Structure, functions and perspectives of practical application of the signal molecules inducing development of rhizobia-legume symbiosis

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract


Soil bacteria rhizobia establish nitrogen-fixing symbiosis with legume plants. Mutual recognition of symbiotic partners and initiation of nodule formation occur via exchange by molecular signals secreted both by plant and bacteria. This review summarizes recent data about structural diversity, genetic control of biosynthesis and functional role of Nod-factors. The possibilities of practical application of flavonoids and Nod-factors in agriculture are discussed

About the authors

Aleksandra O Ovtsyna

All-Russia Research Institute for Agricultural Microbiology, Saint-Petersburg, RF

Igor A Tikhonovich

All-Russia Research Institute for Agricultural Microbiology, Saint-Petersburg, RF

Email: arriam@arriam.spb.ru. contact@arriam.spb.ru Podbelskiy Ch., 3, Saint-Petersburg, Pushkin-8

References

  1. Atkinson E.M., Pakic M.M., Hindsgaul O. Long S.R. Biosynthesis of Rhizobium meliloti lipooligosaccharide Nod factors: NodA is required for an N-acyltransferase activity//Proc Natl Acad Sci USA. -1994.-Vol.91,N 18. -P.8418-22.
  2. Baev N., Endre G, Petrovics G. et al. 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, -1992. -Vol.228. -P. 113-124.
  3. Bakkers J., Semino C.E., Slroband H. et al. An important developmental role for oligosaccharides during early embryogenesis of cyprinid fish//Proc. Natl. Acad. Sci. USA. -1997. -Vol. 94, P. 7982-7986.
  4. Bauer P., Ratet P., Crespi M.D. et al. Nod factors and cytokinins induce similar cortical cell division, amyloplast deposition and MsENODl 2A expression patterns in alfalfa roots//Plant Journal. -1996, -Vol. 10. -P. 91-105.
  5. Bec-Ferte M.P., Krishnan H.B., Prome D. Structures of nodulation factors from the nitrogen-fixing soybean symbiont Rhizobium fredii USDA257//Biochemistry. -1994. -Vol. 33. -P. 11782-11788.
  6. Bec-Ferte M. P., Krishnan H. В., Savagnac A. et al. Rhizobium fredii synthesizes an array of lipooligosaccharides, including a novel compound with glucose inserted into the backbone of the molecule//FEBS Lett. -1996. -Vol. 393. -P. 273-79.
  7. Begum A.A., Leibovitch S., Migner P., Zhang F. Specific flavonoids induced nod gene expression and pre-activated nod genes of Rhizobium leguminosarum increased pea (Pisum sativum L.) and lentil (Lens culinaris L.) nodulation in controlled growth chamber environments. J. Experimental Botany. -2001. -Vol. 52, N 360. -P.1537-1543.
  8. Bloemberg G.V., Thomas-Oates J.E., Lugtenberg B.J.J, et al. Nodulation protein NodL of Rhizobium leguminosarum O-acetylates lipo-oligosaccharides, chitin fragments and N-acetylglucosamine in vitro//Mol. Microbiol. -1994. -Vol. 11, N 4. -P. 793-804.
  9. Bloemberg G. V., Kamst E., Harteveld M. et al. A central domain of Rhizobium NodE protein mediates host specificity by determining the hydrophobicity of fatty acyl moieties of nodulation factors//Mol. Microbiol.-1995, -Vol. 16,N6, -P. 1123-1136.
  10. Boone СМ., Olsthoorn M.M.A., Dakora F.D. et al. Structural characterisation of lipo-chitin oligosaccharides isolated from Bradyrhizobium aspalati, microsymbionts of commercially important South African legumes//Carbohydr. Res. -1999. -Vol. 317. -P. 55-63.
  11. Boot K.J.M., van Brussel A.A.N., Так Т. et al. Lipochitin oligosaccharides from Rhizobium leguminosarum bv. viciae reduce auxin transport capacity in Vicia sativa subsp. nigra roots//Mol. Plant-Microbe Interact. -1999. -Vol. 12. -P. 839-844.
  12. Broughton W.J., Zhang F., Staehelin C. 2002. Signals exchanged between legumes and Rhizobium: agricultural uses and perspectives//Plant and Soil. -Vol. 252. -P. 129-137.
  13. Cardenas L., Dominguez J., Quinto С et al. Isolation, chemical structures and biological activity of the lipo-chitin oligosaccharide nodulation signals from Rhizobium elti.//Plant Mol. Biol. -1995. -Vol. 29. -P. 453-464.
  14. Cardenas L., Dominquez J., Santana J., Quinto С Role of the nodi and nodj Genes in the transport of Nod metabolites in Rhizobium etli//Gene 1996. -Vol. 173. -P. 183-87.
  15. Cardenas L., Holdaway-Clarke T.L., Sanchez F. et al. Ion changes in legume root hairs responding to Nod factors//Plant Physiology. -2000. -Vol. 123. -P. 443^51.
  16. Carlson R.W., Sanjuan J., Bhat U.V. et al. The structures and biological activities of the lipooligosaccharide nodulation signals produced by type-I and type-II strains of Bradyrhizobium japonicum//J. Biol. Chem. -1993. -Vol. 268. -P. 8372-381.
  17. Cullimore J. V., Ranjeva R., Bono J. -J. Perception of lipo-chitooligo-saccharidic Nod factors in legumes//Trends Plant Sci. -2001. -Vol.6,Nl. -P.24-30.
  18. Cullimore J, Denarie J. Plant sciences. How legumes select their sweet talking symbionts//Science. -2003. -Vol. 302, N 5645. -P. 575-578.
  19. D'Haeze W., Van-MontaguM., Prome J.-C, HolstersM. Carbamoylation of azorhizobial Nod factors is mediated by NodU//Mol. Plant-Microbe Interact. -1999. -Vol. 12. -P. 68-73.
  20. De Billy F, Grosjean C, May S. et al. Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development//Mol. Plant -Microbe Interact. -2001, -Vol. 14. -P. 267-277.
  21. De Jong A.J., Heidslra R., Spaink HP. et al. Rhizobium lipooligosaccharides resque a carrot somatic embrio mutant//The Plant Cell. -1992. -Vol. 5. -P. 615-620.
  22. Debelie F., Rosenberg C, Denarie J. The Rhizobium, Bradyrhizobium, and Azorhizobium NodC proteins are homologous to yeast chitin synthases//Mol. Plant-Microbe Interact. -1992. -Vol. 5.-P. 443-446.
  23. Demoni N., Debelie F., Aurelle H. et al. Role of the Rhizobium meliloti nodF and nodE genes in the biosynthesis of lipo-oligosaccharidic nodulation factors//J. Biol. Chem. -1993. -Vol.268. -P. 20134-42.
  24. Demont N., Ardourel M., Maillet F. et al. The Rhizobium meliloti regulatory nodD3 and syrM genes control the synthesis of a particular class of nodulation factors N-acylated by (omega-l)-hydroxylated fatty acids//EMBO J. -1994. -Vol. 13, N9. -P. 2139-49.
  25. Demonl-Caulet N., Mailetl F., Tailler D. et al. Nodule -inducing activity of synthetic Sinorhizobium meliloti nodulation factors and related lipo -chitooligosaccharides on alfalfa. Importance of the acyl chain structure//Plant Physiology. -1999. -Vol. 120. -P. 83-92.
