Nitrogen Fixing Root Nodule Symbioses: Legume Nodules and Actinorhizal Nodules

Biotechnology Annual Review

Volumn 2, Issue C, 1996, Pages 151-184

  Pawlowski, Katharina ^a   Ribeiro, Ana ^a   Bisseling, Ton ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

actinorhiza; Frankia; legume; nodulin; Rhizobium; root hair deformation; root nodule; symbiotic nitrogen fixation

Indexed keywords

EID: 77956861904     PISSN: 13872656     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1387-2656(08)70009-7     Document Type: Article

References (239)

1. Heichel G.H., and Vance C.P. Legume nitrogen: symbiotic fixation and recovery by subsequent crops. In: Helsel Z.R. (Ed). Energy in Plant Nutrition and Pest Control (1987), Elsevier, Amsterdam 63-80
2. Paul E.A. Towards the year 2000: Directions for future nitrogen research. In: Wilson J.R. (Ed). Advances in Nitrogen Cycling in Agricultural Ecosystems (1988), CAB International, Wallingford, UK 417-425
3. Howard J.B., and Rees D.C. Nitrogenase-a nucleotide-dependent molecular switch. Ann Rev Biochem 63 (1994) 235-264
4. Shaw V.K., and Brill W.J. Isolation of an iron-molybdenum cofactor from nitrogenase. Proc Natl Acad Sci USA 74 (1977) 1493-1497
5. Burris R.H. Nitrogenases. J Biol Chem 266 (1991) 9339-9342
6. Bergman B., Johansson C., and Söderbäck E. The Nostoc-Gunnera symbiosis. New Phytologist 122 (1992) 379-400
7. Elmerich C., Zimmer W., and Vieille C. Associative nitrogen-fixing bacteria. In: Stacey G., Burris R.H., and Evans H.J. (Eds). Biological Nitrogen Fixation (1992), Chapman and Hall, New York 212-258
8. Okon Y., and Labandera-Gonzalez C.A. Agronomic applications of Azospirillum-an evaluation of 20 years worldwide field inoculation. Soil Biol Biochem 26 (1994) 1591-1601
9. In: Khush G.F., and Bennett J. (Eds). Nodulation and Nitrogen Fixation in Rice: Potentials and Prospects (1992), International Rice Research Institute, Manila
10. Hellriegl H. Welche Stickstoffquellen stehen der Pflanze zu Gebote?. Zeitschrift des Verbands für die Rübenzucker-Industrie des Deutschen Reiches 36 (1886) 863-877
11. Beyerinck M.W. Die Bakterien der Papilionaceen-Knöllchen. Bot Zeitung 46-50 (1888) 725-804
12. De Bruijn F.J. The unusual symbiosis between the diazotrophic stem-nodulating bacterium Azorhizobium caulinodans ORS571 and its host, the tropical legume Sesbania rostrata: plant and bacterial aspects. In: Kosuge T., and Nester E.W. (Eds). Plant-Microbe Interactions (1989), Macmillan, New York 457-493
13. Marvel D.J., Torrey J.G., and Ausubel F.M. Rhizobium symbiotic genes required for nodulation of legume and nonlegume hosts. Proc Natl Acad Sci USA 84 (1987) 1319-1323
14. Weeden N., Kneen B.E., and LaRue T.A. Genetic analysis of Sym genes and other nodule-related genes in Pisum sativum. In: Gresshoff P.M. (Ed). Nitrogen Fixation: Achievement and Objectives (1990), Chapman and Hall, New York 323-330
15. Caetano-Anollés G., and Gresshoff P.M. Plant genetic control of nodulation. Ann Rev Microbiol 45 (1991) 345-382
16. Kolchinsky A., Funke R., and Gresshoff P.M. Dissecting molecular mechanisms of nodulation: taking a leaf from Arabidopsis. Plant Molec Biol 26 (1994) 549-552
17. Carroll B.J., McNeil D.L., and Gresshoff P.M. Mutagenesis of soybean (Glycine max (L.) Merr.) and the isolation of nonnodulating mutants. Plant Sci 47 (1986) 109-114
18. Nutman P.S. Improving nitrogen fixation in legumes by plant breeding; the relevance of host selection experiments in red clover (Trifolium pratense L.) and subterranean clover (T. subterraneum L.). Plant Soil 82 (1984) 285-301
19. Häser A., Robinson D.L., Due G., and Vance C.P. A mutation in Vicia faba results in ineffective nodules with impaired bacteroid differentiation and reduced synthesis of late nodulins. J Exp Bot 43 (1992) 1397-1407
20. Landau-Ellis D., Angermuller S.A., Shoemaker R.C., and Gresshoff P.M. The genetic locus controlling supernodulation in soybean (Glycine max L.) co-segregates tightly with a cloned molecular marker. Molec Gen Genet 228 (1991) 221-226
21. Landau-Ellis D., and Gresshoff P.M. Supernodulating soybean mutant alleles nts382 and nts1007 show no recombination with the same restriction length polymorphism marker. Molec Plant Microbe Interact 5 (1992) 428-429
22. Kneen B.E., Weeden N.F., and LaRue T.A. Nonnodulating mutants of Pisum sativum (L.) cv Sparkle. J Hered 85 (1994) 129-133
23. Sánchez F., Padilla J.E., Péréz H., and Lara M. Control of nodulin genes in root-nodule development and metabolism. Ann Rev Plant Physiol Plant Molec Biol 42 (1991) 507-528
24. Verma D.P.S. Signals in root nodule organogenesis and endocytosis of Rhizobium. Plant Cell 4 (1992) 373-382
25. Franssen H.J., Vijn I., Yang W.-C., and Bisseling T. Developmental aspects of the Rhizobium-legume symbiosis. Plant Molec Biol 19 (1992) 89-107
26. Mylona P., Pawlowski K., and Bisseling T. Symbiotic nitrogen fixation. Plant Cell 7 (1995) 869-885
27. Van Kammen A. Suggested nomenclature for plant genes involved in nodulation and symbiosis. Plant Molec Biol Report 2 (1984) 43-45
28. Taylor E.R., Nie X.Z., MacGregor A.W., and Hill R.D. A cereal haemoglobin gene is expressed in seed and root tissues under anaerobic conditions. Plant Molec Biol 24 (1994) 853-862
29. Miao G.-H., and Verma D.P.S. Soybean nodulin-26 gene encoding a channel protein is expressed only in the infected cells of nodules and is regulated differently in roots of homologous and heterologous plants. Plant Cell 5 (1993) 781-794
30. Scheres B., Van de Wiel C., Zalensky A., Horvath B., Spaink H., Van Eck H., Zwartkruis F., Wolters A.M., Gloudemans T., van Kammen A., and Bisseling T. The ENOD12 product is involved in the infection process during pea-Rhizobium interaction. Cell 60 (1990) 281-294
