1887

Chapter 22 : Differentiation of Free-Living Rhizobia into Endosymbiotic Bacteroids

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Differentiation of Free-Living Rhizobia into Endosymbiotic Bacteroids, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818166/9781555811587_Chap22-1.gif /docserver/preview/fulltext/10.1128/9781555818166/9781555811587_Chap22-2.gif

Abstract:

This chapter outlines the complexities of bacterial invasion and bacteroid differentiation. Because the early plant-bacterial signal exchange has been the subject of many excellent recent reviews the chapter emphasizes the later stages about which less is known. The strategies that both bacteria and plant use to maintain the symbiosis and prevent pathogenesis are also discussed. The formation of effective nodules containing differentiated, nitrogen-fixing bacteroids consists of a defined series of stages. In response to chemical signals secreted by plant roots, rhizobia attach to root hairs, which are cells on the root surface that project outward into the soil. Chemotaxis plays an important role in the initial attraction of rhizobia to plant root hairs. The signal transduction pathway leading to the formation of the nodule must have unique characteristics, because nodules are completely different from other normal plant structures. Mutants lacking succinoglycan were first isolated by the inability of colonies to fluoresce on plates containing the laundry whitener Calcofluor. Such mutants still complete Nod factor-dependent events, such as root hair deformation, cortical cell divisions, and infection thread initiation. Immunological studies with monoclonal antibodies have documented changes in lipopolysaccharide (LPS) structure during bacteroid differentiation and when free-living rhizobia are cultured in different media. Knockout strategies are useful because it is easy to map and clone the affected genes and because many functions in bacteroid development are probably not essential for free-living cells.

Citation: Margolin W. 2000. Differentiation of Free-Living Rhizobia into Endosymbiotic Bacteroids, p 441-466. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch22
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

Root nodules on alfalfa induced by S. meliloti.

Citation: Margolin W. 2000. Differentiation of Free-Living Rhizobia into Endosymbiotic Bacteroids, p 441-466. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch22
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

Scanning electron micrograph of S. meliloti bacteroids in an alfalfa nodule homogenate. The arrows highlight bacteroids, which include a Y-shaped cell in the center of the image and two other elongated cells. The other large structures visible are starch granules.

Citation: Margolin W. 2000. Differentiation of Free-Living Rhizobia into Endosymbiotic Bacteroids, p 441-466. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch22
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Initial interaction between S. meliloti and alfalfa root hairs. S. meliloti cells expressing GFP (appearing bright on the darker background) were photographed by confocal microscopy at different stages, including initial attachment to the root hair (A), entrapment by the curled root hair (B), and migration down the infection thread (C). (Images courtesy of Daniel J. Gage, University of Connecticut.)

Citation: Margolin W. 2000. Differentiation of Free-Living Rhizobia into Endosymbiotic Bacteroids, p 441-466. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch22
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4
FIGURE 4

Outline of bacteroid development, from release to differentiation. A 4-week-old indeterminate nodule like that formed by the S. meliloti-alfalfa symbiosis is shown, as adapted from the results of Vasse et al. (1990). The inset at the top depicts bacterial proliferation within the infection thread and subsequent endocytosis into the plant cell and engulfment by the PBM. The cells within the nodule represent a sample of each zone, denoted at the right of the nodule. Bacteroid types and zones are as described in the text and in Vasse et al., 1990.

Citation: Margolin W. 2000. Differentiation of Free-Living Rhizobia into Endosymbiotic Bacteroids, p 441-466. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch22
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555818166.chap22
1. Albrecht, C.,, R. Geurts,, and T. Bisseling. 1999. Legume nodulation and mycorrhizae formation; two extremes in host specificity meet. EMBO J. 18:281288.
2. Almon, L. 1933. Concerning the reproduction of bacteroids. Zentbl. Bakteriol. Parasitenkol. Infectionskr. Hyg. Abt. II 87:289297.
3. Ames, P.,, and K. Bergman. 1981. Competitive advantage provided by bacterial motility in the formation of nodules by Rhizobium meliloti. J. Bacteriol. 148:728729.
4. Arcondeguy, T.,, I. Huez,, P. Tillard,, C. Gang-neux,, F. de Billy,, A. Gojon,, G. Truchet,, and D. Kahn. 1997. The Rhizobium melilotiPII protein, which controls bacterial nitrogen metabolism, affects alfalfa nodule development. Genes Dev. 11: 11941206.
5. Armitage, J. P.,, and R. Schmitt. 1997. Bacterial chemotaxis: Rhodobacter sphaeroides and Sinorhizobium meliloti—variations on a theme? Microbiology 143:36713682.
6. Bal, A. K.,, S. Shantharam,, and D. P. Verma. 1980. Changes in the outer cell wall of Rhizobium during development of root nodule symbiosis in soybean. Can. J. Microbiol. 26:10961103.
7. Barnett, M. J.,, and S. R. Long. 1990. DNA sequence and translational product of a new nodulation-regulatory locus: syrM has sequence similarity to NodD proteins. J. Bacteriol. 172:36953700.
