Is the Legume Nodule a Modified Root or Stem or an Organ sui generis?

Critical Reviews in Plant Sciences

Volumn 16, Issue 4, 1997, Pages 361-392

  Hirsch, Ann M ^a   LaRue, Thomas A ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Boyce Thompson Institute for Plant Research   (United States)

Author keywords

Homology; Legume phylogeny; Nodule development; Regulatory genes

Indexed keywords

BRADYRHIZOBIUM; FRANKIA; PAPILIONOIDEAE; PARASPONIA; RHIZOBIACEAE;

EID: 0000544655     PISSN: 07352689     EISSN: None     Source Type: Journal    
DOI: 10.1080/713608153     Document Type: Article

References (143)

1. Allen, E. K., Allen, O. N., and Newman, A. S. 1953. Pseudonodulation of leguminous plants induced by 2-bromo-3,5-dichlorobenzoic acid. Am. J. Bot., 40: 429-435.
2. Allen, O. N. and Allen, E. K. 1940. Response of the peanut plant to inoculation with rhizobia, with special reference to morphological development of the nodules. Bot. Gaz., 102: 121-142.
3. Allen, O. N. and Allen, E. K. 1981. The Leguminosae. University of Wisconsin Press, Madison. MacMillan Publishing Co., London.
4. Allison, L. A., Kiss, G. B., Bauer, P., Poiret, M., Pierre, M., Savoure, A., Kondorosi, E., and Kondorosi, A. 1993. Identification of two alfalfa early nodulin genes with homology to members of the pea Enod-12 gene family. Plant Mol. Biol., 21: 375-380.
5. Al-Mallah, M. K., Davey, M. R., and Cocking, E. C. 1989. Formation of nodular structures on rice seedlings by rhizobia. J. Exp. Bot., 40: 473-476.
6. Akkermans, A. D. L. and Hirsch, A. M. 1997. A reconsideration of terminology in Frankia research: a need for congruence. Physiol. Plant., 96: 574-578.
7. Anonymous. 1979. Tropical legumes: Resources for the Future. National Academy of Sciences, Washington, D.C., 21-45.
8. Asad, S., Fang, Y., Wycoff, K. L., and Hirsch, A. M. 1994. Isolation and characterization of cDNA and genomic clones of MsENOD40; transcripts are detected in meristematic cells of alfalfa. Protoplasma, 183: 10-23.
9. Baron, C. and Zambryski, P.C. 1995. The plant response in pathogenesis, symbiosis, and wounding - variations on a common theme. Annu. Rev. Genet., 29: 107-129.
10. Bauer, P., Ratet, P., Crespi, M. D., Schultze, M., and Kondorosi, A. 1996. Nod factors and cytokinin induce similar cortical cell division, amyloplast deposition and MsEnod12A expression patterns in alfalfa roots. Plant J., 10: 91-105.
11. Baylis, G. T. S., McNabb, R. F. R., and Morrison, T. M. 1963. The mycorrhizal nodules of podocarps. Trans. Br. Mycol. Soc., 46: 378-384.
12. Bender, G. L., Goydych, W., Rolfe, B. G., and Nayudu, M. 1987. The role of Rhizobium conserved and host-specific nodulation genes in the infection of the non-legume Parasponia andersonii. Mol. Gen. Genet., 210: 299-306.
13. Berry, A. M. and Sunell, L. A. 1990. The infection process and nodule development. In: The Biology of Frankia and Actinorhizal Plants. Schwintzer, C. R. and Tjepkema, J. D., Eds., Academic Press, San Diego, 61-81.
14. Bogusz, D., Appleby, C. A., Landsman, J., Dennis, E. S., Trinick, M. J., and Peacock, W. J. 1988. Functioning hemoglobin genes in non-nodulating plants. Nature, 331: 178-180.
15. Bond, L. 1948. Origin and developmental morphology of root nodules of Pisum sativum. Bot. Gaz., 109: 411-134.
16. Bowman, J. L., Smyth, D. R., and Meyerowitz, E. M. 1989. Genes directing flower development in Arabidopsis. Plant Cell, 1: 37-52.