31. Kouchi H., and Hata S. Isolation and characterization of novel cDNAs representing genes expressed at early stages of soybean nodule development. Molec Gen Genet 238 (1993) 106-119
32. Yang W.-C., Katinakis P., Hendriks P., Smolders A., de Vries F., Spee J., van Kammen A., Bisseling T., and Franssen H. Characterization of GmENOD40, a gene showing novel patterns of cell-specific expression during soybean nodule development. Plant J 3 (1993) 573-585
33. Nap J.P., and Bisseling T. Developmental biology of a plant-prokaryote symbiosis: the legume root nodule. Science 250 (1990) 948-954
34. Becana M., and Klucas R.V. Oxidation and reduction of leghemoglobin in root nodules of leguminous plants. Plant Physiol 98 (1992) 1217-1221
35. Fisher R.F., and Long S.R. Rhizobium-plant signal exchange. Nature 357 (1992) 655-660
36. Spaink H.P. Rhizobial lipopolysaccharides: Answers and questions. Plant Molec Biol 20 (1992) 977-986
37. Dénarié J., and Cullimore J. Lipo-oligosaccharide nodulation factors: a new class of signalling molecules mediating recognition and morphogenesis. Cell 74 (1993) 951-954
38. Roche P., Debellé F., Maillet F., Lerouge P., Truchet G., Dénarié J., and Promé J.-C. Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell 67 (1991) 1131-1143
39. Journet E.P., Pichon M., Dedieu A., de Billy F., Truchet G., and Barker D.G. Rhizobium meliloti Nod factors elicit cell-specific transcription of the ENOD12 gene in transgenic alfalfa. Plant J 6 (1994) 241-249
40. Okker R.J.H., Schlaman H.R.M., Spaink H.P., and Lugtenberg B.J.J. Function of nodulation genes of Rhizobium. Symbiosis 14 (1993) 283-295
41. Van Rhijn P., and Vanderleyden J. The Rhizobium-plant symbiosis. Microbiol Rev 59 (1995) 124-142
42. Peters N.K., Frost J.W., and Long S.R. A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233 (1986) 977-980
43. Goethals K., Van Montagu M., and Holsters M. Conserved motifs in a divergent nod box of Azorhizobium caulinodans ORS571 reveals a common structure in promoters regulated by LysR-type proteins. Proc Natl Acad Sci USA 89 (1992) 1646-1650
44. Lerouge P., Roche P., Faucher C., Maillet F., Truchet G., Promé J.-C., and Dénarié J. Symbiotic host specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344 (1990) 781-784
45. Spaink H.P., Sheely D.M., van Brussel A.A.N., Glushka J., York W.S., Tak T., Geiger O., Kennedy E.P., Reinhold V.N., and Lugtenberg B.J.J. A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354 (1991) 125-130
46. Van Brussel A.A.N., Bakhuizen R., Van Spronsen P.C., Spaink H.P., Tak T., and Lugtenberg B.J.J. Induction of preinfection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium. Science 257 (1992) 70-71
47. Horvath B., Heidstra R., Lados M., Moerman M., Spaink H.P., Prome J.-C., Van Kammen A., and Bisseling T. Induction of pea early nodulin gene expression by Nod factors of Rhizobium. Plant J 4 (1993) 727-733
48. Vijn I., Das Neves L., Van Kammen A., Franssen H., and Bisseling T. Nod factors and nodulation in plants. Science 260 (1993) 1764-1765
49. Stokkermans T.J.W., and Peters N.K. Bradyrhizobium elkanii lipooligosaccharide signal induce complete nodule structures on Glycine soja Siebold et Zucc. Planta 193 (1994) 413-420
50. Chandler M.R., Date R.A., and Roughley R.J. Infection and root nodule development in Stylosanthes species by Rhizobium. J Exp Bot 33 (1982) 47-57
51. Dreyfus B.L., Alazard D., and Dommergues Y.R. Stem-nodulating rhizobia. In: Klug M.C., and Reddy C.E. (Eds). Current Perspectives in Microbial Ecology (1986), American Society of Microbiology, Washington, DC 161-169
52. De Faria S.M., Hay G.T., and Sprent J.I. Entry of rhizobia into roots of Mimosa scabrella Bentham occurs between epidermal cells. J Gen Microbiol 134 (1988) 2291-2296
53. Fahraeus G. The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J Gen Microbiol 16 (1957) 374-381
54. Heidstra R., Geurts R., Franssen H., Spaink H.P., Van Kammen A., and Bisseling T. Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiol 105 (1994) 787-797
55. Cook D., Dreyer D., Bonnet D., Howell M., Nony E., and VandenBosch K. Transient induction of a peroxidase gene in Medicago truncatula precedes infection by Rhizobium meliloti. Plant Cell 7 (1995) 43-55
56. Scheres B., Van Engelen F., Van der Knaap E., Van de Wiel C., Van Kammen A., and Bisseling T. Sequential induction of nodulin gene expression in the developing pea nodule. Plant Cell 2 (1990) 687-700
57. Vijn I., Martinez-Abarca F., Yang W.-C., Das Neves L., Van Brussel A., van Kammen A., and Bisseling T. Early nodulin gene expression during Nod factor-induced processes in Vicia sativa. Plant J 8 (1995) 111-119
58. Goethals K., Leyman B., Van den Eede G., Van Montagu M., and Holsters M. An Azorhizobium caulinodans ORS571 locus involved in lipopolysaccharide production and nodule formation on Sesbania rostrata stems and roots. J Bacteriol 176 (1994) 92-99
59. Pichon M., Journet E.-P., de Billy F., Dedieu A., Huguet T., Truchet G., and Barker D.G. Rhizobium meliloti elicits transient expression of the early nodulin gene ENOD12 in the differentiating root epidermis of transgenic alfalfa. Plant Cell 4 (1992) 1199-1211
60. Csanadi G., Szecsi J., Kalo P., Kiss P., Endre G., Kondorosi A., Kondorosi E., and Kiss G.B. ENOD12, an early nodulin gene, is not required for nodule formation and efficient nitrogen fixation in alfalfa. Plant Cell 6 (1994) 201-213
61. Callaham D., and Torrey J.G. The structural basis for infection of root hairs of Trifolium repens by Rhizobium. Can J Bot 59 (1981) 1647-1664
62. Bakhuizen R. The Plant Cytoskeleton in the Rhizobium-Legume Symbiosis. PhD Thesis, Leiden University, Leiden, The Netherlands, 1988.
