Regulation of plant morphogenesis by lipo-chitin oligosaccharides

Critical Reviews in Plant Sciences

Volumn 15, Issue 5-6, 1996, Pages 559-582

  Spaink, Herman P ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Chitin; Host specificity; Nodulation; Organogenesis; Review

Indexed keywords

ANIMALIA; FABACEAE; RHIZOBIACEAE;

EID: 0001430226     PISSN: 07352689     EISSN: None     Source Type: Journal    
DOI: 10.1080/713608137     Document Type: Article

References (153)

1. Aderem, A. 1992. Signal transduction and the actin cytoskeleton: the roles of MARCKS and profilin. TIBS 17: 438-443.
2. + currents and on cytoskeletal behavior. In: Advances in Molecular Genetics of Plant-Microbe Interactions. III. p. 107-114. Daniels, M. J., Downie, J. A., and Osbourne, A. E., Eds., Kluwer: Dordrecht.
3. Ardourel, M., Lortet, G., Maillet, F., Roche, P., Truchet, G., Prome, J. C., and Rosenberg, C. 1995. In Rhizobium meliloti, the operon associated with the nod box n5 comprises nodL, noeA and noeB, three host-range genes specifically required for the nodulation of particular Medicago species. Mol. Microbiol. 17: 687-699.
4. Asad, S., Fang, Y. W., 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.
5. 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. U.S.A. 91: 8418-8422.
6. Baev, N., Endre, G., Petrovics, G., Banfalvi, Z., and Kondorosi, A. 1991. Six nodulation genes of nod box locus 4 in Rhizobium meliloti are involved in nodulation signal production: nodM codes for D-glucosamine synthetase. Mol. Gen. Genet. 228: 113-124.
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. Baureithel, K., Felix, G., and Boller, T. 1994. Specific, high-affinity binding of chitin fragments to tomato cells and membranes -Competitive inhibition of binding by derivatives of chitooligosaccharides and a Nod factor of Rhizobium. J. Biol. Chem. 269: 17931-17938.
9. 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.
10. Bibb, M. J., Biro, S., Motamedi, H., Collins, J. F., and Hutchinson, C. R. 1989. Analysis of the nucleotide sequence of the Streptomyces glaucescens tcm1 genes provide key information about the enzymology of polyketide antibiotic biosynthesis. EMBO J. 9: 2727-2736.
11. Bloemberg, G. V., Thomas-Oates, J. E., Lugtenberg, B. J. J., and Spaink, H. P. 1994. Nodulation protein NodL of Rhizobium leguminosarum O-acetylates lipo-oligosaccharides, chitin fragments and N-acetylglucosamine in vitro. Mol. Microbiol. 11: 793-804.
12. 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. 1995a. 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.
13. Bloemberg, G. V., Lagas, R., van Leeuwen, S., van der Marel, G., van Boom, J. H., Lugtenberg, B. J. J., and Spaink, H. P. 1995b. Substrate specificity and kinetic studies of nodulation protein NodL of Rhizobium leguminosarum. Biochemistry 34: 12712-12720.
14. 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-oligosaccharidic NodRm factors in particulate fractions prepared from roots. Plant J. 7: 253-260.
15. Bourdineaud, J. P., Bono, J. J., Ranjeva, R., and Cullimore, J. V. 1995. Enzymatic radiolabelling to a high specific activity of legume lipo-oligosaccharidic nodulation factors from Rhizobium meliloti. Biochem. J. 306: 259-264.
16. Brewin, N. J. 1991. Development of the legume root nodule. Ann. Rev. Cell Biol. 7: 191-226.
17. Bulawa, C. E. and Wasco, W. 1991. Chitin and nodulation. Nature(London) 353: 710.
18. Cardenas, L., Dominquez, J., Quinto, C., López-Lara, I. M., Lugtenberg, B. J. J., Spaink, H. P., Rademaker, G. J., Haverkamp, J., and Thomas-Oates, J. E. 1995. Isolation, chemical structure and biological activity of the lipo-chitin oligosaccharide nodulation signals from Rhizobium etli. Plant Mol. Biol. 29: 453-464.
