Nodulation genes in the Rhizobium-plant signal exchange

• Autorzy: Lorkiewicz Z.
• Języki publikacji: EN

Abstrakty

EN

The process of the host-plant recognition by rhizobia is complex and multi- step. The interaction between legumes and microorganisms results in the induction of the root nodule. This symbiotic interaction is highly host-specific. Bacteria within nodules fix atmospheric nitrogen. This process is of immense ecological and economic significance. The subject of this presentation is the molecular mechanism by which the bacterium determines its host-specific characteristics. First flavonoids secreted by the plant roots induce the tran­scription of bacterial genes involved in nodulation, the so-called nod genes. This leads to the next step of the signalling system, i.e. the production and secretion of lipo-oligosaccharide molecules by rhizobia. These signal molecules have various discernible effects on the roots of the host leguminous plants. The bacterial nodulation factors were isolated and structurally identified as substi­tuted and N-acylated chitin oligosaccharides. These prokaryotic signals play a key role in the symbiosis by controlling the host specificity of the bacteria. They constitute a new class of signalling molecules able to elicit nodule organogene­sis in leguminous plants in the absence of bacteria. More recent studies impli­cate involvement of root cell membrane depolarization and ion selective chan­nels in the communication processes that initiate nodule formation.

Słowa kluczowe

EN

legume; plant root; nodulation gene; plant flavonoid; atmospheric nitrogen; host specificity; Rhizobium; bacterial gene; microorganism; cell depolarization

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 1997
• Tom: 44
• Numer: 1
• Opis fizyczny: p.1-12,fig.

Twórcy

autor

Lorkiewicz Z.