63. Turgeon B.G., and Bauer W.D. Ultrastructure of infection-thread development during the infection of soybean by Rhizobium japonicum. Planta 163 (1985) 328-349
64. Brewin N.J. Development of the legume root nodule. Ann Rev Cell Biol 7 (1991) 191-226
65. Kijne J.W. The Rhizobium infection process. In: Stacey G., Burris R.H., and Evans H.J. (Eds). Biological Nitrogen Fixation (1992), Chapman and Hall, New York 349-398
66. Dart P.J. The infection process. In: Quispel A. (Ed). Biology of Nitrogen Fixation (1974), North Holland Publishing Company, Amsterdam 381-429
67. VandenBosch K.A., Bradley D.J., Knox J.P., Perotto S., Butcher G.W., and Brewin N.J. Common components of the infection thread matrix and the intercellular space identified by immunochemical analysis of pea nodules and uninfected roots. EMBO J 8 (1989) 335-342
68. Rae A.L., Bontante-Fasolo P., and Brewin N.J. Structure and growth of infection threads in the legume symbiosis with Rhizobium leguminosarum. Plant J 2 (1992) 385-395
69. Yang W.-C., de Blank C., Meskiene I., Hirt H., Bakker J., van Kammen A., Franssen H., and Bisseling T. Rhizobium Nod factors reactivate the cell cycle during infection and nodule primordium formation, but the cycle is only completed in primordium formation. Plant Cell 6 (1994) 1415-1426
70. Newcomb W. A correlated light and electron microscopic study of symbiotic growth and differentiation in Pisum sativum root nodules. Can J Bot 54 (1976) 21630-21860
71. Newcomb W. Nodule morphogenesis and differentiation. Int Rev Cytol 13 (1981) S247-S297 (Suppl)
72. Tsien H.C., Dreyfus B.L., and Schmidt E.L. Initial stages in the morphogenesis of nitrogen-fixing stem nodules of Sesbania rostrata. Molec Gen Genet 206 (1983) 291-299
73. Schaede R. Die Knöllchen der adventiven Wasserwurzeln von Neptunia oleracea und ihre Bakteriensymbiose. Planta 31 (1940) 1-21
74. James E.K., Sprent J.I., Sutherland J.M., McInroy S.G., and Michin R.T. The structure of nitrogen fixing root nodules on the aquatic mimosoid legume Neptunia plena. Ann Bot 69 (1992) 173-180
75. Chandler M.R. Some observations on infection of Arachis hupogaea L. by Rhizobium. J Exp Bot 29 (1978) 749-755
76. Alazard D., and Duhoux E. Development of stem nodules in a tropical forage legume, Aeschynomene afraspera. J Exp Bot 41 (1990) 1199-1206
77. Libbenga K.R., and Bogers R.J. Root-nodule morphogenesis. In: Quispel A. (Ed). The Biology of Nitrogen Fixation (1974), North-Holland Publishing Company, Amsterdam 430-472
78. Asad S., Fang Y., Wycoff K.L., and Hirsch A.M. Isolation and characterization of cDNA and genomic clones of MsENOD40; transcripts are detected in meristematic cells of alfalfa. Protoplasma 183 (1994) 10-23
79. Matvienko M., van de Sande K., Yang W.-C., van Kammen A., Bisseling T., and Franssen H. Comparison of soybean and pea ENOD40 cDNA clones representing genes expressed during both early and late stages of nodule development. Plant Molec Biol 26 (1994) 487-493
80. Gresshoff P.M., and Delves A.C. Plant genetic approaches to symbiotic nodulation and nitrogen fixation in legumes. In: Blonstein A.D., and King P.J. (Eds). A Genetic Approach to Plant Biochemistry (1986), Springer, Heidelberg 159-206
81. Rolfe B.G., and Gresshoff P.M. Genetic analysis of legume nodule initiation. Ann Rev Plant Physiol Plant Molec Biol 39 (1988) 297-319
82. Libbenga K.R., and Harkes P.A.A. Initial proliferation of cortical cells in the formation of root nodules in Pisum sativum L. Planta 114 (1973) 17-28
83. Ardourel M., Demont N., Debellé F., Maillet F., de Billy F., Promé J.-C., Dénarié J., and Truchet G. Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell 6 (1994) 1357-1374
84. Hirsch A.M., Bhuvaneswari T.V., Torrey J.G., and Bisseling T. Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc Natl Acad Sci USA 86 (1989) 1244-1248
85. Cooper J.B., and Long S.R. Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 6 (1994) 215-225
86. Roth L.E., and Stacey G. Bacterium release into host cells of nitrogen-fixing soybean nodules: the symbiosome membrane comes from three sources. Euro J Cell Biol 49 (1989) 13-23
87. Perotto S., Donovan N., Droback B.K., and Brewin N.J. Differential expression of a glycosyl inositol phospholipid antigen on the peribacteroid membrane during pea nodule development. Molec Plant-Microbe Interact 8 (1995) 560-568
88. Mellor R.B., and Werner D. Peribacteroid membrane biogenesis in mature legume root nodules. Symbiosis 3 (1987) 89-114
89. Mellor R.B. Bacteroides in the Rhizobium-legume symbiosis inhabit a plant internal lytic compartment: implication for other microbial endosymbioses. J Exp Bot 40 (1989) 831-839
90. Kinnback A., Mellor R.B., and Werner D. α-Mannosidase II isoenzyme in the peribacteroid space of Glycine max root nodules. J Exp Bot 38 (1987) 1373-1377
91. Mellor R.B., Mšrschel E., and Werner D. Legume root response to symbiotic infection: enzymes of the peribacteroid space. Z Naturforsch 39 (1984) 123-125
92. Zhang Y., and Roberts D.M. Expression of soybean nodulin-26 in transgenic tobacco. Targeting to the vacuolar membrane and effects on floral and seed development. Molec Biol Cell 6 (1995) 109-117