19. Cardenas, L., Dominquez, J., Santana J., and Quinto, C. 1996. Role of the nodI and nodJ genes in the transport of Nod metabolism in Rhizobium etli. Gene in press.
20. Carlson, R. W., Sanjuan, J., Bhat, R., Glushka, J., Spaink, H. P., Wijfjes, A. H. M., van Brussel, A. A. N., Stokkermans, T. J. W., Peters, 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.
21. Carlson, R. W., Price, N. P. J., and Stacey, G. 1994. The biosynthesis of rhizobial lipooligosaccharide nodulation signal molecules. Mol. Plant-Microbe Int. 7: 684-695.
22. Cooper, J. A. 1987. Effects of cytochalasin and phalloidin on actin. J. Cell. Biol. 105: 1473-1478.
23. Cooper, J. B. and Long, S. R. 1994. Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 6: 215-225.
24. Crespi, M. D., Jurkevitch, E., Poiret, M., Daubentoncarafa, 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.
25. Csanadi, G., Szecsi, J., Kalo, 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.
26. de Boer, A. H., van Duijn, B., Giesberg, P., Wegner, J., Obermeyer, G., Köhler, G., and Linz, K. W. 1995. Laser micro-surgery: a versatile tool in plant (electro)physiology. Protoplasma 178: 1-10.
27. De Jong, A. J., Heidstra, R., Spaink, H. P., Hartog, M. V., Hendriks, T., Lo Schavio, F., Terzi, M., Bisseling, T., van Kammen, A., and de Vries, S. 1993. A plant somatic embryo mutant is rescued by rhizobial lipo-oligosaccharides. Plant Cell 5: 615-620.
28. Deiannino, N. I., Pueppke, S. G., and Ugalde, R. A. 1995. Biosynthesis of the Nod factor chito-oligosaccharide backbone in Rhizobium fredii is controlled by the concentration of UDP-N-acetyl-D-glucosamine. Mol. Plant-Microbe Int. 8: 292-301.
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 nodulation 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. Diaz, C. L., Spaink, H. P., Wijffelman, C. A., and Kijne, J. W. 1995. Genomic requirements of Rhizobium for nodulation of white clover hairy roots transformed with the pea lectin gene. Mol. Plant-Microbe Int. 8: 348-356.
33. 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 Int. 6: 715-721.
34. Downie, J. A. 1991. A nod of recognition. Curr. Opin. Biol. 1: 382-384.
35. Downie, J. A. 1994. Signalling strategies for nodulation of legumes by rhizobia. Trends. Microbiol. 2: 318-324.
36. Ehrhardt, D. W., Atkinson, E. M., Faull, K. F., Freedberg, D. L. 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.
37. 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.
38. Fellay, R., Perret, X., Viprey, V., Broughton, W. J., and Brenner, S. 1995. Organization of host-inducible transcripts on the symbiotic plasmid of Rhizobium sp NGR234. Mol. Microbiol. 16:657-667.
39. Felle, H. H., Kondorosi, E., Kondorosi, A., and Schultze, M. 1995. Nod signal-induced plasma membrane potential changes in alfalfa root hairs are differentially sensitive to structural modifications of the lipochitooligosaccharide. Plant J. 7: 939-947.
40. Fernández-López, M., D'Haeze, W., Mergaert, P., Verplancke, C., Promé, J.-C., Van Montagu, M., and Holsters, M. 1996. Role of nodI and nodJ in lipo-chitooligosaccharide secretion in Azorhizobium caulinodans and Escherichia coli. Mol. Microbiol. 20: 993-1000.
41. Firmin, J. L., Wilson, K. E., Carlson, R. W., Davies, A. E., and Downie, J. A. 1993. Resistance to nodulation of cv Afghanistan peas is overcome by nodX which mediates an O-acetylation of 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 (London) 357:655-660.