  26. Denarie J., Debelie F., Prome J.С Rhizobium lipochitooligosac-charide nodulation factors: Signaling molecules mediating recognition and morphogenesis//Ann. Rev. Biochem. -1996. -Vol. 65. -P. 531-535.
  27. Dyachok J.V., Wiweger M., Kenne L., von Arnolds. Endogenous Nod-Factor-Like Signal Molecules Promote Early Somatic Embryo Development in Norway Spruce//Plant Physiology.-2002.-Vol. 128. -P. 523-533.
  28. Ehrhardt D.W., Atkinson E.M., LongS.R. Depolarisation of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors//Science. -1992. -Vol. 256. -P. 998-1000.
  29. Ehrhardt D. W., Wais R., Long S. R. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals//Cell. -1996.-Vol. 85, N5. -P. 673-681.
  30. Evans I.J., Downie J. A. The nodi product of Rhizobium leguminosarum is closely related to ATP-binding bacterial transport proteins: nucleotide sequence of the nodi and nodJ genes//Gene. -1986. -Vol.43. -P. 95-101.
  31. Fel/e H.H., Kondorosi E., Kondorosi A., Schultze M. Nod signal-induced plasma membrane potential changes in alfalfa root hairs are differently sensitive to structural modifications of lipochitooligosac-charide//Plant J. -1995. -Vol. 7. -P. 939-947.
  32. 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. -Vol. 324. -P. 90-92.
  33. Firmin J.L., Wilson K.E., Carlson R.W. et al. Resistance to nodulation of cv. Afghanistan peas is overcome by nodX which mediates an O-acetylaton of the Rhizobium leguminosarum lipo-oligosaccharide nodulation factor//Mol. Microbiol. -1993. -Vol. 10, N2. -P. 351-360.
  34. Fisher R.F, LongS.R. Rhizobium -plant signal exchange//Nature. -1992. -Vol. 357. -P. 655-660.
  35. Folch-Mallol J.L., Marroqui S., Sousa S. et al. Characterization of Rhizobium tropicii CIAT899 nodulation factors: the role of nodH and nodPQ genes in their sulphation. Mol. Plant-Microbe Interact.-1996.-Vol. 9.-P. 151-63.
  36. Frieberg C, Fellay R., BairochA. et al. Molecular basis for symbiosis between Rhizobium and legumes//Nature. -1997. -Vol. 387. -P. 394-401.
  37. Gadella T. W. Jr., Vereb G.Jr., HadriA.E. et al. Microspectroscopic imaging of nodulation factor-binding sites on living Vicia sativa roots using a novel bioactive fluorescent nodulation factor//Biophys. J. -1997. -Vol. 72. -P. 1986-1996.
  38. Geelen D., Mergaert P., Geremia R.A.et al. Identification of nodSUIJ genes in Nod locus 1 of Azorhizobium caulinodans: Evidence that nodS encodes a methyltransferase involved in Nod factor modification//Mol. Microbiol. -1993. -Vol. 9. -P. 145-154.
  39. Geremia R.A., Mergaert P., Geelen D. et al. The NodC protein of Azorhizobium caulinodans is an N-acetylglucosaminotransferase//Proc. Natl. Acad. Sci. USA. -1994. -Vol. 91. -P. 2669-73.
  40. Gil-Serrano A.M., Franco-Rodrigues G., Tejero-Mateo P. et al. Structural determination of the lipo-oligosaccharide nodulation signals produced by Rhizobium fredii HH103. Carbohydr. Res. -1997. -Vol. 303. -P. 435^13
  41. Goedhart J., Rohrig H., Hink MA. et al. Nod factors integrate spontaneously in biomembranes and transfer rapidly between membranes and to root hairs, but transbilayer flip-flop does not occur//Biochemistry. -1999. -Vol. 38, N 33. -P. 10898-907.
  42. Goedhart J., HinkM.A., Visser A.J. In vivo fluorescence correlation microscopy (FCM) reveals accumulation and immobilization of Nod factors in root hair cell walls//Plant J. -2000. -Vol. 21, N 1. -P. 109-19.
  43. Goedhart J., Bono J.J., Bisseling Т., Gadella T. W. Jr. Identical accumulation and immobilization of sulfated and nonsulfated Nod factors in host and nonhost root hair cell walls//Mol. Plant -Microbe Interact. -2003. -Vol. 16, N 10. -P. 884-92.
  44. Hanin M., Jabbouri S., Quesada-Vincens D. et al. Sulphation of Rhizobium sp. NGR234 Nod factors is dependent on noeE, a new host-specificity gene//Mol. Microbiol. -1997. -Vol. 24.-P. 1119-29.
  45. Hadwiger L.A. Host-parasite interactions: elicitation of defense responses in plants with chitosan//EXS. -1999. -Vol. 87. -P. 185-200.
  46. Heidstra R., Geurts R., Franssen H. et al. Root hair deformation activity of nodulation factors and their fate on Vicia sativa//Plant Physiol. -1994. -Vol. 105. -P. 787-797.
  47. Hirsch A.M., Bhwaneswari T. V., Torrey J.G., Bisseling T. Earlyno-duline genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors//Pros. Natl. Acad. Sci. -1989. -Vol. 86. -P. 1244-1248.
  48. Hirsch A.M., Fang Y. Plant hormones and nodulation: what's the connection//Plant Molecular Biology. -1994. -Vol. 26. -P. 5-9.
  49. HirschA.M., LaRue T.A. Is the legume nodule a modified root or stem or an organ sui eneris?//Crit Rev Plant Sci. -1998. -Vol. 16. -P. 361-392.
  50. Hirsch A.M., Lum M.R. andDownie J.A. What Makes the Rhizobia-Legume Symbiosis So Special?//Plant Physiol. -2001. -Vol. 127.-P. 1484-1492.
  51. Hogg В., Davies A.E., Wilson K.E. et al. Competitive nodulation blocking of cv. Afghanistan pea is related to high levels of nodulation factors made by some strains of Rhizobium leguminosarum bv. viciae. 2002. Mol. Plant -Microbe Interact. -Vol. 15, N1. -P. 60-68.
  52. Jabbouri S., Fellay R., Talmont F. el al. Involvement of nodS in N-methylation and nodU in 6-O-carbamoylation of Rhizobium sp. NGR234 Nod factors//J.Biol Chem. -1995. -Vol. 270, N 39. -P. 22968-22973.
  53. Jacobs M., Rubery P.H. Naturally occuring auxin transport regulators//Science. -1988. -Vol. 241. -P. 346-349.
  54. John M., Rohrig H., Schmidt J. et al. Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase//Proc. Natl. Acad. Sci. -1993. -Vol. 90. -P. 625-629.
  55. Kistner C, Parniske M. Evolution of signal transduction in intracellular symbiosis//Trends Plant Sci. -2002. -Vol. 7, N 11. -P. 511-518.
  56. Lerouge P., Roche P., Faucher C. et al. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulfated and acylated glucosamine oligosaccharide//Nature. -1990. -Vol. 344. -P. 781-784.
  57. Limpens E., Bisseling T. Signaling in symbiosis//Curr Opin Plant Biol. -2003. -Vol. 6, N 4. -P. 343-50.
  58. Lian В., Souleimanov A., ZhouX., SmithD.L. In vitro induction of lipo-chitooligosaccharide production in Bradyrhizobium japonicum cultures by root extracts from non-leguminous plants//Microbiol Res.-2002. -Vol. 157.N3. -P. 157-60.
  59. Lopez-LaraI.M.,vandenBerg J.D.J., Thomas-OatesJ.E. Structural identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti//Mol. Microbiol. -1995a. -Vol. 15. -P. 627-38.