8. Barnett, M. J.,, and S. R. Long. 1997. Identification and characterization of a gene on Rhizobium meliloti pSyma, syrB, that negatively affects syrM expression. Mol. Plant-Microbe Interact. 10:550559.
9. Barnett, M. J.,, J. A. Swanson,, and S. R. Long. 1998. Multiple genetic controls on Rhizobium meliloti syrA, a regulator of exopolysaccharide abundance. Genetics 148:1932.
10. Barsomian, G. D.,, A. Urzainqui,, K. Lohman,, and G. C. Walker. 1992. Rhizobium meliloti mutants unable to synthesize anthranilate display a novel symbiotic phenotype. J. Bacteriol. 174: 44164426.
11. 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 89:56255629.
12. Batut, J.,, and P. Boistard. 1994. Oxygen control in Rhizobium. Antonie Leeuwenhoek 66:129150.
13. Batut, J.,, M. L. Daveran-Mingot,, M. David,, J. Jacobs,, A. M. Garnerone,, and D. Kahn. 1989. fixK, a gene homologous with fnr and crp from Escherichia coli, regulates nitrogen fixation genes both positively and negatively in Rhizobium meliloti. EMBOJ. 8:12791286.
14. Bisseling, T.,, R. C. van den Bos,, M. W. West-strate,, M. J. Hakkaart,, and A. van Kammen. 1979. Development of the nitrogen-fixing and protein-synthesizing apparatus of bacteroids in pea root nodules. Biochim. Biophys. Acta 562:515526.
15. Bladergroen, M. R.,, and H. P. Spaink. 1998. Genes and signal molecules involved in the rhizobia-Leguminoseae symbiosis. Curr. Opin. Plant Biol. 1:353359.
16. Boesten, B.,, J. Batut,, and P. Boistard. 1998. DctBD-dependent and -independent expression of the Sinorhizobium (Rhizobium) meliloti C4-dicar-boxylate transport gene (dctA) during symbiosis. Mol. Plant-Microbe Interact. 11:878886.
17. Bohlool, B. B.,, and E. L. Schmidt. 1976. Immunofluorescent polar tips of Rhizobium japonicum: possible site of attachment or lectin binding. J. Bacteriol. 125:11881194.
18. Bowden, M. G.,, and H. B. Kaplan. 1998. The Myxococcus xanthus lipopolysaccharide O-antigen is required for social motility and multicellular development. Mol. Microbiol. 30:275284.
19. Brewin, N. J. 1991. Development of the legume root nodule. Annu. Rev. Cell Biol. 7:191226.
20. Brewin, N. J.,, and I. V. Kardailsky. 1997. Legume lectins and nodulation by Rhizobium. Trends Plant Sci. 2:9298.
21. Brown, C. M.,, and M. J. Dilworth. 1975. Ammonia assimilation by rhizobium cultures and bacteroids. J. Gen. Microbiol. 86:3948.
22. Caetano-Anolles, G.,, D. K. Crist-Estes,, and W. D. Bauer. 1988. Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J. Bacteriol. 170:31643169.
23. Cheng, H.-P.,, and G. C. Walker. 1998. Succino-glycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J. Bacteriol. 180:51835191.
24. Ching, T. M.,, S. Hedtke,, and W. Newcomb. 1977. Isolation of bacteria, transforming bacteria, and bacteroids from soybean nodules. Plant Physiol. 60:771774.
25. Clover, R. H.,s J. Kieber,, and E. R. Signer. 1989. Lipopolysaccharide mutants of Rhizobium meliloti are not defective in symbiosis. J. Bacteriol. 171: 39613967.
26. Cook, D.,, D. Dreyer,, D. Bonnet,, M. Howell,, E. Nony,, and K. VandenBosch. 1995. Transient induction of a peroxidase gene in Medicago trunculata precedes infection by Rhizobium meliloti. Plant Cell 7:4355.
27. Cren, M.,, A. Kondorosi,, and E. Kondorosi. 1995. NolR controls expression of the Rhizobium meliloti nodulation genes involved in the core Nod factor synthesis. Mol. Microbiol. 15:733747.
28. David, M.,, M. L. Daveran,, J. Batut,, A. Dedieu,, O. Domergue,, J. Ghai,, C. Hertig,, P. Boistard,, and D. Kahn. 1988. Cascade regulation of nif gene expression in Rhizobium meliloti. Cell 54:671683.
29. Dazzo, F. B.,, G. L. Truchet,, J. E. Sherwood,, E. M. Hrabak,, M. Abe,, and S. H. Pankratz. 1984. Specific phases of root hair attachment in the Rhizobium trifolii-clover symbiosis. Appl. Environ. Microbiol. 48:11401150.
30. de Maagd, R. A.,, C. A. Wijffelman,, E. Pees,, and B. J. Lugtenberg. 1988. Detection and subcellular localization of two Sym plasmid-dependent proteins of Rhizobium leguminosarum biovar viciae. J. Bacteriol. 170:44244427.