43. Folch-Mallol, J. L., Marroqui, S., Sousa, S., Manyani, H., López-Lara, I. M., van der Drift, K. M. G. M., Haverkamp, J., Quinto, C., Gil-Serrano, A., Thomas-Gates, J. E., Spaink, H. P., and Megias, M. 1996. Characterization of Rhizobium tropicii CIAT899 nodulation factors: the role of nodH and nodPQ genes in their sulphation. Mol. Plant-Microbe Int. 9: 151-163.
44. Franssen, H. J., Vijn, I., Yang, W. C., and Bisseling, T. 1992. Developmental aspects of the Rhizobium-legume symbiosis. Plant Mol. Biol. 19:89-107.
45. Gadella Jr., T. W. J., Jovin, T. M., and Clegg, R. M. 1993. Fluorescence lifetime imaging microscopy (FLIM): spatial resolution of microstructures on the nanosecond time scale. Biophys. Chem. 48: 221-239.
46. Geelen, D., Mergaert, P., Geremia, R. A., Goormachtig, S., Van Montagu, M., and Holsters, M. 1993. Identification of nodSUIJ genes in locus 1 of Azorhizobium caulinodans: evidence that nodS encodes a rnethyltransferase involved in Nod factor modification. Mol. Microbiol. 9: 145-154.
47. Geelen, D., Leyman, B., Mergaert, P., Klarskov, K., Vanmontagu, M., Geremia, R., and Holsters, M. 1995. NodS is an S-adenosyL-L-methionine-dependent methyltransferase that methylates chitooligosaccharides deacetylated at the non-reducing end. Mol. Microbiol. 17: 387-397.
48. Geiger, O., Spaink, H. P., and Kennedy, E. P. 1991. Isolation of the Rhizobium leguminosarum nodF nodulation protein: NodF carries a 4′-phosphopantetheine prosthetic group. J. Bacteriol. 173: 2872-2878.
49. Geremia, R. A., Mergaert, P., Geelen, D., Vanmontagu, M., and Holsters, M. 1994. The NodC protein of Azorhizobium caulinodans is an N-acetylglucosaminyltransferase. Proc. Natl. Acad. Sci. U.S.A. 91: 2669-2673.
50. Goormachtig, S., Valerio-Lepiniec, M., Szczyglowski, K., Van Montagu, M., Holsters, M., and de Bruijn, F. J. 1995. Use of differential display to identify novel Sesbania rostrata genes enhanced by Azorhizobium caulinodans infection. Mol. Plant-Microbe Int. 8: 816-824.
51. Göttfert, M. 1993. Regulation and function of rhizobial nodulation genes. FEMS Microbiol. Rev. 104: 39-64.
52. Handberg, K. and Stougaard, J. 1992. Lotus japonicus, an autogamus, diploid legume species for classical and molecular genetics. Plant J. 2: 487-496.
53. Haseloff, J. and Amos, B. 1995. GFP in plants. TIG 11: 328-329.
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. Heese-Peck, A., Cole, R. N., Borkhsenious, O. N., Hart, and Raikhel, N. V. 1995. Plant nuclear pore complex proteins are modified by novel oligosaccharides with terminal N-acetylglucosamine. Plant Cell 7: 1459-1471.
56. Heidstra, R., Geurts, R., Franssen, H., Spaink, H. P., van Kammen, A., and Bisseling, T. 1994. Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiol. 105: 787-797.
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. 1992. Developmental biology of legume nodulation. New Phytol. 122: 211-237.
59. Horvath, B., Heidstra, R., Lados, M., Moerman, M., Spaink, H. P., Promé, J.-C., van Kammen, A., and Bisseling, T. 1993. Induction of pea early nodulin expression by nod factors of Rhizobium. Plant J. 4: 727-733.
60. Ikeshita, S., Sakamoto, A., Nakahara, Y., and Ogawa, T. 1994. Synthesis of the root nodule-inducing factor NodRm-IV(C16: 2,S) of Rhizobium meliloti and related compounds. Tetrahedron Lett. 35: 3123-3126.
61. Jabbouri, S., Fellay, R., Talmont, F., Kamalaprija, P., Burger, U., Relic, B., Promé, J.-C., and Broughton, W.J. 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.
62. 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. U.S.A. 90: 625-629.
63. Journet, E. P., Pichon, M., Dedieu, A., Debilly, F., Truchet, G., and Barker, D. G. 1994. Rhizobium meliloti Nod factors elicit cell-specific transcription of the ENOD12 gene in transgenic alfalfa. Plant J. 6: 241-249.
64. 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.
65. Koncz, C., Nemeth, K., Redei, G., and Schell, J. 1992. T-DNA insertional mutagenesis in Arabidopsis. Plant Mol. Biol. 20: 963-976.
66. 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.
67. Kovacs, L. G., Balatti, P. A., Krishnan, H. B., and Pueppke, S. G. 1995. Transcriptional organization and expression of noIXWBTUV, a locus that regulates cultivar-specific nodulation of soybean by Rhizobium fredii USDA257. Mol. Microbiol. 17: 923-933.
68. Kozik, A., Heidstra, R., Horvath, B., Kulikova, O., Tikhonovich, I., Ellis, T. H. N., van Kammen, A., Lie, T. A., and Bisseling, T. 1995. Pea lines carrying sym1 or sym2 can be nodulated by Rhizobium strains containing nodX; sym1 and sym2 are allelic. Plant Sci. 108: 41-49.
69. Krishnan, H. B., Kuo, C. I., and Pueppke, S. G. 1995. Elaboration of flavonoid-induced proteins by the nitrogen-fixing soybean symbiont Rhizobium fredii is regulated by both nodD1 and nodD2, and is dependent on the cultivar-specificity locus, noIXWBTUV. Microbiology-UK. 141: 2245-2251.
70. Kurkdjian, A. C. 1995. Role of the differentiation of root epidermal cells in Nod factor (from Rhizobium meliloti)-induced root-hair depolarization of Medicago sativa. Plant Physiol. 107: 783-790.
71. Kuster, H., Schroder, G., Fruhling, M., Pich, U., Rieping, M., Schubert, I., Perlick, A. M., and Pühler, A. 1995. The nodule-specific VfENODGRP3 gene encoding a glycine-rich early nodulin is located on chromosome I of Vicia faba L and is predominantly expressed in the interzone II- III of root nodules. Plant Mol. Biol. 28: 405-421.
72. 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 sulphated and acylated glucosamine oligosaccharide signal. Nature (London) 344: 781-784.
73. Lerouge, P. 1994. Symbiotic host specificity between leguminous plants and rhizobia is determined by substituted and acylated glucosamine oligosaccharide signals. Glycobiology. 4: 127-134.
74. 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: 19-39.
75. Löbler, M. and Hirsch, A. M. 1993. A gene that encodes a prolm-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.
76. López-Lara, I. M., van den Berg, J. D. J., Thomas-Oates, J. E., Glushka, J., Lugtenberg, B. J. J., and Spaink, H. P. 1995a. Structural identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti. Mol. Microbiol. 15: 627-638.
77. Löpez-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. 1995b. 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: 465-477.
78. Löpez-Lara, I. M., Blok-Tip, L., Quinto, C., Garcia, M. L., Bloemberg, G. V., Lamers, G. E. M., Kafetzopoulos, D., Stacey, G., Lugtenberg, B. J. J., Thomas-Oates, J. E., and Spaink, H. P. 1996. NodZ of Bradyrhizobium extends the nodulation host range of Rhizobium by adding a fucosyl residue to nodulation factors. Mol. Microbiol. in press.
79. Marie, C., Barny, M. A., and Downie, J. A. 1992. Rhizobium leguminosarum has two glucosamine synthases, GlmS and NodM, required for nodulation and development of nitrogen- fixing nodules. Mol. Microbiol. 6: 843-851.
80. Matvienko, M., Vandesande, 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.
81. Mckay, I. A. and Djordjevic, M. A. 1993. Production and excretion of Nod metabolites by Rhizobium leguminosarum bv. trifolii are disrupted by the same environmental factors that reduce nodulation in the field. Appl. Env. Microbiol. 59: 3385-3392.
82. Mergaert, P., Van Montagu, M., Promé, J.-C., and Holsters, M. 1993. Three unusual modifications, a D-arabinosyl, a N-methyl, and a carbamoyl group, are present on the Nod factors of Azorhizobium caulinodans strain ORS571. Proc. Natl. Acad. Sci. U.S.A. 90: 1551-1555.
83. 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 NodABC proteins by expression of the genes in Escherichia coli. J. Biol. Chem. 270: 29217-29223.
84. Mergaert, P., D'Haeze, W., Fernández-López, M., Geelen, D., Goethals, K., Promé, J.-C., Van Montagu, M., and Holsters, M. 1996. Fucosylation and arabinosylation of Nod factors in Azorhizobium caulinodans: involvement of noIK as well as noeC and/or downstream genes. Mol. Microbiol. in press.
85. Mylona, P., Pawlowski, K., and Bisseling, T. 1995. Symbiotic nitrogen fixation. Plant Cell 7: 869-885.
86. Ndoye, I., Debilly, S. F., Vasse, J., Dreyfus, B., and Truchet, G. 1994. Root Nodulation of Sesbania Rostrata. J. Bacteriol. 176: 1060-1068.
87. Nicolaou, K. C., 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.
88. Orgambide, G. G., Lee, J., Hollingsworth, R. I., and Dazzo, F. B. 1995. Structurally diverse chitolipooligosaccharide nod factors accumulate primarily in membranes of wild-type Rhizobium leguminosarum biovar trifolii. Biochemistry 34: 3832-3840.
89. 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.
90. 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 differentiating root epidermis of transgenic alfalfa. Plant Cell 40: 1199-1211.
91. Pillon, E., Terzi, M., Baldan, B., Mariani, P., and Lo Schiavo, F. 1996. A protocol for obtaining embryogenic cell lines from Arabidopsis. Plant J. 9: 573-577.
92. Plazanet, C., Refregier, G., Demont, N., Truchet, G., and Rosenberg, C. 1995. The Rhizobium meliloti region located downstream of the nod box n6 is involved in the specific nodulation of Medicago lupulina. FEMS Microbiol. Lett. 133: 285-291.
93. Poupot, R., Martinez-Romero, E., Gautier, N., and Promé, J. C. 1995a. Wild-type Rhizobium etli, a bean symbiont, produces acetyl-fucosylated, N-methylated, and carbamoylated nodulation factors. J. Biol. Chem. 270: 6050-6055.
94. Poupot, R., Martinezromero, E., Maillet, F., and Promé, J. C. 1995b. Rhizobium tropici nodulation factor sulfation is limited by the quantity of activated form of sulfate. FEBS Lett. 368: 536-540.
95. Poupot, R., Martinez-Romero, E., and Promé, J.-C. 1993. Nodulation factors from Rhizobium tropici are sulfated or non-sulfated chitopentasaccharides containing an N-methyl-N-acylglucosaminyl terminus. Biochemistry 32: 10430-10435.
96. Price, N. P. J., Relic, B., Taimont, 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 sulphated. Mol. Microbiol. 6: 3575-3584.
97. Quinto, C., Wijfjes, A. H. M., Bloemberg, G. V., Blok-Tip, L., López-Lara, I. M., Lugtenberg, B. J. J., Thomas-Oates, J. E., and Spaink, H. P. 1996. In vitro enzymatic activity and substrate specificity of nodulation protein NodZ, a bacterial fucosyl transferase. Abstract 8th International Congress Molecular Plant-Microbe Interactions, Knoxville, Tennessee, U.S.A.
98. Relic, B., Talmont, F., Kopcinska, J., Golinowski, W., Promé, J. C., and Broughton, W. J. 1993. Biological activity of Rhizobium sp. NGR234 Nod-factors on Macroptilium atropurpureum. Mol. Plant-Microbe Int. 6: 764-774.
99. Relic, B., Perret, X., Estradagarcia, 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.
100. Ritsema, T., Geiger, O., Vandillewijn, P., Lugtenberg, B. J. J., and Spaink, H. P. 1994. Serine residue 45 of nodulation protein NodF from Rhizobium leguminosarum bv viciae is essential for its biological function. J. Bacteriol. 176: 7740-743.
