The determinants of the actinorhizal symbiosis

Microbes and Environments

Volumn 25, Issue 4, 2010, Pages 241-252

  Kucho, Ken Ichi ^a   Hay, Anne Emmanuelle ^b   Normand, Philippe ^b  

^a KAGOSHIMA UNIVERSITY   (Japan)

^b University of Lyon   (France)

Author keywords

Actinorhizal plant; Frankia; Nitrogen fixation; Root nodule; Symbiosis

Indexed keywords

BACTERIAL PROTEIN;

FRANKIA; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT; PLANT PHYSIOLOGY; REVIEW; RHIZOBIUM; SYMBIOSIS;

BACTERIAL PROTEINS; FRANKIA; GENE EXPRESSION REGULATION, BACTERIAL; PLANT PHYSIOLOGICAL PHENOMENA; PLANTS; RHIZOBIUM; SYMBIOSIS;

BACTERIA (MICROORGANISMS); FRANKIA; RHIZOBIUM;

EID: 78650036431     PISSN: 13426311     EISSN: 13426311     Source Type: Journal    
DOI: 10.1264/jsme2.ME10143     Document Type: Review

References (120)

1. Albus, U., R. Baier, O. Holst, A. Puhler, and K. Niehaus. 2001. Suppression of an elicitor-induced oxidative burst reaction in Medicago sativa cell cultures by Sinorhizobium meliloti lipopolysaccharides. New Phytol. 151:597-606.
2. Alloisio, N., S. Félix, J. Maréchal, P. Pujic, Z. Rouy, D. Vallenet, C. Medigue, and P. Normand. 2007. Frankia alni proteome under nitrogen-fixing and nitrogen-replete conditions. Physiol. Plant. 13:440-453.
3. Alloisio, N., C. Queiroux, P. Fournier, et al. 2010. The Frankia alni symbiotic transcriptome. Mol. Plant Microb. Interact. 23:593-607.
4. Bagnarol, E., J. Popovici, J. Maréchal, N. Alloisio, P. Pujic, P. Normand, and M. Fernandez. 2007. Frankia proteins induced by phenolic extracts from Myricaceae seeds. Emphasis on oxidative stress and iron metabolism. Physiol. Plant. 130:380-390.
5. Baker, D. 1987. Relationships among pure-cultured strains of Frankia based on host specificity. Physiol. Plant 70:245-248.
6. Barabote, R.D., G. Xie, D.H. Leu, et al. 2009. Complete genome of the cellulolytic thermophile Acidothermus cellulolyticus 11B provides insights into its ecophysiological and evolutionary adaptations. Genome Res. 19:1033-1043.
7. Barnett, M.J., C.J. Toman, R.F. Fisher, and S.R. Long. 2004. A dual-genome Symbiosis Chip for coordinate study of signal exchange and development in a prokaryote-host interaction. Proc. Natl. Acad. Sci. USA 101:16636-16641.
8. Battisti, L., J.C. Lara, and J.A. Leigh. 1992. Specific oligosaccharide form of the Rhizobium meliloti exopolysaccharide promotes nodule invasion in alfalfa. Proc. Natl. Acad. Sci. USA 89:5625-5629.
9. Benson, D.R., and W.B. Silvester. 1993. Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol. Rev. 57:293-319.
10. Berry, A., R. Kahn, and M. Booth. 1989. Identification of indole compounds secreted by Frankia HFPArI3 in defined culture medium. Plant & Soil 118:205-209.
11. Berry, A.M., and L.A. Sunell. 1990. The infection process and nodule development, p. 61-81. In C.R. Schwintzer, and J.D. Tjepkema (ed.), The Biology of Frankia and Actinorhizal Plants. Academic Press, Inc., San Diego.
12. Berry, A., O. Harriott, R. Moreau, S. Osman, D. Benson, and A. Jones. 1993. Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc. Natl. Acad. Sci. USA 90:6091-6094.
13. Bhagwat, A.A., A. Mithofer, P.E. Pfeffer, C. Kraus, N. Spickers, A. Hotchkiss, J. Ebel, and D.L. Keister. 1999. Further studies of the role of cyclic beta-glucans in symbiosis. An NdvC mutant of Bradyrhizobium japonicum synthesizes cyclodecakis-(1-->3)-betaglucosyl. Plant Physiol. 119:1057-1064.