93. Kannenberg E.L., and Brewin N.J. Expression of a cell surface antigen from Rhizobium leguminosarum 3841 is regulated by oxygen and pH. J Bacteriol 171 (1989) 4543-4548
94. Hirsch A.M., and Smith C.A. Effects of Rhizobium meliloti nif and fix mutants on alfalfa root nodule development. J Bacteriol 169 (1987) 1137-1146
95. Van de Wiel C., Scheres B., Franssen H., van Lierop M.J., van Lammeren A., van Kammen A., and Bisseling T. The early nodulin transcript ENOD2 is located in the nodule parenchyma (inner cortex) of pea and soybean root nodules. EMBO J 9 (1990) 1-7
96. Vasse J., de Billy F., Camut S., and Truchet G. Correlation between ultrastructural differentiation of bacteroides and nitrogen fixation in alfalfa nodules. J Bacteriol 172 (1990) 4295-4306
97. Yang W.-C., Horvath B., Hontelez J., van Kammen A., and Bisseling T. In situ localization of Rhizobium mRNAs in pea root nodules: nifA and nifH localization. Molec Plant-Microbe Interact 4 (1991) 464-468
98. De Maagd R.A., Yang W.-C., Goosen-de Roo L., Mulders I.H.M., Roest H.P., Spaink H.P., Bisseling T., and Lugtenberg B.J.J. Downregulation of expression of the Rhizobium leguminosarum outer membrane protein gene ropA occurs abruptly in interzone II-III of pea nodules and can be uncoupled from nif gene activation. Molec Plant-Microbe Interact 7 (1993) 276-281
99. Kardailsky I., Yang W.-C., Zalensky A., van Kammen A., and Bisseling T. The pea late nodulin gene PsNOD6 is homologous to the early nodulin genes PsENOD3/14 and is expressed after leghaemoglobin genes. Plant Molec Biol 23 (1993) 1029-1037
100. 2 fixation: gene expression within the alfalfa root nodule. Proc Natl Acad Sci USA 92 (1995) 3759-3763
101. Pladys D., and Rigaud J. Senescence in French bean nodules: occurrence of different proteolytic activities. Physiol Plant 63 (1985) 43-48
102. Pladys D., and Vance C.P. Proteolysis during development and senescence of effective and plant gene-controlled ineffective alfalfa nodules. Plant Physiol 103 (1993) 379-384
103. Manen J.F., Simon P., van Slooten J.-C., Østerås M., Frutiger S., and Hughes G.J. A nodulin specifically expressed in senescent nodules of winged bean is a protease inhibitor. Plant Cell 3 (1991) 170-259
104. Garbers C., Meckbach R., Mellor R.B., and Werner D. Protease (thermolysin) inhibition in the peribacteroid space of Glycine max root nodules. J Plant Physiol 132 (1988) 442-445
105. Benson D.R., and Silvester W.B. Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 57 (1993) 293-319
106. Simonet P., Normand P., Hirsch A.M., and Akkermans A.D.L. The genetics of the Frankia actinorhizal symbiosis. In: Gresshoff P.M. (Ed). The Molecular Biology of Symbiotic Nitrogen Fixation (1990), CRC Press, Boco Raton, FL 77-109
107. Baker D.D., and Mullin B.C. Actinorhizal symbioses. In: Stacey G., Burns R.H., and Evans H.J. (Eds). Biological Nitrogen Fixation (1992), Chapman and Hall, New York 259-292
108. Meyen J. Über das Hervorwachsen parasitischer Gebilde aus den Wurzeln anderer Pflanzen. Flora 12 (1829) 49-64
109. Hiltner L. Über die Bedeutung der Wurzelknöllchen von Alnus glutinosa für die Stickstoffernährung dieser Pflanze. Landwirschaft Verständ Stud 46 (1985) 153-161
110. Krebber O. Untersuchungen über die Wurzelknöllchen der Erle. Arch Microbiol 3 (1932) 588-608
111. Schaede R. Über die Symbionten in den Knöllchen der Erle und des Sanddomes und die cytologischen Verhältnisse in ihnen. Planta 19 (1933) 389-416
112. Dawson J.O. Actinorhizal plants: their use in forestry and agriculture. Outl Agric 15 (1986) 202-208
113. Albouchi A. Comparative study of 2 young windbreaks of Cupressus sempervirens and Casuarina glauca. Ann Instit Nat Rech Agron Tunisie (1989) 74-83
114. Adegbehin J.O., Igboanugo A.B.I., and Omijeh J.E. Potentials of agroforestry for sustainable food and wood production in the savanna areas of Nigeria. Savanna 11 (1990) 12-26
115. Diem H.G., and Dommergues Y.R. Current and potential uses and management of Casuarinaceae in the tropics and subtropics. In: Schwintzer C.R., and Tjepkema J.D. (Eds). The Biology of Frankia and Actinorhizal Plants (1990), Academic Press, New York 317-342
116. El-Lakany M.H. Provenance trials of Casuarina glauca and C. cunninghamiana in Egypt. In: El-Lakany M.H., Turnbull J.W., and Brewbaker J.L. (Eds). Advances in Casuarina Research and Utilization (1990), American University in Cairo, Desert Development Center, Cairo 12-22
117. Skoupy J. The role of trees in agroforestry. Desert Cont Bull (UNEP) 19 (1991) 38-45
118. Sundararaju R., and Chinnathurai A.K. Technology packages for reclamation and development of wastelands. Indian Forester 118 (1992) 609-615
119. Puri S., Singh S., and Bhushan B. Evaluation of fuelwood quality of indigenous and exotic tree species of India's semiarid region. Agroforest Syst 26 (1994) 123-130
120. Sagwal S.S. Casuarina on farm: A plant of economic importance. Indian Farming 43 (1993) 12-14
121. AL. In: Williams S.T., Sharpe M.E., and Holt H.G. (Eds). Bergey's Manual of Systematic Bacteriology, vol 4 (1989), Williams and Wilkins, Baltimore, MD 2410-2417