31. Demont, N.,, M. Ardourel,, F. Maillet,, D. Promé,, M. Ferro,, J. C. Promé,, and J. Dénarié. 1994. The Rhizobium meliloti regulatory nodD3 and syrM genes control the synthesis of a particular class of nodulation factors N-acylated by (omega-l)-hy-droxylated fatty acids. EMBO J. 13:21392149.
32. Dénarié, J.,, F. Debelle,, and J. C. Promé. 1996. Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 65: 503535.
33. D'Hooghe, I.,, J. Michiels,, and J. Vanderleyden. 1998. The Rhizobium etli FixL protein differs in structure from other known FixL proteins. Mol. Gen. Genet. 257:576580.
34. Dickstein, R.,, T. Bisseling,, V. N. Reinhold,, and F. M. Ausubel. 1988. Expression of nodule-specific genes in alfalfa root nodules blocked at an early stage of development. Genes Dev. 2:677687.
35. Dilworth, M.,, and A. Glenn. 1984. How does a legume nodule work? Trends Biochem. Sci. 9: 519523.
36. Dilworth, M.,, and D. C. Williams. 1967. Nucleic acid changes in bacteroids of Rhizobium lupini during nodule development. J. Gen. Microbiol. 48: 3136.
37. Djordjevic, M. A.,, D. W. Gabriel,, and B. G. Rolfe. 1987. Rhizobium—the refined parasite of legumes. Annu. Rev. Phytopathol. 25:145168.
38. Dudley, M. E.,, T. W. Jacobs,, and S. R. Long. 1987. Microscopic studies of cell divisions induced in alfalfa roots by Rhizobium meliloti. Planta 171: 289301.
39. Durmowicz, M. C.,, and R. J. Maier. 1998. The FixK2 protein is involved in regulation of symbiotic hydrogenase expression in Bradyrhizobium japonicum. J. Bacteriol. 180:32533256.
40. Ehrhardt, D. W.,, E. M. Atkinson,, and S. R. Long. 1992. Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science 256:9981000.
41. Ehrhardt, D. W.,, R. Wais,, and S. R. Long. 1996. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85:673681.
42. Engelke, T.,, D. Jording,, D. Kapp,, and A. Pühler. 1989. Identification and sequence analysis of the Rhizobium meliloti dctA gene encoding the C4-dicarboxylate carrier. J. Bacteriol. 171:55515560.
43. Estabrook, E. M.,, and C. Sengupta-Gopalan. 1991. Differential expression of phenylalanine ammonia-lyase and chalcone synthase during soybean nodule development. Plant Cell 3:299308.
44. Fellay, R.,, M. Hanin,, G. Montorzi,, J. Frey,, C. Freiberg,, W. Golinowski,, C. Staehelin,, W. J. Broughton,, and S. Jabbouri. 1998. nodD2 of Rhizobium sp. NGR234 is involved in the repression of the nodABC operon. Mol. Microbiol. 27: 10391050.
45. Felle, H. H.,, E. Kondorosi,, A. Kondorosi,, and M. Schultze. 1998. The role of ion fluxes in Nod factor signalling in Medicago sativa. Plant J. 13: 455464.
46. Finan, T. M.,, A. M. Hirsch,, J. A. Leigh,, E. Johan-sen,, G. A. Kuldau,, S. Deegan,, G. C. Walker,, and E. R. Signer. 1985. Symbiotic mutants of Rhizobium meliloti that uncouple plant from bacterial differentiation. Cell 40:869877.
47. Finlay, B. B.,, and P. Cossart. 1997. Exploitation of mammalian host cell functions by bacterial pathogens. Science 276:718725.
48. Finlay, B. B.,, and S. Falkow. 1997. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61:136169.
49. Fischer, H. M. 1994. Genetic regulation of nitrogen fixation in rhizobia. Microbiol. Rev. 58:352386.
50. Fischer, H. M. 1996. Environmental regulation of rhizobial symbiotic nitrogen fixation genes. Trends Microbiol. 4:317320.
51. Flores, M.,, P. Mavingui,, L. Girard,, X. Perret,, W. J. Broughton,, E. Martinez-Romero,, G. Davila,, and R. Palacios. 1998. Three replicons of Rhizobium sp. strain NGR234 harbor symbiotic gene sequences. J. Bacteriol. 180:60526053.
52. Fougere, F.,, and D. Le Rudulier. 1990. Uptake of glycine betaine and its analogues by bacteroids of Rhizobium meliloti. J. Gen. Microbiol. 136:157163.
53. Foussard, M.,, A.-M. Garnerone,, F. Ni,, E. Soupéne,, P. Boistard,, and J. Batut. 1997. Negative autoregulation of the Rhizobium meliloti fixK gene is indirect and requires a newly identified regulator, FixT. Mol. Microbiol. 25:2737.
54. Freiberg, C.,, R. Fellay,, A. Bairoch,, W. J. Broughton,, A. Rosenthal,, and X. Perret. 1997. Molecular basis of symbiosis between Rhizobium and legumes. Nature 387:394401.