  60. Lopez-Lara I.M., van der Drift K.M.G.M., van Brussel A.A.N, et al. Induction of nodule primordia on Phaseolus and Acacia by lipo -chitin oligosaccaride nodlation signals from broad -host -range Rhizobium strain GRH2//Plant Mol. Biol. -1995b. -Vol. 29. -P. 465-477.
  61. Lopez-Lara I. M., Blok-Tip L., Quinto C. et al. NodZ of Bradyrhizobium extends the nodulation host range of Rhizobium by adding a fucosyl residue to nodulation signals//Mol. Microbiol. -1996. -Vol.21,N2. -P.397-408.
  62. Lorquin J., Lortet G, Ferro M. et al. Sinorhizobium teranga bv. acaciae ORS1073 and Rhizobium sp. strain ORS1001, two distantly related Acacia-nodulating strains, produce similar Nod factors that are O-carbamoylated, N-methylated, and mainly sulphated//J. Bacterid. -1997a. -Vol. 179. -P. 3079-83.
  63. Lorquin J., Lortet G., Ferro M. et al. Nod factors from Sinorhizobium saheli and S.teranga bv. sesbaniae are both arabinosylated and fucosylated, a structural feature specific to Sesbania rostrata symbionts//Mol. Plant-Microbe Interact. -1997b. -Vol. 10. -P. 879-90.
  64. Mathesius U., SchlamanH.R.M., SpainkH.P. etal. Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides//Plant J. -1998. -Vol. 14. -P. 23-34.
  65. McCoy E. Infection by Bact. Radicicola in relation to the microchemist-ry of the host's cell walls//Proc.R. Soc. (London) Ser.B. -1932. -Vol. 110. -P. 514-533.
  66. Mergaert P., D'Haeze W., Fernandez-Lopez M. etal. Fucosylation and arabinosylation of Nod factors in Azorhizobium caulinodans: involvement of nolK, nodZ, as well as noeC and/or downstream genes//Mol. Microbiol. -1996. -Vol. 21, N 2. -P. 409^119.
  67. Mergaert P., VanMontagu M., Holsters M. Molecular mechanisms ofNod factor diversity//Mol. Microbiol. -1997. -Vol. 25. -P. 811-17.
  68. Minami E., KouchiH., CohnJ.R., Ogawa Т., Stacey G. Expression of the early nodulin, ENOD40, in soybean roots in response to various lipo-chitin signal molecules//Plant Journal. -1996.-Vol. 10.-P. 23-32.
  69. Oldroyd G.E.D. Dissecting Symbiosis: Developments in Nod Factor Signal Transduction//Annals of Botany. -2001. -Vol. 87. -P. 709-718.
  70. Olsthoorn M.M.A., Lopez-Lara 1.М., Petersen BO. et al. Novel branched Nod factor structure results from oc-(l-3) fucosyl transferase activity: the major lipo-chitin oligosaccharides from Mesorhizobium loti strain NZP2213 bear an (3-(l-3) fucosyl substituent on a non-terminal backbone residue//Biochemistry. -1998. -Vol. 37. -P. 9024-32.
  71. Ovtsyna A.O., Rademaker G.-J., Esser E. et al. 1999. Comparison of characteristics of the nodX genes from various Rhizobium leguminosarum strains//Mol. Plant -Microbe Interact., Vol. 12, N 3. -P. 252-258.
  72. Ovtsyna A.O., Schultze M., Tikhonovich I.A. el al. Nod factors of Rhizobium leguminosarum bv. viciae and their fucosylated derivatives stimulate a Nod factor cleaving activity in pea roots and are hydrolyzed in vitro by plant chitinases at different rates//Mol. Plant-Microbe Interact. -2000. -Vol. 13, N 8. -■ P. 799-807.
  73. Ovtsyna АО. and Staehelin C. Bacterial signals required for the Rhizobium-legume symbiosis. In: «Recent Research Developments in Microbiology». Керала, Индия: Transworld Research Network, подано в печать.
  74. Pacios-Bras С, van der Burgt Y.E.M., Deelder A.M. et al. Novel lipo-chitin oligosaccharide structures produced by Rhizobium etli KIM5s//Carbohydrate Research. -2002. -Vol. 337. -1193-1202.
  75. Perret X., Staehelin C, Broughton W.J. Molecular basis of symbiotic promiscuity//Microbiol. Mol. Biol. Rev. -2000. -Vol. 64. -P. 180-201.
  76. Peters N.K., Frost J. W., LongS.R. A plant flavone, luteolin, induces expression of Rhizobium meliloti genes//Science. -1986. -Vol.233.-P. 977-980.
  77. Poupot R., Martinez-Romero E., Prome J. -C. Nodulation factors from Rhizobium tropici are sulfated or nonsulfated chitopentasaccharides containing an N-methyl-N-acylglucosaminyl terminus//Biochemistry. -1993. -Vol. 32. -P. 10430-35.
  78. Poupot R., Martinez-Romero E., Gautier N. Prome J.-C. Wild-type Rhizobium etli, a bean symbiont, produces acetyl-fucosylated, N-methylated, and carbamoylated nodulation factors//J. Biol. Chem. -1995. -Vol. 270. -P. 6050-55.
  79. Price N.P.J., Relic В., Taimont F. et al. Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated//Mol. Microbiol. -1992. -Vol. 6. -P. 3575-84.
  80. Prithiviraj В., ZhouX., Souleimanov A., Kahn W.M., Smith DL. A host-specific bacteria-to-plant signal molecule (Nod factor) enhances germination and early growth of diverse crop plants//Planta. -2003. -Vol. 216, N 3. -P. 437^15.
  81. Pueppke S.G., Broughton W.J. Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges//Mol. Plant-Microbe Interact. -1999. -Vol. 12. -P. 293-318.
  82. Recourt K., Schripsema J., Kijne J.W. et al. Inoculation of Vicia sativa subsp. nigra roots with Rhizobium leguminosarum bv viciae results in release of nod gene activating flavanones and chalcones//Plant Mol. Biol. -1991. -Vol. 16. -P. 841-852.
  83. Redmond J. W., BatleyM., Djorjevic M.A. etal. Flavones induce expression of nodulation genes in Rhizobium//Nature. -1986. -Vol.323. -P. 632-635.
  84. Relic В., Perret X., Estrada-Garcia M. T. el al. Nod factors of Rhizobium are a key to the legume door//Mol. Microbiol. -1994. -Vol. 13,N1. -P. 171-178.
  85. Ritsema Т., Wijffelman A.H.M., Lugtenberg B.J.J., Spaink HP. Rhizobium nodulation protein NodA is a host -specific determinant of the transfer of fatty acids in Nod factor biosynthesis//Mol. Gen. Genet. -1996. -Vol. 251. -P. 44-51.
  86. Roche P., Debelle F., Mailett F. et al. Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipooligosaccharide signals//Cell. -1991. -Vol. 67. P. 1131-1143.
  87. Rosa F., Sargent T.D., Rebbert M.L. et al. Accumulation and decay of DG42 geneproduct follow a gradient pattern during Xenopus embryogenesis//Developmental Biology. -1988. -Vol. 129.-P. 114-23.
  88. Sanjuan J., Carlson R. W., Spaink H.P. et al. A 2-O-methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum//Proc. Natl. Acad. Sci. -USA. -1992. -Vol. 89. -P. 8789-93.
  89. Savoure A., Magyar Z., Pierre M. et al. Activation of the cell cycle machinery and the isoflavonoid biosynthesis pathway by active Rhizobium meliloti Nod signal molecules in Medicago microcallus suspensions//EMBO J. -1994. -Vol. 13. -P. 1093-1102.