101. Ritsema, T., Wijfjes, A. H. M., Lugtenberg, B. J. J., and Spaink, H. P. 1996. Rhizobium nodulation protein NodA is a host-specific determinant of the transfer of fatty acids in Nod factor biosynthesis. Mol. Gen. Genet. 251: 44-51.
102. Rivilla, R., Sutton, J. M., 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.
103. Roche, P., Debellé, F., Maillet, F., Lerouge, P., Faucher, C., Truchet, G., Dénarié, J., and Promé, J. C. 1991a. Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipooligosaccharides signals. Cell 67: 1131-1143.
104. Roche, P., Lerouge, P., Promé, J. C., Faucher, C., Vasse, J., Maillet, F., Camut, S., de Billy, F., Dénarié, J., and Truchet, G. 1991b. NodRm1, a sulfated lipo-oligosaccharide signal of Rhizobium meliloti elicits hair deformation, cortical cell division and nodule organogenesis on alfalfa roots. In:Advances In Molecular Genetics of Plant-Microbe Interactions. p. 119-126. Hennecke, H. and Verma, D. P. S. Kluwer Academic Publishers: Dordrecht.
105. Rosa, F., Sargent, T. D., Rebbert, M. L., Michaels, G. S., Jamrich, M., Grunz, H., Jonas, E., Winkles, J. A., and Dawid, I. B. 1988. Accumulation and decay of DG42 gene products follow a gradient pattern during Xenopus embryogenesis. Devel. Biol. 129: 114-123.
106. Roussis, A., Vandesande, K., Papadopoulou, K., Drenth, J., Bisseling, T., Franssen, H., and Katinakis, P. 1995. Characterization of the soybean gene GmENOD40-2. J. Exp. Bot. 46: 719-724.
107. Röhrig, H., Schmidt, J., Wieneke, U., Kondorosi, E., Barlier, I., Schell, J., and John, M. 1994. Biosynthesis of lipooligosaccharide nodulation factors -rhizobium-NodA protein is involved in Af-acylation of the chitooligosaccharide backbone. Proc. Natl. Acad. Sci. U.S.A. 91: 3122-3126.
108. 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.
109. Sandal, N. N. and Marcker, K. A. 1990. Some nodulin and Nod proteins show similarity to specific animal proteins. In: Nitrogen Fixation: Achievements and Objectives. p. 687-692. Gresshoff, P. M., Roth, L. E., Stacey, G., and Newton, W. E., Chapman and Hall: New York.
110. 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. U.S.A. 89: 8789-8793.
111. Sautter, C., Waldner, H., Neuhaus-Url, G., Galli, A., Neuhaus, G., and Potrykus, I. 1991. Micro-targeting: high-efficiency gene transfer using a novel approach for the acceleration of micro-projectiles. Biotechnology 9: 1080-1085.
112. Savouré, A., Magyar, Z., Pierre, M., Brown, S., Schultze, M., Dudits, D., Kondorosi, A., and Kondorosi, E. 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.
113. 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.
114. Scheres, B., van Engelen, F., van der Knaap, E., van der Wiel, C., van Kammen, A., and Bisseling, T. 1990b. Sequential induction of nodulin gene expression in the developing pea nodule. The Plant Cell 2: 687-700.
115. Schmidt, J., Röhrig, H., John, M., Wieneke, U., Stacey, G., Koncz, C., and Schell, J. 1993. Alteration of plants growth and development by Rhizobium nodA and nodB genes involved in the synthesis of oligosaccharide signal molecules. Plant J. 4: 651-658.
116. Schultze, M., Quiclet-Sire, B., Kondorosi, E., Virelizier, H., Glushka, J. N., Endre, G., Géro, S. D., and Kondorosi, A. 1992. Rhizobium meliloti produces a family of sulphated lipooligosaccharides exhibiting different degrees of plant host specificity. Proc. Natl. Acad. Sci. U.S.A. 89: 192-196.
117. 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.
118. Schultze, M., Staehelin, 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. U.S.A. 92: 2706-2709.
119. Schwedock, J. and Long, S. R. 1990. ATP sulfurylase activity of the nodP and nodQ gene products of Rhizobium meliloti. Nature (London) 348: 644-647.