122. Lechevalier M.P., and Lechevalier H.A. Systematics, isolation, and culture of Frankia. In: Schwintzer C.R., and Tjepkema J.D. (Eds). The Biology of Frankia and Actinorhizal Plants (1990), Academic Press, New York 35-60
123. Quispel A., Burggraaf A.J.P., Borsje H., and Tak T. The role of lipids in the growth of Frankia isolates. Can J Bot 61 (1983) 2801-2806
124. Quispel A., Svendsen A.B., Schripsema J., Baas W.J., Erkelens C., and Lugtenberg J. Identification of dipterocarpol as isolation factor for the induction of primary isolation of Frankia from root nodules of Alnus glutinosa (L.) Gaertner. Molec Plant-Microbe Interact 2 (1989) 107-112
125. Baker D.D. Relationships among pure cultured strains of Frankia based on host specificity. Physiol Plant 70 (1987) 245-248
126. Torrey J.G. Initiation and development of root nodules of Casuarina (Casuarinaceae). Am J Bot 63 (1976) 335-344
127. Berry A.M., McIntyre L., and McCully M.E. Fine structure of root hair infection leading to nodulation in the Frankia-Alnus symbiosis. Can J Bot 64 (1986) 292-305
128. Callaham D., Newcomb W., Torrey J.G., and Peterson R.L. Root hair infection in actinomycete-induced root nodule initiation in Casuarina, Myrica, and Comptonia. Bot Gaz 140 (1979) S1-S9 (Suppl)
129. Miller I.M., and Baker D.D. The initiation, development and structure of root nodules in Elaeagnus angustifolia L. (Elaeagnaceae). Protoplasma 128 (1985) 107-119
130. Liu Q., and Berry A.M. The infection process and nodule initiation in the Frankia-Ceanothus root nodule symbiosis: a structural and histochemical study. Protoplasma 163 (1991) 82-92
131. Racette S., and Torrey J.G. Root nodule initiation in Gymnostoma (Casuarinaceae) and Shepherdia (Elaeagnaceae) induced by Frankia strain HFPGpI1. Can J Bot 67 (1989) 2873-2879
132. Berry A.M., and Sunell L.A. The infection process and nodule development. In: Schwintzer C.R., and Tjepkema J.D. (Eds). The Biology of Frankia and Actinorhizal Plants (1990), Academic Press, New York 61-81
133. Burggraaf A.J.P., van der Linden J., and Tak T. Studies on the localization of infectible cells of Alnus glutinosa roots. Plant Soil 74 (1983) 175-188
134. Prin Y., and Rougier M. Preinfection events in the establishment of Alnus-Frankia symbiosis: Study of the root hair deformation step. Plant Physiol (Life Sci Adv) 6 (1987) 99-108
135. Berry A.M., and Torrey J.G. Root hair deformation in the infection process of Alnus rubra. Can J Microbiol 61 (1983) 2863-2976
136. Burgess D., and Peterson R.L. Development of Alnus japonica root nodules after inoculation with Frankia strain HFPArI3. Can J Bot 65 (1987) 1647-1657
137. Callaham D., and Torrey J.G. Prenodule formation and primary nodule development in roots of Comptonia (Myricaceae). Can J Microbiol 51 (1977) 2306-2318
138. Mian S., and Bond G. The onset of nitrogen fixation in young alder plants and its relation to differentiation in the nodular endophyte. New Phytologist 80 (1978) 187-192
139. Schwintzer C.R., Berry A.M., and Disney L.D. Seasonal patterns of root nodule growth, endophyte morphology, nitrogenase activity and shoot development in Myrica gale. Can J Bot 60 (1982) 746-757
140. Liu Q.Q., and Berry A.M. Localization and characterization of pectic polysaccharides in roots and root nodules of Ceanothus spp. during intercellular infection by Frankia. Protoplasma 163 (1991) 93-101
141. Sunell L.A., and Berry A.M. Preinfection cell wall formation in roots and developing nodules of Alnus rubra bong. Protoplasma 168 (1992) 87-93
142. Bond G. Root-nodule symbiosis with actinomycete-like organisms. In: Quispel A. (Ed). The Biology of Nitrogen Fixation (1974), North-Holland Publishing Company, Amsterdam 342-378
143. Silvester W.B., Harris S.L., and Tjepkema J.D. Oxygen regulation and hemoglobin. In: Schwintzer C.R., and Tjepkema J.D. (Eds). The Biology of Frankia and Actinorhizal Plants (1990), Academic Press, New York 157-176
144. Ribeiro A., Akkermans A.D.L., Van Kammen A., Bisseling T., and Pawlowski K. A nodule-specific gene encoding a subtilisin-like protease is expressed in early stages of actinorhizal nodule development. Plant Cell 7 (1995) 785-794
145. Lalonde M. Immunological and ultrastructural demonstration of nodulation of the European Alnus glutinosa (L.) Gaertn. host plant by an actinomycetal isolate from the North American Comptonia peregrina (L.) Coult) root nodule. Bot Gaz 140 S (1979) 35-43
146. Fontaine M.F., Lancelle S.A., and Torrey J.G. Initiation and ontogeny of vesicles in cultured Frankia spp. strain HFPArI3. J Bacteriol 160 (1984) 921-927
147. Huss-Danell K., and Bergman B. Nitrogenase in Frankia from root nodules of Alnus incana (L.) Moench: Immunolocalization of the Fe- and MoFe-proteins during vesicle differentiation. New Phytologist 116 (1990) 443-455
148. Pawlowski K., Akkermans A.D.L., van Kammen A., and Bisseling T. Expression of Frankia nif genes in actinorhizal nodules of Alnus glutinosa. Plant Soil 170 (1995) 371-376