  90. Schmidt J., Rohgrig H., John M. et al. Alteration of plant growth and development by Rhizobium nodA and nodB genes involved in the synthesis of oligosaccharide signal molecules//The Plant J. -1993. -Vol. 4, N 4. -P. 651-658.
  91. Schmidt P.E., Broughton W.J., Werner D. Nod factors of Bradyrhizobium japonicum and Rhizobium sp. NGR234 induce flavonoid accumulation in soybean root exudates//MPMI. -1994. -Vol. 7, N 3. -P. 384-390.
  92. Schultze M., Kondorosi A. Regulation of symbiotic root nodule development//Ann. Rev Genet. -1998. -Vol. 32. -P. 33-57.
  93. Schwedock J., Long S.R. ATPsulphurylaseactivityofthenodPand nodQ gene products of Rhizobium meliloti//Nature. -1990. -Vol.348. -P. 644-647.
  94. Shearman C.A., RossenL., Johnston A. W.B., DownieJ.A. 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//TheEMBOJ.-1986. -Vol. 5, N4. -P. 647-652.
  95. Semino C.E., Specht C.A., RaimondiA., Robbins P. W. Homologs of 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. USA. -1996. -Vol.93. -P. 4548-4553.
  96. Slabas A.R., Chase D., Nishida I. et al. Molecular cloning of higher-plant 3-oxoacyl-(acyl carrier protein) reductase -Sequence identities with the nodG-gene product of the nitrogen-fixing soil bacterium Rhizobium meliloti//Biochem. J. -1992. -Vol.283.-P. 321-326.
  97. Soria-Diaz M.E., Tejero-Mateo P., Espartero J.L. et al. Structural determination of the lipo-chitin oligosaccharide nodulation signals produced by Rhizobium giardinii bv. giardinii H152//Carbohydrate Research. -2003. -Vol. 338. -P. 237-250.
  98. Spaink H.P., Wijffelman C.A., Pees E. etal. Rhizobium nodulation gene nodD as a determinant of host specificity//Nature. -1987. -Vol.328. -P. 337-340.
  99. Spaink H.P., Sheeley D.M., van Brussel A.A.N, etal. A novel, highly unsaturated, fatty acid moiety of lipooligosaccharide signals determines host specificity of Rhizobium leguminosarum//Nature. -1991. -Vol.354. -P. 125-130.
  100. Spaink H.P. Bloemberg G.V., Van Brussel A.A.N, et al. Host specificity of Rhizobium leguminosarum is determined by the hydrophobisity of highly unsaturated fatty acyl moieties of the nodulation factors//Mol. Plant-Microbe Interact. -1995a. -Vol. 8.-P. 155-164.
  101. Spaink H.P., Wijfjes A.H.M., Lugtenberg B.J.J. Rhizobium Nodi and NodJ proteins play a role in the efficiency of secretion of lipochitin oligosaccarides Hi. Bacteriol. -1995b. -Vol. 177. -P. 6276-6281.
  102. Spaink H.P. Regulation of plant morphogenesis by lipo-chitin oligosaccharides//Crit. Rev. Plant Sci. -1996. -Vol. 15. -P. 559-582.
  103. Spaink H.P. Root nodulation and infection factors produced by rhizobial bacteria//Annual Review of Microbiology. -2000. -Vol.54. -P. 257-288.
  104. Stacey G., Luka S., Sanjuan J. et al. NodZ, a unique host -specific nodulation gene, is involved in the fucosylation of the lipooligosaccharide nodulation signal of Brady rhizobium japonicum//J. Bacteriol. -1994. -Vol. 176. -P. 620-633.
  105. Staehelin С, Schultze M., Kondorosi E. et al. Structural modifications in Rhizobium meliloti Nod factors influence their stability against hydrolysis by root chitinases//The Plant J. -1994. -Vol. 5. -N 3. -P. 319-330.
  106. Staehelin C, Schultze M., Kondorosi E., Kondorosi A. Lipo-chitooligosaccharide Nodulation Signals from Rhizobium meliloti Induce Their Rapid Degradation by the Host Plant Alfalfa//Plant Physiol,-1995.-Vol. 108. -P. 1607-1614.
  107. Stokkermans T.J. W., Ikeshita S., Cohn J. et al. Structural requirements of synthetic and natural product lipo-chitin oligosaccharides for induction of nodule primordia on Glycine soja//Plant Physiol.-1995.-Vol. 108.-P. 1587-1595
  108. Timmers A.C.J., Auriac M.-C, de Billy F., Truchet G. Nod factor internalization and microtubular cytoskeleton changes occur concomitantly during nodule differentiation in alfalfa//Development. -1998. -Vol. 125. -P. 339-349.
  109. Truchet G, Roche P., Lerouge P. et al. Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa//Nature. -1991. -Vol. 351. -P. 670-673.
  110. Van Brussel A.A.N., Zaat S.A.J., Canter Cremers H.C.J, et я/. Role of plant root exudate and Sym plasmid-localised nodulation genes in the synthesis by Rhizobium leguminosarum of Tsr factor, which causes thick and short roots on common vetch//J.Bacteriol. -1986. -Vol. 165. -P. 517-522.
  111. Van Brussel A.A.N., Recourt K, Pees E. et al. Abiovar -specific signal of Rhizobium leguminosarum bv. viciae induces increased nodulation gene -inducing activity in root exudates of Vicia sativa subsp. nigra//J. Bacteriol. -1990. -Vol. 172. -P. 5394-5401.
  112. Van Brussel A.A.N., Bakhuizen R., van Spronsen P.C. et al. Induction of pre -infection thread structures in the leguminous host plant by mitogenic lipooligosaccharides of Rhizobium//Science. -1992. -Vol. 257. -P. 70-72.
  113. van der Drift K.M.G.M., Spaink HP., Bloemberg G.V. et al. Rhizobium leguminosarum bv. trifolii produces lipochitin oligosaccharides with nodE-dependent highly unsaturated fatty acyl moieties: an electrospray ionisation and collision induced dissociation tandem mass spectrometric study//J. Biol. Chem. -1996. -Vol. 271. -P. 22563-69.
  114. vander Hoist P.P.G., Schlaman H.R.M. and Spaink HP. Proteins involved in the production and perception of oligosaccharides in relation to plant and animal development//Current Opinion in Structural Biology. -2001. -Vol. 11. -P. 608-616.
  115. van Hengel A. J., Tadesse Z., Immerzeel P. et al. N-Acetyl-glucosamine and Glucosamine-Containing Arabinogalactan Proteins Control Somatic Embryogenesis//Plant Physiology. -2001. -Vol. 125.-P. 1880-1890.
  116. Vazquez M., Santana O., Quinto C. The Nodi and NodJ proteins from Rhizobium and Bradyrhizobium strains are similar to capsular polysaccharide secretion protein from Gram-negative bacteria//Mol. Microbiol. -1993. -Vol. 8, N 1. -P. 369-377.
  117. Xie Z.-P., Staehelin C, Vierheilig H. et al. 1995. Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans//Plant Physiol. -Vol. 108. -P. 1519-1525.
  118. Yang G.-P., Debelle F., Savagnac A. et al. 1999. Structure of the Mesorhizobium huakuii and Rhizobium galegae Nod factors: a cluster of phylogenetically related legumes are nodulated by rhizobia producing Nod factors with a, b-unsaturated N-acyl substitutions//Mol. Microbiol. -Vol. 34. -P. 227-37.
  119. Zaat S. A.J., Wijffelman С A., Mulders H.M. etal. Root exudates of various host plant of Rhizobium leguminosarum contain different sets of inducers of Rhizobium nodulation genes//Plant Physiol. -1988. -Vol. 86. -P. 1298-1303.