55. Gage, D. J.,, and S. R. Long. 1998. α-Galactoside uptake in Rhizobium meliloti: isolation and characterization of agpA, a gene encoding a periplasmic binding protein required for melibiose and raffinose utilization. J. Bacteriol. 180:57395748.
56. Gage, D. J.,, T. Bobo,, and S. R. Long. 1996. Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and alfalfa (Medicago sativa). J. Bacteriol. 178:71597166.
57. Gilles-González, M. A.,, G. S. Ditta,, and D. R. Helinski. 1991. A haemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti. Nature 350:170172.
58. Glazebrook, J.,, and G. C. Walker. 1989. A novel exopolysaccharide can function in place of the cal-cofluor-binding exopolysaccharide in nodulation of alfalfa by Rhizobium meliloti. Cell 56:661672.
59. Glazebrook, J.,, A. Ichige,, and G. C. Walker. 1993. A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development. Genes Dev. 7:14851497.
60. González, J. E.,, B. L. Reuhs,, and G. C. Walker. 1996a. Low molecular weight EPS II of Rhizobium meliloti allows nodule invasion in Medicago sativa. Proc. Natl. Acad. Sci. USA 93:86368641.
61. González, J. E.,, G. M. York,, and G. C. Walker. 1996b. Rhizobium meliloti exopolysaccharides: synthesis and symbiotic function. Gene 179:141146.
62. González, J. E.,, C. E. Semino,, L. X. Wang,, L. E. Castellano-Torres,, and G. C. Walker. 1998. Biosynthetic control of molecular weight in the polymerization of the octasaccharide subunits of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti. Proc. Natl. Acad. Sci USA 95:1347713482.
63. Goormachtig, S.,, S. Lievens,, W. Van de Velde,, M. Van Montagu,, and M. Holsters. 1998. Srchi13, a novel early nodulin from Sesbania rostrata, is related to acidic class III chitinases. Plant Cell 10: 905915.
64. Gottfert, M.,, P. Grob,, and H. Hennecke. 1990. Proposed regulatory pathway encoded by the nod V and nodW genes, determinants of host specificity in Bradyrhizobium japonicum. Proc. Natl. Acad. Sci. USA 87:26802684.
65. Gotz, R.,, and R. Schmitt. 1987. Rhizobium meliloti swims by unidirectional, intermittent rotation of right-handed flagellar helices. J. Bacteriol. 169: 31463150.
66. Gouffi, K.,, V. Pichereau,, J. P. Rolland,, D. Thomas,, T. Bernard,, and C. Blanco. 1998. Sucrose is a nonaccumulated osmoprotectant in Sinorhizobium meliloti. J. Bacteriol. 180:50445051.
67. Gresshoff, P. M.,, and B. G. Rolfe. 1978. Viability of Rhizobium bacteroids isolated from soybean nodule protoplasts. Planta 142:329333.
68. Gresshoff, P. M.,, M. L. Skotnicki,, J. F. Eadie,, and B. G. Rolfe. 1977. Viability of Rhizobium trifolii bacteroids from clover root nodules. Plant Sci. Lett. 10:299304.
69. Heithoff, D. M.,, C. P. Conner,, and M. J. Mahan. 1997. Dissecting the biology of a pathogen during infection. Trends Miaobiol. 5:509513.
70. Hirsch, A. M.,, and C. A. Smith. 1987. Effects of Rhizobium meliloti nif and fix mutants on alfalfa root nodule development. J. Bacteriol. 169:11371146.
71. Hirsch, A. M.,, K.J. WilsonJ,. D. Jones,, M. Bang,, V. V. Walker,, and F. M. Ausubel. 1984. Rhizobium meliloti nodulation genes allow Agrobacterium tumefaciens and Escherichia coli to form pseudonodules on alfalfa. J. Bacteriol. 158:11331143.
72. Hochman, A. 1997. Programmed cell death in pro-karyotes. Crit. Rev. Microbiol. 23:207214.
73. Ichige, A.,, and G. C. Walker. 1997. Genetic analysis of the Rhizobium meliloti bacA gene: functional interchangeability with the Escherichia coli sbmA gene and phenotypes of mutants. J. Bacteriol. 179: 209216.
74. Jensen, E. O.,, K. Paludan,, J. J. Hyldig-Nielsen,, P. Jorgensen,, and K. A. Marcker. 1981. The structure of a chromosomal leghaemoglobin gene from soybean. Nature 291:677679.
75. Jordan, D. C.,, and W. H. Coulter. 1965. On the cytology and synthetic capacities of natural and artificially produced bacteroids of Rhizobium leguminosarum. Can. J. Microbiol. 11:709720.
76. Kaiser, B. N.,, P. M. Finnegan,, S. D. Tyerman,, L. F. Whitehead,, F. J. Bergersen,, D. A. Day,, and M. K. Udvardi. 1998. Characterization of an ammonium transport protein from the peribacteroid membrane of soybean nodules. Science 281: 12021206.
77. Kamst, E.,, H. P. Spaink,, and D. Kafetzopoulos. 1998. Biosynthesis and secretion of rhizobial lipochitin-oligosaccharide signal molecules. Subcell. Biochem. 29:2971.