149. Séguin A., and Lalonde M. Expression of actinorhizins in the development of the Frankia-Alnus symbiosis. In: Polsinelli M., Materassi R., and Vincenzini M. (Eds). Developments in Plant and Soil Sciences: Nitrogen Fixation (1991), Kluwer Academic Publishers, Dordrecht 602-608
150. Fleming A.I., Wittenberg J.B., Wittenberg B.A., Dudman W.F., and Appleby C.A. The purification, characterization and ligand-binding kinetics of hemoglobins from root nodules of the nonleguminous Casuarina glauca-Frankia symbiosis. Biochim Biophys Acta 911 (1987) 209-220
151. Jacobsen-Lyon K., Østergaard-Jensen E., Jørgensen J.-E., Marcker K.A., Peacock J., and Dennis E. Symbiotic and nonsymbiotic hemoglobin genes of Casuarina glauca. Plant Cell 7 (1995) 213-223
152. Goetting-Minesky M.P., and Mullin B.C. Differential gene expression in an actinorhizal symbiosis: Evidence for a nodule-specific cysteine proteinase. Proc Natl Acad Sci USA 91 (1994) 9891-9895
153. Pawlowski K., Guan C., Ribeiro A., van Kammen A., Akkermans A.D.L., and Bisseling T. Genes involved in Alnus glutinosa nodule development. In: Kiss G.B., and Endre G. (Eds). Proceedings of the 1st European Nitrogen Fixation Conference (1994), Officina Press, Szeged 220-224
154. Twigg PG. Isolation of a Nodule-Specific cDNA Encoding a Putative Glycine-Rich Protein from Alnus glutinosa. PhD Dissertation, University of Tennessee, Knoxville, TN, USA 1993.
155. Tjepkema J.D., and Yocum C.S. Measurement of oxygen partial pressure within soybean nodules by oxygen microelectrodes. Planta 119 (1974) 351-360
156. Appleby C.A. Leghemoglobin and Rhizobium respiration. Ann Rev Plant Physiol 35 (1984) 443-2478
157. Witty J.F., Minchin F.R., Skøt L., and Sheely J.E. Nitrogen fixation and oxygen in legume root nodules. Oxford Surv Plant Cell Biol 3 (1986) 275-315
158. David M., Daveran M.L., Batut J., Dedieu A., Domergue O., Ghai J., Hertig C., Boistard P., and Kahn D. Cascade regulation of nif gene expression in Rhizobium meliloti. Cell 54 (1988) 671-683
159. Parsons R., and Day D.A. Mechanism of soybean nodule adaptation to different oxygen pressures. Plant Cell Environ 13 (1990) 501-512
160. Purcell L.C., and Sinclair T.R. Soybean (Glycine max) nodule physical traits associated with permeability responses to oxygen. Plant Physiol 103 (1993) 149-156
161. Denison R.F., and Kinraide T.B. Oxygen-induced membrane depolarizations in legume root nodules-possible evidence for an osmoelectrical mechanism controlling nodule gas permeability. Plant Physiol 108 (1995) 235-240
162. Vikman P.-A. The symbiotic vesicle is a major site for respiration in Frankia from Alnus incana root nodules. Can J Microbiol 38 (1992) 779-784
163. Bond G. Some features of root growth in nodulated plants of Myrica gale L. Ann Bot 16 (1952) 467-475
164. Silvester W.B., Silvester J.K., and Torrey J.G. Adaptation of nitrogenase to varying oxygen tension and the role of the vesicle in root nodules of Alnus incana subsp rugosa. Can J Bot 66 (1988) 1772-1779
165. Silvester W.B., Whitbeck J., Silvester J.K., and Torrey J.G. Growth, nodule morphology and nitrogenase activity of Myrica gale grown with roots at various oxygen levels. Can J Bot 66 (1988) 1762-1771
166. 2. Plant Soil 118 (1989) 97-109
167. Hafeez F., Akkermans A.D.L., and Chaudhary A.H. Observations on the ultrastructure of Frankia spp. in root nodules of Datisca cannabina L. Plant Soil 79 (1984) 383-402
168. Parsons R., Silvester W.B., Harris S., Gruijters W.T.M., and Bullivant S. Frankia vesicles provide inducible and absolute oxygen protection for nitrogenase. Plant Physiol 83 (1987) 728-731
169. Meesters T.M., Van Vliet W.M., and Akkermans A.D.L. Nitrogenase is restricted to the vesicles in Frankia strain EAN1pec. Physiol Plant 70 (1987) 267-271
170. Berry A.M., Harriot O.T., Moreau R.A., Osman S.F., Benson D.R., and Jones A.D. Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc Natl Acad Sci USA 90 (1993) 6091-6094
171. Berg R.H. Symbiotic vesicle ultrastructure in high pressure-frozen, freeze-substituted actinorhizae. Protoplasma 183 (1994) 37-48
172. Newcomb W., and Wood S.M. Morphogenesis and fine structure of Frankia (Actinomycetales): the microsymbiont of nitrogen-fixing actinorhizal root nodules. Int Rev Cytol 109 (1987) 1-88
173. Berg R.H., and McDowell L. Endophyte differentiation in Casuarina actinorhizae. Protoplasma 136 (1987) 104-117
174. Henry M.F. Étude ultrastructurale de l'endophyte présent dans les nodusités radiculaires de Myrica gale L. Bull Soc Bot France 124 (1977) 291-300
175. Berg R.H., and McDowell L. Cytochemistry of the wall of infected cells in Casuarina actinorhizae. Can J Bot 66 (1987) 2038-2047
176. Zeng S., Tjepkema J.D., and Berg R.H. Gas diffusion pathway in nodules of Casuarina cunninghamiana. Plant Soil 118 (1989) 119-123
177. Sellstedt A., Reddell P., Rosbrook P.A., and Ziehr A. The relations of haemoglobin and lignin-like compounds to acetylene reduction in symbiotic Casuarina. J Exp Bot 42 (1991) 1331-1337
178. Zeng S., and Tjepkema J.D. The wall of the infected cell may be the major diffusion barrier in nodules of Myrica gale L. Soil Biol Biochem 5 (1994) 633-639