  120. Zhang F. and Smith D.L. Preincubation ofBradyrhizobiumjaponicum with genistein accelerates nodule development of soybean [Glycine max (L.) Merr.] at suboptimal root zone temperatures//Plant Physiol. -1995. -Vol. 108. -P. 961-968.
  121. Atkinson E.M., Pakic M.M., Hindsgaul O. Long S.R. Biosynthesis of Rhizobium meliloti lipooligosaccharide Nod factors: NodA is required for an N-acyltransferase activity//Proc Natl Acad Sci USA. -1994.-Vol.91,N 18. -P.8418-22.
  122. Baev N., Endre G, Petrovics G. et al. 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, -1992. -Vol.228. -P. 113-124.
  123. Bakkers J., Semino C.E., Slroband H. et al. An important developmental role for oligosaccharides during early embryogenesis of cyprinid fish//Proc. Natl. Acad. Sci. USA. -1997. -Vol. 94, P. 7982-7986.
  124. Bauer P., Ratet P., Crespi M.D. et al. Nod factors and cytokinins induce similar cortical cell division, amyloplast deposition and MsENODl 2A expression patterns in alfalfa roots//Plant Journal. -1996, -Vol. 10. -P. 91-105.
  125. Bec-Ferte M.P., Krishnan H.B., Prome D. Structures of nodulation factors from the nitrogen-fixing soybean symbiont Rhizobium fredii USDA257//Biochemistry. -1994. -Vol. 33. -P. 11782-11788.
  126. Bec-Ferte M. P., Krishnan H. В., Savagnac A. et al. Rhizobium fredii synthesizes an array of lipooligosaccharides, including a novel compound with glucose inserted into the backbone of the molecule//FEBS Lett. -1996. -Vol. 393. -P. 273-79.
  127. Begum A.A., Leibovitch S., Migner P., Zhang F. Specific flavonoids induced nod gene expression and pre-activated nod genes of Rhizobium leguminosarum increased pea (Pisum sativum L.) and lentil (Lens culinaris L.) nodulation in controlled growth chamber environments. J. Experimental Botany. -2001. -Vol. 52, N 360. -P.1537-1543.
  128. Bloemberg G.V., Thomas-Oates J.E., Lugtenberg B.J.J, et al. Nodulation protein NodL of Rhizobium leguminosarum O-acetylates lipo-oligosaccharides, chitin fragments and N-acetylglucosamine in vitro//Mol. Microbiol. -1994. -Vol. 11, N 4. -P. 793-804.
  129. Bloemberg G. V., Kamst E., Harteveld M. et al. A central domain of Rhizobium NodE protein mediates host specificity by determining the hydrophobicity of fatty acyl moieties of nodulation factors//Mol. Microbiol.-1995, -Vol. 16,N6, -P. 1123-1136.
  130. Boone СМ., Olsthoorn M.M.A., Dakora F.D. et al. Structural characterisation of lipo-chitin oligosaccharides isolated from Bradyrhizobium aspalati, microsymbionts of commercially important South African legumes//Carbohydr. Res. -1999. -Vol. 317. -P. 55-63.
  131. Boot K.J.M., van Brussel A.A.N., Так Т. et al. Lipochitin oligosaccharides from Rhizobium leguminosarum bv. viciae reduce auxin transport capacity in Vicia sativa subsp. nigra roots//Mol. Plant-Microbe Interact. -1999. -Vol. 12. -P. 839-844.
  132. Broughton W.J., Zhang F., Staehelin C. 2002. Signals exchanged between legumes and Rhizobium: agricultural uses and perspectives//Plant and Soil. -Vol. 252. -P. 129-137.
  133. Cardenas L., Dominguez J., Quinto С et al. Isolation, chemical structures and biological activity of the lipo-chitin oligosaccharide nodulation signals from Rhizobium elti.//Plant Mol. Biol. -1995. -Vol. 29. -P. 453-464.
  134. Cardenas L., Dominquez J., Santana J., Quinto С Role of the nodi and nodj Genes in the transport of Nod metabolites in Rhizobium etli//Gene 1996. -Vol. 173. -P. 183-87.
  135. Cardenas L., Holdaway-Clarke T.L., Sanchez F. et al. Ion changes in legume root hairs responding to Nod factors//Plant Physiology. -2000. -Vol. 123. -P. 443^51.
  136. Carlson R.W., Sanjuan J., Bhat U.V. et al. The structures and biological activities of the lipooligosaccharide nodulation signals produced by type-I and type-II strains of Bradyrhizobium japonicum//J. Biol. Chem. -1993. -Vol. 268. -P. 8372-381.
  137. Cullimore J. V., Ranjeva R., Bono J. -J. Perception of lipo-chitooligo-saccharidic Nod factors in legumes//Trends Plant Sci. -2001. -Vol.6,Nl. -P.24-30.
  138. Cullimore J, Denarie J. Plant sciences. How legumes select their sweet talking symbionts//Science. -2003. -Vol. 302, N 5645. -P. 575-578.
  139. D'Haeze W., Van-MontaguM., Prome J.-C, HolstersM. Carbamoylation of azorhizobial Nod factors is mediated by NodU//Mol. Plant-Microbe Interact. -1999. -Vol. 12. -P. 68-73.
  140. De Billy F, Grosjean C, May S. et al. Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development//Mol. Plant -Microbe Interact. -2001, -Vol. 14. -P. 267-277.
  141. De Jong A.J., Heidslra R., Spaink HP. et al. Rhizobium lipooligosaccharides resque a carrot somatic embrio mutant//The Plant Cell. -1992. -Vol. 5. -P. 615-620.
  142. Debelie F., Rosenberg C, Denarie J. The Rhizobium, Bradyrhizobium, and Azorhizobium NodC proteins are homologous to yeast chitin synthases//Mol. Plant-Microbe Interact. -1992. -Vol. 5.-P. 443-446.
  143. Demoni N., Debelie F., Aurelle H. et al. Role of the Rhizobium meliloti nodF and nodE genes in the biosynthesis of lipo-oligosaccharidic nodulation factors//J. Biol. Chem. -1993. -Vol.268. -P. 20134-42.
  144. Demont N., Ardourel M., Maillet F. et al. The Rhizobium meliloti regulatory nodD3 and syrM genes control the synthesis of a particular class of nodulation factors N-acylated by (omega-l)-hydroxylated fatty acids//EMBO J. -1994. -Vol. 13, N9. -P. 2139-49.
  145. Demonl-Caulet N., Mailetl F., Tailler D. et al. Nodule -inducing activity of synthetic Sinorhizobium meliloti nodulation factors and related lipo -chitooligosaccharides on alfalfa. Importance of the acyl chain structure//Plant Physiology. -1999. -Vol. 120. -P. 83-92.
  146. Denarie J., Debelie F., Prome J.С Rhizobium lipochitooligosac-charide nodulation factors: Signaling molecules mediating recognition and morphogenesis//Ann. Rev. Biochem. -1996. -Vol. 65. -P. 531-535.
  147. Dyachok J.V., Wiweger M., Kenne L., von Arnolds. Endogenous Nod-Factor-Like Signal Molecules Promote Early Somatic Embryo Development in Norway Spruce//Plant Physiology.-2002.-Vol. 128. -P. 523-533.
  148. Ehrhardt D.W., Atkinson E.M., LongS.R. Depolarisation of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors//Science. -1992. -Vol. 256. -P. 998-1000.
  149. Ehrhardt D. W., Wais R., Long S. R. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals//Cell. -1996.-Vol. 85, N5. -P. 673-681.