78. Kaneshiro, T.,, F. L. Baker,, and D. E. Johnson. 1983. Pleomorphism and acetylene-reducing activity of free-living rhizobia. J. Bacteriol. 153: 10451050.
79. Kannenberg, E. L.,, and N. J. Brewin. 1989. Expression of a cell surface antigen from Rhizobium leguminosarum 3841 is regulated by oxygen and pH. J. Bacteriol. 171:45434548.
80. Kannenberg, E. L.,, and N. J. Brewin. 1994. Host-plant invasion by Rhizobium: the role of cell-surface components. Trends Microbiol. 2:277283.
81. Kannenberg, E. L.,, S. Perotto,, V. Bianciotto,, E. A. Rathbun,, and N. J. Brewin. 1994. Lipopolysaccharide epitope expression of Rhizobium bacteroids as revealed by in situ immunolabelling of pea root nodule sections. J. Bacteriol. 176:20212032.
82. Kapranov, P.,, T. J. Jensen,, C. Poulsen,, F. J. de Bruijn,, and K. Szczyglowski. 1999. A protein phosphatase 2C gene, LJNPP2C1, froml Lotus japonicus induced during root nodule development. Proc. Natl. Acad. Sci. USA 96:17381743.
83. Kidby, D. K.,, and D. J. Goodchild. 1966. Host influence on the ultrastructure of root nodules of Lupinus luteus and Omithopus sativus. J. Gen. Microbiol. 45:147152.
84. Kijne, J. W., 1992. The Rhizobium infection process, p. 349398. In G. Stacey,, R. H. Bums,, and H. J. Evans (ed.), Biological Nitrogen Fixation. Chapman and Hall, New York, N.Y.
85. Kijne, J. W.,, M. A. Bauchrowitz,, and C. L. Diaz. 1997. Root lectins and rhizobia. Plant Physiol. 115: 869873.
86. Klein, S.,, A. M. Hirsch,, C. A. Smith,, and E. R. Signer. 1988. Interaction of nod and exo Rhizobium meliloti in alfalfa nodulation. Mol. Plant-Microbe Interact. 1:94100.
87. Kurz, W. G. W.,, and T. A. La Rue. 1975. Nitrogenase activity in rhizobia in the absence of plant host. Nature 256:407408.
88. Latch, J. N.,, and W. Margolin. 1997. Generation of buds, swellings, and branches instead of filaments after blocking the cell cycle of Rhizobium meliloti. J. Bacteriol. 179:23732381.
89. Latchford, J. W.,, D. Borthakur,, and A. W. Johnston. 1991. The products of Rhizobium genes, psi and pss, which affect exopolysaccharide production, are associated with the bacterial cell surface. Mol. Microbiol. 5:21072114.
90. Legocki, R. P.,, and D. P. Verma. 1980. Identification of "nodule-specific" host proteins (nodulins) involved in the development of rhizobium-legume symbiosis. Cell 20:153163.
91. Leigh, J. A.,, and D. L. Coplin. 1992. Exopolysac-charides in plant-bacterial interactions. Annu. Rev. Microbiol. 46:307346.
92. Leigh, J. A.,, and G. C. Walker. 1994. Exopolysaccharides of Rhizobium: synthesis, regulation and symbiotic function. Trends Genet. 10:6367.
93. Leigh, J. A.,, E. R. Signer,, and G. C. Walker. 1985. Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc. Natl. Acad. Sci. USA 82:62316235.
94. Loh, J.,, M. Garcia,, and G. Stacey. 1997. NodV and NodW, a second flavonoid recognition system regulating nod gene expression in Bradyrhizobium japonicum. J. Bacteriol. 179:30133020.
95. Loh, J.,, M. G. Stacey,, M. J. Sadowsky,, and G. Stacey. 1999. The Bradyrhizobium japonicum nolA gene encodes three functionally distinct proteins. J. Bacteriol. 181:15441554.
96. Loh, J. T.,, S. C. Ho,, A. W. de Feijter,, J. L. Wang,, and M. Schindler. 1993. Carbohydrate binding activities of Bradyrhizobium japonicum: unipolar localization of the lectin BJ38 on the bacterial cell surface. Proc. Natl. Acad. Sci. USA 90:30333037.
97. Long, S.,, S. McCune,, and G. C. Walker. 1988. Symbiotic loci of Rhizobium meliloti identified by random TnphoA mutagenesis. J. Bacteriol. 170: 42574265.
98. Long, S. R. 1996. Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8:18851898.
99. Long, S. R.,, and B. J. Staskawicz. 1993. Prokaryotic plant parasites. Cell 73:921935.
100. Lucas, M. M.,, J. L. Peart,, N. J. Brewin,, and E. L. Kannenberg. 1996. Isolation of monoclonal antibodies reacting with the core component of lipopolysaccharide from Rhizobium leguminosarum strain 3841 and mutant derivatives. J. Bacteriol. 178: 27272733.
101. Ludwig, R. A.,, and E. R. Signer. 1977. Glutamine synthetase and control of nitrogen fixation in Rhizobium. Nature 267:245248.
102. MacKenzie, C. R.,, W. J. Vail,, and D. C. Jordan. 1973. Ultrastructure of free-living and nitrogen-fixing forms of Rhizobium meliloti as revealed by freeze-etching. J. Bacteriol. 113:387393.
103. Maddock, J. R.,, M. R. Alley,, and L. Shapiro. 1993. Polarized cells, polar actions. J. Bacteriol. 175: 71257129.
104. Mahan, M. J.,, J. M. Slauch, andj. J. Mekalanos. 1993. Selection of bacterial virulence genes that are specifically induced in host tissues. Science 259: 686688.
105. Manoil, C.,, and J. Beckwith. 1985. TnphoA: a transposon probe for protein export. Proc. Natl. Acad. Sci. USA 82:81298133.
106. Margolin, W.,, and S. R. Long. 1994. Rhizobium meliloti contains a novel second homolog of the cell division gene fisZ. J. Bacteriol. 176:20332043.
107. Mateos, P. F.,, J. I. Jimenez-Zurdo,, J. Chen,, A. S. Squartini,, S. K. Haack,, E. Martinez-Molina,, D. H. Hubbell,, and F. B. Dazzo. 1992. Cell-associated pectinolytic and cellulolytic enzymes in Rhizobium leguminosarum biovar trifolii. Appl. Environ. Microbiol. 58:18161822.
108. McComb, J. A.,, J. Elliott,, and M. J. Dilworth. 1975. Acetylene reduction by Rhizobium in pure culture. Nature 256:409410.
109. McRae, D. G.,, R. W. Miller,, and W. B. Berndt. 1989. Viability of alfalfa nodule bacteroids isolated by density gradient centrifugation. Symbiosis 7: 6780.
110. Mergaert, P.,, M. Van Montagu,, and M. Holsters. 1997. Molecular mechanisms of Nod factor diversity. Mol. Microbiol. 25:811817.
111. Miao, G. H.,, Z. Hong,, and D. P. Verma. 1992. Topology and phosphorylation of soybean nodulin-26, an intrinsic protein of the peribacteroid membrane. J. Cell Biol. 118:481490.
112. Michiels, J.,, M. Moris,, B. Dombrecht,, C. Verreth,, and J. Vanderleyden. 1998. Differential regulation of Rhizobium etli rpoN2 gene expression during symbiosis and free-living growth. J. Bacteriol. 180:36203628.
113. Milner, J. L.,, R. S. Araujo,, and J. Handelsman. 1992. Molecular and symbiotic characterization of exopolysaccharide-deficient mutants of Rhizobium tropici strain CIAT899. Mol. Microbiol. 6: 31373147.
114. Moreau, S.,, M. J. Davies,, C. Mathieu,, D. Herouart,, and A. Puppo. 1996. Leghemoglobin-derived radicals. Evidence for multiple protein-derived radicals and the initiation of peribacteroid membrane damage. J. Biol. Chem. 271: 3255732562.
115. Muñoz, J. A.,, C. Coronado,, J. Perez-Hormaeche,, A. Kondorosi,, P. Ratet,, and A. J. Palomares. 1998. MsPG3, a medicago sativa polygalacturonase gene expressed during the alfalfa-Rhizobium meliloti interaction. Proc. Natl. Acad. Sci. USA 95:96879692.
116. Murphy, P. J.,, N. Heycke,, S. P. Trenz,, P. Ratet,, F. J. de Bruijn,, and J. Schell. 1988. Synthesis of an opine-like compound, a rhizopine, in alfalfa nodules is symbiotically regulated. Proc. Natl. Acad. Sci. USA 85:91339137.
117. Mylona, P.,, K. Pawlowski,, and T. Bisseling. 1995. Symbiotic nitrogen fixation. Plant Cell 7: 869885.
118. Nellen-Anthamatten, D.,, P. Rossi,, O. Preisig,, I. Kullik,, M. Babst,, H. M. Fischer,, and H. Hennecke. 1998. Bradyrhizobium japonicum FixK2, a crucial distributor in the FixLJ-dependent regulatory cascade for control of genes inducible by low oxygen levels. J. Bacteriol. 180:52515255.
119. Newcomb, W. 1981. Nodule morphogenesis and differentiation. Int. Rev. Cytol. 13(Suppl.): 247296.
120. Niehaus, K.,, and A. Becker. 1998. The role of microbial surface polysaccharides in the Rhizobium-legume interaction. Subcell. Biochem. 29:73116.
121. Niehaus, K.,, A. Lagares,, and A. Pühler. 1998. A Sinorhizobium meliloti lipopolysaccharide mutant induces effective nodules on the host plant Medicago sativa (alfalfa) but fails to establish a symbiosis with Medicago truncatula. Mol. Plant-Microbe Interact. 11: 906914.
122. Noel, K. D.,, G. Stacey,, S. R. Tandon,, L. E. Silver,, and W. J. Brill. 1982. Rhizobium japonicum mutants defective in symbiotic nitrogen fixation. J. Bacteriol. 152:485494.
