Intracellular and extracellular PGPR: Commonalities and distinctions in the plant-bacterium signaling processes

Soil Biology and Biochemistry

Volumn 37, Issue 3, 2005, Pages 395-412

  Gray, E J ^a   Smith, D L ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Interorganismal signaling; Lipo oligosaccharides; Nod factors; Plant growth; Plant growth promoting rhizobacteria (PGPR); Rhizobia

Indexed keywords

PLANT GROWTH PROMOTING BACTERIA (PGPR); RHIZOBIA; RHIZOSPHERE; SIGNALING MECHANISMS;

NITROGEN; PLANT CELL CULTURE; PLANTS (BOTANY);

BACTERIA;

LEGUME; RHIZOBACTERIUM; SYMBIOSIS;

BACTERIA (MICROORGANISMS); EMBRYOPHYTA; FRANKIA; RHIZOBIACEAE; RHIZOBIALES;

EID: 11144347583     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2004.08.030     Document Type: Review

References (210)

1. A.D.L. Akkermans, W. Roelofsen, J. Blom, K. Huss-Danell, and R. Harkink Utilization of carbon and nitrogen compounds by Frankia in synthetic media and in root nodules of Alnus glutinosa, Hippophae rhamnoides, and Datisca cannabina Can. J. Bot. 61 1983 2793 2800
2. A.R. Alagawadi, and A.C. Gaur Associative effect of Rhizobium and phosphate-solubilizing bacteria on the yield and nutrient uptake of chickpea Plant Soil 105 1988 241 246
3. N. Amarger, V. Macheret, and G. Laguerre Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules Int. J. Syst. Bacteriol. 47 1997 996 1006
4. K.L. Andrade, R.G. Mihara, G. Linderman, and G.J. Bethlenfalvay Bacteria from rhizosphere and hyphosphere soils of different arbuscular-mycorrhizal fungi Plant Soil 192 1997 71 79
5. M. Bacilio-Jimenez, S. Aguilar-Flores, E. Ventura-Zapata, E. Perez-Campos, S. Bouquelet, and E. Zenteno Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria Plant Soil 249 2003 271 277
6. Y. Bai, A. Souleimanov, and D.L. Smith An inducible activator produced by Serratia proteamaculans strain and its soybean growth-promoting activity under greenhouse conditions J. Exp. Bot. 53 2002 1495 1502
7. Y. Bai, F. D'Aoust, D.L. Smith, and B.T. Driscoll Isolation of plant-growth-promoting Bacillus strains from soybean root nodules Can. J. Microbiol. 48 2002 230 238
8. H.P. Bais, S.W. Park, T.L. Wier, R.M. Callaway, and J.M. Vivanco How plants communicate using the underground information superhighway Trends Plant Sci. 9 2004 26 32
9. P. Barbieri, T. Zanelli, E. Galle, and G. Zanetti Effect on wheat root development of innoculation with an Azospirillum brasilense mutant with altered indole-3-acetic acid production Res. Microbiol. 144 1993 69 75
10. 3 by Acetobacter diazotrophicus and Herbaspirillum seropedicae in chemically-defined culture media Plant Growth Reg. 24 1998 7 11
11. M. Beijerinck Die Bakterien de Papilionaceenknollchen Botanische Zeitung 46 1988 725 804 In Milestones in Microbiology: 1556 to 1940, translated and edited by Thomas D. Brock, ASM Press, 1998, p. 220
12. A.M. Belkheir, X. Zhou, and D.L. Smith Variability in yield and yield component responses to genistein pre-incubated Bradyrhizobium japonicum by soybean (Glycine max L. Merr) cultivars Plant Soil 229 2001 41 46
13. O. Berge, J. Fages, D. Mulard, and J. Balandreau Effects of inoculation with Bacillus circulans and Azospirillum lipoferum on crop-yield in field grown maize Symbiosis 9 1990 259 266
14. J.C. Biswas, J.K. Ladha, F.B. Dazzo, Y.G. Yanni, and B.G. Rolfe Rhizobial inoculation influences seedling vigor and yield of rice Agron. J. 92 2000 880 886
15. R.M. Boddey, S. Urquiaga, B.J.R. Alves, and V. Reis Endophytic nitrogen fixation in sugarcare: present knowledge and future applications Plant Soil 252 2003 139 149
16. R.M. Bringhurst, Z.G. Cardon, and D.J. Gage Galactosides in the rhizosphere: utilization by Sinorhizobium meliloti and development of a biosensor PNAS 98 2001 4540 4545
17. W.J. Broughton, F. Zhang, X. Perret, and C. Staehelin Signals exchanged between legumes and Rhizobium: agricultural uses and perspectives Plant Soil 252 2003 129 137
18. M.E. Brown Seed and root bacterization Annu. Rev. Phytopath. 12 1974 181 197
19. A.J.P. Burggraaf, A. Quispel, T. Tak, and J. Valstar Methods of isolation and cultivation of Frankia species from actinorhizas Plant Soil 61 1981 157 168
20. S. Buysens, J. Poppe, and M. Hofte Role of siderophores in plant growth simulation and antagonism by Pseudomonas aeruinosa 7NSK2 M.H. Ryder P.M Stephens D.G. Bowen Improving Plant Productivity with Rhizosphere Baceria 1994 Commonwealth Science and Industrial Research Organization Adelaide, Australia 139 141
21. J.M. Caba, L. Recalde, and F. Ligero Nitrate-induced ethylene biosynthesis and the control of nodulation in alfalfa Plant Cell Environ. 21 1998 87 93
22. L. Cardenas, T.L. Holdaway-Clarke, F. Sanchez, C. Qunito, J.A. Feijo, J.G. Kunkel, and P.K. Hepler Ion changes in legume root hairs responding to nod factors Plant Phys. 123 2000 443 452