120. Schwedock, J. S., Liu, C. X., Leyh, T. S., and Long, S. R. 1994. Rhizobium meliloti NodP and NodQ form a multifunctional sulfate-activating complex requiring GTP for activity. J. Bacteriol. 176: 7055-7064.
121. Scott, D. B., Young, C. A., Collins-Emerson, J. E., Terzaghi, E. A., Rockman, E. S., Lewis, P. E., and Pankhurst, C. E. 1996. Novel and complex chromosomal arrangement of Rhizobium loti nodulation genes. Mol. Plant-Microbe Int. 9: 187-197.
122. Semino, C. E. and Robbins, P. W. 1995. Synthesis of "Nod"-like chitin oligosaccharides by the Xenopus developmental protein DG42. Proc. Natl. Acad. Sci. U.S.A. 92: 3498-3501.
123. Semino, C. E., Specht, C. A., Raimondi, A., and Robbins, P. W. 1996. Homologs of the Xenopus development gene DG42 are present in zebrafish and mouse and are involved in the synthesis of Nod-like chitin oligosaccharides during early embryogenesis. Proc. Natl. Acad. Sci. U.S.A. 93: 4548-4553.
124. Smit, G., de Koster, C. C., Schripsema, J., Spaink, H. P., van Brussel, A. A. N., and Kijne, J. W. 1995. Uridine, a cell division factor in pea roots. Plant Mol. Biol. 29: 869-873.
125. Spaink, H. P., Weinman, J., Djordjevic, M. A., Wijffelman, C. A., Okker, R. J. H., and Lugtenberg, B. J. J. 1989. Genetic analysis and cellular localization of the Rhizobium host specificity- determining NodE protein. EMBO J. 8: 2811-2818.
126. Spaink, H. P., Sheeley, 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. 1991. A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature (London) 354: 125-130.
127. Spaink, H. P., Aarts, A., Stacey, G., Bloemberg, G. V., Lugtenberg, B. J. J., and Kennedy, E. P. 1992. Detection and separation of Rhizobium and Bradyrhizobium Nod metabolites using thin layer chromatography. Mol. Plant-Microbe Int. 5: 72-80.
128. Spaink, H. P., Wijfjes, A. H. M., van Vliet, T. B., Kijne, J. W., and Lugtenberg, B. J. J. 1993. Rhizobial lipo-oligosaccharide signals and their role in plant morphogenesis: are analogous lipophilic chitin derivatives produced by the plant ? Aust. J. Plant Physiol. 20: 381-392
129. Spaink, H. P., Bloemberg, G. V., Wijfjes, A. H. M., Ritsema, T., Geiger, O., López-Lara, I. M., Harteveld, M., Kafetzopoulos, D., van Brussel, A. A. N., Kijne, J. W., Lugtenberg, B. J. J., van der Drift, K. M. G. M., Thomas-Oates, J. E., Potrykus, I., and Sautter, C. 1994a. The molecular basis of host-specificity in the Rhizobium leguminosarum-plant interaction. In: Advances in Molecular Genetics of Plant-Microbe Interactions. 3. p. 91-98. Daniels, M. J., Downie, J. A., and Osbourn, A. E., Eds., Kluwer Academic Publishers: Dordrecht.
130. Spaink, H. P., Wijfjes, A. H. M., van der Drift, K. M. G. M., Haverkamp, J., Thomas-Oates, J. E., and Lugtenberg, B. J. J. 1994b. Structural identification of metabolites produced by the NodB and NodC proteins of Rhizobium leguminosarum. Mol. Microbiol. 13: 821-831.
131. 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.
132. 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 Int. 8: 155-164.
133. Spaink, H. P., Wijfjes, A. H. M., and Lugtenberg, B. J. J. 1995. Rhizobium NodI and NodJ proteins play a role in the efficiency of secretion of lipochitin oligosaccharides. J. Bacteriol. 177: 6276-6281.