  150. Evans I.J., Downie J. A. The nodi product of Rhizobium leguminosarum is closely related to ATP-binding bacterial transport proteins: nucleotide sequence of the nodi and nodJ genes//Gene. -1986. -Vol.43. -P. 95-101.
  151. Fel/e H.H., Kondorosi E., Kondorosi A., Schultze M. Nod signal-induced plasma membrane potential changes in alfalfa root hairs are differently sensitive to structural modifications of lipochitooligosac-charide//Plant J. -1995. -Vol. 7. -P. 939-947.
  152. 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. -Vol. 324. -P. 90-92.
  153. Firmin J.L., Wilson K.E., Carlson R.W. et al. Resistance to nodulation of cv. Afghanistan peas is overcome by nodX which mediates an O-acetylaton of the Rhizobium leguminosarum lipo-oligosaccharide nodulation factor//Mol. Microbiol. -1993. -Vol. 10, N2. -P. 351-360.
  154. Fisher R.F, LongS.R. Rhizobium -plant signal exchange//Nature. -1992. -Vol. 357. -P. 655-660.
  155. Folch-Mallol J.L., Marroqui S., Sousa S. et al. Characterization of Rhizobium tropicii CIAT899 nodulation factors: the role of nodH and nodPQ genes in their sulphation. Mol. Plant-Microbe Interact.-1996.-Vol. 9.-P. 151-63.
  156. Frieberg C, Fellay R., BairochA. et al. Molecular basis for symbiosis between Rhizobium and legumes//Nature. -1997. -Vol. 387. -P. 394-401.
  157. Gadella T. W. Jr., Vereb G.Jr., HadriA.E. et al. Microspectroscopic imaging of nodulation factor-binding sites on living Vicia sativa roots using a novel bioactive fluorescent nodulation factor//Biophys. J. -1997. -Vol. 72. -P. 1986-1996.
  158. Geelen D., Mergaert P., Geremia R.A.et al. Identification of nodSUIJ genes in Nod locus 1 of Azorhizobium caulinodans: Evidence that nodS encodes a methyltransferase involved in Nod factor modification//Mol. Microbiol. -1993. -Vol. 9. -P. 145-154.
  159. Geremia R.A., Mergaert P., Geelen D. et al. The NodC protein of Azorhizobium caulinodans is an N-acetylglucosaminotransferase//Proc. Natl. Acad. Sci. USA. -1994. -Vol. 91. -P. 2669-73.
  160. Gil-Serrano A.M., Franco-Rodrigues G., Tejero-Mateo P. et al. Structural determination of the lipo-oligosaccharide nodulation signals produced by Rhizobium fredii HH103. Carbohydr. Res. -1997. -Vol. 303. -P. 435^13
  161. Goedhart J., Rohrig H., Hink MA. et al. Nod factors integrate spontaneously in biomembranes and transfer rapidly between membranes and to root hairs, but transbilayer flip-flop does not occur//Biochemistry. -1999. -Vol. 38, N 33. -P. 10898-907.
  162. Goedhart J., HinkM.A., Visser A.J. In vivo fluorescence correlation microscopy (FCM) reveals accumulation and immobilization of Nod factors in root hair cell walls//Plant J. -2000. -Vol. 21, N 1. -P. 109-19.
  163. Goedhart J., Bono J.J., Bisseling Т., Gadella T. W. Jr. Identical accumulation and immobilization of sulfated and nonsulfated Nod factors in host and nonhost root hair cell walls//Mol. Plant -Microbe Interact. -2003. -Vol. 16, N 10. -P. 884-92.
  164. Hanin M., Jabbouri S., Quesada-Vincens D. et al. Sulphation of Rhizobium sp. NGR234 Nod factors is dependent on noeE, a new host-specificity gene//Mol. Microbiol. -1997. -Vol. 24.-P. 1119-29.
  165. Hadwiger L.A. Host-parasite interactions: elicitation of defense responses in plants with chitosan//EXS. -1999. -Vol. 87. -P. 185-200.
  166. Heidstra R., Geurts R., Franssen H. et al. Root hair deformation activity of nodulation factors and their fate on Vicia sativa//Plant Physiol. -1994. -Vol. 105. -P. 787-797.
  167. Hirsch A.M., Bhwaneswari T. V., Torrey J.G., Bisseling T. Earlyno-duline genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors//Pros. Natl. Acad. Sci. -1989. -Vol. 86. -P. 1244-1248.
  168. Hirsch A.M., Fang Y. Plant hormones and nodulation: what's the connection//Plant Molecular Biology. -1994. -Vol. 26. -P. 5-9.
  169. HirschA.M., LaRue T.A. Is the legume nodule a modified root or stem or an organ sui eneris?//Crit Rev Plant Sci. -1998. -Vol. 16. -P. 361-392.
  170. Hirsch A.M., Lum M.R. andDownie J.A. What Makes the Rhizobia-Legume Symbiosis So Special?//Plant Physiol. -2001. -Vol. 127.-P. 1484-1492.
  171. Hogg В., Davies A.E., Wilson K.E. et al. Competitive nodulation blocking of cv. Afghanistan pea is related to high levels of nodulation factors made by some strains of Rhizobium leguminosarum bv. viciae. 2002. Mol. Plant -Microbe Interact. -Vol. 15, N1. -P. 60-68.
  172. Jabbouri S., Fellay R., Talmont F. el al. Involvement of nodS in N-methylation and nodU in 6-O-carbamoylation of Rhizobium sp. NGR234 Nod factors//J.Biol Chem. -1995. -Vol. 270, N 39. -P. 22968-22973.
  173. Jacobs M., Rubery P.H. Naturally occuring auxin transport regulators//Science. -1988. -Vol. 241. -P. 346-349.
  174. John M., Rohrig H., Schmidt J. et al. Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase//Proc. Natl. Acad. Sci. -1993. -Vol. 90. -P. 625-629.
  175. Kistner C, Parniske M. Evolution of signal transduction in intracellular symbiosis//Trends Plant Sci. -2002. -Vol. 7, N 11. -P. 511-518.
  176. Lerouge P., Roche P., Faucher C. et al. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulfated and acylated glucosamine oligosaccharide//Nature. -1990. -Vol. 344. -P. 781-784.
  177. Limpens E., Bisseling T. Signaling in symbiosis//Curr Opin Plant Biol. -2003. -Vol. 6, N 4. -P. 343-50.
  178. Lian В., Souleimanov A., ZhouX., SmithD.L. In vitro induction of lipo-chitooligosaccharide production in Bradyrhizobium japonicum cultures by root extracts from non-leguminous plants//Microbiol Res.-2002. -Vol. 157.N3. -P. 157-60.
  179. Lopez-LaraI.M.,vandenBerg J.D.J., Thomas-OatesJ.E. Structural identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti//Mol. Microbiol. -1995a. -Vol. 15. -P. 627-38.
  180. Lopez-Lara I.M., van der Drift K.M.G.M., van Brussel A.A.N, et al. Induction of nodule primordia on Phaseolus and Acacia by lipo -chitin oligosaccaride nodlation signals from broad -host -range Rhizobium strain GRH2//Plant Mol. Biol. -1995b. -Vol. 29. -P. 465-477.
  181. Lopez-Lara I. M., Blok-Tip L., Quinto C. et al. NodZ of Bradyrhizobium extends the nodulation host range of Rhizobium by adding a fucosyl residue to nodulation signals//Mol. Microbiol. -1996. -Vol.21,N2. -P.397-408.