123. O'Brian, M. R. 1996. Heme synthesis in the rhizobium-legume symbiosis: a palette for bacterial and eukaryotic pigments. J. Bacteriol. 178:24712478.
124. O'Brian, M. R.,, P. M. Kirshbom,, and R. J. Maier. 1987. Bacterial heme synthesis is required for expression of the leghemoglobin holoprotein but not the apoprotein in soybean root nodules. Proc. Natl. Acad. Sci. USA 84:83908393.
125. Ogawa, J.,, and S. R. Long. 1995. The Rhizobium meliloti groELc locus is required for regulation of early nod genes by the transcription activator NodD. Genes Dev. 9:714729.
126. Oke, V.,, and S. R. Long. 1999. Bacterial genes induced within the nodule during the Rhizobium-legume symbiosis. Mol. Microbiol. 32:837849.
127. Paau, A. S.,, J. Oro,, and J. R. Cowles. 1979. DNA content of free living rhizobia and bacteroids of various Rhizobium-legume associations. Plant Physiol. 63:402405.
128. Paau, A. S.,, C. B. Bloch,, and W. J. Brill. 1980. Developmental fate of Rhizobium meliloti bacteroids in alfalfa nodules. J. Bacteriol. 143:14801490.
129. Pagan, J. D.,, J. J. Child,, W. R. Scowcroft,, and A. H. Gibson. 1975. Nitrogen fixation by Rhizobium cultured on a defined medium. Nature 256: 406407.
130. Pankhurst, C. E.,, and A. S. Craig. 1978. Effect of oxygen concentration, temperature and combined nitrogen on the morphology and nitrogenase activity of Rhizobium sp. strain 32H1 in agar culture. J. Gen. Microbiol. 106:207219.
131. Petrovics, G.,, P. Putnoky,, B. Reuhs,, J. Kim,, T. A. Thorp,, K. D. Noel,, R. W. Carlson,, and A. Kondorosi. 1993. The presence of a novel type of surface polysaccharide in Rhizobium meliloti requires a new fatty acid synthase-like gene cluster involved in symbiotic nodule development. Mol. Microbiol. 8:10831094.
132. Pingret, J. L.,, E. P. Journet,, and D. G. Barker. 1998. Rhizobium Nod factor signaling. Evidence for a G protein-mediated transduction mechanism. Plant Cell 10:659672.
133. Preisig, O.,, D. Anthamatten,, and H. Hennecke. 1993. Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. Proc. Natl. Acad. Sci. USA 90:33093313.
134. Priefer, U. B. 1989. Genes involved in lipopolysaccharide production and symbiosis are clustered on the chromosome of Rhizobium leguminosarum biovar viciae VF39. J. Bacteriol. 171:61616168.
135. Putnoky, P.,, E. Grosskopf,, D. T. Ha,, G. B. Kiss,, and A. Kondorosi. 1988. Rhizobium fix genes mediate at least two communication steps in symbiotic nodule development. J. Cell Biol. 106:597607.
136. Putnoky, P.,, G. Petrovics,, A. Kereszt,, E. Grosskopf,, D. T. Ha,, Z. Banfalvi,, and A. Kondorosi. 1990. Rhizobium meliloti lipopolysaccharide and exopolysaccharide can have the same function in the plant-bacterium interaction. J. Bacteriol. 172:54505458.
137. Putnoky, P.,, A. Kereszt,, T. Nakamura,, G. Endre,, E. Grosskopf,, P. Kiss,, and A. Kondorosi. 1998. The pha gene cluster of Rhizobium meliloti involved in pH adaptation and symbiosis encodes a novel type of K+ efflux system. Mol. Microbiol. 28:10911101.
138. Rana, D.,, and H. B. Krishnan. 1995. A new root-nodulating symbiont of the tropical legume Ses-bania, Rhizobium sp. SIN-1, is closely related to R. galegae, a species that nodulates temperate legumes. FEMS Microbiol. Lett. 134:1925.
139. Reibach, P. H.,, P. L. Mask, andj. G. Streeter. 1981. A rapid one-step method for the isolation of bacteroids from root nodules of soybean plants, utilizing self-generating Percoll gradients. Can. J. Microbiol. 27:491495.
140. Relic, B.,, X. Perret,, M. T. Estrada-Garcia,, J. Kopcinska,, W. Golinowski,, H. B. Krishnan,, S. G. Pueppke,, and W. J. Broughton. 1994. Nod factors of Rhizobium are a key to the legume door. Mol. Microbiol. 13:171178.
141. Reuber, T. L.,, S. Long,, and G. C. Walker. 1991. Regulation of Rhizobium meliloti exo genes in free-living cells and in planta examined by using TnphoA fusions. J. Bacteriol. 173:426434.
142. Reuhs, B. L.,, R. W. Carlson,, and J. S. Kim. 1993. Rhizobium fredii and Rhizobium meliloti produce 3-deoxy-D-manno-2-octulosonic acid-containing polysaccharides that are structurally analogous to group II K antigens (capsular polysaccharides) found in Escherichia coli. J. Bacteriol. 175: 35703580.