14. Blaise, B.J., J. Giacomotto, B. Elena, M.E. Dumas, P. Toulhoat, L. Segalat, and L. Emsley. 2007. Metabotyping of Caenorhabditis elegans reveals latent phenotypes. Proc. Natl. Acad. Sci. USA 104:19808-19812.
15. Bordage, E. 1916. Le repeuplement végétal et animal des îles Krakatoa depuis l'éruption de 1883. Annales Géographie 25:1-22.
16. Breedveld, M.W., and K.J. Miller. 1994. Cyclic beta-glucans of members of the family Rhizobiaceae. Microbiol. Rev. 58:145-161.
17. Brink, B.A., J. Miller, R.W. Carlson, and K.D. Noel. 1990. Expression of Rhizobium leguminosarum CFN42 genes for lipopolysaccharide in strains derived from different R. leguminosarum soil isolates. J. Bacteriol. 172:548-555.
18. Burleigh, S.H., and J.O. Dawson. 1991. In vitro sporulation of Frankia strain HFPCcI3 from Casuarina cunninghamiana. Can. J. Microbiol. 37:897-901.
19. Campbell, G.R., B.L. Reuhs, and G.C. Walker. 2002. Chronic intracellular infection of alfalfa nodules by Sinorhizobium meliloti requires correct lipopolysaccharide core. Proc. Natl. Acad. Sci. USA 99:3938-3943.
20. Ceremonie, H. 1998. Interactions moleculaires et genetiques de la symbiose Frankia-aulne. Ph. D. Thesis Lyon1, Lyon.
21. Ceremonie, H., F. Debelle, and M.P. Fernandez. 1999. Structural and functional comparison of Frankia root hair deforming factor and rhizobia Nod factor. Can. J. Bot. 77:1293-1301.
22. Cheng, H.P., and G.C. Walker. 1998. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J. Bacteriol. 180:5183-5191.
23. Clawson, M.L., A. Bourret, and D.R. Benson. 2004. Assessing the phylogeny of Frankia-actinorhizal plant nitrogen-fixing root nodule symbioses with Frankia 16S rRNA and glutamine synthetase gene sequences. Mol. Phylogenet. Evol. 31:131-138.
24. Cournoyer, B., and P. Normand. 1992. Electropermeabilization of Frankia intact cells to plasmid DNA. Acta Ecologica 13:369-378.
25. D'Haeze, W., J. Glushka, R. De Rycke, M. Holsters, and R.W. Carlson. 2004. Structural characterization of extracellular polysaccharides of Azorhizobium caulinodans and importance for nodule initiation on Sesbania rostrata. Mol. Microbiol. 52:485-500.
26. Denarie, J., F. Debelle, and C. Rosenberg. 1992. Signaling and host range variation in nodulation. Annu. Rev. Microbiol. 46:497-531.
27. Djordjevic, S.P., H. Chen, M. Batley, J.W. Redmond, and B.G. Rolfe. 1987. Nitrogen fixation ability of exopolysaccharide synthesis mutants of Rhizobium sp. strain NGR234 and Rhizobium trifolii is restored by the addition of homologous exopolysaccharides. J. Bacteriol. 169:53-60.
28. Dylan, T., P. Nagpal, D.R. Helinski, and G.S. Ditta. 1990. Symbiotic pseudorevertants of Rhizobium meliloti ndv mutants. J. Bacteriol. 172:1409-1417.
29. Faucher, C., F. Maillet, J. Vasse, C. Rosenberg, A.A. van Brussel, G. Truchet, and J. Denarie. 1988. Rhizobium meliloti host range nodH gene determines production of an alfalfa-specific extracellular signal. J. Bacteriol. 170:5489-5499.
30. Faucher, C., S. Camut, J. Denarie, and G. Truchet. 1989. The nodH and nodQ host range genes of Rhizobium meliloti behave as avirulence genes in R. leguminosarum bv. viciae and determine changes in the production of plant-specific extracellular signals. Mol. Plant Microbe Interact. 2:291-300.
31. Ferguson, G.P., A. Datta, R.W. Carlson, and G.C. Walker. 2005. Importance of unusually modified lipid A in Sinorhizobium stress resistance and legume symbiosis. Mol. Microbiol. 56:68-80.
32. Flaherty, C., D.E. Minnikin, and I.C. Sutcliffe. 1996. A chemotaxonomic study of the lipoglycans of Rhodococcus rhodnii N445 (NCIMB 11279). Zentralbl. Bakteriol. 285:11-19.
33. Flaherty, C., and I.C. Sutcliffe. 1999. Identification of a lipoarabinomannan-like lipoglycan in Gordonia rubropertincta. Syst. Appl. Microbiol. 22:530-533.
34. Franche, C., D. Diouf, Q.V. Le, D. Bogusz, A. N'Diaye, H. Gherbi, C. Gobé, and E. Duhoux. 1997. Genetic transformation of the actinorhizal tree Allocasuarina verticillata by Agrobacterium tumefaciens. Plant J. 11:897-904.
35. Fraysse, N., F. Couderc, and V. Poinsot. 2003. Surface polysaccharide involvement in establishing the rhizobium-legume symbiosis. Eur. J. Biochem. 270:1365-1380.
36. Galibert, F., T.M. Finan, S.R. Long, et al. 2001. The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668-672.
37. Garton, N.J., M. Gilleron, T. Brando, H.H. Dan, S. Giguere, G. Puzo, J.F. Prescott, and I.C. Sutcliffe. 2002. A novel lipoarabinomannan from the equine pathogen Rhodococcus equi. Structure and effect on macrophage cytokine production. J. Biol. Chem. 277:31722-31733.
38. Gherbi, H., K. Markmann, S. Svistoonoff, et al. 2008. SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proc. Natl. Acad. Sci. USA 105:4928-4932.
39. Gilleron, M., N.J. Garton, J. Nigou, T. Brando, G. Puzo, and I.C. Sutcliffe. 2005. Characterization of a truncated lipoarabinomannan from the Actinomycete Turicella otitidis. J. Bacteriol. 187:854-861.
40. Giraud, E., L. Moulin, D. Vallenet, et al. 2007. Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316:1307-1312.
41. Gonzalez, J.E., B.L. Reuhs, and G.C. Walker. 1996. Low molecular weight EPS II of Rhizobium meliloti allows nodule invasion in Medicago sativa. Proc. Natl. Acad. Sci. USA 93:8636-8641.
42. Gualtieri, G., and T. Bisseling. 2000. The evolution of nodulation. Plant Mol. Biol. 42:181-194.
43. Hammad, Y., J. Marechal, B. Cournoyer, P. Normand, and A.M. Domenach. 2001. Modification of the protein expression pattern induced in the nitrogen-fixing actinomycete Frankia sp. Strain ACN14a-tsr by root exudates of its symbiotic host Alnus glutinosa and cloning of the sodF gene. Can. J. Microbiol. 47:541-547.
44. Hammad, Y., R. Nalin, J. Marechal, K. Fiasson, R. Pepin, A.M. Berry, P. Normand, and A.-M. Domenach. 2003. A possible role for phenylacetic acid (PAA) in Alnus glutinosa nodulation by Frankia. Plant & Soil 254:193-205.
45. Horvath, B., C.W. Bachem, J. Schell, and A. Kondorosi. 1987. Host-specific regulation of nodulation genes in Rhizobium is mediated by a plant-signal, interacting with the nodD gene product. EMBO J. 6:841-848.
46. Ingram, B.O., C. Sohlenkamp, O. Geiger, and C.R. Raetz. Altered lipid A structures and polymyxin hypersensitivity of Rhizobium etli mutants lacking the LpxE and LpxF phosphatases. Biochim. Biophys. Acta 1801:593-604.
47. Kaneko, T., Y. Nakamura, S. Sato, et al. 2000. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res. 7:331-338.
48. Krumholz, G.D., M.S. Chval, M.J. McBride, and L.S. Tisa. 2003. Germination and physiological properties of Frankia spores. Plant & Soil 254:57-67.
49. Kucho, K., K. Kakoi, M. Yamaura, S. Higashi, T. Uchiumi, and M. Abe. 2009. Transient transformation of Frankia by fusion marker genes in liquid culture. Microbes Environ. 24:231-240.
50. Lagares, A., G. Caetano-Anolles, K. Niehaus, J. Lorenzen, H.D. Ljunggren, A. Puhler, and G. Favelukes. 1992. A Rhizobium meliloti lipopolysaccharide mutant altered in competitiveness for nodulation of alfalfa. J. Bacteriol. 174:5941-5952.
51. Laus, M.C., T.J. Logman, A.A. Van Brussel, R.W. Carlson, P. Azadi, M.Y. Gao, and J.W. Kijne. 2004. Involvement of exo5 in production of surface polysaccharides in Rhizobium leguminosarum and its role in nodulation of Vicia sativa subsp. nigra. J. Bacteriol. 186:6617-6625.
52. Laus, M.C., A.A. van Brussel, and J.W. Kijne. 2005. Exopolysaccharide structure is not a determinant of host-plant specificity in nodulation of Vicia sativa roots. Mol. Plant Microbe Interact. 18:1123-1129.
53. Lawrence, D., and L. Hulbert. 1950. Growth stimulation to adjacent plants by lupin and alder on recent glacier deposits in South-Eastern Alaska. Bull. Ecol. Soc. Amer. 31:58.
54. Lawrence, D., R. Schoenike, A. Quispel, and G. Bond. 1967. The role of Dryas drummondii in vegetation development following ice recession at Glacier Bay, Alaska, with special reference to its nitrogen fixation by root nodules. J. Ecol. 55:793-813.
55. Lea-Smith, D.J., J.S. Pyke, D. Tull, M.J. McConville, R.L. Coppel, and P.K. Crellin. 2007. The reductase that catalyzes mycolic motif synthesis is required for efficient attachment of mycolic acids to arabinogalactan. J. Biol. Chem. 282:11000-11008.
56. Lea-Smith, D.J., K.L. Martin, J.S. Pyke, D. Tull, M.J. McConville, R.L. Coppel, and P.K. Crellin. 2008. Analysis of a new mannosyltransferase required for the synthesis of phosphatidylinositol mannosides and lipoarabinomannan reveals two lipomannan pools in corynebacterineae. J. Biol. Chem. 283:6773-6782.
57. Leigh, J.A., E.R. Signer, and G.C. Walker. 1985. Exopolysaccharidedeficient mutants of Rhizobium meliloti that form ineffective nodules. Proc. Natl. Acad. Sci. USA 82:6231-6235.
58. Leul, M., P. Normand, and A. Sellstedt. 2009. The phylogeny of uptake hydrogenases in Frankia. Int. Microbiol. 12:23-28.
59. Madsen, E.B., L.H. Madsen, S. Radutoiu, et al. 2003. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637-640.
60. Marechal, J., B. Clement, R. Nalin, C. Gandon, S. Orso, J.H. Cvejic, M. Bruneteau, A. Berry, and P. Normand. 2000. A recA gene phylogenetic analysis confirms the close proximity of Frankia to Acidothermus. Int. J. Syst. Evol. Microbiol. 50:781-785.
61. Marechal, J., R. Santos, N. Alloisio, Y. Hammad, A. Domenach, and P. Normand. 2003. Characterization of the sodF gene region of Frankia sp. strain ACN14a and complementation of Escherichia coli sod mutant. Can. J. Microbiol. 49:294-300.
62. Mastronunzio, J.E., Y. Huang, and D.R. Benson. 2009. Diminished exoproteome of Frankia spp. in culture and symbiosis. Appl. Environ. Microbiol. 75:6721-6728.
63. Mazur, A., J.E. Krol, J. Wielbo, T. Urbanik-Sypniewska, and A. Skorupska. 2002. Rhizobium leguminosarum bv. trifolii PssP protein is required for exopolysaccharide biosynthesis and polymerization. Mol. Plant Microbe Interact. 15:388-397.
64. McIver, J., M.A. Djordjevic, J.J. Weinman, G.L. Bender, and B.G. Rolfe. 1989. Extension of host range of Rhizobium leguminosarum bv. trifolii caused by point mutations in nodD that result in alterations in regulatory function and recognition of inducer molecules. Mol. Plant Microbe Interact. 2:97-106.
65. Miller, I.M., and D.D. Baker. 1986. Nodulation of actinorhizal plants by Frankia strains capable of both root hair infection and intercellular penetration. Protoplasma 131:82-91.
66. Mithöfer, A., A.A. Bhagwat, M. Feger, and J. Ebel. 1996. Suppression of fungal β-glucan-induced plant defence in soybean (Glycine max L.) by cyclic 1,3-1,6-β-glucans for the symbiont Bradyrhizobium japonicum. Planta 199:270-275.
67. Mort, A., P. Normand, and M. Lalonde. 1983. 2-O-methyl-Dmannose, a key sugar in the taxonomy of Frankia. Can. J. Microbiol. 29:993-1002.
68. Moulin, L., A. Munive, B. Dreyfus, and C. Boivin-Masson. 2001. Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature 411:948-950.
69. Mullin, B.C., and C.S. An. 1990. The molecular genetics of Frankia, p. 195-214. In C.R. Schwintzer, and J.D. Tjepkema (ed.), The Biology of Frankia and Actinorhizal Plants. Academic Press, San Diego.
70. Myers, A.K., and L.S. Tisa. 2003. Effect of electroporation conditions on cell viability of Frankia EuI1c. Plant & Soil 254:83-88.
71. Niehaus, K., D. Kapp, and A. Puhler. 1993. Plant defence and delayed infection of alfalfa pseudonodules induced by an exopolysaccharide (EPS I)-deficient Rhizobium meliloti mutant. Planta 190:415-425.
72. Nigou, J., M. Gilleron, and G. Puzo. 2003. Lipoarabinomannans: from structure to biosynthesis. Biochimie 85:153-166.
73. Noel, K.D., K.A. Vandenbosch, and B. Kulpaca. 1986. Mutations in Rhizobium phaseoli that lead to arrested development of infection threads. J. Bacteriol. 168:1392-1401.
74. Noel, K.D., L.S. Forsberg, and R.W. Carlson. 2000. Varying the abundance of O antigen in Rhizobium etli and its effect on symbiosis with Phaseolus vulgaris. J. Bacteriol. 182:5317-5324.
75. Normand, P., S. Orso, B. Cournoyer, P. Jeannin, C. Chapelon, J. Dawson, L. Evtushenko, and A.K. Misra. 1996. Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae. Int. J. Syst. Bacteriol. 46:1-9.
76. Normand, P., P. Lapierre, L.S. Tisa, et al. 2007. Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res. 17:7-15.
77. Normand, P., C. Queiroux, L. Tisa, D. Benson, S. Cruveiller, Z. Rouy, and C. Medigue. 2007. Exploring the genomes of Frankia sp. Physiol. Plant. 13:331-343.
78. Normand, P., and M. Fernandez. 2009. Evolution and diversity of Frankia, p. 103-125. In K. Pawlowski (ed.), Prokaryotic Symbionts in Plants, vol. 8. Springer Verlag, Berlin, Heidelberg.
79. th volume. Bergey's Manual Trust, Athens, Ga.
80. Parniske, M., P.E. Schmidt, K. Kosch, and P. Müller. 1994. Plant defense response of host plants with determinate nodules induced by EPS defective exoB mutants of Bradyrhizobium japonicum. Mol. Plant Microbe Interact. 7:631-638.
81. Parsons, R., W.B. Silvester, S. Harris, W.T. Gruijters, and S. Bullivant. 1987. Frankia vesicles provide inducible and absolute oxygen protection for nitrogenase. Plant Physiol. 83:728-731.
82. Peck, M.C., R.F. Fisher, and S.R. Long. 2006. Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti. J. Bacteriol. 188:5417-5427.
83. Pellock, B.J., H.P. Cheng, and G.C. Walker. 2000. Alfalfa root nodule invasion efficiency is dependent on Sinorhizobium meliloti polysaccharides. J. Bacteriol. 182:4310-4318.
84. Peret, B., S. Svistoonoff, B. Lahouze, F. Auguy, C. Santi, P. Doumas, and L. Laplaze. 2008. A Role for auxin during actinorhizal symbioses formation? Plant Signal Behav. 3:34-35.