17. Brewin, N. J. 1991. Development of the legume root nodule. Annu. Rev. Cell Biol., 7: 191-226.
18. Bryan, J. A., Berlyn, G. P., and Gordon, J. C. 1996. Toward a new concept of the evolution of symbiotic nitrogen fixation in the Leguminosae. Plant Soil, 186: 151-159.
19. Caetano-Anollés, G. and Gresshoff, P. M. 1992. Plant genetic suppression of the nonnodulation phenotype of Rhizobium meliloti host range nodH mutants: gene-for-gene interaction in the alfalfa-Rhizobium symbiosis? Theor. Appl. Genet., 84: 624-632.
20. Caetano-Anollés, G., Goshi, P. A., and Gresshoff, P. M. 1993. Nodule morphogenesis in the absence of Rhizobium. In: New Horizons in Nitrogen Fixation. Palacios, R., Mora, J., and Newton, W. E., Eds. Kluwer Academic Publishers, Dordrecht 297-302.
21. Chandler, M. R. 1978. Some observations on the infection of Arachis hypogaea L. by Rhizobium. J. Exp. Bot., 29: 749-755.
22. Chandler, M. R., Date, R. A., and Roughley, R. J. 1982. Infection and root-nodule development in Stylosanthes species by Rhizobium. J. Exp. Bot., 33: 47-57.
23. Cheng, Y., Signer, E. R., and Hirsch, A. M. 1992. Nodules initiated by Rhizobium meliloti exopolysaccharide mutants lack a discrete, persistent nodule meristem. Plant Physiol., 98: 143-151.
24. Coba de la Peña, T., Frugier, F., McKhann, H. I., Bauer, P., Brown, S., Kondrosi, A., and Crespi, M. 1997. A carbonic anydrase gene is induced in the nodule primordium and its cell-specific expression is controlled by the presence of Rhizobium during development. Plant J., 11: 407-420.
25. Coen, E. S. and Meyerowitz, E. M. 1991. The war of the whorls: genetic interactions controlling flower development. Nature, 353: 31-37.
26. Cook, D., Dreyer, D., Bonnet, D., Howell, M., Nony, E., and VandenBosch, K. 1995. Transient induction of a peroxidase gene in Medicago truncatula precedes infection by Rhizobium meliloti. Plant Cell 7: 43-55.
27. Crespi M. D., Jurkevitch, E., Poiret, M., d-Aubenton-Carafa, Y., Petrovics, G., Kondorosi, E., and Kondorosi, A. 1994. enod40, a gene expressed during nodule organogenesis. codes for a non-translatable RNA involved in plant growth. EMBO J., 13: 5099-5112.
28. Dabydeen, S. and Sirju-Charran, G. 1990. The developmental anatomy of the root system in yam bean, Pachyrhizus erosus Urban. Ann. Bot., 66: 313-320.
29. Dart, P. J. 1977. Infection and development of leguminous nodules. In: A Treatise on Dinitrogen Fixation. Hardy, R. W. F., Ed. Wiley, New York, 367-472.
30. Dickstein, R., Bisseling, T., Reinhold, V. N., and Ausubel, F. M. 1988. Expression of nodule-specific genes in alfalfa root nodules blocked at an early stage of nodule development. Genes Dev., 2: 677-687.
31. Dickstein, R., Prusty, R., Peng, T., Ngo, W., and Smith, M. E. 1993. ENOD8, a novel early nodule-specific gene, is expressed in empty alfalfa nodules. Mol. Plant-Microbe Inter., 6: 715-721.
32. de Bruijn, F. J., Jing, Y., and Dazzo, F. B. 1995. Potential and pitfalls of trying to extend the symbiotic interactions of nitrogen-fixing organisms to presently nonnodulated plants, such as rice. Plant Soil, 174: 225-240.
33. de Faria, S. M., Sutherland, J. M., and Sprent, J. I. 1986a. A new type of infected cell in root nodules of Andira spp. (Leguminosae). Plant Sci., 45: 143-147.
34. de Faria, S. M., McInroy, S. G., and Sprent, J. I. 1986b. The occurrence of infected cells, with persistent infection threads, in legume root nodules. Can. J. Bot., 65: 553-558.