23. C.V. Carpenter, L.R. Robertson, J.C. Gordon, and D.A. Perry The effect of four new Frankia isolates on growth and nitrogenase activity in clones of Alnus rubra and Alnus sinuata Can. J. Forest Res. 14 1984 701 706
24. D. Castignetti, and J.J. Smarrelli First year field performance of spruce seedlings inoculated with plant growth promoting rhizobacteria Can. J. Microbiol. 39 1986 1084 1088
25. C. Cha, P. Gao, Y.C. Chen, P.D. Shaaw, and S.K. Farrand Production of acyl-homoserine lactone quorum-sensing signals by Gram-negative plant-associated bacteria Mol. Plant Microbe Inter. 11 1998 1119 1129
26. C.P. Chanway, R.K. Hynes, and L.M. Nelson Plant growth-promoting rhizobacteria: effects on growth and nitrogen fixation of lentil (Lens escuienta Moench) and pea (Pisum sativum L.) Soil Biol. Biochem. 21 1989 511 517
27. C.P. Chanway, R.A. Radley, and F.B. Holl Inoculation of conifer seed with plant growth promoting Bacillus strains causes increased seedling emergence and biomass Soil Biol. Biochem. 23 1991 575 580
28. W.X. Chen, G.H. Yan, and J.L. Li Numerical taxonomic study of fast-growing soybean rhizobia and a proposal that Rhizobium fredii be assigned to Sinorhizobium gen. nov Int. J. Syst. Bacteriol. 38 1988 392 397
29. Y.X. Chen, R.H. Mei, S. Lu, L. Liu, and J.W. Kloepper The use of yield increasing bacteria (YIB) as plant growth-promoting rhizobacteria in Chinese agriculture R.S. Utkehede V.K. Gupta Management of Soil-Borne Disease 1996 Kalyani New Delhi 165 184
30. L. Chiarini, A. Bevivino, S. Tabacchioni, and C. Dalmastri Inoculation of Burkholderia cepacia, Pseudomonas fluorescens and Enterbacter sp. on Sorghum biclor: root colonization and plant growth promotion of dual strain inocula Soil Biol. Biochem. 30 1998 81 87
31. M.L. Clawson, and D.R. Benson Natural diversity of Frankia strains in actinorhizal root nodules from promiscuous hosts in the family Myricaceae Appl. Environ. Microbiol. 65 1999 4521 4527
32. R.E. Cleland Auxin and cell elongation P.J. Davies Plant Hormones and their Role in Plant Growth and Development 1990 Kluwer Academic Publishers Dordrecht, The Netherlands 132 148
33. B. Cournoyer, and P. Normand Characterization of a spontaneous thiostrepton-resistant Frankia alni infective isolate using PCR-RFLP of nif and glnII genes Soil Biol. Biochem. 26 1994 553 559
34. W.K. Crannell, Y. Tanaka, and D.D. Myrold Calcium and pH interaction on root nodulation of nursery-grown red alder (Alnus rubra Bong.) seedlings by Frankia Soil Biol. Biochem. 26 1994 607 614
35. D.E. Crowley, C.P.P. Reid, and P.J. Szaniszlo Utilization of microbial siderophores in iron acquisition by oat Plant Phys. 87 1988 680 685
36. J.V. Cullimore, R. Ranjeva, and J.J. Bono Perception of lipo-chitooligosaccharidic Nod factors in legumes Trends Plant Sci. 6 2001 24 30
37. N. Dashti, F. Zhang, R. Hynes, and D.L. Smith Application of plant growth-promoting rhizobacteria to soybean (Glycine max (L.) Merr.) increases protein and dry matter yield under short-season conditions Plant Soil 188 1997 33 41
38. N. Dashti, B. Prithiviraj, R.K. Hynes, and D.L. Smith Root and rhizosphere colonization of soybean (Glycine max (L.) Merr.) by plant-growth-promoting rhizobacteria at low root zone temperatures and under short-season conditions J. Agron. Crop Sci. 185 2001 15 22
39. J.R. De Freitas, and J.J. Germida Pseudomonas cepacia and Pseudomonas putida as winter wheat inoculants for biocontrol of Rhizobium solani Can. J. Microbiol. 37 1991 780 789
40. G. Degrassi, C. Aguilar, M. Bosco, S. Zahariev, S. Pongor, and V. Venturi Plant growth-promoting Pseudomonas putida WCS358 produces and secretes four cyclic dipeptides: cross-talk with quorum sensing bacterial sensors Curr. Microbiol. 45 2002 250 254
41. P. de Lajudie, A. Willems, G. Nick, F. Moreira, F. Molouba, B. Hoste, U. Torck, M. Neyra, M.D. Collins, K. Lindstrom, B. Dreyfus, and M. Gillis Characterization of tropical tree rhizobia and description of Mesorhizobium plurifarium sp. nov Int. J. Syst. Bacteriol. 48 1998 369 382
42. P. de Lajudie, E. Laurent-Fulele, A. Willems, U. Torck, R. Coopman, M.D. Collins, K. Kersters, B. Dreyfus, and M. Gillis Allorhizobium undicola gen. nov., sp. nov., nitrogen-fixing bacteria that efficiently nodulate Neptunia natans in Senegal Int. J. Syst. Bacteriol. 48 1998 1277 1290
43. N. Demont-Caulet, F. Maillet, D. Tailer, J.C. Jacquinet, J.C. Prome, K.C. Nicolaou, G. Truchet, J.M. Beau, and J. Denarie Nodule-inducing activity of synthetic Sinorhizobium meliloti nodulation factors and related lipo-chitooligosaccharides on alfalfa. Importance of the acyl chain structure Plant Phys. 120 1999 83 92
44. J. Denarie, and F. Debelle Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis Ann. Rev. Biochem. 65 1996 503 535
45. H.G. Diem, and Y.R. Dommergues In vitro production of specialized reproductive torulose hyphae by Frankia strain ORS 021001 isolated from Casuarina junghuhniana root nodules Plant Soil 81 1985 17 29
46. B. Dreyfus, J.L. Garcia, and M. Gillis Characterization of Azorhizobium caulinodans gen. nov., sp. nov., a stem-nodulating nitrogen-fixing bacterium isolated from Sesbania rostrata Int. J. Syst. Bacteriol. 38 1988 89 98
47. A.N. Dubeikovesky, E.A. Modokhova, V.V. Kocheskov, F.P. Polikarpova, and A.M. Boronin Growth promotion of blackcurrant softwood cuttings by recombinant strain Pseudomonas fluorescens BSP53a synthesizing an increased amount of indole-3-acetic acid Soil Biol. Biochem. 25 1993 1211 1221
48. D. Dubnau Genetic competence in B. subtilis Microbiol. Rev. 55 1991 395 424
49. E.T. Du Cros, G. Jung, and M. Bariteau Alder-Frankia interaction and alder-poplar association for biomass production Plant Soil 78 1984 235 243
50. J. Ebel, and A. Mithofer Early events in the elicitation of plant defense Planta 206 1998 335 348
51. D.W. Ehrhardt, R. Wais, and S.R. Long Calcium spiking in plant root hairs responding to Rhizobium nodulation signals Cell 85 1996 673 681
52. J.J. Esseling, F.G.P. Lhuissier, and A.M.C. Emons Nod factor-induced root hair curling: continuous polar growth towards the point of nod factor application Plant Physiol. 132 2003 1982 1988
53. M.E. Etzler, G. Kalsi, N.N. Ewing, N.J. Roberts, R.B. Day, and J.B. Murphy A Nod factor binding lectin with apyrase activity from legume roots PNAS 96 1999 5856 5861
54. H.H. Felle, E. Kondorosi, A. Kondorosi, and M. Schultze The role of ion fluxes in Nod factor signaling in Medicago sativa Plant J. 13 1998 455 463
55. R.F. Fisher, T.T. Egelhoff, J.T. Mulligan, and S.R. Long Specific binding of proteins from Rhizobium meliloti cell-free extracts containing NodD to DNA sequences upstream of inducible nodulation genes Genes Dev. 2 1988 282 293
56. R.C. Foster, A.D. Rovira, and T.W. Cock Ultrastructure of the Root-Soil Interface 1983 The American Phytopathological Society St Paul, MN p. 157
57. R.G. Fray Altering plant-microbe interaction through artificially manipulating bacterial quorum sensing Ann. Bot. 89 2002 245 253
58. I.E. Garcia de Salamone, R.K. Hynes, and L.M Nelson Cytokinin production by plant growth promoting rhizobacteria and selected mutants Can. J. Microbiol. 47 2001 404 411
59. I.C. Gardner, D.M. Clelland, and A. Scott Mycorrhizal improvement in non-leguminous nitrogen-fixing associations with particular reference to Hippophae rhamnoides L Plant Soil 78 1984 189 199
60. O. Geiger, J. Glushka, B.J.J. Lugtenberg, H.P. Spaink, and J.E. Thomas-Oates NodFE-dependent fatty acids that lack an alpha-beta unsaturation are subject to differential transfer, leading to novel phospholipids Mol. Plant Microbe Inter. 11 1998 33 44
61. R. Geurts, and T. Bisseling Rhizobium Nod factor perception and signaling Plant Cell 14 2002 S239 S249
62. B.R. Glick The enhancement of plant growth by free-living bacteria Can. J. Microbiol. 41 1995 109 117
63. B.R. Glick, D.M. Penrose, and J. Li A model for the lowering of plant ethylene concentrations by plant growth promoting bacteria J. Theor. Biol. 190 1998 63 68
64. B.R. Glick Bacterial ACC deaminase and the alleviation of plant stress Adv. Appl. Microbiol. 56 2004 291 312
65. J. Goedhart, H. Rohrig, M.A. Hink, A. Van Hoek, A.J. Visser, T. Bisseling, and T.W. Gadella Nod factors integrate spontaneously in biomembranes and transfer rapidly between membranes and to root hairs, but transbilayer flip-flop does not occur Biochemistry 28 1999 10898 10907
66. K.M. Gray Intercellular communication and group behavior in bacteria Trends Microbiol. 5 1997 184 188
67. F. Gressent, S. Drouillard, N. Mantegazza, E. Samain, R.A. Geremia, H. Canut, A. Niebel, H. Driguez, R. Ranjeva, J. Cullimore, and J.J. Bono Ligand specificity of a high-affinity binding site for lipo-chitooligosaccharidic Nod factors in Medicago cell suspension cultures PNAS 96 1999 4704 4709
68. A.D. Grossman Genetic networks controlling the initiation of sporulation and the development of competence in Bacillus subtilis Ann. Rev. Genet. 29 1995 477 508
69. M.L. Guerinot, and B.K. Chelm Isolation and expression of the Bradyrhizobium japonicum adenylate cyclase gene (cya) in Escherichia coli J. Bacteriol. 159 1984 1068 1071
70. N.L. Guterson, T.J. Layton, J.S. Ziegle, and G.J. Warren Molecular cloning of genetic determinants for inhibition of fungal growth by a fluorescent pseudomonas J. Bacteriol. 165 1986 696 703
71. F.J. Gutierrez Manero, N. Acero, J.A. Lucas, and A. Probanza The influence of native rhizobacteria on European alder (Alnus glutinosa L. Gaertn.) growth. II. Characterization and biological assays of metabolites from growth promoting and growth inhibiting bacteria Plant Soil 182 1996 67 74
72. F.J. Gutierrez Munero, B. Ramos-Solano, A. Probanza, J. Mehouachi, F.R. Tadeo, and M. Talon The plant-growth-promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins Physiol. Plant 111 2001 206 211
73. Hackett, B.P., 1985. Hormonal regulation of leaf senescence in Rumex: ethylene and cytokinins. Dissertation Abstracts International B Sciences & Engineering 46 (4) 1018B.