85. Perotto, S., N.J. Brewin, and E.L. Kannenberg. 1994. Cytological evidence for a host-defense response that reduces cell and tissue invasion in pea nodules by lipopolysaccharide-defective mutants of Rhizobium-Leguminosarum strain-3841. Mol. Plant Microbe Interact. 7:99-112.
86. Perret, X., C. Staehelin, and W.J. Broughton. 2000. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64:180-201.
87. Radutoiu, S., L.H. Madsen, E.B. Madsen, et al. 2003. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585-592.
88. Radutoiu, S., L.H. Madsen, E.B. Madsen, et al. 2007. LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J. 26:3923-3935.
89. Reuhs, B.L., M.N. Williams, J.S. Kim, R.W. Carlson, and F. Cote. 1995. Suppression of the Fix-phenotype of Rhizobium meliloti exoB mutants by lpsZ is correlated to a modified expression of the K polysaccharide. J. Bacteriol. 177:4289-4296.
90. Roy, S., D.P. Khasa, and C.W. Greer. 2007. Combining alders, frankiae, and mycorrhizae for the revegetation and remediation of contaminated ecosystems. Can. J. Bot. 85:237-251.
91. Santos, C., J. Vieira, P. Normand, P. Moradas-Ferreira, and F. Tavares. 2007. Expression, activity and phylogeny of catalases: a global approach to Frankia alni ACN14a oxidative stress response. Physiol. Plant. 130:454-463.
92. Schorey, J.S., and L. Sweet. 2008. The Mycobacterial Glycopeptidolipids: structure, function and their role in pathogenesis. Glycobiology 18:832-841.
93. Sharypova, L.A., K. Niehaus, H. Scheidle, O. Holst, and A. Becker. 2003. Sinorhizobium meliloti acpXL mutant lacks the C28 hydroxylated fatty acid moiety of lipid A and does not express a slow migrating form of lipopolysaccharide. J. Biol. Chem. 278:12946-12954.
94. Silvester, W., S. Harris, and J.D. Tjepkema. 1990. Oxygen regulation and hemoglobin, p. 157-176. In C.R. Schwintzer, and J.D. Tjepkema (ed.), The Biology of Frankia and Actinorhizal Plants. Academic Press, New York, NY.
95. Simonet, P., P. Normand, A.M. Hirsch, and A.D.L. Akkermans. 1990. The genetics of the Frankia-actinorhizal symbiosis, p. 77-109. In P.M. Gresshoff (ed.), Molecular Biology of Symbiotic Nitrogen Fixation. CRC Press, Boca Raton.
96. Skorupska, A., M. Janczarek, M. Marczak, A. Mazur, and J. Krol. 2006. Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb. Cell Fact. 5:7.
97. Spaink, H.P., J. Weinman, M.A. Djordjevic, C.A. Wijffelman, R.J. Okker, and B.J. Lugtenberg. 1989. Genetic analysis and cellular localization of the Rhizobium host specificity-determining NodE protein. EMBO J. 8:2811-2818.
98. Stacey, G., J.S. So, L.E. Roth, S.B. Lakshmi, and R.W. Carlson. 1991. A lipopolysaccharide mutant of Bradyrhizobium japonicum that uncouples plant from bacterial differentiation. Mol. Plant Microbe Interact. 4:332-340.
99. Stokkermans, T.J., and N.K. Peters. 1994. Bradyrhizobium elkanii lipo-oligosaccharide signals induce complete nodule structures on Glycine soja Siebold et Zucc. Planta 193:413-420.
100. Sutcliffe, I.C. 1994. The lipoteichoic acids and lipoglycans of Gram-positive bacteria: a chemotaxonomic perspective. Syst. Appl. Microbiol. 17:467-480.
101. Sutcliffe, I.C. 1995. Identification of a lipoarabinomannan-like lipoglycan in Corynebacterium matruchotii. Arch. Oral Biol. 40:1119-1124.
102. Sutcliffe, I.C. 2000. Characterisation of a lipomannan lipoglycan from the mycolic acid containing actinomycete Dietzia maris. Antonie van Leeuwenhoek 78:195-201.
