizobial and actinorhizal symbioses: What are the shared features? Plant Cell, 8, 1899-1913.PubMedCrossRefGoogle Scholar
  69. Pawlowski, K., Swensen, S., Guan, C., 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.PubMedCrossRefGoogle Scholar
  70. Penmetsa, R. V., and Cook, D. R. (1997). A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science, 275, 527-530.PubMedCrossRefGoogle Scholar
  71. Phillips, D. A. (2000). Biosynthesis and release of rhizobial nodulation gene inducers by legumes. In E. W. Triplett (Ed.), Prokaryotic nitrogen fixation: A model system for the analysis of a biological process (pp. 349-363). Wymondham, UK: Horizon Scientific Press.Google Scholar
  72. Pizelle, G. (1965). L’azote minéral et la nodulation de l’aulne glutineux (Alnus glutinosa). Observations sur des plantes cultivées avec systémes racinaires compartimentés. Bulletin de l’Ecole Nationale Supérieure Agronomique, 7, 55-63.Google Scholar
  73. Pizelle, G. (1966). L’azote minéral et la nodulation de l’aulne glutineux (Alnus glutinosa). II. Observations sur l’action inhibitrice de l’azote minéral á l’égard de la nodulation. Annales de l’Institut Pasteur, 111, 259-264.Google Scholar
  74. Prin, Y., and Rougier, M. (1986). Cytological and histochemical characterization of the axenic root surface of Alnus glutinosa. Can. J. Bot., 64, 2216-2226.CrossRefGoogle Scholar
  75. Pueppke, S. G., and Broughton, W. J. (1999). Rhizobiumsp. strain NGR234 and R. frediiUSDA257 share exceptionally broad, nested host-ranges. Mol. Plant-Microbe Interact., 12, 293-318.PubMedCrossRefGoogle Scholar
  76. Ramirez-Saad, H., Janse, J. D., and Akkermans, A. D. L. (1998). Root nodules of Ceanothus arboreus contain the N2-fixing Frankia endophyte and a phylogenetically related Nod-/Fix- actinomycete. Can. J. Microbiol., 44, 140-148.CrossRefGoogle Scholar
  77. Reddell, P., Yun, Y., and Shipton, W. A. (1997). Do Casuarina cunninghamiana seedlings dependent on symbiotic N2 fixation have higher phosphorus requirements than those supplied with adequate fertilizer nitrogen? Plant Soil, 189, 213-219.CrossRefGoogle Scholar
  78. Redondo-Nieto, M., Rivilla, R., El-Hamdaoui, A., Bonilla, I., and Bolaños, L. (2001). Boron deficiency affects early infection events in the pea-Rhizobium symbiotic interaction. Aust. J. Plant. Physiol., 28, 819-823.Google Scholar
  79. Ritchie, N. J., and Myrold, D. D. (1999b). Phylogenetic placement of uncultured Ceanothus microsymbionts using 16S rRNA gene sequences. Can. J. Bot., 77, 1208-1213.CrossRefGoogle Scholar
  80. Rodelas, B., Lithgow, J. K., Wisniewski-Dye, F., Hardman, A., Wilkinson, A., et al. (1999). Analysis of quorum-sensing-dependent control of rhizosphere-expressed (rhi) genes in Rhizobium leguminosarum bv. viciae. J. Bacteriol., 181, 3816-3823.PubMedGoogle Scholar
  81. Scheres, B., van Engelen, F., van der Knaap, E., van de Wiel, C., van Kammen, A., and Bisseling, T. (1990). Sequential induction of nodulin gene expression in the developing pea nodule. Plant Cell, 2, 687-700.PubMedCrossRefGoogle Scholar
  82. Searle, I. R., Men, A. E., Laniya, T. S., Buzas, D. M., Iturbe-Ormaetxe, I., et al. (2003). Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science, 299, 109-112.PubMedCrossRefGoogle Scholar
  83. Sequerra, J., Capellano, A., Faure-Raynard, M., and Moiroud, A. (1993). Root hair infection process and myconodule formation on Alnus incana by Penicillium nodositatum. Can. J. Bot., 72, 955-962.Google Scholar
  84. Smolander, A., and Sundman, V. (1987). Frankia in acid soils of forests devoid of actinorhizal plants. Physiol. Plant., 70, 297-303.CrossRefGoogle Scholar
  85. Soltis, D. E., Soltis, P. S., Morgan, D. R., Swensen, S. M., Mullin, B. C., et al. (1995). Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc. Natl. Acad. Sci. U.S.A., 92, 2647-2651.PubMedCrossRefGoogle Scholar
  86. Spaink, H. (2000). Root nodulation and infection factors produced by rhizobial bacteria. Annu. Rev. Microbiol., 54, 257-88.PubMedCrossRefGoogle Scholar
  87. Swensen, S. (1996). The evolution of actinorhizal symbioses: Evidence for multiple origins of the symbiotic association. Am. J. Bot., 83, 1503-1512.CrossRefGoogle Scholar
  88. Swensen, S. M., and Mullin, B. C. (1997). Phylogenetic relationships among actinorhizal plants. The impact of molecular systematics and implications for the evolution of actinorhizal symbiosis. Physiol. Plant., 99, 565-573.CrossRefGoogle Scholar
  89. Thomas, K. A., and Berry, A. M. (1989). Effects of continuous nitrogen application and nitrogen preconditioning on nodulation and growth of Ceanothus griseus var. horizontalis. Plant Soil, 118, 181-187.CrossRefGoogle Scholar
  90. Tjepkema, J. D. (1978). The role of oxygen diffusion from the shoots and nodule roots in nitrogen fixation by root nodules of Myrica galeL. Can. J. Bot., 61, 2898-2909.Google Scholar
  91. Torrey, J. G. (1990). Cross-inoculation groups within Frankia and host-endosymbiont associations. In C. R. Schwintzer and J. D. Tjepkma (Eds.), The biology ofFrankiaand actinorhizal plants (pp. 83-106). San Diego, CA: Academic Press.Google Scholar
  92. Tsai, S. M., and Phillips, D. A. (1991). Flavonoids released naturally from alfalfa promote development of symbiotic Glomusspores in vitro. Appl. Environ. Microbiol., 57, 1485-1488.PubMedGoogle Scholar
  93. Valverde, C. (2000). La simbiosis Discaria trinervis-Frankia.Regulación de la nodulación radicular. Ph.D. thesis. Facultad de Ciencias exactas, Universidad Nacional de La Plata, La Plata, Argentina.Google Scholar
  94. Valverde, C., and Wall, L. G. (1999a). Time course of nodule development in Discaria trinervis (Rhamnaceae)-Frankia symbiosis. New Phytol., 141, 345-354.CrossRefGoogle Scholar
  95. Valverde, C., and Wall, L. G. (1999b). Regulation of nodulation in Discaria trinervis (Rhamnaceae)- Frankia symbiosis. Can. J. Bot., 77, 1302-1310.CrossRefGoogle Scholar
  96. Valverde, C., and Wall, L. G. (2002). Nodule distribution on the roots of actinorhizal Discaria trinervis (Rhamnaceae) in pots. Environ. Exp. Bot., 47, 95-100CrossRefGoogle Scholar
  97. Valverde, C., and Wall, L. G. (2003). The regulation of nodulation, nitrogen fixation and ammonium assimilation under a carbohydrate shortage stress in the Discaria trinervis-Frankia symbiosis. Plant Soil, 254, 139-153.CrossRefGoogle Scholar
  98. Valverde, C., Ferrari, A., and Wall, L. G. (2002). Phosphorus and the regulation of nodulation in the actinorhizal symbiosis between Discaria trinervis(Rhamnaceae) and FrankiaBCU110501. New Phytol., 153, 43-52CrossRefGoogle Scholar
  99. Valverde, C., Wall, L. G., and Huss-Danell, K. (2000). Regulation of nodulation and nodule mass relative to nitrogenase activity and nitrogen demand in seedlings of Discaria trinervis (Rhamnaceae). Symbiosis, 28, 49-62.Google Scholar
  100. van Ghelue, M., Løvaas, E., Ringø, E., and Solheim, B. (1997). Early interactions between Alnus glutinosa and Frankia strain ArI3. Production and specificity of root hair deformation factor(s). Physiol. Plant., 99, 579-587.CrossRefGoogle Scholar
  101. Wall, L. G., and Huss-Danell, K. (1997). Regulation of nodulation in Alnus-Frankia symbiosis. Physiol. Plant., 99, 594-600.CrossRefGoogle Scholar
  102. Wall, L. G. (2000). The actinorhizal symbiosis. J. Plant Growth Reg., 19, 167-182Google Scholar
  103. Wall, L. G., Chaia, E., Valverde, C., and Lucki, G. (2000a). Specificity in Discaria-Frankiasymbioses. In F. O. Pedrosa, M. Hungria, M. G. Yates, and W. E. Newton (Eds.), Nitrogen fixation: From molecules to crop productivity(pp. 461-462). Dordrecht, The Netherlands: Kluwer Academic.Google Scholar
  104. Wall, L. G., Hellsten, A., and Huss-Danell, K. (2000b). Nitrogen, phosphorous, and the ratio between them affect nodulation in Alnus incana and Trifolium pratense. Symbiosis, 29, 91-105Google Scholar
  105. Wall, L. G., Valverde, C., and Huss-Danell, K. (2003). Regulation of nodulation in the absence of N2 is different in actinorhizal plants with different infection pathways. J. Exp. Bot., 385, 1253-1258.CrossRefGoogle Scholar
  106. Werner, D. (1992). Symbiosis of plants and microbes. London, UK: Chapman and Hall.Google Scholar
  107. Wolters, D. J. (1998). IneffectiveFrankiain wet alder soil. Ph.D. thesis. Wageningen Agricultural University, Wageningen, The Netherlands.Google Scholar
  108. Wopereis, J., Pajuelo, E., Dazzo, F. B., Jiang, Q., Gresshoff, P. M., et al. (2000). Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J., 23, 97-114.PubMedCrossRefGoogle Scholar
  109. Yang, Y., Shipton, W. A., and Reddel, P. (1997). Effects of phosphorus supply on in vitro growth and phosphatase activity of Frankia isolates from Casuarina. Plant Soil, 189, 75-79.CrossRefGoogle Scholar
  110. Yang, Y. (1995). The effect of phosphorus on nodule formation and function in the Casuarina-Frankia symbiosis. Plant Soil, 176, 161-169.CrossRefGoogle Scholar

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© Springer 2007

Authors and Affiliations

  • L. G. Wall
    • 1
  • A. M. Berry
    • 2
  1. 1.Programa de Investigación Interacciones BiológicasUniversidad Nacional de QuilmesR. Sñenz Peña 180Argentina
  2. 2.Department of Environmental Horticulture One Shields AvenueUniversity of CaliforniaDavisU.S.A

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