Nod factor-induced host responses and mechanisms of Nod factor perception

New Phytologist

Volumn 133, Issue 1, 1996, Pages 25-43

  Heidstra, Renze ^a   Bisseling, Ton ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Nod factor; Nodulation; Receptor; Rhizobium; sym2

Indexed keywords

EID: 0002847519     PISSN: 0028646X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1469-8137.1996.tb04339.x     Document Type: Article

References (132)

1. + currents and on cytoskeleton behavior. In: Daniels MG, Downie JA, Osbourne AE, eds. Advances in Molecular Genetics of Plant-Microbe Interactions, vol. 3. Dordrecht, The Netherlands: Kluwer Academic Publishers, 107-114.
2. Ardourel M, Demont N, Debellé F, Maillet F, de Billy F, Promé J-C, Dénarié J, 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. The Plant Cell 6: 1357-1374.
3. Asad S, Fang Y, Wycoff KL, Hirsch AM. 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 EM, Long SR. 1992. Homology of Rhizobium meliloti NodC topolysaccharide polymerizing enzymes. Molecular Plant-Microbe Instructions 5, 439-442.
5. Atkinson EM, Palcic MM, Hindsgaul O, Long SR. 1994. Biosynthesis of Rhizobium meliloti lipooligosaccharide Nod factors: NodA is required for an N-acetyltransferase activity. Proceedings of the National Academy of Sciences USA 91 : 8418-8422.
6. Baev N, Endre G, Petrovics G, Banfalvi Z, Kondorosi A. 1991. Sic nodulation genes of nod box locus 4 in Rhizobium meliloti are involved in nodulation signal production: nodM codes for D-glucosamine synthetase. Molecular and General Genetics 228: 113-124.
7. Bec-Ferté MP, Krishnan HB, Promé D, Savagnac A, Pueppke SG, Promé J-C. 1994. Structures of nodulation factors from the nitrogen-fixing soybean symbiont Rhizobium fredii USDA257. Biochemistry 33: 11782-11788.
8. Bibb MJ, Biro S, Motamedi H, Collins JF, Hutchinson DR. 1989. Analysis of the nucleotide sequence of the Streptomyces glaucescens tcm1 genes provide key information about the enzymology of polyketide antibiotic biosynthesis. EMBO Journal 9: 2727-2736.
9. Bloemberg GV, Thomas-Oates JE, Lughtenberg BJJ, Spaink HP. 1994. Nodulation protein NodL of Rhizobium leguminosarum O-acetylates lipo-oligosaccharides, chitin fragments and N-acetylglucosamine in vitro. Molecular Microbiology 11, 793-804.
10. Bono J-J, Riond J, Nicolaou KC, Bockovich NJ, Estevez VA, Cullimore JV, Ranjeva R. 1995. Characterization of a binding site for chemically-synthesized lipo-oligosaccharidic NodRm factors in particulate fractions prepared from roots. Plant Journal 7 : 253-260.
11. Brewin NJ, 1991. Development of the legume root nodule. Annual Reviews in Cell Biology 7: 191-226.
12. Bulawa CE, Wasco W. 1991. Chitin and nodulation. Nature 353 : 710.
13. Callaham DA, Torrey JG. 1981. The structural basis of infection of root hairs of Trifolium repens by Rhizobium. Canadian Journal of Botany 59: 1647-1664.
14. Calvert HE, Pence MK, Pierce M, Malik NSA, Bauer WD. 1984. Anatomical analysis of the development and distribution of Rhizobium infections in soyabean roots. Canadian Journal of Botany 62: 2375-2384.
15. Carlson RW, Sanjuan J, Bhat R, Glushka J, Spaink HP, Wijfjes AHM, Van Brussel AAN, Stokkermans TJW, Peters K, Stacey G. 1993. The structures and biological activities of the lipo-ohgosaccharide nodulation signals produced by Type I and Type II strains of Bradyrhizobium japonicum. Journal of Biological Chemistry 268: 18372-18381.
16. Carlson RW, Price NPJ, Stacey G. 1995. The biosynthesis of rhizobial lipo-oligosaccharide nodulation signal molecules. Molecular Plant-Microbe Interactions 7: 684-695.
17. Cervantes E, Sharma SB, Maillet F, Vasse J, Truchet G, Rosenberg C. 1989. The product of host-specific nodQ gene of Rhizobium meliloti shares homology with translation, elongation and initiation factors. Molecular Microbiology 3: 745-755.
18. Cheong JJ, Hahn MG. 1991. A specific, high-affinity binding site for the hepta-β-glucoside elicitor excists in soybean membranes. The Plant Cell 3: 137-147.
19. Clark CA, Beltrame J, Manning PA. 1991. The oac gene encoding a lipopolysaccharide O-antigen acetylase maps adjacent to the integrase-encoding gene on the genome of Shigella flexneri bacteriophase SF6. Gene 106: 43-52.
20. Cook D, Dreyer D, Bonnet D, Howell M, Nony E, Vanden-Bosch K. 1995. Transient induction of a peroxidase gene in Medicago truncatula precedes infection by Rhizobium meliloti. The Plant Cell 7: 43-55.
21. Cooper JB, Long SR. 1994. Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. The Plant Cell 6: 215-225.
22. Crespi MD, Jurkevitch E, Poiret M, d'Aubenton-Carafa Y, Petrovics G, Kondorosi E, Kondorosi A. 1994. enod40, a gene expressed during nodule organogenesis, codes a nontranslatable RNA involved in plant growth. EMBO Journal 13: 5099-5112.
23. Davis EO, Evans IJ, Johnston AWB. 1988. Identification of nodX, a gene that allows Rhizobium leguminosarum biovar. viciae strain TOM to nodulate Afghanistan peas. Molecular and General Genetics 212: 531-535.
24. Dazzo FB, Truchet GL, Hollingsworth RI, Hrabak EM, Pankratz HS, Philip-Hollingsworth S, Salzwedel J, Chapman K, Appenzeller L, Squartini A, Gerhold D, Orgambide G. 1991. Rhizobium lipopolysaccharide modulates infection threat development in white clover root hairs. Journal of Bacteriology 173, 5371-5384.
25. Debellé F, Rosenberg C, Vasse J, Maillet F, Martinez E, Dénarié J, Truchet G. 1986. Assignment of symbiotic developmental phenotypes to common and specific nodulation (nod) genetic loci of Rhizobium meliloti. Journal of Bacteriology 168:1075-1086.
26. Debellé F, Rosenberg C, Dénarié J. 1992. The Rhizobium, Bradyrhizobium and Azorhizobium NodC proteins are homologous to yeast chitin synthases. Molecular Plant-Microbe Interactions 3: 317-326.
27. De Jong AJ, Heidstra R, Spaink HP, Hartog MH, Meijier EA, Hendriks T, Lo Schiavo F, Terzi M, Besseling T, van Kammen A, de Vries SC 1993. Rhizobium lipo-oligosaccharides rescue a carrot somatic embryo variant. The Plant Cell 5: 615-620.
28. De Maagd RA, Spaink HP, Pees E, Mulders IHM, Wijfjes A, Wijffelman CA, Okker RJH, Lughtenberg BJJ. 1989. Localization and symbiotic function of a region on the Rhizobium leguminosarum Sym plasmid pRL1JI responsible for a secreted, flavonoid-inducible 50-kilodalton protein. Journal of Bacteriology 171: 1151-1157.
29. Demont N, Debellé F, Aurelle H, Dénarié J, Promé J-C. 1993. Role of the Rhizobium meliloti nodF and nodE genes in the biosynthesis of lipo-oligosaccharide nodulation factors. Journal of Biological Chemistry 268: 20134-20142.
30. Dénarié J, Cullimore J. 1993. Lipo-oligosaccharide nodulation factors: a new class of signalling molecules mediating recognition and morphogenesis. Cell 74: 951-954.
31. Dénarié J, Debellé F, Rosenberg C. 1992. Signalling and host range variation in nodulation. Annual Reviews in Microbiology 46: 497-531.
32. Dockendorf TC, Sanjuan J, Grob P, Stacey G. 1994. No1A represses nod gene expression in Bradyrhizobium japonicum. Molecular Plant-Microbe Interactions 7: 596-602.
33. Downie, JA. 1989. The nodL gene from Rhizobium leguminosarum is homologous to the acetyl transferases encoded by lacA and cysE. Molecular Microbiology 3: 1649-1651.
34. Downie JA, Economou A, Scheu AK, Johnston AWB, Firmin JL, Wilson KE, Cubo MT, Mavridou A, Marie C, Davies A, Surin BP. 1990. The Rhizobium leguminosarum bv. viciae NodO protein compensates for the exported signal made by the host-specific nodulation genes. In: Gresshoff PM, Roth LE, Stacey G, Newton WE, eds. Nitrogen Fixation: Achievements and Objectives. London: Chapman and Hall, 201-206.
35. Downie JA, Surin BP. 1990. Either of two nod gene loci can complement the nodulation defect of a nod deletion mutant of Rhizobium leguminosarum bv. viciae. Molecular and General Genetics 222: 81-86.
36. Duckett CM, Oparka KJ, Prior DAM, Dolan L, Roberts K. 1994. Dye-coupling in the root epidermis of Arabidopsis is progressively reduced during development. Development 120: 3247-3255.
37. Dylan T, Ielpi L, Sanfield S, Kashyap L, Douglas C, Yanofsky M, Nester E, Helinski DR, Ditta G. 1986. Proceedings of the National Academy of Sciences USA 83: 4403-4407.
38. Economou A, Davies AE, Johnson AWB, Downie JA. 1994. The Rhizobium leguminosarum biovar. viciae nodO gene can enable a nodE mutant of Rhizobium leguminosarum biovar. trifolii to nodule vetch. Microbiology 140: 2341-2347.
39. Ehrhardt DW, Atkinson EM, Long SR. 1992. Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science 256: 998-1000.
40. Erwee MG, Goodwin PB. 1985. Symplastic domains in extrastellar tissues of Egeria Densa Planch. Planta 163: 9-19.
41. Faucher C, Camut S, Dénarié J, Truchet G. 1989. The nodH and nodQ host ranges genes of Rhizobium meliloti behave as avirulence genes in R. leguminosarum bv. viciae and determine changes in the production of plant-specific extracellular signals. Molecular Plant-Microbe Interactions 2: 291-300.
42. Felle HH, Kondorosi E, Kondorosi A, Schultze M. 1995. Nod signal-induced plasma membrane potential changes in alfalfa root hairs are differentially sensitive to structural modifications of the lipochitooligosaccharide. Plant Journal 7: 939-947.
43. Firmin JL, Wilson KE, Carlson RW, Davies AE, Downie JA. 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. Molecular Microbiology 10: 351-360.
44. Fisher RF, Long SR. 1992. Rhizobium-plant signal exchange. Nature 357: 655-660.
45. Geiger O, Thomas-Oates JE, Glushka J, Spaink HP, Lughtenberg BJJ. 1994. Phospholipids of Rhizobium contain nodE determined highly unsaturated fatty acid moieties. Journal of Biological Chemistry 269: 11090-11097.
46. Geiger O, Spaink HP, Kennedy EP 1991. Isolation of the Rhizobium leguminosarum NodF nodulation protein: NodF carries a 4′-phosphopantetheine prostetic group. Journal of Bacteriology 173: 2872-2878.
47. Geremia RA, Margaert P, Geelen D, Van Montagu M, Holsters M. 1994. The NodC protein of Azorhizobium caulinodans is an N-acetylglucosaminyltransferase. Proceedings of the National Academy of Sciences USA 91: 2669-2673.
48. Gibson AH. 1963. Physical environment and symbiotic nitrogen fixation. Australian Journal of Biological Science 16: 28-42.
49. Gibson AH. 1968. Nodulation failure in Trifolium subterraneum L. cv. Woogenellup (syn. Marrar). Australian Journal of Agricultural Research 19: 907-918.
50. Goethals K, Van Montagu M, Holsters M. 1992. Conserved motifs in a divergent nod box of Azorhizobium caulinodans ORS571 reveals a common structure in promoters regulated by LysR-type proteins. Proceedings of the National Academy of Sciences USA 89: 1646-1650.
51. Heidstra R, Geurts R, Franssen H, Spaink HP, van Kammen A, Bisseling T. 1994. Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiology 105: 787-797.
52. Heidstra R, Kozik A, Bisseling T, Lie TA. 1993. Pea Nodmutants and Nod factor perception. In: Palacios R, Mora R, Newton WE, eds. New Horizons in Nitrogen Fixation. Dordrecht, The Netherlands: Kluwer Academic Publishers, 267-268.
53. Herskowitz I. 1987. Functional inactivation of genes by dominant negative mutations. Nature 329: 219-222.
54. Hirsch AM, Bhuvaneswari TV, Torrey JG, Bisseling T. 1989. Early nodulin genes are induced in alfalfa root outgrowths elicited by Auxin transport inhibitors. Proceedings of the National Academy of Sciences USA 86: 1244-1248.
55. Horvath B, Heidstra R, Lados M, Moerman M, Spaink HP, Promé J-C, Van Kammen A, Bisseling T. 1993. Induction of pea early nodulin gene expression by Nod factors of Rhizobium. Plant Journal 4: 727-733.
56. Horvath B, Kondorosi E, John M, Schmidt J, Torok I, Gyorgypal Z, Barabas I, Wieneke U, Schell J, Kondorosi A. 1986. Organization, structure and symbiotic function of Rhizobium meliloti nodulation genes determining host specificity for alfalfa. Cell 46: 335-343.
57. John M, Röhrig H, Schmidt J, Wieneke U, Schell J. 1993. Rhizobium NodB protein involved in modulation signal synthesis is a chitooligosaccharide deacetylase. Proceedings of the National Academy of Sciences USA 90: 625-629.
58. Journet EP, Pichon M, Dedieu A, de Billy F, Truchet G, Barker DG. 1994. Rhizobium meliloti Nod factors elicit cell-specific transcription of the ENOD12 gene in transgenic alfalfa. Plant Journal 6: 241-249.
59. Kafetzpoulos D, Thireos G, Vournakis JN, Bouriotis V. 1993. The primary structure of a fungal chitin deacetylase reveals the function for two bacterial gene products. Proceedings of the National Academy of Sciences USA 90: 8005-8008.
60. Kijne JW. 1992. The Rhizobium infection process. In: Stacey G, Burris RH, Evans HJ, eds. Biological Nitrogen Fixation. New York: Chapman and Hall, 349-398.
61. Kouchi H, Hata S. 1993. Isolation and characterization of novel cDNAs representing genes expressed at early stages of soybean nodule development. Molecular and General Genetics 238: 106-119.
62. Kozik A, Heidstra R, Horvath B, Kulikova O, Tikhonovich I, Noel Ellis TH, Van Kammen A, Lie TA, Bisseling T. 1995. Pea lines carrying sym1 or sym2 can be nodulated by Rhizobium strains containing nodX; sym1 and sym2 are allelic. Plant Science 108: 41-49.
63. Kurkdjian AC. 1995. Role of the differentiation of root epidermal cells in Nod factor (from Rhizobium meliloti)-induced root-hair depolarization of Medicago sativa. Plant Physiology 107: 783-790.
64. LaRue TA, Weeden NF. 1994. The symbiosis genes of the host. Proceedings of the 1st European Nitrogen Fixation Conference, Szeged, Hungary, 147-151.
65. Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Promé J-C, Dénarié J. 1990. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344: 781-784.
66. Lewis-Henderson WR, Djordjevic MA. 1991a. nodT, a positively-acting cultivar specificity determinant controlling nodulation of Trifolium subterraneum by Rhizobium leguminosarum biovar trifolii. Plant Molecular Biology 16: 515-526.
67. Lewis-Henderson WR, Djordjevic MA. 1991b. A cultivar specific interaction between Rhizobium leguminosarum bv. trifolii and subterranean clover is conditioned by nodM, other bacterial cultivar specificity genes and a single recessive host gene Journal of Bacteriology 173: 2791-2799.
68. Libbenga KR, Van Iren F, Bogers RJ, Schraag-Lammers MF, 1973. The role of hormones and gradients in the initiation of cortex proliferation and nodule formation in Pisum sativum L. Planta 114: 29-39.
69. Lie, TA. 1971a. Symbiotic nitrogen fixation under stress conditions. Plant and Soil Special Volume: 117-127.
70. Lie TA. 1971b. Temperature-dependent root-nodule formation in pea cv. Iran. Plant and Soil 34: 751-752.
71. Lie TA, Hille Ris Lambers D, Houwers A. 1976. Symbiotic specialisation in pea plants: some environmental effects on nodulation and nitrogen fixation. In : Nutman PS, ed. Symbiotic Nitrogen Fixation in Plants. Cambridge: Cambridge University Press, 319-333.
72. Lie TA. 1978. Symbiotic specialization in pea plants: The requirement of specific Rhizobium strains for peas from Afghanistan. Annals of Applied Biology 88: 445-487.
73. Lie TA. 1984. Host genes in Pisum sativum L. conferring resistance to European Rhizobium leguminosarum strains. Plant and Soil 82: 415-425.
74. Lopez-Lara IM, Van den Berg JDJ, Thomas-Oates JE, Glushka J, Lughtenberg BJJ, Spaink HP. 1995. Structural identification of the lipochitin oligosaccharide nodulation signals from Rhizobium loti. Molecular Microbiology 15: 627-638.
75. Marie C, Barny M-A, Downie JA. 1992. Rhizobium leguminosarum has two glucosamine synthases. GlmS and NodM, required for nodulation and development of nitrogen-fixing nodules. Molecular Microbiology 6: 843-851.
76. Matvienko M, van de Sande K, Yang WC, van Kammen A, Bisseling T, Franssen H. 1994. Comparison of soybean and pea ENOD40 cDNA clones representing genes expressed during both early and late stages of nodule development. Plant Molecular Biology 26: 487-493.
77. Mergaert P, van Montagu M, Promé J-C, Holsters M. 1993. Three unusual modifications, a D-arabinosyl, an N-methyl, and a carbomoyl group are present on Nod factors of Azorhizobium caulinodans strain ORS571. Proceedings of the National Academy of Sciences USA 90: 1551-1555.
78. Newcomb W, Sippel D, Peterson RL. 1979. The early morphogenesis of Glycine max and Pisum sativum root nodules. Canadian Journal of Botany 57: 2603-2616.
79. Niehaus K, Kapp D, Pühler A. 1993. Plant defence and delayed infection of alfalfa pseudonodules induced by an exopolysaccharide (EPS I)-deficient Rhizobium meliloti mutant. Planta 190: 415-425.
80. Pichon M, Journet E-P, Dedieu A, de Billy F, Truchet G, Barker DG. 1992. Rhizobium meliloti elicits transient expression of the early nodulin gene ENOD 12 in the differentiating root epidermis of transgenic Alfalfa. The Plant Cell 4: 1199-1211.
81. Poupot R, Martinez-Romero E, Promé J-C. 1993. Nodulation factors from Rhizobium tropici are sulfated or non-sulfated chitopentasaccharides containing an N-methyl-N-acylglucos-aminyl terminus. Biochemistry 32: 10430-10435.
82. Price NPJ, Relic B, Talmont F, Lewin A, Promé D, Pueppke SG, Maillet F, Dénarié J, Promé J-C, Broughton WJ. 1992. Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated. Molecular Microbiology 6: 3575-3584.
83. Priem WJE, Wijffelman CA. 1984. Selection of strains cured of the Rhizobium leguminosarum Sym-plasmid pRL1JI by using small bacteriocin. FEMS Microbiology Letters 25: 247-251.
84. Relic B, Talmont F, Kopcinska J, Golinowski W, Promé J-C, Broughton WJ. 1993. Biological activity of Rhizobium sp. NGR234 Nod-factors on Macroptilium atropurpureum. Molecular Plant-Microbe Interactions 6: 764-774.
85. Ritsema T, Geiger O, Van Dillewijn P, Lughtenberg BJJ, Spaink HP. 1994, Serine residue 45 of nodulation protein NodF from Rhizobium leguminosarum bv. viciae is essential for its biological activity. Journal of Bacteriology 176: 7740-7743.
86. Roche P, Debellé F, Maillet F, Lerouge P, Truchet G, Dénarié J, Promé J-C. 1991a. Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell 67: 1131-1143.
87. Roche P, Lerouge P, Ponthus C, Promé J-C. 1991b. Structural determination of bacterial nodulation factors involved in the Rhizobium meliloti-alfalfa symbiosis. Journal of Biological Chemistry 266: 10933-10940
88. Röhrig H, Schmidt J, Wieneke U, Kondorosi E, Barlier I, Schell J, John M. 1994. Biosynthesis of lipooligosaccharide nodulation factors : Rhizobium NodA protein is involved in N-acylation of the chitooligosaccharide backbone. Proceedings of the National Academy of Sciences USA 91: 3122-3126.
89. Röhrig H, Schmidt J, Walden R, Czaja I, Miklasevics E, Wieneke U, Schell J, John M. 1995. Growth of tobacco protoplasts stimulated by synthetic lipo-chitooligosaccharides. Science 269: 841-843.
90. Sadowsky MJ, Cregan PB. 1992. The soybean Rj4 allele restricts nodulation by Bradyrhizobium japonicum serocluster USDA1 23 strains. Applied Environmental Microbiology 58: 720-723.
91. Sadowsky MJ, Cregan PB, Rodriguez-Quinones F, Keyser H. 1990. Microbial influence on gene-for-gene interaction in the legume-Rhizobium symbiosis. Plant and Soil 129: 53-60.
92. Sadowsky MJ, Cregan PB, Gottfert M, Sharma A, Gerhold D, Rodriguez-Quinones F, Keyser F, Hennecke H, Stacey G. 1991. The Bradyrhizobium japonicum nolA gene and its involvement in the genotype-specific nodulation of soybeans. Proceedings of the National Academy of Sciences USA 88: 637-641.
93. Sanjuan J, Carlson RW, Spaink HP, Bhat R, Mark Barbour W, Glushka J, Stacey J. 1992. A 2-O-methylfucose moiety is present in the lipopolysaccharide nodulation signal of Bradyrhizobium japonicum. Proceedings of the National Academy of Sciences USA 89: 8789-8793.
94. Scheres B, van de Wiel C, Zalensky A, Horvath B, Spaink HP, van Eck H, Zwartkruis F, Wolters A-M, Gloudemans T, van Kammen A, Bisseling T. 1990a. The ENOD12 gene product is involved in the infection process during pea-Rhizobium interaction. Cell 60: 281-294.
95. Scheres B, van Engelen F, van der Knaap E, van de Wiel C, van Kammen A, Bisseling T. 1990b. Sequential induction of nodulin gene expression in the developing pea nodule. The Plant Cell 8: 687-700.
96. Schlaman HRW, Horvath B, Vijgenboom E, Okker RJH, Lugtenberg BJJ. 1991. Evidence for a new negative regulation mechanism involved in the suppression of nodulation gene expression of Rhizobium leguminosarum bv. viciae. Journal of Bacteriology 173: 4277-4287.
97. Schmidt J, Röhrig H, John M, Wieneke U, Koncz C, Schell J. 1993. Alteration of plant growth and development of Rhizobium nodA and nodB genes involved in the synthesis of oligosaccharide signal molecules. Plant Journal 4: 651-658.
98. Schmidt WE, Ebel J. 1987. Specific binding of a fungal glucan phytoalexin elicitor to membrane fractions from soybean Glycine max. Proceedings of the National Academy of Sciences USA 84: 4117-4121.
99. Schultze M, Quiclet-Sire B, Kondorosi E, Virelizier H, Glushka JN, Endre G, Géro SD, Kondorosi A. 1992. Rhizobium meliloti produces a family of sulfated lipo-oligosaccharides exhibiting different degrees of plant host specificity. Proceedings of the National Academy of Sciences USA 89: 192-196.
100. Schultze M, Staehelin C, Röhrig H, John M, Schmidt J, Kondorosi E, Schell J, Kondorosi A. 1995. In vitro sulfotransferase activity of Rhizobium meliloti NodH protein : lipochitooligosaccharide nodulation signals are sulfated after synthesis of the core structure. Proceedings of the National Academy of Sciences USA 92: 2706-2709.
101. Schwedock JS, Long SR. 1990. ATP sulphurylase activity of the nodP and nodQ gene products of Rhizobium meliloti. Nature 348: 644-647.
102. Schwedock JS, Long SR. 1992. The two copies of nodPQ and a new locus, saa. Genetics 132: 899-909.
103. Schwedock JS, Liu CX, Leyh TS, Long SR. 1994. Rhizobium meliloti NodP and NodQ form a multifunctional sulfate-activating complex requiring GTP for activity. Journal of Bacteriology 176: 7055-7064.
104. Sharma SB, Signer ER. 1990. Temporal and spatial regulation of the symbiotic genes of Rhizobium meliloti in planta revealed by transposon Tn5-gusA. Genes in Development 4: 344-356.
105. Shearman CA, Rossen L, Johnston AWB, Downie JA. 1986. The Rhizobium leguminosarum nodulation gene nodF encodes a polypeptide similar to acyl carrier protein and is regulated by nodD plus a factor in pea root exudate. EMBO Journal 5: 647-652.
106. Sherman DH, Malpartida F, Bibb MJ, Kieser HM, Hopwood DA. 1989. Structure and deduced function of the granaticin-producing polyketide synthase gen cluster of Streptomyces violaceoruber Tu22. EMBO Journal 8: 2717-2725.
107. Smit G, van Brussel AAN, Kijne JW. 1993. Inactivation of a root factor by ineffective Rhizobium: a molecular key to autoregulation of nodulation in Pisum sativum. In: Palacios R, Mora J, Newton WE, eds. New Horizons in Nitrogen Fixation. Dordrecht, The Netherlands: Kluwer Academic Publishers, 371.
108. Spaink HP. 1992. Rhizobial lipo-oligosaccharides: answers and questions. Plant Molecular Biology 20: 977-986.
109. Spaink HP, Bloemberg GY, Van Brussel AAN, Lughtenberg BJJ, van der Drift KMGM. Haverkamp J, Thomas-Oates JE. 1995. Host specificity of Rhizobium leguminosarum is determined by the hydrophobicity of highly unsaturated fatty acyl moieties of the nodulation factors. Molecular Plant-Microbe Interactions 8: 155-164.
110. Spaink HP, Sheely DM, van Brussel AAN, Glushka J, York WS, Tak T, Geiger O, Kennedy EP, Reinhold VN, Lugtenberg BJJ. 1991. A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354: 125-130.
111. Spaink HP, Weinman J, Djordjevic MA, Wijffelman CA, Okker RJH, Lughtenberg BJJ. 1989. Genetic analysis and cellular localization of the Rhizobium host specificity-determining NodE protein. EMBO Journal 8: 2811-2818.
112. Spaink HP, Wijfjes AHM, van der Drift KMGM, Haverkamp J, Thomas-Oates JE, Lughtenberg BJJ. 1994. Structural identification of metabolites produced by the NodB and NodC proteins of Rhizobium leguminosarum. Molecular Microbiology 13: 821-831.
113. Staehelin C, Granado J, Müller J, Wiemken A, Mellor RB, Felix G, Regenaas M, Broughton WJ, Boiler T. 1994a. Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases. Proceedings of the National Academy of Sciences USA 91: 2196-2200.
114. Staehlin C, Schultze M, Kondorosi E, Mellor RB, Boiler T, Kondorosi A. 1994b. Structural modifications in Rhizobium meliloti Nod factors influence their stability against hydrolysis by root chitinases. Plant Journal 5: 319-330.
115. Stokkermans TJW, Peters NK. 1994. Bradyrhizobium elkanii lipooligosaccharide signal induce complete nodule structures on Glycine soja Siebold et Zucc. Planta 193: 413-420.
116. Stokkermans TJW, Sanjuan J, Ruan X, Peters NK. 1992. Bradyrhizobium japonicum Rhizobitoxe mutants with altered host-range on Rj4 soybeans. Molecular Plant-Microbe Interactions 5: 504-512.
117. Sutton MJ, Lea EJA. Downie AJ. 1994. The nodulation-signalling protein nodO from Rhizobium leguminosarum biovar viciae forms ion channels in membranes. Proceedings of the National Academy of Sciences USA 91: 9990-9994.
118. Truchet G, Roche P, Lerouge P, Vasse J, Camut S, de Billy F, Promé J-C, Dénarié J. 1991. Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351: 670-673.
119. Van Brussel AAN, Bakhuizen R, van Spronsen PC, Spaink HP, Tak T, Lugtenberg BJJ, Kijne JW. 1992. Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium. Science 257: 70-71.
120. Van de Wiel C, Scheres B, Franssen H, van Lierop MJ, van Lammeren A, van Kammen A, Bisseling T. 1990. The early nodulin transcript ENOD2 is located in the nodule parenchyma (inner cortex) of pea and soybean root nodules. EMBO Journal 9: 1-7.
121. Van Kammen A. 1984. Suggested nomenclature for plant genes involved in nodulation and synbiosis. Plant Molecular Biology Reports 2: 43-45.
122. Van Spronsen PC, Bakhuizen R, van Brussel AAN, Kijne JW. 1994. Cell wall degradation during infection thread formation by the root nodule bacterium Rhizobium leguminosarum is a two-step process. European Journal of Cell Biology 64: 88-94.
123. Verma DPS. 1992. Signals in root nodule organogenesis and endocytosis of Rhizobium. The Plant Cell 4: 373-382.
124. Vest G, Caldwell BE. 1972. Rj4-A gene conditioning ineffective nodulation in soybean. Crop Science 692.
125. Vijn I, Martinez-Abarca F, Yang WC, das Neves L, van Brussel A, van Kammen A, Bisseling T. 1995a. Early nodulin gene expression during Nod factor-induced processes in Vicia sativa. Plant Journal 8: 111-119.
126. Vijn I, Yang WC, Pallisgård N, Østergaard Jensen E, van Kammen A, Bisseling T. 1995b. VsENOD5, VsENOD12 and VsENOD40 expression during Rhizobium-induced nodule formation on Vicia sativa roots. Plant Molecular Biology 28: 1111-1119.
127. Walden R, Hayashi H, Lubenow H, Czaja I, Schell J. 1994. Auxin inducibility and developmental expression of axi 1 : a gene directing independent growth in tobacco protoplasts. EMBO Journal 13: 4729-4736.
128. Weeden NF, Kneen BE, LaRu TA. 1990. Genetic analysis of sym genes and other nodule-related genes in Pisum sativum. In : Gresshoff PM, Roth LE, Stacey G, Newton WE, eds. Nitrogen Fixation : Achievements and Objectives. London : Chapman and Hall, 323-330.
129. Wilson CW, Long F, Maruoka EM, Cooper JB. 1994. A new proline-rich early nodulin from Medicago truncatula is highly expressed in nodule meristematic cells. The Plant Cell 6: 1265-1275.
130. Wipf L, Cooper DC. 1938. Chromosome numbers in nodules and roots of red clover, common vetch, and garden pea. Proceedings of the National Academy of Sciences USA 24: 87-91.
131. Yang WC, Katinakis P, Hendriks P, Smolders A, de Vries F, Spee J, van Kammen A, Bisseling T, Franssen H. 1993. Characterization of GmENOD40, a gene showing novel patterns of cell-specific expression during soybean nodule development. Plant Journal 3: 573-585.
132. Yang WC, de Blank C, Meskiene I, Hirt H, Bakker J, van Kammen A, Franssen H, 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. The Plant Cell 6: 1415-1426.