103. Sutcliffe, I.C., and N. Shaw. 1991. Atypical lipoteichoic acids of gram-positive bacteria. J. Bacteriol. 173:7065-7069.
104. Sy, A., E. Giraud, P. Jourand, et al. 2001. Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J. Bacteriol. 183:214-220.
105. Tagawah, H. 1964. Study of the volcanic vegetation in Sakurajima. Mem. Fac. Sci. Kyushu Univ. Ser. E (Biol.) 3:166-223.
106. Triplett, E.W., and M.J. Sadowsky. 1992. Genetics of competition for nodulation of legumes. Annu. Rev. Microbiol. 46:399-428.
107. Truchet, G., P. Roche, P. Lerouge, J. Vasse, S. Camut, F. de Billy, J. Promé, and J. Dénarié. 1991. Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351:670-673.
108. Tzean, S.S., and J.G. Torrey. 1989. Spore germination and the life cycle of Frankia in vitro. Can. J. Microbiol. 35:801-806.
109. Vallenet, D., L. Labarre, Z. Rouy, et al. 2006. MaGe: a microbial genome annotation system supported by synteny results. Nucleic Acids Res. 34:53-65.
110. van Rhijn, P., N.A. Fujishige, P.O. Lim, and A.M. Hirsch. 2001. Sugar-binding activity of pea lectin enhances heterologous infection of transgenic alfalfa plants by Rhizobium leguminosarum biovar viciae. Plant Physiol. 126:133-144.
111. Vanderlinde, E.M., A. Muszynski, J.J. Harrison, S.F. Koval, D.L. Foreman, H. Ceri, E.L. Kannenberg, R.W. Carlson, and C.K. Yost. 2009. Rhizobium leguminosarum biovar viciae 3841, deficient in 27-hydroxyoctacosanoate-modified lipopolysaccharide, is impaired in desiccation tolerance, biofilm formation and motility. Microbiology 155:3055-3069.
112. Vedam, V., E.L. Kannenberg, J.G. Haynes, D.J. Sherrier, A. Datta, and R.W. Carlson. 2003. A Rhizobium leguminosarum AcpXL mutant produces lipopolysaccharide lacking 27-hydroxyoctacosanoic acid. J. Bacteriol. 185:1841-1850.
113. Vershinina, Z.R., A.K. Baimiev, and A.V. Chemeris. 2010. Symbiotic reactions of sea-buckthorn roots transformed with the pea lectin gene. Russian J. Plant Physiol. 57:101-109.
114. Wang, J.C. 2005. Finding primary targets of transcriptional regulators. Cell Cycle 4:356-358.
115. Wang, L.X., Y. Wang, B. Pellock, and G.C. Walker. 1999. Structural characterization of the symbiotically important lowmolecular-weight succinoglycan of Sinorhizobium meliloti. J. Bacteriol. 181:6788-6796.
116. Wei, M., T. Yokoyama, K. Minamisawa, et al. 2008. Soybean seed extracts preferentially express genomic loci of Bradyrhizobium japonicum in the initial interaction with soybean, Glycine max (L.) Merr. DNA Res. 15:201-214.
117. Wielbo, J., A. Mazur, J. Krol, M. Marczak, J. Kutkowska, and A. Skorupska. 2004. Complexity of phenotypes and symbiotic behaviour of Rhizobium leguminosarum biovar trifolii exopolysaccharide mutants. Arch. Microbiol. 182:331-336.
118. Williams, M.N., R.I. Hollingsworth, S. Klein, and E.R. Signer. 1990. The symbiotic defect of Rhizobium meliloti exopolysaccharide mutants is suppressed by lpsZ+, a gene involved in lipopolysaccharide biosynthesis. J. Bacteriol. 172:2622-2632.
119. Wu, D., P. Hugenholtz, K. Mavromatis, et al. 2009. A phylogenydriven genomic encyclopaedia of Bacteria and Archaea. Nature 462:1056-1060.
120. Yang, C., E.R. Signer, and A.M. Hirsch. 1992. Nodules initiated by Rhizobium meliloti exopolysaccharide mutants lack a discrete, persistent nodule meristem. Plant Physiol. 98:143-151.