74. G. Hagen The control of gene expression by auxin P.J. Davies Plant Hormones and their Role in Plant Growth and Development 1990 Kluwer Academic Publishers Dordrecht, The Netherlands 149 163
75. J. Hallmann, A. Quadt-Hallmann, W.F. Mahaffee, and W. Kloepper Bacterial endophytes in agricultural crops Can. J. Microbiol. 43 1997 895 914
76. L.J. Halverson, and J. Handelsman Enhancement of soybean nodulation by Bacillus cereus UW85 in the field and in a growth chamber Appl. Environ. Microbiol. 57 1991 2767 2770
77. J. Handelsman, S. Raffel, E.H. Mester, L. Wunderlich, and C.R. Crau Biological control of damping-off of alfalfa seedlings with Bacillus cereus UW85 Appl. Environ. Microbiol. 56 1990 713 718
78. B. Hause, W. Maier, O. Miersch, R. Kramell, and D. Strack Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots Plant Physiol. 130 2002 1213 1220
79. H. Hellriegel, and H. Wilfarth Untersuchungen uber die Stickstoffnahrung der Gramineen und Leguminosen Beilageheft zu der Zeitschrift des Vereins fur Rubenzucker-Industrie Deutschen Reichs 1888 234
80. A. Hirsh Role of lectins (and rhizobial exopolysarrharides) in legume nodulation Curr. Opin. Plant Biol. 2 1999 320 326
81. A.M. Hirsh, M.R. Lum, and J.A. Downie What makes the rhizobia-legume symbiosis so special? Plant Physiol. 127 2001 1484 1492
82. B. Horvath, E. Kondorosi, M. John, J. Schmidt, I. Torok, Z. Gyorgypal, L. Barabas, U. Weineke, J. Schell, and A. Kondorosi Organization structure and symbiotic function of Rhizobium meliloti nodulation genes determining host specificity for alfalfa Cell 46 1986 335 343
83. M. Hungria, and G. Stacey Molecular signals exchanged between host plants and rhizobia: basic aspects and potential application in agriculture Soil Biol. Biochem. 29 1997 819 830
84. J. Inbar, and I. Chet Evidence that chitinase produced by Aeromonas caviae is involved in the biological control of soil-borne plant pathogens by bacterium Soil Biol. Biochem. 23 1991 974 978
85. H. Ip, F. D'Aoust, A.A. Begum, H. Zhang, D.L. Smith, B.T. Driscoll, and T.C. Charles Bradyrhizobium japonicum mutant with enhanced sensitivity to genistein resulting in altered nod gene regulation Mol. Plant-Microbe Inter. 14 2001 1404 1410
86. J. Jiang, H. Yang, J. Huang, B. Zhu, H. Liu, Y. Zhong, and Y. Bifang Isolation and cultivation of Frankia strain ACC13 from root nodules of Alnus cremastogyne Wei Sheng Wu Hsueh Pao 24 1984 37 40
87. M. John, J. Schmidt, R. Walden, I. Czaja, M. Dulz, J. Schell, and H. Rohrig Lipochitooligosaccharide-induced tobacco cells release a peptide as mediator of the glycolipid signal PNAS 94 1997 10178 10182
88. C. Keel, U. Schnider, M. Maurhofer, C. Voisard, J. Laville, U. Burger, P. Wirthner, D. Haas, and G. Defago Suppression of root diseases by Pseudomonas fluorescens CHAO: importance of the bacterial secondary metabolite 2, 4-diacetylphloroglucinol Mol. Plant Microbe Inter. 5 1992 4 13
89. W. Khan, B. Prithiviraj, and D.L. Smith Photosynthetic responses of corn and soybean to foliar application of salicylates J. Plant Physiol. 160 2003 485 492
90. J.W. Kloepper, and M.N. Schroth Plant growth-promoting rhizobacteria on radishes Fourth International Conference on Plant Pathogen Bacteria, Angers, France vol. 2 1978 pp. 879-882
91. J.W. Kloepper, M.N. Schroth, and W. Miller Effects of rhizosphere colonization by plant growth-promoting rhizobacteria on potato plant development and yield Ecol. Epidemiol. 70 1980 1078 1082
92. J.W. Kloepper, J. Leong, M. Teintze, and M.N. Schroth Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria Nature 286 1980 885 886
93. D.A. Kluepfel, and T.M. McInnis Biological control of ring nematodes by Pseudomonas aureofaciens Phytopathology 81 1991 1178 1186
94. C.D. Knight, L. Rossen, J.G. Robertson, B. Wells, and J.A. Downie Nodulation inhibition by Rhizobium leguminosarum multi copy nod ABC genes and analysis of early stages of plant infection J. Bacteriol. 166 1986 552 558
95. M. Kobayashi, T. Suzuki, T. Fujita, M. Masuda, and S. Shimizu Occurrence of enzymes involved in biosynthesis of indole-3-acetic acid from indole-3-acetonitrile in plant-associated bacteria, Agrobacterium and Rhizobium PNAS 92 1995 714 718
96. M. Korem, A.S. Sheoran, Y. Gov, S. Tzipori, I. Borovok, and N. Balaban Characterization of RAP, a quorum sensing activator of Staphylococus aureus FEMS Microbiol. Lett. 223 2003 167 175
97. B. Lambert, H. Joos, S. Dierick, R. Vantomme, J. Swings, K. Kerters, and M. Van Montagu Identification and plant interaction of Phyllobacterium sp., a predominant rhizobacterium of young sugar beat Appl. Environ. Microboil. 56 1990 1093 1102
98. S.A. Lancelle, J.G. Torrey, P.K. Hepler, and D.A. Callaham Ultrastructure of freeze-substituted Frankia strain HFPCcI3, the actinomycete isolated from root nodules of Casuarina cunninghamiana Protoplasma 127 1985 64 72
99. G.J. Law, and A.J. Northrop Synthetic peptides to mimic the role of GTP binding proteins in membrane traffic and fusion Ann. NY Acad. Sci. 710 1994 196 208
100. C.A. Lee Type III secretion systems: machines to deliver bacterial proteins into eukaryotic cells? Trends Microbiol. 5 1997 149 156
101. S.J. Lee, S.Y. Park, J.J. Lee, D.Y. Yum, B.T. Koo, and J.K. Lee Genes encoding the N-acyl homoserine lactone-degrading enzyme are widespread in many subspecies of Bacillus thuringiensis Appl. Environ. Microbiol. 68 2002 3919 3924
102. J.A. Leigh, and C.C. Lee Characterization of polysaccharides of Rhizobium meliloti exo mutants that form ineffective nodules J. Bacteriol. 170 1988 3327 3332
103. P. Lerouge, P. Roche, C. Faucher, F. Maillet, G. Truchet, J.C. Prome, and J. Denarie Symbiotic host-specificity of Rhizobium meliloti is determined by a sulfated and acylated glucosamine oligosaccharide signal Nature 344 1990 781 784
104. D. Li, and M. Alexander Co-inoculation with antibiotic-producing bacteria to increase colonization and nodulation by rhizobia Plant Soil 108 1988 211 219
105. B. Lian, B. Prithiviraj, A. Souleimanov, and D.L. Smith Evidence for the production of chemical compounds analogous to Nod factor by the silicate bacterium Bacillus circulans GY92 Micro Res. 156 2001 289 292
106. H. Lim, Y. Kim, and S. Kim Pseudomonas stutzeri YPL-1 genetic transformation and antifungal mechanisms against Fusarium solani, an agent of plant root rot Appl. Environ. Microbiol. 57 1991 510 516
107. K. Lindstrom Rhizobium galegae, a new species of legume root nodule bacteria Int. J. Syst. Bacteriol. 39 1989 365 367
108. J.K. Lithgow, A. Wilkinson, A. Hardman, B. Rodelas, F. Wisniewski-Dye, P. Williams, and J.A. Downie The regulatory locus cinR1 in Rhizobium leguminosarum controls a network of quorum-sensing loci Mol. Microbiol. 37 2000 81 97
109. C. Lodewyckx, J. Vangronsveld, F. Porteous, E.R.B. Moore, S. Taghavi, M. Mezgeay, and D. Van der Lelie Endophytic bacteria and their potential applications Crit. Rev. Plant Sci. 21 2002 583 606
110. J. Loh, M. Garcia, and G. Stacey NodV and NodW, a second flavanoid recognition system regulating nod gene expression in Bradyrhizobium japonicum J. Bacteriol. 179 1997 3013 3020
111. J. Loh, J.P.Y. Yuen-Tsai, A. Welborn, and G. Stacey Population density-dependent regulation of the Bradyrhizobium japonicum nodulation genes Mol. Microbiol. 42 2001 3746
112. J. Loh, E.A. Pierson, L.S. Pierson, G. Stacey, and A. Chatterjee Quorum sensing in plant-associated bacteria Curr. Opin. Plant Biol. 5 2002 1 6
113. 2 fixation as affected by period of exposure to a low root zone temperature Physiol. Plant 88 1993 212 223
114. W.F. Mahaffee, and J.W. Kloepper Temporal changes in the bacterial communities of soil, rhizosphere, and endorhiza associated with field-grown cucumber (Cucumis sativus L.) Microb. Ecol. 34 1997 210 223
115. S.R. Mansour, A. Dewedar, and J.G. Torrey Isolation, culture, and behavior of Frankia strain HFPCgI4 from root nodules of Casuarina glauca Bot. Gaz. 151 1990 490 496
116. E. Martinez-Romero, and E.T. Wang Sesbania herbacea-Rhizobium huautlense nodulation in flooded soils and comparative characterization of S. herbaces nodulating rhizobia in different environments Microbe Ecol. 41 2000 25 32
117. U. Mathesius, S. Mulders, M. Gao, M. Teplitski, G. Caetano-Anolles, B.G. Rolfe, and W.D. Bauer Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals PNAS 100 2003 1444 1449
118. M. Maurhofer, C. Keel, U. Schnider, C. Voisard, D. Hass, and G. Defago Influence of enhanced antibiotic production in Pseudomonas fluorescens strain CHAO on its disease suppressive capacity Phytopathology 82 1992 190 195
119. S. Mayak, T. Tirosh, and B.R. Glick Effect of wild-type and mutant plant growth-promoting rhizobacteria on the rooting of mung bean cuttings J. Plant Growth Reg. 18 1999 49 53
120. I.A. McKay, and M.A. Djordjevic Production and excretion of Nod metabolites by Rhizobium legminosarum bv. trifolii are disrupted by the same environmental factors that reduce nodulation in the field Environ. Microbiol. 59 1993 3385 3392
121. J.P. Metraux Systemic acquired resistance and salicylic acid: current state of knowledge Eur. J. Plant Pathol. 107 2001 13 18
122. E. Miklashevichs, H. Rohig, J. Schell, and J. Schmidt Perception and signal transduction of rhizobial NOD factors Crit. Rev. Plant Sci. 20 2001 373 394
123. M.J. Mueller, and W. Brodschelm Quantification of jasmonic acid by capillary gas chromatography - negative chemical ionization - mass spectrometry Analyt. Biochem. 218 1994 425 435
124. J.T. Mulligan, and S.R. Long A family of activator genes regulates expression of Rhizobium meliloti nodulation genes Genetics 122 1989 7 18
125. P. Mylona, K. Pawlowski, and T. Bisseling Symbiotic nitrogen fixation Plant Cell 7 1995 869 885
126. K.H. Nealson, and J.W. Hastings Bacterial bioluminescence: its control and ecological significance Microbiol. Rev. 43 1979 496 518
127. E.B. Nelson Biological control of pythium seed rot and preemergence damping-off of cotton with Enterobacter cloacae and Ervinis herbicola applied as seed treatments Plant Dis. 72 1998 140 142
128. G. Nick, P. de Lajudie, B.D. Eardly, S. Soumalainen, L. Paulin, X. Zhang, M. Gillis, and K. Lindstrom Sinorhizobium arboris sp. nov. and Sinorhizobium kostiense sp. nov., isolated from leguminous trees in Sudan and Kenya Int. J. Syst. Bacteriol. 49 1999 1359 1368
129. A. Nickel, O. Pelz, D. Hahn, M. Saurer, R. Siegwolf, and J. Zeyer Effect of inoculation and leaf litter amendment on establishment of nodule-forming Frankia populations in soil Appl. Environ. Microbiol. 67 2001 2603 2609
130. A. Niebel, J.J. Bono, R. Ranjeva, and J.V. Cullimore Identification of a high affinity binding site for lipo-oligosaccharidic NodRm factors in the microsomal fraction of Medicago cell suspension cultures Mol. Plant Microbe Inter. 10 1997 132 134
131. S.M. Nour, M.P. Fernandez, P. Normand, and J.C. Cleyet-Marel Rhizobium ciceri sp. nov., consisting of strains that nodulate chickpeas (Cicer arietinum L.) Int. J. Syst. Bacteriol. 44 1994 511 522
132. J. Nowak Benefits of in vitro 'biotization' of plant tissue cultures with microbial inoculants In Vitro Cell. Dev. Biol. Plant 34 1998 122 130
133. G.E. Oldroyd, E.M. Engstrom, and S.R. Long Ethylene Inhibits the Nod factor signal transduction pathyway of Medicago truncatula Plant Cell 13 2001 1835 1849
134. G.E. Oldroyd, R.M. Mitra, R.J. Wais, and S.R. Long Evidence for structurally specific negative feedback in the Nod factor signal transduction pathway Plant J. 28 2001 191 199
135. A. Ordentlich, Y. Elad, and I. Chet The role of chitinase of Serratia marcescens for control of Sclerotium rolfsii Soil Boil. Biochem. 19 1988 747 751
136. P.A.I. Oremus Occurrence and infective potential of the endophyte Frankia of Hippophae rhamnoides L. ssp. rhamnoides in coastal sand-dune areas Plant Soil 56 1980 123 139
137. D.J. O'Sullivan, and F. O'Gara Traits of fluorescent Pseudomonas spp. involved in suppression of plant root pathogens Microbiol. Rev. 56 1992 662 676
138. B. Pan, J.K. Vessey, and D.L. Smith Response of field-grown soybean to co-inoculation with the plant growth promoting rhizobacteria Serratia proteamaculans or Serratia liquefaciens, and Bradyrhizobium japonicum pre-incubated with genistein Eur. J. Agron. 17 2002 143 153
139. R. Parsons, and R. Sunley Nitrogen nutrition and the role of root-shoot nitrogen signalling particularly in symbiotic systems J. Exp. Bot. 52 2001 435 443
140. R.V. Penmetsa, and D.R. Cook A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont Science 275 1997 527 530
141. X. Perret, C. Staehelin, and W.J. Broughton Molecular basis of symbiotic promiscuity Microbiol. Mol. Cell Biol. Rev. 64 2000 180 201
142. R. Pinton, Z. Varanini, and P. Nannipieri The rhizosphere as a site of biochemical interactions among soil components, plants, and microorganisms R. Pinton Z. Varanini P. Nannipieri The Rhizosphere 2001 Mercel Dekker, Inc New York, USA 1 18
143. B. Prithiviraj, A. Souleimanov, X. Zhou, and D.L. Smith Differential response of soybean (Glycine max (L.) Merr) genotypes to lipo-chito- oligosaccharide Nod Bj V (C18:1 MeFuc) J. Exp. Bot. 51 2000 2045 2051
144. B. Prithiviraj, X. Zhou, A. Souleimanov, W. Kahn, and D.L. Smith A host-specific bacteria-to-plant signal molecule (Nod factor) enhances germination and early growth of diverse crop plants Planta 216 2003 437 445
145. A. Probanza, J.A. Lucas Garcia, M.R. Ruiz Palomino, B. Ramos, and F.J. Gutierrez Manero Pinus pinea L. seedling growth and bacterial rhizosphere structure after inoculation with PGPR Bacillus (B. licheniformis CET 5106 and B. pumilus CECT 5105) Appl. Soil Ecol. 20 2002 75 84
146. N.A. Provorov, and I.A. Tikhonovich Genetic resources for improving nitrogen fixation in legume-rhizobia symbiosis Genet. Resour. Crop Evol. 50 2003 89 99
147. A.N. Rai, E. Soderback, and E. Bergman Cyanobacterium-plant symbiosis New Phytol. 147 2000 449 481
148. H.C. Ramos, T. Hoffmann, H. Nedjari, E. Presecan-Siedel, O. Dreesen, P. Glaser, and D. Jahn Fermentative metabolism of Bacillus subtilis: physiology and regulation of gene expression J. Bacteriol. 182 2000 3072 3080
149. B. Ramos, J.A. Lucas Garcia, A. Probanza, M.L. Barrientos, and F.J. Gutierrez Manero Alterations in the rhizobacterial community associated with European alder growth when inoculated with PGPR strain Bacillus licheniformis Environ. Exp. Bot. 2003 2003 61 68
150. U. Rasmussen, and M.M. Svenning Fingerprinting of cyanobacteria based on PCR with primers derived from short and long tandemly repeated repetitive sequences Appl. Environ. Microbiol. 64 1998 265 272
151. P. Reddell, and A.V. Spain Transmission of infective Frankia (actinomycetales) propagules in casts of the endogeic earthworm Pontoscolex corethrurus (Oligochaeta: Glossoscolecidae) Soil Biol. Biochem. 23 1991 775 778
152. P. Reymond, and E.E. Farmer Jasmonate and salicylate as global signals for defense gene expression Curr. Opin. Plant Biol. 5 1998 404 411
153. D. Rodriguez, M. Oijen, A.H.M.C van Schapendonk, and C.C. Lingra A sink-source model to simulate the impact of climate change and management on grassland productivity New Phytol. 144 1999 359 368
154. N.S. Rojas, C.Y. Li, D.A. Perry, and L.M. Ganio Frankia and nodulation of red alder and snowbrush grown on soils from Douglas-fir forests in the H.J. Andrews experimental forest of Oregon Appl. Soil Ecol.: Sect. Agric. Ecosys. Environ. 17 2001 141 149
155. S. Rome, M.P. Fernandez, B. Brunel, P. Normand, and J.C. Cleyet-Marel Sinorhizobium medicae sp. nov., isolated from annual Medicago spp Int. J. Syst. Bacteriol. 46 1996 972 980
156. E.A. Rosa Global climate change: background and sociological contributions Soc. Nat. Res. 14 2001 491 499
157. P.A. Rosbrook, and P. Reddell Isolation of Frankia from root nodules of three species of Casuarina Soil Biol. Biochem. 27 1995 427 429
158. M.H. Ryder, and D.A. Jones Biological control of crown gall D. Hornby R.J. Cook Y. Henis Biological Control of Soil-Borne Plant Pathogens 1990 CAB International Oxford, UK 45 63
159. M.H. Ryder, Z. Yan, T.E. Terrace, A.D. Rovira, W. Tang, and R.L. Correll Use of strains of Bacillus isolated in China to suppress take-all and rhizoctonia root rot, and promote seedling growth of glasshouse-grown wheat in Australian soils Soil Biol. Biochem. 31 1999 19 29
160. C.M. Ryu, M.A. Farag, C.H. Hu, M.S. Reddy, H.X. Wei, P.W. Pare, and J.W. Kloepper Bacterial volatiles promote growth in Arabidopsis PNAS 100 2003 4927 4932
161. B. Scheres, C. Van de Wiel, A. Zalensky, B. Horvath, H. Spaink, H. Van Eck, F. Zwartkruis, A.M. Wolters, T. Gloudemans, A. Van Kammen, and T. Bisseling The ENOD12 gene product is involved in the infection process during the pea-Rhizobium interaction Cell 60 1990 281 294
162. H.R.M. Schlaman, R.J.H. Okker, and B.J.J. Lugtenberg Regulation of nodulation gene expression by NodD in rhizobia. L. Bacteriology 174 1992 5177 5182
163. J.S. Schmidt, J.E. Harper, T.K. Hoffman, and A.F. Bent Regulation of soybean nodulation independent of ethylene signaling Plant Physiol. 119 1999 951 960
164. U. Schnider, C. Blumer, J. Troxler, G. Defago, and D. Haas Overproduction of the antibiotics 2,4-diacetylphloroglucinol and pyoluteorin in Pseudomonas fluorescens strain CHAO M.H. Ryder P.M. Stephens G.D. Bowen Improving Plant Productivity with Rhizosphere Bacteria 1994 Commonwealth Science and Industrial Research Organization Adelaide, Australia 120 121
165. M.H. Scholla, and G.H. Elkan Rhizobium fredii sp. nov., a fast-growing species that effectively nodulates soybeans Int. J. Syst. Bacteriol. 34 1984 484 486
166. L. Segovia, J.P.W. Young, and E. Matinez-Romero Reclassification of American Rhizobium leguminosarum biovar Phaseoli type I strains as Rhizobium etli sp. nov Int. J. Syst. Bacteriol. 43 1993 374 377
167. U.P. Singh, B.K. Sarma, and D.P. Singh Effect of plant growth-promoting rhizobacteria and culture filtrate of Sclerotium rolfsii on phenolic and salicylic acid contents in chickpea (Cicer arietinum) Curr. Microbiol. 46 2003 131 140
168. G. Smit, V. Puvanesarajah, R.W. Carlson, W.M. Barbour, and G. Stacey Bradyrhizobium japonicum nod D1 can be specifically induced by soybean flavanoids that do not induce the nodYABCSUIJ operon J. Biol. Chem. 267 1992 310 318
169. Smith, D.L., Zhang, F., 1999. Composition for Enhancing Grain Yield and Protein Yield of Legumes Grown under Environmental Conditions that Inhibit or Delay Nodulation Thereof. US Patent 5922316.
170. A. Souleimanov, B. Prithiviraj, R.W. Carlson, B. Jeyaretnam, and D.L. Smith Isolation and characterization of the major Nod factor of Bradyrhizobium japonicum strain 532C Microbiol. Res. 157 2002 25 28
171. A. Souleimanov, B. Prithiviraj, and D.L. Smith The major Nod factor Bradyrhizobium japonicum promotes early growth of soybean and corn J. Exp. Bot. 53 2002 1929 1934
172. H.P. Spaink, J. Weinman, M.A. Djorjevic, C.A. Wijffelman, R.J.H. Okker, and B.J.J. Lugtenberg A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium Nature 354 1991 125 130
173. H.P. Spaink, A.H.M. Wijfjes, and B.J.J. Lugtenberg Rhizobium NodI and NodJ proteins play a role in the efficiency of secretion of lipochitin oligosaccharides J. Bacteriol. 177 1995 6276 6281
174. M. Srinivasan, D.J. Peterson, and F.B. Holl Influence of IAA producing Bacillus isolates on the nodulation of Phaseolus vulgaris by Rhizobium etli Can. J. Microbiol. 42 1996 1006 1014
175. G. Stacey, S. Luka, J. Sanjuan, Z. Banfalvi, A.J. Nieuwkoop, J.Y. Chun, L. Forsberg, and R.W. Carlson nodZ, a unique host-specific nodulation gene, is involved in the fucosylation of the lipopolysaccharide nodulation signal of Bradyrhizobium japonicum J. Bacteriol. 176 1994 620 633
176. G. Stacey, J. Sanjuan, S. Lka, T. Dockendorff, and R.W. Carlson Signal exchange in the Bradyrhizobium-soybean symbiosis Soil Biol. Biochem. 27 1995 473 483
177. C. Staehelin, J. Granado, J. Muller, A. Wiemken, R.B. Mellor, G. Felix, M. Regenass, W.J. Broughton, and T. Boller Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases PNAS 91 1994 2196 2200
178. A. Steidle, M. Allesen-Holm, K. Riedel, G. Berg, M. Givskov, S. Molin, and L. Eberl Identification and characterization of an N-acylhomoserine lactone-dependent quorum-sensing system in Pseudomonas putida strain IsoF Appl. Environ. Microbiol. 68 2002 6371 6382
179. G. Stenlid Cytokinins as inhibitors of root growth Physiol. Plant 56 1982 500 506
180. J. Stougard Regulators and regulation of legume root nodule development Plant Physiol. 124 2000 531 540
181. A.V. Sturz, B.R. Christie, and J. Nowak Bacterial endophytes: Potential role in developing sustainable systems of crop production Crit. Rev. Plant Sci. 19 2000 1 30
182. J.A. Swanson, J.K. Tu, J.M. Ogawa, R. Sanga, R. Fisher, and S.R. Long Extended region of nodulation genes in Rhizobium meliloti 1021: I. Phenotypes of Tn5 insertion mutants Genetics 117 1987 181 189
183. A. Tannii, T. Takeuchi, and H. Horita Biological control of scab, black scruff and soft rot of potato by seed bacterization D. Hornby R.J. Cook Y. Henis Biological Control of Soil-Borne Plant Pathogens 1990 CAB International Oxford, UK 143 146
184. T.M. Tien, M.H. Gaskins, and D.H. Hubbell Plant growth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum L.) Appl. Environ. Microbiol. 37 1979 1016 1023
185. J.T. Turner, and P.A. Blackman Factors related to peanut yield increases following Bacillus subtilis seed treatment Plant Dis. 75 1991 347 353
186. C. Valverde, and L.G. Wall Nodule distribution on the roots of actinorhizal Discaria trinervis (Rhamnaceae) growing in pots Environ. Exp. Bot. 47 2002 95 100
187. K.A. Vanden Bosch, and E.H. Newcomb Immunogold localization of nodule-specific uricase in developing soybean nodules Planta 167 1986 198 201
188. Vandendergh, P.A., Gonzalez, C.F., 1984. Methods for protecting the growth of plants employing mutant siderophore producing strains of Pseudomonas putida. US Patent No. US4 479936.
189. P.C. Van Spronsen, T. Tak, A.M.M. Rood, A.A.N. Van Brussel, J.W. Kijne, and K.J.M. Boot Salicylic acid inhibits indeterminate-type nodulation but not determinate-type nodulation Mol. Plant Microbe Inter. 16 2003 83 91
190. E. Velazquez, J.M. Igual, A. Willems, M.P. Fernandex, E. Munoz, P.F. Mateos, A. Abril, N. Toro, P. Normand, E. Cervantes, M. Gillis, and E. Martinez-Molina Mesorhizobium chacoense sp. nov., a novel species that nodulates Prosopis alba in the Chaco Arido region (Argentina) Int. J. Syst. Evol. Microbiol. 51 2001 1011 1021
191. K.V. Vessey Plant growth promoting rhizobacteria as biofertlizers Plant Soil 255 2003 571 586
192. S. Visser, R.M. Danielson, and D. Parkinson Field performance of Elaeagnus commutata and Shepherdia canadensis (Elaeagnaceae) inoculated with soil containing Frankia and vesicular-arbuscular mycorrhizal fungi Can. J. Bot. 69 1991 1321 1328
193. K.M. Vlassak, and J. Vanderleyden Factors influencing nodule occupancy by inoculant rhizobia Crit. Rev. Plant Sci. 16 1997 163 229
194. J.P. Vogel, K.E. Woeste, A. Theologis, and J.J. Kieber Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively Plant Biol. 95 1998 4766 4771
195. C. Voisard, C. Keel, D. Haas, and G. Defago Cyanide production by Pseudomonas fluorescens helps suppress Black Root Rot of tobacco under gnotobiotic conditions EMBO J. 8 1989 351 358
196. F. Waelkens, T. Voets, K. Vlassak, J. Vanderleyden, and P. Van Rhijn The nodS gene of Rhizobium tropici CIAT899 is necessary for nodulation of Phaseolus vulgaris and Leucaena leucocephala Mol. Plant Microbe Inter. 8 1995 147 154
197. R.J. Wais, D.H. Keating, and S.R. Long Structure-function analysis of Nod factor-induced root hair calcium spiking in Rhizobium-legume symbiosis Plant Physiol. 129 2002 211 224
198. R.A. Weidhase, J. Lehmann, H. Kramell, G. Sembdner, and B. Parthier Degradation of ribulose-1,5-bisphosphate carboxylase and chlorophyll in senescing barley leaf segments triggered by jasmonic acid methylester, and counteraction by cytokinin Physiol. Plant 69 1987 161 166
199. N. Wood Nodulation by numbers: the role of ethylene in symbiotic nitrogen fixation Trends Plant Sci. 6 2001 501 502
200. S.M. Wood, W. Newcomb, and D. Nelson Fine structure of the microsymbiont of the actinorhizal root nodules of mountain mahogany (Cercocarpus ledifolius, family Rosaceae) Can. J. Bot. 67 1989 116 120
201. Z. Yan, M.S. Reddy, and J.W. Kloepper Survival and colonization of rhizobacteria in a tomato transplant system Can. J. Microbiol. 49 2003 383 389
202. S.F. Yang, and N.E. Hoffman Ethylene biosynthesis and its regulation in higher plants Ann. Rev. Plant Physiol. 35 1986 155 189
203. G.Y. Yuen, M.N. Schroth, and A.H. McCain Reduction of Fusarium wilt of carnation with suppressive soils and antagonistic bacteria Plant Dis. 69 1985 1071 1075
204. E. Zakharova, A. Shcherbakov, V. Brudnik, N. Skripko, N. Sh. Bulkhin, and V. Ignatov Biosynthesis of indole-3-acetic acid in Azospirillum brasilense: insights from quantum chemistry Eur. J. Biochem. 259 1999 572 576
205. F. Zhang, and D.L. Smith Preincubation of Bradyrhizobium japonicum with genistein accelerates nodule development of soybean at suboptimal root zone temperatures Plant Physiol. 108 1995 961 968
206. F. Zhang, and D.L. Smith Genistein accumulation in soybean (Glycine max (L.) Merr.) root systems under suboptimal root zone temperatures J. Exp. Bot. 47 1996 785 792
207. F. Zhang, N. Dhasti, R. Hynes, and D.L. Smith Plant growth promoting rhizobacteria and soybean [Glycine max (L.) Merr.] nodulation and nitrogen fixation at suboptimal root zone temperatures Ann. Bot. 77 1996 453 459
208. R. Zhang, and D.L. Smith Application of genistein to inocula and soil to overcome low spring soil temperature inhibition of soybean nodulation and nitrogen fixation Plant Soil 192 1997 141 151
209. H. Zhang, B. Prithiviraj, A. Souleimanov, F. D'Aoust, T.C. Charles, B.T. Driscoll, and D.L. Smith The effect of temperature and genistein concentration on lipo-chitooligosaccharide (LCO) production by wild-type and mutant strains of Bradyrhizobium japonicum Soil Biol. Biochem. 34 2002 1175 1180
210. X.M. Zhou, A.F. Mackenzie, C.A. Madramootoo, and D.L. Smith Effects of stem-injected plant growth regulators, with or without sucrose, on grain production, biomass and photosynthetic activity of field-grown corn plants J. Agron. Crop Sci. 183 1999 103 110