  182. Lorquin J., Lortet G, Ferro M. et al. Sinorhizobium teranga bv. acaciae ORS1073 and Rhizobium sp. strain ORS1001, two distantly related Acacia-nodulating strains, produce similar Nod factors that are O-carbamoylated, N-methylated, and mainly sulphated//J. Bacterid. -1997a. -Vol. 179. -P. 3079-83.
  183. Lorquin J., Lortet G., Ferro M. et al. Nod factors from Sinorhizobium saheli and S.teranga bv. sesbaniae are both arabinosylated and fucosylated, a structural feature specific to Sesbania rostrata symbionts//Mol. Plant-Microbe Interact. -1997b. -Vol. 10. -P. 879-90.
  184. Mathesius U., SchlamanH.R.M., SpainkH.P. etal. Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides//Plant J. -1998. -Vol. 14. -P. 23-34.
  185. McCoy E. Infection by Bact. Radicicola in relation to the microchemist-ry of the host's cell walls//Proc.R. Soc. (London) Ser.B. -1932. -Vol. 110. -P. 514-533.
  186. Mergaert P., D'Haeze W., Fernandez-Lopez M. etal. Fucosylation and arabinosylation of Nod factors in Azorhizobium caulinodans: involvement of nolK, nodZ, as well as noeC and/or downstream genes//Mol. Microbiol. -1996. -Vol. 21, N 2. -P. 409^119.
  187. Mergaert P., VanMontagu M., Holsters M. Molecular mechanisms ofNod factor diversity//Mol. Microbiol. -1997. -Vol. 25. -P. 811-17.
  188. Minami E., KouchiH., CohnJ.R., Ogawa Т., Stacey G. Expression of the early nodulin, ENOD40, in soybean roots in response to various lipo-chitin signal molecules//Plant Journal. -1996.-Vol. 10.-P. 23-32.
  189. Oldroyd G.E.D. Dissecting Symbiosis: Developments in Nod Factor Signal Transduction//Annals of Botany. -2001. -Vol. 87. -P. 709-718.
  190. Olsthoorn M.M.A., Lopez-Lara 1.М., Petersen BO. et al. Novel branched Nod factor structure results from oc-(l-3) fucosyl transferase activity: the major lipo-chitin oligosaccharides from Mesorhizobium loti strain NZP2213 bear an (3-(l-3) fucosyl substituent on a non-terminal backbone residue//Biochemistry. -1998. -Vol. 37. -P. 9024-32.
  191. Ovtsyna A.O., Rademaker G.-J., Esser E. et al. 1999. Comparison of characteristics of the nodX genes from various Rhizobium leguminosarum strains//Mol. Plant -Microbe Interact., Vol. 12, N 3. -P. 252-258.
  192. Ovtsyna A.O., Schultze M., Tikhonovich I.A. el al. Nod factors of Rhizobium leguminosarum bv. viciae and their fucosylated derivatives stimulate a Nod factor cleaving activity in pea roots and are hydrolyzed in vitro by plant chitinases at different rates//Mol. Plant-Microbe Interact. -2000. -Vol. 13, N 8. -■ P. 799-807.
  193. Ovtsyna АО. and Staehelin C. Bacterial signals required for the Rhizobium-legume symbiosis. In: «Recent Research Developments in Microbiology». Керала, Индия: Transworld Research Network, подано в печать.
  194. Pacios-Bras С, van der Burgt Y.E.M., Deelder A.M. et al. Novel lipo-chitin oligosaccharide structures produced by Rhizobium etli KIM5s//Carbohydrate Research. -2002. -Vol. 337. -1193-1202.
  195. Perret X., Staehelin C, Broughton W.J. Molecular basis of symbiotic promiscuity//Microbiol. Mol. Biol. Rev. -2000. -Vol. 64. -P. 180-201.
  196. Peters N.K., Frost J. W., LongS.R. A plant flavone, luteolin, induces expression of Rhizobium meliloti genes//Science. -1986. -Vol.233.-P. 977-980.
  197. Poupot R., Martinez-Romero E., Prome J. -C. Nodulation factors from Rhizobium tropici are sulfated or nonsulfated chitopentasaccharides containing an N-methyl-N-acylglucosaminyl terminus//Biochemistry. -1993. -Vol. 32. -P. 10430-35.
  198. Poupot R., Martinez-Romero E., Gautier N. Prome J.-C. Wild-type Rhizobium etli, a bean symbiont, produces acetyl-fucosylated, N-methylated, and carbamoylated nodulation factors//J. Biol. Chem. -1995. -Vol. 270. -P. 6050-55.
  199. Price N.P.J., Relic В., Taimont F. et al. Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated//Mol. Microbiol. -1992. -Vol. 6. -P. 3575-84.
  200. Prithiviraj В., ZhouX., Souleimanov A., Kahn W.M., Smith DL. A host-specific bacteria-to-plant signal molecule (Nod factor) enhances germination and early growth of diverse crop plants//Planta. -2003. -Vol. 216, N 3. -P. 437^15.
  201. Pueppke S.G., Broughton W.J. Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges//Mol. Plant-Microbe Interact. -1999. -Vol. 12. -P. 293-318.
  202. Recourt K., Schripsema J., Kijne J.W. et al. Inoculation of Vicia sativa subsp. nigra roots with Rhizobium leguminosarum bv viciae results in release of nod gene activating flavanones and chalcones//Plant Mol. Biol. -1991. -Vol. 16. -P. 841-852.
  203. Redmond J. W., BatleyM., Djorjevic M.A. etal. Flavones induce expression of nodulation genes in Rhizobium//Nature. -1986. -Vol.323. -P. 632-635.
  204. Relic В., Perret X., Estrada-Garcia M. T. el al. Nod factors of Rhizobium are a key to the legume door//Mol. Microbiol. -1994. -Vol. 13,N1. -P. 171-178.
  205. Ritsema Т., Wijffelman A.H.M., Lugtenberg B.J.J., Spaink HP. Rhizobium nodulation protein NodA is a host -specific determinant of the transfer of fatty acids in Nod factor biosynthesis//Mol. Gen. Genet. -1996. -Vol. 251. -P. 44-51.
  206. Roche P., Debelle F., Mailett F. et al. Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipooligosaccharide signals//Cell. -1991. -Vol. 67. P. 1131-1143.
  207. Rosa F., Sargent T.D., Rebbert M.L. et al. Accumulation and decay of DG42 geneproduct follow a gradient pattern during Xenopus embryogenesis//Developmental Biology. -1988. -Vol. 129.-P. 114-23.
  208. Sanjuan J., Carlson R. W., Spaink H.P. et al. A 2-O-methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum//Proc. Natl. Acad. Sci. -USA. -1992. -Vol. 89. -P. 8789-93.
  209. Savoure A., Magyar Z., Pierre M. et al. Activation of the cell cycle machinery and the isoflavonoid biosynthesis pathway by active Rhizobium meliloti Nod signal molecules in Medicago microcallus suspensions//EMBO J. -1994. -Vol. 13. -P. 1093-1102.
  210. Schmidt J., Rohgrig H., John M. et al. Alteration of plant growth and development by Rhizobium nodA and nodB genes involved in the synthesis of oligosaccharide signal molecules//The Plant J. -1993. -Vol. 4, N 4. -P. 651-658.
  211. Schmidt P.E., Broughton W.J., Werner D. Nod factors of Bradyrhizobium japonicum and Rhizobium sp. NGR234 induce flavonoid accumulation in soybean root exudates//MPMI. -1994. -Vol. 7, N 3. -P. 384-390.
  212. Schultze M., Kondorosi A. Regulation of symbiotic root nodule development//Ann. Rev Genet. -1998. -Vol. 32. -P. 33-57.