35. Doyle, J. J. 1994. Phylogeny of the legume family: An approach to understanding the origins of nodulation. Annu. Rev. Ecol. Syst., 25: 325-349.
36. Doyle, J. J. and Doyle, J. L. 1997. Phylogenetic perspectives on the origins and evolution of nodulation in the legumes and allies. In: NATO ASI Series, Vol. G 39. Biological Fixation of Nitrogen for Ecology and Sustainable Agriculture. Legocki, A., Bothe, H., and Pühler, A., Eds., Springer-Verlag, Berlin, 307-312.
37. -) obtained in pea (Pisum sativum L.) and fababean (Vicia faba L.). Plant Sci., 60: 215-222.
38. Dudley, M. E., Jacobs, T. W., and Long, S. R. 1987. Microscopic studies of cell divisions induced in alfalfa roots by Rhizobium meliloti. Planta, 171: 289-301.
39. Dudley, M. E. and Long, S. R. 1989. A nonnodulating alfalfa mutant displays neither root hair curling nor early cell division in response to Rhizobium meliloti. Plant Cell, 1: 65-72.
40. Ehrhardt, D. S., Atkinson, E. M., and Long, S. R. 1992. Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science, 256: 998-1000.
41. Ehrhardt D. W., Wais, R., and Long, S. R. 1996. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell, 85: 673-682.
42. Fang, Y. and Hirsch, A. M. Studies of ENOD40 genes in transgenic alfalfas and defining the cis-acting region involved in gene expression and induction by Nod factors and cytokinin. submitted for publication.
43. Franssen, J. J., Nap, J-P., Gloudemans, T., Stiekema, W., van Dam, H., Govers, F., Louwerse, J., van Kammen, A., and Bisseling T. 1987. Characterization of cDNA for nodulin-75 of soybean: a gene produced involved in early stages of root nodule development. Proc. Natl. Acad. Sci. U.S.A., 84: 4495-4499.
44. Fuller, F., Künstner, P. W., Nguyen, T., and Verma, D. P. S. 1983. Soybean nodulin genes: analysis of cDNA clones reveals several major tissue-specific sequences in nitrogen-fixing root nodules. Proc. Natl. Acad. Sci. U.S.A., 80: 2594-2598.
45. Fyson, A. and Sprent, J. I. 1980. A light and scanning electron microscopy study of stem nodules in Vicia faba L. J. Exp. Bot., 31: 1101-1106.
46. Gloudemans, T., Bhuvaneswari, T. V., Moerman, M., van Brussel, T., van Kammen, A., and Bisseling, T. 1989. Involvement of Rhizobium leguminosarum nodulation genes in gene expression in pea root hairs. Plant Mol. Biol., 12: 157-167.
47. Goethe, J. W., von. 1870. Versuch die Metamorphose der Pflanzen zu erklären. Ettinger, Gotha.
48. Goetting-Minesky, M. P. and Mullin, B. C. 1994. Differential gene expression in an actinorhizal symbiosis: evidence for a nodule-specific cysteine proteinase. Proc. Natl. Acad. Sci. U.S.A., 91: 9891-9895.
49. Govers, F., Nap, J.-P., van Kammen, A., and Bisseling, T. 1987. Nodulins in the developing nodule: an overview. Plant Physiol. Biochem., 25: 309-322.
50. Guinel, F. and LaRue, T. A. 1991. Light microscopy study of nodule initiation in Pisum sativum L. cv. Sparkle and its low-nodulation mutant E2 (sym5). Plant Physiol, 97: 1206-1211.
51. Harrier, L. A. 1995. Non-nodulating African Species of Acacia. Ph.D. thesis, University of Dundee, Dundee, Scotland.
52. Harrison, M. J. and Dixon, R. A. 1993. Isoflavonoid accumulation and expression of defense gene transcripts during the establishment of vesicular-arbuscular mycorrhizal associations in roots of Medicago truncatula. Mol. Plant-Microbe Inter., 6: 643-654.
53. Harrison, M. J. and Dixon, R. A. 1994. Spatial patterns of expression of flavonoid/isoflavonoid pathway genes during interactions between roots of Medicago truncatula and the mycorrhizal fungus Glomus versiforme. Plant J., 6: 9-20.
54. Heard, J. and Dunn, K. 1995. Symbiotic induction of a MADS-box gene during development of alfalfa root nodules. Proc. Natl. Acad. Sci. U.S.A., 92: 5273-5277.
55. Herendeen, P. S. and Dilcher, D. L. 1992. Advances in Legume Systematics, IV. The Fossil Record. Royal Botanic Gardens, Kew.
56. Hirsch, A. M. 1992. Tansley Review No. 40. Developmental biology of legume nodulation. New Phytol., 122: 211-237.
57. Hirsch, A. M., Bhuvaneswari, T. V., Torrey, J. G., and Bisseling, T. 1989. Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc. Natl. Acad. Sci. U.S.A., 86: 1244-1248.
58. Hirsch, A. M., Fang, Y., Asad, S., and Kapulnik, Y. 1997. The role of phytohormones in plant-microbe symbioses. Plant Soil, in press.
59. Holm, T. 1924. Apios luberosa Moench. Am. Mid. Natur., 9: 118-136.
60. Joshi, P. A., Caetano-Anollés, A., Graham, E. T., and Gresshoff, P. M. 1991. Ontogeny and ultrastructure of spontaneous nodules in alfalfa (Medicago sativum). Protoplasma, 162: 1-11.
61. Kamalay, J. C. and Goldberg, R. B. 1980. Regulation of structural gene expression in tobacco. Cell, 19: 935-946.
62. Kaplan, D. R. 1984. The concept of homology and its central role in the elucidation of plant systematic relationships. In: Cladistics: Perspectives on the Reconstruction of Evolutionary History. Duncan T. and Stuessy T. F., Eds., Columbia University Press, New York, 51-70.
63. Kaplan, D. R. 1989. Principles of Plant Morphology. Text for Plant Biology 107, University of California, Berkeley.
64. Koide, R. T. and Schreiner, R. P. 1992. Regulation of the vesicular-arbuscular mycorrhizal symbiosis. Annu. Rev. Plant Physiol. Plant Mol. Biol., 43: 557-581.
65. Kouchi, H. and Hata, S. 1993. Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol. Gen. Genet., 238: 106-119.
66. Kozik, A., Matvienko, M., Scheres, B., Paruvangada, V. G., Bisseling, T., van Kammen, A., Noel Ellis, T. H., LaRue, T, and Weeden, N. 1996. The pea early nodulin gene PsENOD7 maps in the region of linkage group I containing sym2 and leghaemoglobin. Plant Mol. Biol., 31: 149-156.
67. Krause, A., Sigrist, C. J. A., Dehning, I., Sommer H., and Broughton, W. J. 1994. Accumulation of transcripts encoding a lipid transfer-like protein during deformation of nodulation-competent Vigna unguiculata root hairs. Mol. Plant-Microbe Int., 7: 411-418.
68. 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.
69. 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.
70. Landsman, J., Dennis, E. S., Higgins, T. J. V., Appleby, C. A., Kortt, A. A., and Peacock, W. J. 1986. Common evolutionary origin of legume and non-legume plant hemoglobins. Nature, 324: 166-168.
71. LaRue, T. and Weeden, N. F. 1994. The symbiosis genes of the host. In: Proc. First European Nitrogen Fixation Conference. Kiss, G. B. and Endre, G., Eds., Officina Press, Szeged, 147-151.
72. Lawson, C. G. R, Djordjevic, M. A., Weinman, J. J., and Rolfe, B. G. 1994. Rhizobium inoculation and physical wounding result in the rapid induction of the same chalcone synthase copy in Trifolium subterraneum. Mol Plant-Microbe Inter., 7: 498-507.
73. Legocki, R. P. and Verma, D. P. S. 1979. A nodule-specific plant protein (nodulin-35) from soybean. Science, 205: 190-191.
74. Legocki, R. P. and Verma, D. P. S. 1980. Identification of ''nodule-specific" host proteins (nodulins) involved in the development of the Rhizobium-legume symbiosis. Cell 20: 153-163
75. Libbenga, K. R. and Bogers, R. J. 1974. Root-nodule morphogenesis. In: The Biology of Nitrogen Fixation. Quispel, A., Ed., North-Holland, Amsterdam, 430-472.
76. Libbenga, K. R. and Harkes, P. N. N. 1973. Initial proliferation of cortical cells in the formation of root nodules in Pisum sativum L. Planta, 114: 1728.
77. Libbenga, K. R., van Iren, F., Bogers, R. J., and Schraag-Lamers, M.F. 1973. The role of hormones and gradients in the initiation of cortex proliferation and nodule formation in Pisum sativum L. Planta, 114: 17-28.
78. 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.
79. Löbler, M. and Hirsch, A. M. 1993. A gene that encodes a proline-rich nodulin with limited homology to PsENOD12 is expressed in the invasion zone of Rhizobium meliloti-induced alfalfa nodules. Plant Physiol., 103: 21-30.
80. Long, S. R. 1992. Genetic analysis of Rhizobium nodulation. In: Biological Nitrogen Fixation. Stacey, G., Burns, R. H., and Evans, H. J., Eds., Chapman and Hall, New York, 560-597.
81. López-Lara, I. M., van Der Drift, K. M. G. M., van Brussel, A. A. N., Haverkamp, J., Lugtenberg, B. J. J., Thomas-Oates, J. E., and Spaink, H. P. 1995. Induction of nodule primordia on Phaseolus and Acacia by lipo-chitin oligosaccharide nodulation signals from broad-host-range Rhizobium strain GRH2. Plant Mol. Biol., 29: 465477.
82. Matvienko, M., van de Sande, K., Yang, W. C., van Kammen, A., Bisseling, T., and Franssen, H. 1994. Comparison of soybean and pea ENOD40 cDNA clones representing genes expressed during both early and late stages of nodule development. Plant Mol. Biol., 26: 487-493.
83. McIver, J., Djordjevic, M. A., Weinman, J. J., and Rolfe, B. G. 1993. Influence of Rhizobium leguminosarum biovar trifolii host-specific nodulation genes on the ontogeny of clover nodulation. Protoplasma, 172: 166-179.
84. McKhann, H. I. and Hirsch, A. M. 1994. Does Rhizobium avoid the host response? In: Bacterial Pathogenesis in Plants and Animals. Current Topics in Microbiology and Immunology. Dangl, J., Ed. Springer-Verlag, Berlin, 139-162.
85. McKhann, H. I., Paiva, N. L., Dixon, R. A., and Hirsch, A. M. 1997. Chalcone synthase transcripts are detected in alfalfa root hairs following inoculation with wild-type Rhizobium meliloti. Mol. Plant-Microbe Inter., 10: 50-58.
86. Meyerowitz, E. M. 1994. The genetics of flower development. Sci. Am., 271: 56-65.
87. Miller, I. M. and Baker, D. D. 1985. Initiation, development and structure of root nodules in Elaeagnus angustifolia L. (Elaeagnaceae). Protoplasma, 128: 107-119.
88. Moerman, M., Nap, J.-P, Govers, F., Schilperoort, R., van Kammen A., and Bisseling, T. 1987. Rhizobium nod genes are involved in the induction of two early nodulin genes in Vicia sativa root nodules. Plant Mol. Biol., 9: 171-179.
89. Musgrave, M. E. and Blackmon, W. J. 1995. Respiration in a new tuber crop, Apios americana. J. Am. Soc. Hort. Sci., 120: 656-660.
90. Mylona, P., Pawlowski, K., and Bisseling, T. 1995. Symbiotic nitrogen fixation. Plant Cell, 7: 869-885.
91. Ndoye, I., De Billy, F., Vasse, J., Dreyfus B., and Truchet, G. 1994. Root nodulation of Sesbania rostrata. J. Bacteriol., 176: 1060-1068.
92. Nutman, P. S. 1948. Physiological studies on nodule formation. I. The relation between nodulation and lateral root formation in red clover. Ann. Bot., 7: 81-96.
93. Nutman, P. S. 1949. Physiological studies on nodule formation. II. The influence of delayed inoculation on the rate of nodulation in red clover. Ann. Bot., 13: 261-283.
94. Papadopoulou, K., Roussis, A., and Katinakis, P. 1996. Phaseolus ENOD40 is involved in symbiotic and non-symbiotic organogenetic processes: expression during nodule and lateral root development. Plant Mol. Biol., 30: 403-417.
95. Patriarca, E. J., Taté, R., Fedorova, E., Riccio, A., Defez, R., and Iaccarino, M. 1996. Down-regulation of the Rhizobium ntr system in the determinate nodule of Phaseolus vulgaris identifies a specific developmental zone. Mol. Plant-Microbe Inter., 9: 243-251.
96. Pawlowski, K. and Bisseling, T. 1996. Rhizobial and actinorhizal symbiosis - what are the shared features? Plant Cell, 8: 1899-1913.
97. Phillips, D. A. 1992. Flavonoids: plant signals to soil microbes. In: Recent Advances in Phytochemistry. Vol. 26. Phenolic Metabolism in Plants. Stafford, H. A. and Ibrahim, R. K., Eds., Plenum Press, New York, 201-231.
98. Phillips, D. A., Joseph, C. M., and Maxwell, C. A. 1992. Trigonelline and stachydrine released from alfalfa seeds activate NodD2 protein in Rhizobium meliloti. Plant Physiol., 99: 1526-1531.
99. Phillips, D. A. and Teuber, L. R. 1992. Plant genetics of symbiotic nitrogen fixation. In: Biological Nitrogen Fixation. Stacey, G., Bums, R. H., and Evans, H. J., Eds. Chapman and Hall, New York, 625-647.
100. Pichon, M., Journet, E. P., Dedieu, A., de Billy, F., Truchet, G., and Barker, D. G. 1992. Rhizobium meliloti elicits transient expression of the early nodulin gene ENOD12 in the differentiated root epidermis of transgenic alfalfa. Plant Cell, 4: 1199-1211.
101. Price, G. D., Mohaptra, S. S., and Gresshoff, P. M. 1984. Structure of the nodules formed by Rhizobium strain ANU289 in the nonlegume Parasponia and the legume siratro (Macroptilium atropurpureum). Bot. Gaz., 145: 444-451.
102. Racette, S. and Torrey, J. G. 1989. Root nodule initiation in Gymnostoma (Casuarinaceae) and Shepherdia (Elaeagnaceae) induced by Frankia strain HFPGp11. Can. J. Bot., 67: 1873-2879.
103. Remane, A. 1952. Die Grundlagen des natürlichen Systems, der vergleichenden Anatomie und der Phylogenetik. Akademisch Verlagsgesellschaft, Leipzig.
104. Remy, W., Taylor, T. N., Hass, H., and Kerp, H. 1994. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Natl. Acad. Sci. U.S.A., 91: 11841-11843.
105. Ribeiro, A., Akkermans, A. D. L., van Kammen, A., and Bisseling, T. 1995. A nodule-specific gene encoding a subtilisin-like protease is expressed in early stages of actinorhizal nodule development. Plant Cell, 7: 785-794.
106. Ridge, R. W., Bender G. L., and Rolfe, B. G. 1992. Nodule-like structures induced on the roots of wheat seedlings by the addition of the synthetic auxin 2, 4-dichlorophenoxyacetic acid and the effects of microorganisms. Aust. J. Plant Physiol., 19: 481-492.
107. Sánchez, F., Quinto, C., Vasquez, M., Spaink, H., Wijffelman, C. A., Cevallos, M. A., de las Peñas, A., Campos, F., Padilla, J., and Lara, M. 1988. The symbiotic association of Phaseolus vulgaris and Rhizobium leguminosarum bv. phaseoli. In: Molecular Genetics of Plant-Microbe Interactions. Palacios, R. and Verma, D. P. S., Eds., APS Press, St. Paul, 370-370.
108. Sánchez, F., Padilla, J. E., Pérez, H., and Lara, M. 1991. Control of nodulin genes in root-nodule development and metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol., 42: 507-528.
109. 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. 1990a. The ENOD12 gene product is involved in the infection process during the pea-Rhizobium interaction. Cell, 60: 281-294.
110. Scheres, B., van Engelen F., van der Knaap, E., van de Wiel, C., van Kammen A., and Bisseling, T. 1990b. Sequential induction of nodulin gene expression in the developing pea nodule. Plant Cell, 2: 687-700.
111. Scheres, B., McKhann, H. I., Zalensky, A., Löbler, M., Bisseling, T., and Hirsch, A. M. 1992. The PsENOD12 gene is expressed at two different sites in Afghanistan pea pseudonodules induced by auxin transport inhibitors. Plant Physiol., 100: 1649-1655.
112. Schultze, M., Quiclet-Sire, G., Kondorosi, E., Virelizier, H., Glushka, J. N., Endre, G., Géro S. D., and Kondorosi, A. 1992. Rhizobium meliloti produces a family of sulfated lipooligosaccharides exhibiting different degrees of plant host specificity. Proc. Natl. Acad. Sci. U.S.A., 89: 191-196.
113. Schwarz-Sommer, Z., Huijser, P., Nacken, W., Saedler, H., and Sommer, H. 1990. Genetic control of flower development: homeotic genes in Antirrhinum majus. Science, 250: 931-936.
114. 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.
115. Smith, C. A., Skvirsky, R. C., and Hirsch, A. M. 1986. Histochemical evidence for the presence of a suberin-like compound in Rhizobium-induced nodules of the nonlegume Parasponia rigida. Can. J. Bot., 64: 1474-1483.
116. Soltis, D. E., Soltis, P. S., Morgan, D. R., Swenson, 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. U.S.A., 92: 2647-2651.
117. Sprent, J. I. 1989. Tansley Review No. 15. Which steps are essential for the formation of functional legume nodules? New Phytol., 111: 129-153.
118. Sprent, J. I. 1997. Co-evolution of legume-rhizobial symbioses: Is it essential for either partner? In: NATO ASI Series, Vol. G 39. Biological Fixation of Nitrogen for Ecology and Sustainable Agriculture. Legocki, A., Bothe, H. and Pühler, A., Eds., Springer-Verlag, Berlin, 313-316.
119. Sprent, J. I and Raven, J. A. 1992. Evolution of nitrogen-fixing symbioses. In: Biological Nitrogen Fixation. Stacey, G., Burns, R. H., and Evans, H. J., Eds., Chapman and Hall, New York, 461-496.
120. Swenson, S. M. 1996. The evolution of actinorhizal symbioses: evidence for multiple origins of the symbiotic association. Am. J. Bot., 83: 1503-1512.
121. Szczyglowski, K. and Legocki, A. B. 1990. Isolation and nucleotide sequence of cDNA clone encoding nodule-specific (hydroxy)proline-rich protein LENOD2 from yellow lupin. Plant Mol. Biol., 15: 361-363.
122. Torrey, J. G. 1976. Initiation and development of root nodules of Casuarina (Casuarinaceae). Am. J. Bot., 63: 335-344.
123. Torrey, J. G. and D. Callaham. 1978. Determinate development of nodule roots in actinomycete-induced root nodules of Myrica gale L. Can. J. Bot., 56: 1357-1364.
124. Torrey, J. G. and D. Callaham. 1979. Early nodule development in Myrica gale. Bot. Gaz., 140 (Suppl.): S10-S14.
125. Troll, W. 1937-1943. Vergleichende Morphologie der höheren Pflanzen. Bd. 1, 1-3. Teil. Gebrüder Borntraeger, Berlin.
126. Truchet, G., Barker, D. G., Camut, S., de Billy, F., Vasse, J., and Huguet, T. 1989. Alfalfa nodulation in the absence of Rhizobium. Mol. Gen. Genet., 219: 65-68.
127. Tsien, H. C., Dreyfus, B. L., and Schmidt, E. L. 1983. Initial stages in the morphogenesis of nitrogen-fixing stem nodules of Sesbania rostrata. J. Bacteriol., 156: 888-897.
128. Van Brussel, A. A. N., Bakuizen, R., van Spronsen, P. C., Spaink, H. P., Tak, T., Lugtenberg, B. J. J., and Kijne, J. W. 1992. Induction of preinfection thread structures in the leguminous host plant by mitogenic lipooligosaccharides of Rhizobium. Science 257: 70-72.
129. VandenBosch, K. A., Bradley, D., Knox, J. P., Perotto, S., Butcher, G. W., and Brewin, N. J. 1989. Common components of the infection thread matrix and the intercellular space identified by immunocytochemical analysis of pea nodules and uninfected roots. EMBO J., 8: 335-342.
130. VandenBosch, K. A., Noel, K. D., Kaneko, Y., and Newcomb, E. H. 1985. Nodule initiation elicited by noninfective mutants of Rhizobium phaseoil. J. Bacteriol., 162: 950-959.
131. Van de Sande K., Pawlowski, K., Czaja, I., Wieneke, U., Schell, J. Schmidt, J., Waiden, R., Matvienko, M., Wellink, J., van Kammen, A., Franssen, H., and Bisseling, T. 1996. Modification of phytohormone response by a peptide encoded by ENOD40 of legumes and a nonlegume. Science, 273: 370-373.
132. Van de Wiel, C., Scheres, B., Franssen, H., van Lierop, M.-J., van Lammeren, A., van Kammen, A., and Bisseling, T. 1990. The early nodulin transcript ENOD2 is located in the nodule parenchyma (inner cortex) of pea and soybean root nodules. EMBO J., 9: 1-7.
133. 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.
134. Van Kammen, A. 1984. Suggested nomenclature for plant genes involved in nodulation and symbiosis. Plant Mol. Biol. Rep., 2: 43-45.
135. Van Rhijn, P. and Vanderleyden, J. 1995. The Rhizobium-plant symbiosis. Microbiol. Rev., 59: 124-142.
136. Van Rhijn, P., Fang, Y., Galili, S., Shaul, O., Atzmon, N., Wininger, S., Eshed, Y., Lum, M., Li, Y., To, V., Kapulnik, Y., and Hirsch, A. M. 1997. Expression of early nodulin genes in alfalfa mycorrhizae indicates that signal transduction pathways used in forming arbuscular mycorrhizae and Rhizobium-induced nodules may be conserved. Proc. Natl. Acad. Sci. U.S.A., 94: 5467-5472.
137. Verma, D. P. S. 1992. Signals in root nodule organogenesis and endocytosis of Rhizobium. Plant Cell, 4: 373-382.
138. Verma, D. P. S. and Delauney, A. J. 1988. Root nodule symbiosis: nodulins and nodulin genes. In: Temporal and Spatial Regulation of Plant Genes. Verma, D. P. S. and Goldberg, R. B., Eds., Springer-Verlag, Vienna, 169-199.
139. Vijn, I., Martinez-Abarca, F., Yang, W.-C., das Neves, L., van Brussel, A., van Kammen A., and Bisseling, T. 1995. Early nodulin gene expression during Nod factor-induced processes in Vicia sativa. Plant J., 8: 111-119.
140. Volpin, H., Phillips, D. A., Okon, Y., and Kapulnik, Y. 1994. Suppression of an isoflavonoid phytoalexin defense response in mycorrhizal alfalfa roots. Plant Physiol., 108: 1449-1454.
141. Wilson, C. S., Long, F., Maruoka, E. M., and Cooper, J. B. 1994. A new proline-rich early nodulin from Medicago truncatula is highly expressed in nodule meristematic cells. Plant Cell, 6: 1265-1275.
142. Yang, W.-C., Katinakis, P., Hendriks, P., Smolders, A., de Vries, F., Spec, J., van Kammen, A., Bisseling T., and Franssen, H. 1993. Characterization of GmENOD40, a gene showing novel patterns of cell-specific expression during soybean nodule development. Plant J., 3: 573-585.
143. Young, J. P. W. and Johnson, A. W. B. 1989. The evolution of specificity in the legume-Rhizobium symbiosis. Trends Ecol. Evol., 4: 341-349.