179. 2. Plant Physiol 107 (1995) 1269-1275
180. 2-reactive heme content of actinorhizal nodules and the roots of some nonnodulating plants. Plant Soil 100 (1987) 225-236
181. Sellstedt A., Reddell P., and Rosbrook P.A. The occurrence of haemoglobin and hydrogenase in nodules of 12 Casuarina-Frankia symbiotic associations. Physiol Plant 82 (1991) 458-464
182. Pathirana S.M., and Tjepkema J.D. Purification of hemoglobin from the actinorhizal root nodules of Myrica gale L. Plant Physiol 107 (1995) 827-831
183. Hadfield K.L., and Bulen W.A. Adenosine triphosphate requirement of nitrogenase from Azotobacter vinelandii. Biochem 8 (1969) 5103-5108
184. Wilson P.W., and Umbreit W.W. Mechanism of symbiotic nitrogen fixation. III. Hydrogen as specific inhibitor. Arch Microbiol 8 (1937) 440-457
185. Emerich D.W., Ruiz-Argüeso T., Ching T.M., and Evans H.J. Hydrogen dependent nitrogenase activity and ATP-formation in Rhizobium japonicum bacteroides. J Bacteriol 137 (1979) 153-160
186. 2-uptake-positive strains of Rhizobium japonicum in an atmosphere supplied with hydrogen gas. Proc Natl Acad Sci USA 76 (1979) 1788-1792
187. De Vries W., Stam H., and Stouthamer A.H. Hydrogen oxidation and nitrogen fixation in rhizobia, with special attention focused on strain ORS571. Antonia van Leeuwenhoek 52 (1984) 85-96
188. Stam H., van Versefeld H., de Vries W., and Stouthamer A.H. Hydrogen oxidation and efficiency of nitrogen fixation in succinate-limited chemostate cultures of Rhizobium ORS571. Arch Microbiol 139 (1984) 53-60
189. Murry M.A., and Lopez M.F. Interaction between hydrogenase, nitrogenase and respiratory activities in a Frankia isolate from Alnus rubra. Can J Microbiol 35 (1989) 636-641
190. 2 Metabolism (1985), Elsevier, New York 3-11
191. -Rhizobium leguminosarum. Indian J Exp Bot 28 (1990) 427-429
192. +Rhizobium. Tropical Agriculture 7212 (1994) 182-187
193. Sørensen G.M., and Wyndaele R. Effect of transfer of symbiotic plasmids and of hydrogenase genes (hup) on symbiotic efficiency of Rhizobium leguminosarum strains. J Gen Microbiol 132 (1986) 317-324
194. -Bradyrhizobium japonicum strain 532C in Ontario soybean field trials. Can J Plant Sci 70 (1990) 661-666
195. Bedmar E.J., and Phillips D.A. Pisum sativum cultivar effects on hydrogen metabolism in Rhizobium. Can J Bot 62 (1983) 1682-1686
196. Truelsen T.A., and Wyndale R. Recycling efficiency in hydrogenase uptake positive strains of Rhizobium legumninosarum. Physiol Plant 62 (1984) 45-50
197. Saini I., Chander D.R., and Hagpal P. Uptake hydrogenase in fast-growing strains of Rhizobium spp. (Sesbania) in relation to nitrogen fixation. J Appl Bacteriol 62 (1987) 449-452
198. Boogerd F.C., Ferdinandy-Van Vlerken M.M.A., Mawadza C., Pronk A.F., Stouthamer A.H., and Van Verseveld H.W. Nitrogen fixation and hydrogen metabolism in relation to the dissolved oxygen tension in chemostat cultures of the wild-type and a hydrogenase-negative mutant of Azorhizobium caulinodans. Appl Environ Microbiol 60 (1994) 1859-1866
199. Huss-Danell K. The physiology of actinorhizal nodules. In: Schwintzer C.R., and Tjepkema J.D. (Eds). The Biology of Frankia and Actinorhizal Plants (1990), Academic Press, New York 129-156
200. Sellstedt A., and Lindblad P. Activities, occurrence, and localization of hydrogenase in free-living and symbiotic Frankia. Plant Physiol 92 (1990) 809-815
201. Schubert K.R. Products of biological nitrogen fixation in higher plants: synthesis, transport, and metabolism. Ann Rev Plant Physiol 37 (1986) 539-574
202. Sellstedt A., and Atkins C.A. Composition of amino compounds transported in xylem of Casuarina spp. J Exp Bot 42 (1991) 1493-1497
203. Yoneyama T., and Kondo M. Sesbania spp., Aeschynomene indica and Crotalaria spp. are amide-exporters. Soil Sci Plant Nutr 36 (1990) 689-693
204. Hirel B., Perrot-Rechenmann C., Maudinas B., and Gadal P. Glutamine synthetase in alder (Alnus glutinosa) root nodules. Purification, properties and cytoimmunochemical localization. Physiol Plant 55 (1982) 197-203
205. Brears T., Walker E.L., and Coruzzi G.M. A promoter sequence involved in cell-specific expression of the pea glutamine synthetase GS3A gene in organs of transgenic tobacco and alfalfa. Plant J 1 (1991) 235-244
206. Miao G.-H., Hirel B., Marsolier M.C., Ridge R.W., and Verma D.P.S. Ammonia-regulated expression of a soybean gene encoding cytosolic glutamine synthetase in transgenic Lotus corniculatus. Plant Cell 3 (1991) 11-22
207. Forde B.G., Day H.M., Turton J.F., Wen-jun S., Cullimore J.V., and Oliver J.E. Two glutamine synthetase genes from Phaseolus vulgaris L. display contrasting developmental and spatial patterns of expression in transgenic Lotus corniculatus plants. Plant Cell 1 (1989) 391-401
208. Hanks J.F., Tolbert N.E., and Schubert K.R. Localization of enzymes of ureide biosynthesis in peroxisomes and microsomes of nodules. Plant Physiol 68 (1981) 65-69
209. Nguyen T., Zelechowska M., Foster V., Bergmann H., and Verma D.P.S. Primary structure of the soybean nodulin-35 gene encoding uricase II localized in the peroxisomes of uninfected cells of nodules. Proc Natl Acad Sci USA 82 (1985) 5040-5044