  213. Schwedock J., Long S.R. ATPsulphurylaseactivityofthenodPand nodQ gene products of Rhizobium meliloti//Nature. -1990. -Vol.348. -P. 644-647.
  214. Shearman C.A., RossenL., Johnston A. W.B., DownieJ.A. 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//TheEMBOJ.-1986. -Vol. 5, N4. -P. 647-652.
  215. Semino C.E., Specht C.A., RaimondiA., Robbins P. W. Homologs of 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. USA. -1996. -Vol.93. -P. 4548-4553.
  216. Slabas A.R., Chase D., Nishida I. et al. Molecular cloning of higher-plant 3-oxoacyl-(acyl carrier protein) reductase -Sequence identities with the nodG-gene product of the nitrogen-fixing soil bacterium Rhizobium meliloti//Biochem. J. -1992. -Vol.283.-P. 321-326.
  217. Soria-Diaz M.E., Tejero-Mateo P., Espartero J.L. et al. Structural determination of the lipo-chitin oligosaccharide nodulation signals produced by Rhizobium giardinii bv. giardinii H152//Carbohydrate Research. -2003. -Vol. 338. -P. 237-250.
  218. Spaink H.P., Wijffelman C.A., Pees E. etal. Rhizobium nodulation gene nodD as a determinant of host specificity//Nature. -1987. -Vol.328. -P. 337-340.
  219. Spaink H.P., Sheeley D.M., van Brussel A.A.N, etal. A novel, highly unsaturated, fatty acid moiety of lipooligosaccharide signals determines host specificity of Rhizobium leguminosarum//Nature. -1991. -Vol.354. -P. 125-130.
  220. Spaink H.P. Bloemberg G.V., Van Brussel A.A.N, et al. Host specificity of Rhizobium leguminosarum is determined by the hydrophobisity of highly unsaturated fatty acyl moieties of the nodulation factors//Mol. Plant-Microbe Interact. -1995a. -Vol. 8.-P. 155-164.
  221. Spaink H.P., Wijfjes A.H.M., Lugtenberg B.J.J. Rhizobium Nodi and NodJ proteins play a role in the efficiency of secretion of lipochitin oligosaccarides Hi. Bacteriol. -1995b. -Vol. 177. -P. 6276-6281.
  222. Spaink H.P. Regulation of plant morphogenesis by lipo-chitin oligosaccharides//Crit. Rev. Plant Sci. -1996. -Vol. 15. -P. 559-582.
  223. Spaink H.P. Root nodulation and infection factors produced by rhizobial bacteria//Annual Review of Microbiology. -2000. -Vol.54. -P. 257-288.
  224. Stacey G., Luka S., Sanjuan J. et al. NodZ, a unique host -specific nodulation gene, is involved in the fucosylation of the lipooligosaccharide nodulation signal of Brady rhizobium japonicum//J. Bacteriol. -1994. -Vol. 176. -P. 620-633.
  225. Staehelin С, Schultze M., Kondorosi E. et al. Structural modifications in Rhizobium meliloti Nod factors influence their stability against hydrolysis by root chitinases//The Plant J. -1994. -Vol. 5. -N 3. -P. 319-330.
  226. Staehelin C, Schultze M., Kondorosi E., Kondorosi A. Lipo-chitooligosaccharide Nodulation Signals from Rhizobium meliloti Induce Their Rapid Degradation by the Host Plant Alfalfa//Plant Physiol,-1995.-Vol. 108. -P. 1607-1614.
  227. Stokkermans T.J. W., Ikeshita S., Cohn J. et al. Structural requirements of synthetic and natural product lipo-chitin oligosaccharides for induction of nodule primordia on Glycine soja//Plant Physiol.-1995.-Vol. 108.-P. 1587-1595
  228. Timmers A.C.J., Auriac M.-C, de Billy F., Truchet G. Nod factor internalization and microtubular cytoskeleton changes occur concomitantly during nodule differentiation in alfalfa//Development. -1998. -Vol. 125. -P. 339-349.
  229. Truchet G, Roche P., Lerouge P. et al. Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa//Nature. -1991. -Vol. 351. -P. 670-673.
  230. Van Brussel A.A.N., Zaat S.A.J., Canter Cremers H.C.J, et я/. Role of plant root exudate and Sym plasmid-localised nodulation genes in the synthesis by Rhizobium leguminosarum of Tsr factor, which causes thick and short roots on common vetch//J.Bacteriol. -1986. -Vol. 165. -P. 517-522.
  231. Van Brussel A.A.N., Recourt K, Pees E. et al. Abiovar -specific signal of Rhizobium leguminosarum bv. viciae induces increased nodulation gene -inducing activity in root exudates of Vicia sativa subsp. nigra//J. Bacteriol. -1990. -Vol. 172. -P. 5394-5401.
  232. Van Brussel A.A.N., Bakhuizen R., van Spronsen P.C. et al. Induction of pre -infection thread structures in the leguminous host plant by mitogenic lipooligosaccharides of Rhizobium//Science. -1992. -Vol. 257. -P. 70-72.
  233. van der Drift K.M.G.M., Spaink HP., Bloemberg G.V. et al. Rhizobium leguminosarum bv. trifolii produces lipochitin oligosaccharides with nodE-dependent highly unsaturated fatty acyl moieties: an electrospray ionisation and collision induced dissociation tandem mass spectrometric study//J. Biol. Chem. -1996. -Vol. 271. -P. 22563-69.
  234. vander Hoist P.P.G., Schlaman H.R.M. and Spaink HP. Proteins involved in the production and perception of oligosaccharides in relation to plant and animal development//Current Opinion in Structural Biology. -2001. -Vol. 11. -P. 608-616.
  235. van Hengel A. J., Tadesse Z., Immerzeel P. et al. N-Acetyl-glucosamine and Glucosamine-Containing Arabinogalactan Proteins Control Somatic Embryogenesis//Plant Physiology. -2001. -Vol. 125.-P. 1880-1890.
  236. Vazquez M., Santana O., Quinto C. The Nodi and NodJ proteins from Rhizobium and Bradyrhizobium strains are similar to capsular polysaccharide secretion protein from Gram-negative bacteria//Mol. Microbiol. -1993. -Vol. 8, N 1. -P. 369-377.
  237. Xie Z.-P., Staehelin C, Vierheilig H. et al. 1995. Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans//Plant Physiol. -Vol. 108. -P. 1519-1525.
  238. Yang G.-P., Debelle F., Savagnac A. et al. 1999. Structure of the Mesorhizobium huakuii and Rhizobium galegae Nod factors: a cluster of phylogenetically related legumes are nodulated by rhizobia producing Nod factors with a, b-unsaturated N-acyl substitutions//Mol. Microbiol. -Vol. 34. -P. 227-37.
  239. Zaat S. A.J., Wijffelman С A., Mulders H.M. etal. Root exudates of various host plant of Rhizobium leguminosarum contain different sets of inducers of Rhizobium nodulation genes//Plant Physiol. -1988. -Vol. 86. -P. 1298-1303.
  240. Zhang F. and Smith D.L. Preincubation ofBradyrhizobiumjaponicum with genistein accelerates nodule development of soybean [Glycine max (L.) Merr.] at suboptimal root zone temperatures//Plant Physiol. -1995. -Vol. 108. -P. 961-968.

Statistics

Views

Abstract - 389

PDF (Russian) - 276

Cited-By


Article Metrics

Metrics Loading ...

PlumX

Dimensions


Copyright (c) 2004 Ovtsyna A.O., Tikhonovich I.A.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies