Rhizobium symbiosis: Nod factors in perspective

Plant Cell

Volumn 8, Issue 10, 1996, Pages 1885-1898

  Long, Sharon R ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RHIZOBIUM;

EID: 0030266347     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.8.10.1885     Document Type: Review

References (121)

1. + currents and cytoskeletal behavior. In Advances in Molecular Genetics of Plant-Microbe Interactions, M.J. Daniels, J.A. Downie, and A.E. Osbourn, eds (Dordrecht, The Netherlands: Kluwer Academic Publishing), pp 107-114.
2. Ardourel, M., Demont, N., Debellé, F., Maillet, F., de Billy, F., Promé, J.-C., Dénarié, J., and Truchet, G. (1994). 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, 1357-1374.
3. 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
4. Atkinson, E.M., Palcic, M.M., Hindsgaul, O., and Long, S.R. (1994). Biosynthesis of Rhizobium meliloti lipooligosaccharide Nod factors. NodA is required for an N-acyltransferase activity. Proc. Natl Acad Sci. USA 91, 8418-8422.
5. Barker, D., Bianchi, S., Blondon, F., Dattee, Y., Duc, G., Essad, S., Flament, T., Gallusci, T., Genier, G., Guy, P., Muel, X., Tourner, J., Dénarié, J., and Huguet, T. (1990). Medicago truncatula, a model plant for studying the molecular genetics of the Rhizobium-legume symbiosis. Plant Mol. Biol. Rep. 8, 40-49.
6. Barney, M., and Downie, J.A. (1993). Identification of the NodC protein in the inner but not the outer membrane of Rhizobium leguminosarum. Mol. Plant-Microbe Interact. 6, 669-672.
7. Bauer, P., Crespi, M.D., Szecsi, J., Allison, L.A., Schultze, M., Ratet, P., Kondorosi, E., and Kondorosi, A. (1994). Alfalfa ENOD12 genes are differentially regulated during nodule development by Nod factors and Rhizobium invasion. Plant Physiol. 105, 585-592.
8. Bec-Ferté, M.P., Krishnan, H.B., Promé, D., Savagnac, A., Pueppke, S.G., and Promé, J.-C. (1994). Structures of nodulation factors from the nitrogen fixing soybean symbiont Rhizobium fredii USDA257. Biochemistry 33, 11782-11788.
9. Bent, A.F. (1996). Plant disease resistance genes: Function meets structure. Plant Cell 8, 1757-1771.
10. Bloemberg, G.V., Kamst, E., Harteveld, M., van der Drift, K.M.G.M., Haverkamp, J., Thomas-Oates, J.E., Lugtenberg, B.J.J., and Spaink, H.P. (1995). A central domain of Rhizobium NodE protein mediates host specificity by determining the hydrophobicity of fatty acyl moieties of nodulation factors. Mol. Microbiol. 16, 1123-1136.
11. Bono, J.-J., Riond, J., Nicolaou, K.C., Bockovich, N.J., Estevez, V.A., Cullimore, J.V., and Ranjeva, R. (1995). Characterization of a binding site for chemically synthesized lipo-oligosaccharide NodRm factors in particulate fractions prepared from roots. Plant J. 7, 253-260.
12. Bourdineaud, J.-P., Bono, J.-J., Ranjeva, R., and Cullimore, J.V. (1995). Enzymatic radiolabeling to a high specific activity of legume lipo-oligosaccharidic nodulation factors from Rhizobium meliloti. Biochem. J. 306, 259-264.
13. Brewin, N.J. (1991). Development of the legume root nodules. Annu. Rev. Cell Biol. 7, 191-226.
14. Brewin, N.J., Downie, J.A., and Young, J. (1992). Nodule formation in legumes. In Encyclopedia of Microbiology, Vol. 3., J. Lederberg, ed (San Diego, CA: Academic Press), pp. 239-248.
15. Caetano-Annolés, G., and Gresshoff, P.M. (1991). Plant genetic control of nodulation. Annu. Rev. Microbiol. 45, 345-382.
16. Cardenas, L., Dominguez, J., Quinto, C., Lopez-Lara, I., Lugtenberg, B., Spaink, H., Rademaker, G., Haverkamp, J., and Thomas-Oates, J. (1995). Isolation, chemical structures and biological activity of the lipo-chitin oligosaccharide nodulation signals from Rhizobium etli. Plant Mol. Biol. 29, 453-464.
17. Carlson, R.W., Sanjuan, 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. (1993). The structures and biological activities of the lipo-oligosaccharide nodulation signals produced by type I and type II strains of Bradyrhizobium japonicum. J. Biol. Chem. 268, 18372-18381.
18. Carlson, R.W., Price, N., and Stacey, G. (1994). The biosynthesis of Rhizobial lipo-oligosaccharide nodulation signal molecules. Mol. Plant-Microbe Interact. 7, 684-695.
19. Cook, O., Dreyer, D., Bonnet, O., 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.
20. Cooper, J.B., and Long, S.R. (1994). Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 6, 215-225.
21. Cren, M., Kondorosi, A., and Kondorosi, E. (1995). NolR controls expression of the Rhizobium meliloti nodulation genes involved in the core Nod factor synthesis Mol. Microbiol. 15, 733-747.
22. Crespi, M.D., Jerkevitch, 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.
23. Csanádi, G., Szécsi, J., Kaló, P., Kiss, P., Endre, G., Kondorosi, A., Kondorosi, E., and Kiss, G.B. (1994). ENOD12, an early nodulin gene, is not required for nodule formation and efficient nitrogen fixation in alfalfa. Plant Cell 6, 201-213.
24. Dangl, J.L., Dietrich, R.A., and Richberg, M.H. (1996). Death don't have no mercy Cell death programs in plant-microbe interactions. Plant Cell 8, 1793-1807.
25. DeBoer, M., and Djordjevic, M. (1995). The inhibition of infection thread development in the cultivar-specific interaction of Rhizobium and subterranean clover is not caused by a hypersensitive response. Protoplasma 185, 58-71
26. de Bruijn, F.J., and Downie, J.A. (1991). Biochemical and molecular studies: Symbiotic nitrogen fixation. Curr. Opin. Biotechnol. 2, 184-192.
27. de Bruijn, F.J., Chen, R., Fujimoto, S.Y., Pinaev, A., Silver, D., and Szczyglowski, K. (1994). Regulation of nodulin gene expression. Plant Soil 161, 59-68.
28. De Jong, A.J., Heidstra, R., Spaink, H.P., Hartog, M.V., Meijer, E.A., Hendriks, T., Lo Schiavo, F., Terzi, M., Bisseling, T., Van Kammen, A., and De Vries, S.C. (1993). Rhizobium lipo-oligosaccharides rescue a carrot somatic embryo mutant. Plant Cell 5, 615-620.
29. Demont, N., Debellé, F., Aurelle, H., Dénarié, J., and Promé, J.-C. (1993). Role of the Rhizobium meliloti nodF and nodE genes in the biosynthesis of lipo-oligosaccharidic nodutation factors. J. Biol. Chem. 268, 20134-20142.
30. Demont, N., Ardourel, M., Maillet, F., Promé, D., Ferro, M., Promé, J.-C., and Dénarié, J. (1994). The Rhizobium meliloti regulatory nodD3 and syrM genes control the synthesis of a particular class of nodulation factors N-acylated by (omega-1)-hydroxylated fatty acids. EMBO J. 13, 2139-2149.
31. Dénarié, J., and Cullimore, J. (1993). Lipo-oligosaccharide nodulation factors: A new class of signaling molecules mediating recognition and morphogenesis. Cell 74, 951-954.
32. Dénarié, J., Debellé, F., and Rosenberg, C. (1992). Signaling and host range variation in nodulation. Annu Rev Microbiol. 46, 497-531.
33. Dockendorff, T.C., Sanjuan, J., Grob, P., and Stacey, G. (1994). NolA represses nod gene expression in Bradyrhizobium japonicum Mol. Plant-Microbe Interact. 7, 596-602.
34. Downie, J.A. (1994). Signaling strategies for nodulation of legumes by Rhizobia. Trends Microbiol. 2, 318-324.
35. Downie, J.A., and Surin, B. (1990). Either of two nod gene loci can complement the nodulation defect of a nod deletion mutant of Rhizobium leguminosarum bv. vociae. Mol. Gen. Genet. 222, 81-86.
36. Ehrhardt, D.W., Atkinson, E.M., and Long, S.R. (1992). Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science 256, 998-1000
37. Ehrhardt, D.W., Atkinson, E.M., Faull, K.F., Freedberg, D.I., Sutherlin, D.P., Armstrong, R., and Long, S.R. (1995). In vitro sulfotransferase activity of NodH, a nodulation protein of Rhizobium meliloti required for host-specific nodulation. J. Bacteriol. 177, 6237-6245.
38. Ehrhardt, D.W., Wais, H., and Long, S.R. (1996). Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85, 673-681
39. Fellay, R., Perret, X., Viprey, V., Broughton, W., and Brenner, S. (1995). Organization of host-inducible transcripts on the symbiotic plasmid of Rhizobium sp. MGR234. Mol. Microbiol. 16, 657-667.
40. Felle, H., Kondorosi, E., Kondorost, A., and Schultze, M. (1995). Nod signal-induced plasma membrane potential changes in alfalfa root hairs are differentially sensitive to structural modifications of the lipo-chitooligosaccharide. Plant J. 7, 939-947.
41. Firmin, J., Wilson, K., Carlson, R., Davies, A., and Downie, J.A. (1993). Resistance to nodulation of cv. Afghanistan peas is overcome by nodX, which mediates an O-acetylation of the Rhizobium leguminosarum lipo-oligosaccharide nodulation factor. Mol. Microbiol. 10, 351-360.
42. Fisher, R.F., and Long, S.R. (1992). Rhizobium-plant signal exchange. Nature 357, 655-660.
43. Fisher, R.F., and Long, S.R. (1993). Interactions of NodD at the nod box: NodD binds to two distinct sites on the same face of the helix and induces a bend in the DNA. J. Mol. Biol. 233, 336-348.
44. Folch-Mallol, J.L., Marroqui, S., Sousa, C., Manyani, H., Lopez-Lara, I.M., van der Drift, K.M.G.M., Haverkamp, J., Quinto, C., Gil-Serrano, A., Thomas-Oates, J., Spaink, H.P., and Megias, M. (1996). Characterization of Rhizobium tropici CIAT899 nodulation factors: The role of nodH and nodPQ genes in their sulfation. Mol. Plant-Microbe Interact. 9, 151-163.
45. Geelen, D., Leyman, B., Mergaert, P., Klarskov, K., Van Montagu, M., Geremia, R., and Holsters, M. (1995). NodS is a S-adenosyl-L-methionine-dependent methyltransferase that methylates chitooligosaccharides deacetylated at the non-reducing end. Mol. Microbiol. 17, 387-397.
46. Geiger, O., Thomas-Oates, J., Glushka, J., Spaink, H., and Lugtenberg, B.J.J. (1994). Phospholipids of Rhizobium contain nodE-determined highly unsaturated fatty acid moieties. J. Biol. Chem. 269, 11090-11097.
47. Gianinazzi-Pearson, V. (1996). Plant cell responses to arbuscular mycorrhizal fungi: Getting to the roots of the symbiosis. Plant Cell 8, 1871-1883.
48. Hammond-Kosack, K.E., and Jones, J.D.G. 1996. Resistance gene-dependent plant defense responses. Plant Cell 8, 1773-1791.
49. Handberg, K., and Stougaard, J. (1992). Lotus japonicus, an autogamous, diploid legume speaes for classical and molecular genetics. Plant J. 2, 487-496.
50. Handelsman, J., and Stabb, E.V. (1996). Biocontrol of soilborne plant pathogens. Plant Cell 8, 1855-1869.
51. Higashi, S. (1993). (Brady)Rhizobium-plant communications involved in infection and nodulation. J. Plant Res. 106, 201-211.
52. Hirsch, A.M. (1992). Developmental biology of legume nodulation. New Phytol. 122, 211-237
53. Hirsch, A.M., and Fang, Y. (1994). Plant hormones and nodulation: What's the connection? Plant Mol. Biol. 26, 5-9.
54. Horvath, B., Heidstra, R., Lados, M., Moerman, M., Spaink, H.P., Promé, J.-C., Van Kammen, A., and Bisseling, T. (1993). Lipooligosaccharides of Rhizobium induce infection-related early nodulin gene expression in pea root hairs. Plant J. 4, 727-733.
55. Jabbourit, S., Fellay, R., Talmont, F., Kamalaprija, P., Burgert, U., Rellc, B., Promé, J.-C., and Broughton, W. (1995). Involvement of nodS in N-methylation and nodU in 6-O-carbamoylation of Rhizobium sp. NGR234 Nod factors J. Biol. Chem. 270, 22968-22973
56. John, M., Röhrig, H., Schmidt, J., Wieneke, U., and Schell, J. (1993). Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase. Proc. Natl. Acad. Sci. USA 90, 625-629.
57. Journet, E., Pichon, M., Dedieu, A., de Billy, F., Truchet, G., and Barker, D. (1994). Rhizobium meliloti Nod factors elicit cell-specific transcription of the ENOD12 gene in transgenic alfalfa. Plant J. 6, 241-249.
58. Jürgens, G., Torres Ruiz, R.A., and Berleth, T. (1994). Embryonic pattern formation in flowering plants. Annu. Rev. Genet. 28, 351-371.
59. Kamst, E., van der Drift, K.M.G.M., Thomas-Oates, J.E., Lugtenberg, B.J.J., and Spaink, H.P. (1995). Mass spectrometric analysis of chitin oligosaccharides produced by Rhizobium NodC protein in Escherichia coli. J. Bacteriol. 177, 6282-6285.
60. Kijne, J.W., Bakhuizen, R., van Brussel, A.A.N., CanterCremers, H.C.J., Diaz, C.L., de Pater, B.S., Smit, G., Spaink, H.P., Swart, S., Wijffelman, C.A., and Lugtenberg, B.J.J. (1992). The Rhizobium trap: Root hair curling in root-nodule symbiosis. In Perspectives in Plant Cell Recognition, Society for Experimental Biology Seminar Series, Vol. 48 (Cambridge, UK: Cambridge University Press), pp. 267-284.
61. Kneen, B., Weeden, N.F., and LaRue, T.A. (1994). Non-nodulating mutants of Pisum sativum (L) cv. Sparkle. Heredity J. 85, 129-133.
62. Kondorosi, A. (1992). Regulation of nodulation genes in Rhizobia. In Molecular Signals in Plant-Microbe Communication, D P.S. Verma, ed (Boca Raton, FL: CRC Press), pp. 325-340.
63. Kurkdjian, A.C. (1995). Role of differentiation of root epidermal cells in Nod factor (from Rhizobium meliloti) induced root hair depolarization of Medicago sativa. Plant Physiol. 107, 783-790.
64. Landau-Ellis, D., and Gresshoff, P. (1994). The RFLP molecular marker closely linked to the supermodulation locus of soybean contains three inserts. Mol. Plant-Microbe Interact. 7, 432-433.
65. Lawson, C., Rolfe, B., and Djordjevic, M. (1995). Rhizobium inoculation induces condition-dependent changes in the flavonoid composition of root exudates in Trifolium subterraneum. Aust. J. Plant Physiol. 23, 93-101.
66. Lerouge, P., Roche, P., Faucher, C., Maillet, F., Truchet, G., Promé, J.-C., and Dénarié, J. (1990). Symbiotic host-specificity of Rhizobium meliloti is determined by a sulfated and acylated glucosamine oligosaccharide signal. Nature 344, 781-784
67. Libbenga, K.R., and Bogers, R.J. (1974). Root-nodule morphogenesis In The Biology of Nitrogen Fixation, A. Quispel, ed (Amsterdam: North-Holland Publishing Co.), pp. 430-472.
68. Löbler, M., and Hirsch, A. (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 root nodules. Plant Physiol. 103, 21-30.
69. Lopez-Lara, I.M., van den Berg, J.D.J., Thomas-Oates, J.E., Glushka, J., Lugtenberg, B.J.J., and Spaink, H.P. (1995). Structural identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti. Mol. Microbiol. 15, 627-638.
70. Meinke, D.W. (1995). Molecular genetics of plant embryogenesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 369-394.
71. Mergaert, J., Van Montagu, M., Promé, J.-C., and Holsters, M. (1993). Three unusual modifications, a D-arabinosyl, an N-methyl, and a carbamoyl group, are present on the Nod factors of Azorhizobium caulinodans ORS571 Proc Natl. Acad. Sci. USA 90, 1551-1555.
72. Mergaert, P., D'Haeze, W., Geelen, D., Promé, D., Van Montagu, M., Geremia, R., Promé, J.-C., and Holsters, M. (1995) Biosynthesis of Azorhizobium caulinodans Nod factors: Study of the activity of the NodABCS proteins by expression of the genes in Escherichia coli. J. Biol Chem. 270, 29217-29223.
73. Miller, J.E., Viands, D.R., and Larue, T.A. (1991) Inheritance of non-nodulating mutants of sweetclover. Crop Sci. 31, 948-952.
74. Nicolaou, N., Bockovich, N.J., Carcanague, D.R., Hummel, C.W., and Even, L.F. (1992). Total synthesis of the NodRm-IV factors, the Rhizobium nodulation signals. J. Am. Chem. Soc. 114, 8701-8702.
75. Pawlowski, K., and Bisseling, T. (1996). Rhizobial and actinorhizal symbioses: What are the shared features? Plant Cell 8, 1899-1913.
76. Peters, N.K., and Crist-Estes, D.K. (1989). Nodule formation is stimulated by the ethylene inhibitor aminoethoxyvinylglycine. Plant Physiol. 91, 690-693.
77. Philip-Hollingsworth, S., Orgambide, G.G., Bradford, J.J., Smith, D.K., Hollingsworth, R.I., and Dazzo, F.B. (1995). Mutation or increased copy number of nodE has no effect on the spectrum of chitolipooligosaccharide Nod factors made by Rhizobium leguminosarum bv trifolii. J. Biol. Chem. 270, 20968-20977.
78. Phillips, D.A., Dakora, F.D., Sande, E., Joseph, C.M., and Zon, J. (1994). Synthesis, release and transmission of alfalfa signals to rhizobial symbionts. Plant Soil 161, 69-80.
79. Pichon, M., Journet, E., de Billy, F., Huguet, T., Truchet, G., and Barker, D. (1994). ENOD12 gene expression as a molecular marker for comparing Rhizobium-dependent and -independent nodulation in alfalfa. Mol. Plant-Microbe Interact. 7, 740-747.
80. Poupot, R., Martinez-Romero, E., and Promé, J.-C. (1993). Nodulation factors from Rhizobium tropici are sulfated or nonsulfated chitopentasaccharides containing an N-methyt-N-acylglucosamine terminus. Biochemistry 32, 10430-10435.
81. Price, N., and Carlson, R. (1995). Rhizobial lipo-oligosaccharide nodulation factors: Multidimensional chromatographic analysis of symbiotic signals involved in the development of legume root nodules. Glycobiology 5, 233-242.
82. Price, N.P.J., Relic, B., Talmont, F., Lewin, A., Promé, D., Pueppke, S.G., Maillet, F., Dénarié, J., Promé, J.-C., and Broughton, W.J. (1992). Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulfated. Mol. Microbiol. 6, 3575-3584.
83. Relic, B., Perret, X., Estrada-Garcia, M.T., Kopcinska, J., Golinowski, W., Krishnan, H.B., Pueppke, S.G., and Broughton, W.J. (1994). Nod factors of Rhizobium are a key to the legume door. Mol. Microbiol. 13, 171-178.
84. Ridge, R. (1992) A model of legume root hair growth and Rhizobium infection. Symbiosis 14, 359-373.
85. Ridge, R. (1995). Micro-vesicles, pyriform vesicles and macro-vesicles associated with the plasma membrane in the root hairs of Vicia hirsuta after freeze-substitution. J Plant Res. 108, 636-638.
86. Rivilla, R., Sutton, J., and Downie, J.A. (1995). Rhizobium leguminosarum NodT is related to a family of outer-membrane transport proteins that includes TolC, PrtF, CyaE and AprF. Gene 161, 27-31.
87. Röhrig, H., Schmidt, J., Wieneke, U., Kondorosi, E., Barlier, I., Schell, J., and John, M. (1994). Biosynthesis of lipo-oligosaccharide nodulation factors: Rhizobium NodA protein is involved in N-acylation of the chitooligosaccharide backbone. Proc. Natl. Acad. Sci. USA 91, 3122-3126.
88. Röhrig, H., Schmidt, J., Walden, R., Czaja, I., Miklasevics, E., Wieneke, U., Schell, J., and John, M. (1995). Growth of tobacco protoplasts stimulated by synthetic lipo-chitooligosaccharides. Science 269, 841-843.
89. Sanchez, F., Cardenas, L., van Spronsen, P., Villanueva, M.A., Valdes, V., Guillen, G., Rongcai, M., Noguez, R., Dantan, E., Vidali, L., Perez, H., Hepler, P., and Quinto, C. (1996). Actin cytoskeleton expression and organization during root-nodule development. Plant Physiol. 111, S3.
90. Sanjuan, J., Carlson, R.W., Spaink, H.P., Bhat, U.R., Barbour, W.M., Glushka, J., and Stacey, G. (1992). A 2-O-methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum. Proc. Natl. Acad. Sci. USA 89, 8789-8793.
91. Sanjuan, J., Grob, P., Göttfert, M., Hennecke, H., and Stacey, G. (1994). NodW is essential for full expression of the common noduiation genes of Bradyrhizobium japonicum. Mol. Plant-Microbe Interact. 7, 364-369.
92. Savoure, A., Magyar, A., Pierre, M., Brown, S., Schultze, M., and Kondorosi, A. (1994). Activation of the cell cycle machinery and the isoflavonoid biosynthesis pathway by active Rhizobium meliloti Nod signal molecules in Medicago microcallus suspensions. EMBO J. 13, 1093-1102.
93. Schlaman, H.R.M., Okker, R.J.H., and Lugtenberg, B.J.J. (1992). Regulation of nodulation gene expression by NodD in Rhizobia. J. Bacteriol. 174, 5177-5182.
94. Schultze, M., Quiclet-Sire, B., Kondorosi, E., Virelizier, H., Glushka, J.N., Endre, G., Gero, S.D., and Kondorosi, A. (1992). Rhizobium meliloti produces a family of sulphated lipo-oligosaccharides exhibiting different degrees of plant host specificity. Proc. Natl Acad. Sci. USA 89, 192-196.
95. Schultze, M., Kondorosi, E., Ratet, P., Buire, M., and Kondorosi, A. (1994). Cell and molecular biology of Rhizobium-plant interactions. Int. Rev. Cytol. 156, 1-75
96. Schultze, M., Staehetin, C., Röhrig, H., John, M., Schmidt, J., Kondorosi, E., Schell, J., and Kondorosi, A. (1995). In vitro sulfotransferase activity of Rhizobium meliloti NodH protein: Lipochitooligosaccharide nodulation signals are sulfated after synthesis of the core structure. Proc. Natl. Acad. Sci. USA 92, 2706-2709.
97. Smit, G., de Koster, C.C., Schripsema, J., Spaink, H.P., van Brussel, A.A., and Kijne, J. (1995). Uridine, a cell division factor in pea roots. Plant Mol. Biol. 29, 869-873
98. Spaink, H.P. (1995). The molecular basis of infection and nodulation by Rhizobia: The ins and outs of sympathogenesis. Annu Rev Phytopathol. 33, 345-368
99. Spaink, H.P., and Lugtenberg, B.J.J. (1994) Role of rhizobial lipochitin oligosaccharide signal molecules in root nodule organogenesis. Plant Mol. Biol. 26, 1413-1422.
100. Spaink, H.P., Sheeley, 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. (1991). A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354, 125-130
101. Spaink, H.P., Wijfjes, A.H.M., van Vliet, T.B., Kijne, J.W., and Lugtenberg, B.J.J. (1993). Rhizobium lipo-polysaccharide signals and their role in plant morphogenesis: Are analogous lipophilic chitin derivatives produced by the plant? Aust J. Plant Physiol. 20, 381-392
102. Spaink, H.P., Bloemberg, G.V., van Brussel, A.A.N., Lugtenberg, B.J.J., van der Drift, K.M.G.M., Haverkamp, J., and Thomas-Oates, J.E. (1995). Host specificity of Rhizobium leguminosarum is determined by the hydrophobicity of highly unsaturated fatty acyl moieties of the nodulation factors. Mol. Plant-Microbe Interact. 8, 155-164.
103. Sprent, J. (1989). Which steps are essential for the formation of functional legume nodules? New Phytol 111, 129-153.
104. Stacey, G., Luka, S., Sanjuan, J., Banfalvi, Z., Nieuwkoop, A.J., Chun, J.Y., and Forsberg, L.S. (1994). NodZ, a unique host specific nodulation gene, is involved in the fucosylation of the lipooligosaccharide nodulation signal of Bradyrhizobium japonicum. J. Bacteriol. 176, 620-633.
105. Staehelin, C., Schultze, M., Kondorosi, E., and Kondorosi, A. (1995). Lipo-chitooligosaccharide nodulation signals from Rhizobium meliloti induce their rapid degradation by the host plant alfalfa. Plant Physiol. 108, 1607-1614.
106. Stokkermans, T., and Peters, N.K. (1994). Bradyrhizobium elkanii lipooligosaccharide signals induce complete nodule structures on Glycine soja Siebold et Zucc. Planta 193, 413-420.
107. Stokkermans, T., Ikeshita, S., Cohn, J., Carlson, R., Stacey, G., Ogawa, T., and Peters, N.K. (1995). Structural requirements of synthetic and natural product lipo-chitin oligosaccharides for induction of nodule primordia on Glycine soja. Plant Physiol. 108, 1587-1595.
108. Sutton, J., Lea, E., and Downie, J.A. (1994) The nodulation-signaling protein NodO from Rhizobium leguminosarum biovar viciae forms ion channels in membranes. Proc Natl. Acad. Sci. USA 91, 9990-9994.
109. Truchet, G., Camut, S., de Billy, F., Odorico, R., and Vasse, J. (1989). The Rhizobium legume symbiosis: Two methods to discriminate between nodules and other root derived structures. Protoplasma 149, 82-88.
110. Truchet, G., Roche, P., Lerouge, P., Vasse, J., Camut, S., de Billy, F., Promé, J.-C., and Dénarié, J. (1991). Sulphated lipooligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351, 670-673.
111. van Brussel, A., Bakhuizen, R., van Spronsen, P., Spaink, H., Tak, T., Lugtenberg, B., and Kijne, J. (1992). Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipooligosaccharides of Rhizobium. Science 257, 70-72.
112. van de Sande, K., Pawlowski, K., Czaja, I., Wieneke, U., Schell, J., Schmidt, J., Walden, R., Matvienko, M., Wellink, J., van Kammen, A., Franssen, H., and Bisselling, T. (1996). Modification of phytohormone response by a peptide encoded by ENOD40 of legumes and a nonlegume. Science 273, 370-373.
113. van Eijsden, R., Diaz, C., de Pater, B.S., and Kijne, J. (1995). Sugar-binding activity of pea (Pisum sativum) lectin is essential for heterologous infection of transgenic white clover hairy roots by Rhizobium leguminosarum biovar viciae. Plant Mol. Biol. 29, 431-439.
114. van Spronsen, P.V., Bakjuizen, R., van Brussel, A.A.N., and Kijne, J. (1994). Cell wall degradation during infection thread formation by the root nodule bacterium Rhizobium leguminosarum is a two-step process Eur. J. Cell Biol. 64, 88-94.
115. van Spronsen, P.V., van Brussel, A.A.N., and Kijne, J. (1995). Nod factors produced by Rhizobium leguminosarum biovar viciae induce ethylene-related changes in root cortical cells of Vicia sativa ssp nigra. Eur J. Cell Biol. 68, 463-469.
116. van Workum, W., van Brussel, A., Tak, T., Wijffelman, C., and Kijne, J. (1995). Ethylene prevents nodulation of Vicia sativa ssp. nigra by exopolysaccharide-deficient mutants of Rhizobium leguminosarum bv viciae. Mol. Plant-Microbe Interact. 8, 278-285.
117. Vijn, I., das Neves, L., Van Kammen, A., Franssen, H., and Bisseling, T. (1993). Nod factors and nodulation in plants. Science 260, 1764-1765
118. Vijn, I., Martinez-Abarca, F., Yang, W.C., das Neves, L., van Brussel, A., Van Kammen, A., and Bisseling, T. (1995a) Early nodulin expression during Nod factor induced processes in Vicia sativa. Plant J. 8, 111-119.
119. Vijn, I., Yang, W.-C., Pallisgard, N.E.O., Jensen, E.O., Van Kammen, A., and Bisseling, T. (1995b) VsENOD5, VsENOD12 and VsENOD40 expression during Rhizobium induced nodule formation on Vicia sativa roots. Plant Mol. Biol. 28, 1111-1119.
120. Wilson, C.W., 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.
121. Yang, W.-C., de Blank, C., Meskiene, I., Hirt, H., Bakker, J., Van Kammen, A., Franssen, H., and Bisseling, T. (1994). 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, 1415-1426.