210. Taté R., Patriarca E.J., Riccio A., Defez R., and Iaccarino M. Development of Phaseolus vulgaris root nodules. Molec Plant-Microbe Interact 7 (1994) 582-589
211. Vaughn K.C. Structural and cytochemical characterization of three specialized peroxisome types in soybean. Physiol Plant 64 (1985) 1-12
212. Selker J.M.L. Three-dimensional organization of uninfected tissue in soybean root nodules and its relation to cell specialization in the central region. Protoplasma 147 (1988) 178-190
213. Pate J.S., Gunning G.E.S., and Briarty L.G. Ultrastructure and functioning of the transport system of the leguminous root nodules. Planta 85 (1969) 11-34
214. Schubert K.R. Enzymes of purine biosynthesis and catabolism in Glycine max. Plant Physiol 86 (1981) 1115-1122
215. Atkins C.A. Ammonia assimilation and export of nitrogen from the legume nodule. In: Dilworth M., and Glenn A. (Eds). Biology and Biochemistry of Nitrogen Fixation (1991), Elsevier, Amsterdam 293-319
216. Martin F., Hirel B., and Gadal P. Purification and properties of ornithine carbamoyl transferase 1 from Alnus glutinosa root nodules. Z Pflanzenphysiol 111 (1983) 413-422
217. Blom J., Roelofsen W., and Akkermans A.D.L. Assimilation of nitrogen in root nodules of alder (Alnus glutinosa). New Phytologist 89 (1981) 321-326
218. Wheeler C.T., and Lawrie A.C. Nitrogen fixation in root nodules of alder and pea in relation to the supply of photosynthetic assimilates. In: Nutman P.S. (Ed). Symbiotic Nitrogen in Plants (1976), Cambridge University Press, Cambridge 497-509
219. Burgess D., and Peterson R.L. Effect of nutrient conditions on root nodule development in Alnus japonica. Can J Bot 65 (1987) 1658-1670
220. Wheeler C.T. The causation of the diurnal changes in nitrogen fixation in the nodules of Alnus glutinosa. New Phytologist 70 (1971) 487-495
221. 2 fixation: Limitation or exquisite adaptation. Ann Rev Plant Physiol Plant Molec Biol 42 (1991) 373-392
222. Wheeler C.T., Watts S.H., and Hillman J.R. Changes in carbohydrates and nitrogenase compounds in the root nodules of Alnus glutinosa in relation to dormancy. New Phytologist 95 (1983) 209-218
223. 14C-labeled organic substances between the roots and shoot of the nodulated legume. Plant Soil 17 (1962) 333-356
224. Morell M., and Copeland L. Sucrose synthase of soybean nodules. Plant Physiology 78 (1985) 149-154
225. Thummler F., and Verma D.P.S. Nodulin-100 of soybean is the subunit of sucrose synthase regulated by the availibility of free heme in nodules. J Biologic Chem 262 (1987) 14730-14736
226. Küster H., Frühling M., Perlick A.M., and Pühler A. The sucrose synthase gene is predominantly expressed in the root nodule tissue of Vicia faba. Molec Plant-Microbe Interact 6 (1993) 507-514
227. Vance C.P., Gregerson R.G., Robinson D.L., Miller S.S., and Gantt J.S. Primary assimilation of nitrogen in alfalfa nodules: molecular features of the enzymes involved. Plant Sci 101 (1994) 51-64
228. Weaver C.D., Shower N.H., Louis C.F., and Roberts D.M. Nodulin-26, a nodule specific symbiosome membrane protein from soybean, is an ion channel. J Biologic Chem 269 (1994) 17858-17862
229. 2 fixation. Plant Physiol 71 (1983) 652-657
230. 2-fixing endophyte of Alnus glutinosa. Physiol Plant 53 (1981) 289-294
231. Soltis D.E., Soltis P.S., Morgan D.R., Swensen S.M., Mullin B.C., Dowd J.M., and Martin P.G. Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc Natl Acad Sci USA 92 (1995) 2647-2651
232. Trinick M.J. Structure of nitrogen-fixing nodules formed by Rhizobium on roots of Parasponia andersonii Planch. Can J Microbiol 25 (1979) 565-578
233. Lancelle S.A., and Torrey J.G. Early development of Rhizobium-induced root nodules of Parasponia rigida. I. Infection and early nodule initiation. Protoplasma 123 (1984) 26-37
234. Lancelle S.A., and Torrey J.G. Early development of Rhizobium-induced root nodules of Parasponia rigida. II. Nodule morphogenesis and symbiotic development. Can J Bot 63 (1984) 25-35
235. Christensen T., Dennis E.S., Peacock J.W., Landsmann J., and Marcker K.A. Hemoglobin genes in nonlegumes: cloning and characterization of a Casuarina glauca hemoglobin gene. Plant Molec Biol 16 (1991) 339-344
236. Schlaman H.R.M., Spaink H.P., Okker R.J.H., and Lugtenberg B.J.J. Subcellular localization of the nodD gene product in Rhizobium leguminosarum. J Bacteriol 171 (1989) 4686-4693
237. Siqueira J.O., Nair M.G., Hammerschmidt R., and Safir G.R. Significance of phenolic compounds in plant-soil-microbial systems. Crit Rev Plant Sci 10 (1991) 63-121
238. Carlson R.W., Juan S.J., Bhat U.R., Glushka J., Spaink H.P., Wijfjes A.H.M., Van Brussel A.A.N., Stokkermans T.J.W., Peters N.K., and Stacey G. The structures and biological activities of the lipo-oligosaccharide nodulation signals produced by type-1 and type-2 strains of Bradyrhizobium japonicum. J Biologic Chem 168 (1993) 18372-18381
239. Price N.P.J., Relic B., Talmont F., Lewin A., Promé J.-C., and Broughton W.J. Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated. Molec Microbiol 6 (1992) 3575-3584