• M.Curie-Sklodowska University, Akademicka 19, 20-033 Lublin, Poland

Bibliografia

• 1. Schultze, M., Kondorosi, E., Ratet, P., Buire, M. & Kondorosi, A. (1994) Cellular and mo­lecular biology of Rhizobium-plant interac­tions. Int. Rev. Cytol. 156, 1-75.
• 2. Ehrhardt, D.W., Atkinson, E.M. & Long, S.M. (1992) Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science 256, 998-1000.
• 3. Pueppke, S.G. (1996) The genetic and bio­chemical basis for nodulation of legumes by rhizobia. Crit. Rev. Biotechnol. 16, 1-51.
• 4. Phillips, DA. (1992) Flavonoids: plant signals to soil microbes; in Phenolic Metabolism in Plants (Stafford, H.A. & Ibachim, R.K, eds.) pp. 201-231.
• 5. Roche, P., Debelle, F., Maillet, F., Lerouge, P., Denarie, J. & Prome, J.C. (1991) Molecular basis of symbiotic host specificity in Rhizo­bium meliloti: nodH and nodP,Q genes en­code the sulfation of lipo-oligosaccharide sig­nals. Cell 67,1131-1143.
• 6. Assmann, S.M. (1995) Electrifying symbiosis. Proc. Natl. Acad. Sci. U.S.A. 92, 1795-1796.
• 7. Derylo, M., Skorupska, A., Bednara, J. & Lorkiewicz, Z. (1986) Rhizobium trifolii mu­tants deficient in exopolysaccharide produc­tion. Physiol. Plant. 66, 699-704.
• 8. Lorkiewicz, Z. & Russa, R (1971) Immuno­chemical studies on Rhizobium mutants. Plant Soil. (Spec, vol.) 105-109.
• 9. Arnold, W., Beckcr, A., Keller, M., Roxlau, A. & Puhler, A. (1993/1994) The role of Rhizo­bium meliloti surface polysaccharides in theinfection of Medicago sativa. Endocytobiosis & Cell Res. 10, 17-28.
• 10. Białek, U., Skorupska, A., Yang, W.C., Bissel- ing, T. & van Lam me ren, A. A. (1995) Dis­turbed gene expression and bacterial develop­ment in Trifolium pratense root nodules in­duced by Tn5 mutants of Rhizobium legumi­nosa rum bv. trifolii defective in polysaccha­ride synthesis. Planta 197, 184-192.
• 11. Leigh, J.A. & Walker, G.C. (1994) Exopolysac- charides of Rhizobium synthesis, regulation and symbiotic function. Trends Genet. 10, 63-67.
• 12. Russa, R & Lorkiewicz, Z. (1974) Fatty acids present in the lipopolysaccharide of Rhizo­bium trifolii. J. Bacteriol. 119, 771-774.
• 13. Russa, R. & Lorkiewicz, Z. (1979) O-Methyl- heptoses in lipopolysaccharides of Rhizobium trifolii 24SM. FEMS Microbiol. Letts. 6, 71-74.
• 14 Skorupska, A. Deryło, M. & Lorkiewicz, Z. (1985) Role of non-carbohydrate substitutions of Rhizobium exopolysaccharide in nodula­tion process. Arch. Microbiol. 143, 307-310.
• 15. Brcedeveld, M.W. & Miller, K.J. (1944) Cyclic p-glucans of members of the family of Rhizo- biaceae. Microbiol. Rev. 58, 145-161.
• 16. Skorupska, A., Deryło, M., Russa, R., Głowacka, M., Stępkowski, T. & Lorkiewicz, Z. (1985) Genetical and immunochemical studies on Rhizobium trifolii. 14th Interna­tional Symposium on Chemistry Natural Products (Zalewski, RI. & Skoklik, J.J., eds.) Elsevier, Amsterdam, pp. 655-666.
• 17. Gray, J. & Rolfe, B.G. (1990) Exopolysaccha­ride production in Rhizobium and its role in invasion. Mol. Microbiol. 4, 1425-1431.
• 18. Carlson, R.W. (1982) Surface chemistry; in Nitrogen Fixation; vol. 2; Rhizobium (Bro- ughton, W.J., ed.) pp. 194-234, Clarendon Press, Oxford.
• 19. Zając, E., Russa, R. & Lorkiewicz, Z. (1975) Lipopolysaccharide as receptor for Rhizobium phage PI. J. Gen. Microbiol. 90, 365-367.
• 20. Russa, R., Urbanik, T., Kowalczuk, E. & Lor­kiewicz, Z. (1982) Correlation between the occurence of plasmid pUCS202 and lipopoly-saccharide alterations in Rhizobium. FE M S Microbiol Lett. 13, 161-165.
• 21. Lorkiewicz, Z., Deryło, M., Russa, R., Skorup­ska, A. & Urbanik-Supniewska, T. (1993) Rhi­zobium leguminosarum bv. trifolii mutants altered in surface structures that are defec­tive in nodulation or nitrogen fixation. Acta Microbiol Polon. 42, 219-234.
• 22. Noel, K.D. (1992) Rhizobial polysaccharides required in symbiosis with legumes; in Mo­lecular Signals in Plant-Microbe Communi­cation (Verma, D.P.S., ed.) pp. 341-358, CRC Press, Boca Raton, FL.
• 23. Dudman, W.F. (1984) The polysaccharides and oligosaccharides of Rhizobium and their role in the infection process; in Advances in Nitrogen Fixation Research (Veegcr, C. & Newton, W.E., eds.) pp. 397-404, M. NijhofT, The Hague, The Netherlands.
• 24. Zając, E., Kowalczuk, E. & Lorkiewicz, Z. (1992) Rhizobium tńfolii strains mutated in early phases of symbiosis. Acta Microbiol Polon. 41, 25-36.
• 25. Kowalczuk, E., Skorupska, A. & Lorkiewicz, Z. (1983) Hybrid plasmid R68-45 harboring nod gene{s) of Rhizobium. Endocytobiology, 2, Walter de Gruyter, Berlin.
• 26. Lorkiewicz, Z., Deryło, M., Głowacka, M., Goszczyński, D. & Skorupska, A. (1983) Clon­ing of Rhizobium trifolii nodulation genes. 5th Int. Symp. Nitrogen Fixation, Noordwijker- hout, The Netherlands, Book Abstr. 9A-28.
• 27. Cren, M., Kondorosi, A. & Kondorosi, E. (1993) All insertional point mutation inacti­vates NolR repressor in Rhizobium meliloti 1021. J. Bacteriol. 176, 518-519.
• 28. Żurkowski, W. & Lorkiewicz, Z. (1977) Bidi­rectional replication of the chromosome in Rhizobium trifolii. Mol Gen. Genet. 156, 215-219.
• 29. Banfalvi, Z. & Kondorosi, A. (1989) Produc­tion of root hair deformation factors by Rhizo­bium meliloti nodulation genes in Escherichia coli: hsnD (nocLH) is involved in the plant host specific modification of the NodABC factor. Plant. Mol. Biol 13, 1-12.
• 30. Żurkowski, W. & Lorkiewicz, Z. (1976) Plas­mid deoxyribonucleic acid in Rhizobium trifo­lii. 128, 481-434.
• 31. Lorkiewicz, Z., Deryło, M., Głowacka, M., Kowalczuk, E., Russa, R. & Skorupska, A (1981) Plasmids controlling symbiotic proper­ties; in Current Perspectives in Nitrogen Fixa­tion (Gibson, A.H. & Newton, W.E., eds.) p. 408, Australian Acad. Sci., Canberra.
• 32. Kowalczuk, E., Skorupska, A. & Lorkiewicz, Z. (1981) Transfer of nodulation ability in Rhizobium using R68-45 derived plasmids. Mol. Gen. Genet. 183, 388-391.
• 33. Martinez, E., Romero, D. & Palacios, R. (1990) The Rhizobium genome. Crit. Rev. Plant Sci. 9, 59-93.
• 34. Goethals, K., Gao, M., Tomekpe, M.t van Mon­tagu, M. & Holsters, M. (1989) Common nodABC genes in nod locus 1 of Rhizobium caulinodans: Nucleotide sequence of plant in­ducible expression. Mol. Gen. Genet. 219, 289-298.
• 35. Appelbaum, E.R., Thompson, D.V., Idler, K. & Chartrain, N. (1988) Bradyrhizobium japonicum USDA 191 has two nodD genes that differ in primary structure and function. J. Bacteriol 170, 12-20.
• 36. Schlam an, H.R.M., Okker, L.J.H. & Lugten- berg, B.J.J. (1992) Regulation of nodulation gene expression by NodD in rhizobia. J. Bac­teriol 174, 5177-5182.
• 37. Denarie, J. & Cullimore, J. (1993) Lipo-oli- gosaccharide nodulation factors. Cell 74, 951-954.
• 38. Demont, N., Debelle, F., Aurelie, H., Denarie, J. & Prome, J.C. (1993) Role of Rhizobium meliloti nodF and nodE genes in the biosyn­thesis of lipo-oligosaccharidic nodulation fac­tors. J. Biol. Chem. 268, 20134-20142.
• 39. Gyórgypal, Z., & Kondorosi, A. (1991) Homol­ogy of the ligand-binding regions of Rhizo­bium symbiotic regulatory protein NodD and vertebrate nuclear receptors. Mol. Gen. Genet. 226, 337-340.
• 40. Hirsch, A.M., Asad, S., Fang, Y., Wyckoff, K & Lobler, M. (1993) Molecular interactions during nodule development; in New Horizons in Nitrogen Fixation (Palacios, R., Mora, J. & Newton, W.E., eds.) pp. 291-296, Kluwer, Dordrecht, The Netherlands.
• 41. Firmin, J.L., Wilson, K.E., Rossen, L. & Johnston, A.W.B. (1986) Flavonoid activation of nodulation genes in Rhizobium reversed by other compounds present in plants. Nature 324, 90-92.
• 42. Peters. N.K. & Long, S.R. (1986) Alfalfa root exudates and compounds which promote or inhibit induction of Rhizobium melUoti nodu­lation genes. Plant Physiol. 88. 396-400.
• 43. HennikofT, S., Haughn, G.W., Calvo, J.M. & Wallace, J.C. (1988) A large family of bacterial activator proteins. Biochemistry 85, 6602- 6604.
• 44. Krishnan, H.B., Kuo, C J. & Pueppke, S.G. (1995) Elaboration of flavonoid-induced pro­teins by the nitrogen-fixing soybean symbiont Rhizobium fredii is regulated by both nodDl and nodD2 and is dependent on the cultivar- specificity locus, nodXWBTUV. Microbiology, 141, 2245-2251.
• 45. Goethals, K., Van Montagu, M. & Holsters, M. ( 1992) Conserved motifs in a divergent nod box of Azorhizobium caulinodans ORS571 re­veal a common structure in promoters regu­lated by LysR type protein. Proc. Natl. Acad. Sci. U.S.A. 89, 1646-1650.
• 46. Van Rhijn, P.J.S., Feys, B., Verreth, C. & Vanderleyden, J. (1993) Multiple copies of nodD in Rhizobium tropici CIAT899 and BR816. J. Bacterial. 175, 438-447.
• 47. Kondorosi, E., Gyuris, J., Schmidt, J., John, M., Duda, E., Hoffmann, B., Schell, J. & Kon­dorosi, A. (1989) Positive and negative control of nod gene expression in Rhizobium meliloti is required for optimal nodulation. EMBO J. 8,1331-1340.
• 48. Davies, E. & Johnston, A.W.B. (1990) Regu­latory functions of three nodD genes of Rhizo­bium leguminosarum biovar phaseoli. Mol. Microbiol. 4, 933-941.
• 49. Firmin, J.L., Wilson, K.E., Carlson, R.W., Davies. A.E. & Downie, J. A. (1993) Resistance of nodulation of cv. Afghanistan peas is over­come by nodX which mediates O-acetylation of the Rhizobium leguminosarum lipooli- gosaccharide nodulation factor. Mol. Micro­biol. 10, 351-360.
• 50. Gottfert, M., Grob, P. & Hennecke, H. (1990) Proposed regulatory pathway encoded by the nodV and nodW genes, determinants of host specificity in Bradyrhizobium japonicum. Proc. Natl. Acad. Sci. U.S.A. 87, 2680-2684.
• 51. Franssen, H., My lona, P., Pawlowski, K, Van de Sande, K., Heikstra, R., Geurts, R., Kozik, A., Matvienko, M., Yang, W.C., Hadr, A.-E., Martin-Barca, F. & Bisseling, T. (1995) Plant genes involved in root nodule development on legumes. Phil. Trans. R. Soc. Lond. B. 350, 101-107.
• 52. van Brussel, A.A.A. (1990) Symbiotic signals in early stages of the morphogenesis of Rhi- zo6zum-induced root nodules. Symbiosis 9, 135-146.
• 53. Reuber, T.L., Reed, J.W., Glazcbroch, J., Ur- zainqui, A. & Walker, G.C. (1991) Analysis of the roles of Rhizobium meliloti exopolysac- charides in nodulation; in Advances in Mo­lecular Genetics of Plant-Microbe Interactions (Hennecke, H. & Verma, D.P.S., eds.) pp. 182-188, Kluwer Acad. Publ., Dordrecht, The Netherlands.
• 54. John, M., Rohring, H., Schmidt, U., Wieneke, U. & 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.
• 55. Rohring, 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. Proc. Natl. Acad. Sci. U.S.A. 91, 3122-3126.
• 56. Long, S.R. (1989) Rhizobium-legume nodula­tion: Life together in the underground. Cell 56, 203-214.
• 57. Bulawa, C.E. (1992) CSD2, CSD3 and CSD4 genes required for chitin synthesis in Sac- charomyces cerevisiae. The CSD2 gene prod­uct is related to chitin synthases and to devel- opmentally regulated proteins in Rhizobium species and Xenopus laevis. Molec. Cell. Biol. 12, 1764-1776.
• 58. Carlson, R.W., Price, N.P.J. & Staccy, G. (1994) The biosynthesis of rhizobial lipo-oli- gosaccharide nodulation signal molecules. Mol. Plant-Microb. Interact. 7, 684-695.
• 59. Truchet, G., Roche, P., Lerouge, P., Vasse, J., Camut, S., de Billy, F., Promé, F. & Dénarié, J. (1991) Sulphated lipo-oligosaccharide sig­nals of«, meliloti elicit root nodule formation organogenesis in alfalfa. Nature 351, 670- 673.
• 60. Stacey, G., Sanjuan, J., Luka, S., Dockendorff, T. & Carlson, R.W. (1995) Signal exchange in the Bradyrhizobium-soybean symbiosis. Soil Biol. Biochem. 27, 473^183.
• 61. Schulze, M., Quiclet-Sire, B., Kondorosi, E., Virelizier, H., Glushka, J.N., Endre, G., Géro, S.D. & Kondorosi, A. (1992) Rhizobium meliloti produces a family of sulfated lipo-oli- gosaccharides exhibiting different degrees of plant host specificity. Proc. Natl. Acad. Sci. U.S.A. 89, 192-196.
• 62. Spaink, H.P. (1993) The molecular basis of the host specificity of Rhizobium bacteria; pp. 1-24, Overdruk van de Bekroonde Inzending voov de Kluyver Prijs.
• 63. Bulawa, C.E. & Wasco, W. (1991) Chitin and nodulation. Nature 353, 710.
• 64. Price, N.P.J., Relic, B., Talmont, F., Lewin, A., Promé, D., Pueppke, S.D., Maillet, F., D., Dénarié, J., Promé, J.C. & Broughton, W.J. (1992) Broad host-range Rhizobium species NGR234 secretes a family of carbamoylated and fiicosylated nodulation signals that are O-acetylated or sulphated. Mol. Microbiol. 6, 3575-3584.
• 65. Carlson, R.W., Juan, S J., Bhat, U.R., Glushka, J., Spaink, H.P., Wijfjes, A.H.M., van Brussel, A.A.N., Stokkcrmans, T.J.W., Peters, N.K. & Stacey, G. (1993) The struc­tures and biological activities of the lipo-oli­gosaccharide nodulation signals produced by type-1 and type-2 strains of Bradyrh izobium japonicum. J. Biol. Chem. 268,18372-18381.
• 66. Mcrgert, P., van Montagu, M., Promé, J.C. & Holsters, M. (1993) Three unusual modifica­tions, a D-arabinosyl, JV-methyl and a car­bamoyl group are present on the Nod factors of Azorhizobium caulinodans strain ORS571 Proc. Nad. Acad. Sci. U.S.A »0, 1551-1554.
• 67. Lerouge, P., Roche, P., Faucher, C., Maillet, F., Truchet, G., Prome, J.C. & Denarie, J. (1990) Symbiotic host-specificity of Rhizo­bium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide sig­nal. Nature 344, 781-784.
• 68. Baev, N. & Kondorosi, A. (1992) Nucleotide sequence of the Rhizobium meliloti nodh gene located in locus n5 of the nod regulon. Plant Mol. Biol. 18, 843-346.
• 69. Spaink, H.P., Sheeley, D.M., van Brussel, AA_A., Glushka, J., York, W.S., Tak, T., Gei- ger, O., Kennedy, E.P., Reinhold, V.N. & Lugtenberg, B.JJ. (1991) A novel highly un­saturated fatty acid moiety of lipooligosaccha- ride signals determines host specificity of Rhi­zobium. Nature 354,125-130.
• 70. Poupot, R., Martinez-Romero, E. & Prome, J.C. (1993) Nodulation factors from Rhizo­bium tropici are sulphated or nonsulphated chitopentasaccharides containing an N-me- thyl-N-acetylglucosaminyl terminus. Bio­chemistry 32,10430-10435.
• 71. Geiger, O., Spaink, H.P. & Kennedy, E.P. (1991) Isolation of the Rhizobium legumi- nosarum Nod F nodulation protein: NodF car­ries a 4'-phosphopantheine prostetic group. J. Bacteriol. 173, 2872-2878.
• 72. Spaink, H.P., Wjjfies, A.H.M. & Lugtenberg, B.JJ. (1995) Rhizobium Nodi and NodJ pro­teins play a role in the efficiency of secretion of lipochitin oligosaccharides. J. Bacteriol. 177, 6276-6281.
• 73. Holsters, M., Geelen, D., Goethals, K, van Montagu, M., Geremia, M., Prome, J.C. & Mergert, P. (1993) Nod factor production by Azorhizobium caulinodans strain ORS57; in Horizons in Nitrogen Fixation (Palacios, R., Mora, J. & Newton, W.E., eds.) Kluwer Acad. Publ., Dordrecht, The Netherlands.
• 74. Schultze, M. & Kondorosi, A. (1995) What makes nodulation signals host plant specific? Trends Microbiol. 3, 370-372.
• 75. Stokkermans, T.J.W., Orlando, J., Kolli, V.S.K., Carlson, R.W. & Peters, N.K (1996) Biological activities and structures of Brady-rhizobium elkanii low abundance lipo chitin- oligosaccharides. Molec. Plant-Microbe Inter­act. 9, 298-304.
• 76. Saiyuan, J.f Carlson, R.W., Spaink, H.P., Bhat, U.R., Barbour, W.M., Glushka, J. & Stacey, G. (1992) A 2-O-methylfucose moiety is present in the lipooligosaccharide nodula- tion signal of Bradyrhizobium japonicum. Proc. Natl. Acad. Sci. U.S. A 89, 8789-8793.
• 77. Stacey, G., Luka, S., Sanjuan, J., Banfalvi, Z., Nieuwkoop, A.J., Chun, J.Y., Forsberg, L.S. & Carlson, R.W. (1994) nodZ, A unique host- specific nodulation gene, is involved in the fucosylation of lipooligosaccharide nodulation signal of Bradyrhizobium japonicum. J. Bac- teriol. 176, 620-633.
• 78. Krishnan, H.B., Lewin, A., Fellay, R., Bro- ughton, W.J. & Pueppke, S.G. (1992) Differ­ential expression of nodS accounts for the varied abilities of Rhizobium fredii USDA257 and Rhizobium sp. strain NGR234 to nodu- late Leucena sp. Mol. Microbiol. 6, 3321- 3330.
• 79. Spaink, H.P., Bloemberg, G.V., van Brussel, A.N., Lugtenberg, B.J.J., van der Drift, K.M.G.M., Havcrkamp, J. & Thomas-Oates, J.E. (1995) Host specificity of Rhizobium legu- minosarum is determined by the hydropho- bicity of highly unsaturated fatty acyl moie­ties of the nodulation factors. Molec. Plant- Microbe Interact. 8, 155-164.
• 80. Semino, C.E. & Robbins, P.W. (1995) Synthe­sis of uNod"-like chitin oligosaccharides by the Xenopus developmental protein DG42. Proc. Natl. Acad. Sci. U.SA. 92, 3498-3501.
• 81. Wildon, D.C., Thain, J.F., Minchin, P.E.H., Gubb, J.R., Reilly, A.J., Skipper, Y.D., Do- herty, H.M., O'Donnel, P.J. & Bowles, D.J. (1992) Electrical signalling and systemic pro­teinase inhibitor induction in the wounded plant. Nature 360, 62-65.
• 82. Sutton, M.J., Lea, E.J. & Downie, J.A. (1994) The nodulation signalling protein NodO from Rhizobium leguminosarum biovar viciae forms ion channels in membranes. Proc. Natl. Acad. Sci. U.SA. 91, 9990-9994.
• 83. Economou, A., Hamilton, W.D.O., Johnston, A.W.B. & Downie, J .A. (1990) The Rhizobium nodulation gene nodO encodes a Ca2*-binding protein that is exported without N-terminal cleavagc and is homologous to haemolysin and related proteins. EMBO J. 9, 349-354.
• 84. Downie, J.A. & Surin, B.P. (1990) Either of two gene loci can complement the nodulation defect of a nod deletion mutant of Rhizobium leguminosarum bv. viciae. Mol. Gen. Genet. 222, 81-86.
• 85. Marie, C., Barny, M.A. & Downie, J.A. (1992) Rhizobium leguminosarum glucosamine syn­thases, GlmS and NodM, required for nodula­tion and development of nitrogen fixing nod­ules. Mol. Microbiol. 6. 843-851.
• 86. van Eijsden, R.R., Diaz, C.L., de Pater, D.S. & Kijne, J.W. (1995) Sugar binding activity of pea (Pisum sativum) lectin is essential for heterologous infection of transgenic white clo­ver hairy roots Rhizobium leguminosarum bv. viciae. Plant Mol. Biol. 29, 431-439.
• 87. Fclle, H.H., Kondorosi, E., Kondorosi, A. & Schultze, M. (1996) Rapid alkalinization in alfalfa root hairs in response to rhizobial lipo- chitooligosaccharide signals. Plant J. 10, 295-301.
• 88. Frelin, C., Vigne, P., Ladoux, A. & Lazdunski, M. (1988) The regulation of the intracellular pH in cells from vertebrates. Eur. J. Biochem. 174, 3-14.
• 89. Gibbon, B.C. & Kropf, D.L. (1994) Cytosolic pH gradients associated with tip growth. Sci­ence 263. 1419-1421.
• 90. Hirsch, A.M. (1992) Developmental biology of legume nodulation. New Phytol. 122, 211- 237.
• 91. Legocki, R.P. & Verma, D.P.S. (1980) Identi­fication of "nodule-specific" host proteins (nodulins) involved in the development ofRhi- zobium-\egume symbiosis. Cell 20, 153-163.
• 92. Szczyglowski, K., Legocki, A.B. (1990) Isola­tion .and nucleotide sequence of cDNA clone encoding nodule-specific (hydroxy) proline- rich LENOD2 from yellow lupin. Plant Mol. Biol. 15, 361-363.
• 93. Felle, H.H., Kondorosi, E., Kondorosi, A. & Schultze, M. (1995) Nod signal induced plasma membrane potential changes in al-falfa root hairs are differentially sensitive to structural modifications of the lipochitooli- gosaccharide. Plant J. 7, 939-947.
• 94. Kurkidijan, A.C. (1995) Role of differentiation of root epidermal cells in Nod factor (from Rhizobium melUoW-wduzed root hair depo­larization of Medicago sativa. Plant Physiol. 107, 783-790.