134. Staehelin, C., Granado, J., Muller, J., Wiemken, A., Mellor, R. B., Felix, G., Regenass, M., Broughton, W. J., and Boller, T. 1994a. Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases. Proc. Natl. Acad. Sci. U.S.A. 91: 2196-2200.
135. Staehelin, C., Schultze, M., Kondorosi, E., Mellor, R. B., Boller, T., and Kondorosi, A. 1994b. Structural modifications in Rhizobium meliloti Nod factors influence their stability against hydrolysis by root chitinases. Plant J. 5: 319-330.
136. 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.
137. Stokkermans, T. J. W., Ikeshita, S., Cohn, J., Carlson, R. W., 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.
138. Stokkermans, T. J. W. and Peters, N. K. 1994. Bradyrhizobium elkanii lipo-oligosaccharide signals induce complete nodule structures on Glycine soja Siebold et Zucc (vol. 193, pg. 413, 1994). Planta 194: 435.
139. Stokkermans, T. J. W., Orlando, R., Kolli, V. S. K., Carlson, R. W., and Peters, N. K. 1996. Biological activities and structures of Bradyrhizobium elkanii low abundance lipo chitin-oligosaccharides. Mol. Plant-Microbe Int. 9: 298-304.
140. Sutton, J. M., Lea, E. J. A., and Downie, J. A. 1994. The nodulation-signaling protein NodO from Rhizobium leguminosarum biovar viciae forms ion channels in membranes. Proc. Natl. Acad. Sci. U.S.A. 91: 9990-9994.
141. IV (S): a sulfated lipotatrasaccharide symbiotic signal from Rhizobium meliloti. J. Chem. Soc. Chem. Commun. 4: 1827-1828.
142. 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.
143. Truchet, G., Roche, P., Lerouge, P., Vasse, J., Camut, S., de Billy, F., Promé, J.-C., and Dénarié, J. 1991. Sulfated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature (London) 351: 670-673.
144. van Brussel, A. A. N., Bakhuizen, R., van Spronsen, P. C., Spaink, H. P., Tak, T., Lugtenberg, B. J. J., and Kijne, J. W. 1992. Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium.. Science 257: 70-72.
145. van Spronsen, P. C., Bakhuizen, R., van Brussel, A. A. N., and Kijne, J. W. 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.
146. van Spronsen, P. C., van Brussel, A. A. N., and Kijne, J. W. 1995. Nod factors produced by Rhizobium leguminosarum biovar viciae induce ethylene-related changes in root cortical cells or Vicia sativa ssp. nigra. Eur. J. Cell Biol. 68: 463-469.
147. Vásquez, M., Santana, O., and Quinto, C. 1993. The Nodi and NodJ proteins from Rhizobium and Bradyrhizobium strains are similar to capsular polysaccharide secretion proteins from Gram-negative bacteria. Mol. Microbiol. 8: 369-377.
148. Vijn, I., Christiansen, H., Lauridsen, P., Kardailsky, I., Quandt, H.-J., Broer, I., Drenth, J., Ostergaard Jensen, E., van Kammen, A., and Bisseling, T. 1995a. A 200 bp region of the pea Enod12 promoter is sufficient for nodule-specific and Nod factor induced expression. Plant Mol. Biol. 28: 1103-1110.
149. Vijn, I., Martinezabarca, F., Yang, W. C., das Neves, L., van Brussel, A. A. N., van Kammen, A., and Bisseling, T. 1995b. Early nodulin gene expression during Nod factor-induced processes in Vicia sativa. Plant J. 8: 111-119.
150. Vijn, I., Yang, W.-C., Pallisgård, N., Ostergaard Jensen, E., van Kammen, A., and Bisseling, T. 1995c. VsENOD5, VsENOD12, and VsENOD40 expression during Rhizobium-induced nodule formation on Vicia sativa roots. Plant Mol. Biol. 28: 1111-1119.
151. Wilson, R. C., Long, F. X., 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.
152. Yang, W. C., Katinakis, P., Hendriks, P., Smolders, A., de Vries, F., Spee, 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.
153. 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 ycle is only completed in primordium formation. Plant Cell 6: 1415-1426.