143. Reuhs, B. L.,, J. S. Kim,, A. Badgett,, and R. W. Carlson. 1994. Production of cell-associated polysaccharides of Rhizobium fredii USDA205 is modulated by apigenin and host root extract. Mol. Plant-Microbe Interact. 7:240247.
144. 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 IpsZ is correlated to a modified expression of the K polysaccharide. J. Bacteriol. 177:42894296.
145. Reyes, V. G.,, and E. L. Schmidt. 1979. Population densities of Rhizobium japonicum strain 123 estimated directly in soil and rhizospheres. Appl. Environ. Microbiol. 37:854858.
146. Robertson, J. G.,, and P. Lyttleton. 1984. Division of peribacteroid membranes in root nodules of white clover. J. Cell Sci. 69:147157.
147. Robertson, J. G.,, P. Lyttleton,, S. Bullivant,, and G. F. Grayston. 1978a. Membranes in lupin root nodules. I. The role of Golgi bodies in the biogenesis of infection threads and peribacteroid membranes. J. Cell Sci. 30:129149.
148. Robertson, J. G.,, M. P. Warburton,, P. Lyttleton,, A. M. Fordyce,, and S. Bullivant. 1978b. Membranes in lupin root nodules. II. Preparation and properties of peribacteroid membranes and bacteroid envelope inner membranes from developing lupin nodules. J. Cell Sci. 30:151174.
149. Robinson, J. B.,, and W. D. Bauer. 1993. Relationships between C4 dicarboxylic acid transport and chemotaxis in Rhizobium meliloti. J. Bacteriol. 175: 22842291.
150. Roth, L. E.,, and G. Stacey,. 1991. Rhizobium-legume symbiosis, p. 255302. In M. Dworkin (ed.), Microbial Cell-Cell Interactions. American Society for Microbiology, Washington, D.C.
151. Sangwan, I.,, and M. R. O'Brian. 1991. Evidence for an inter-organismic heme biosynthetic pathway in symbiotic soybean root nodules. Science 251: 12201222.
152. Santana, M. A.,, K. Pihakaski-Maunsbach,, N. Sandal,, K. A. Marcker,, and A. G. Smith. 1998. Evidence that the plant host synthesizes the heme moiety of leghemoglobin in root nodules. Plant Physiol. 116:12591269.
153. Schell, M. A. 1993. Molecular biology of the LysR family of transcriptional regulators. Annu. Rev. Microbiol. 47:597626.
154. Schlaman, H. R.,, B. Horvath,, E. Vijgenboom,, R. J. Okker,, and B. J. Lugtenberg. 1991. Suppression of nodulation gene expression in bacteroids of Rhizobium leguminosarum biovar viciae. J. Bacteriol. 173:42774287.
155. Schlaman, H. R.,, B. J. Lugtenberg,, and R. J. Okker. 1992. The NodD protein does not bind to the promoters of inducible nodulation genes in extracts of bacteroids of Rhizobium leguminosarum biovar viciae. J. Bacteriol. 174:61096116.
156. Schmidt, E. L. 1979. Initiation of plant root-microbe interactions. Annu. Reu. Microbiol. 33:355376.
157. Schultze, M.,, and A. Kondorosi. 1996. The role of lipochitooligosaccharides in root nodule organogenesis and plant cell growth. Curr. Opin. Genet. Dev. 6:631638. (Erratum, 6:773.)
158. Schultze, M.,, and A. Kondorosi. 1998. Regulation of symbiotic root nodule development. Annu. Rev. Genet. 32:3357.
159. Schultze, M.,, E. Kondorosi,, P. Ratet,, M. Buire,, and A. Kondorosi. 1994. Cell and molecular biology of Rhizobium-plant interactions. Int. Rev. Cytol. 156:175.
160. Sedloi-Lumbroso, R.,, L. Kleiman,, and H. M. Schulman. 1978. Biochemical evidence that leg-haemoglobin genes are present in the soybean but not the Rhizobium genome. Nature 273:558560.
161. Sharma, S. B.,, and E. R. Signer. 1990. Temporal and spatial regulation of the symbiotic genes of Rhizobium meliloti in planta revealed by transposon Tn5-gusA. Genes Dev. 4:344356.
162. Sindhu, S. S.,, N. J. Brewin,, and E. L. Kannen-berg. 1990. Immunochemical analysis of lipopoly-saccharides from free-living and endosymbiotic forms of Rhizobium leguminosarum. J. Bacteriol. 172:18041813.
163. Slauch, J. M.,, M. J. Mahan,, and J. J. Mekalanos. 1994. In vivo expression technology for selection of bacterial genes specifically induced in host tissues. Methods Enzymol. 235:481492.
164. Smit, G.,, J. W. Kijne,, and B. J. Lugtenberg. 1987. Involvement of both cellulose fibrils and a Ca2+-dependent adhesin in the attachment of Rhizobium leguminosarum to pea root hair tips. J. Bacteriol. 169: 42944301.
165. Smit, G.,, S. Swart,, G. Lugtenberg,, and J. Kijne. 1992. Molecular mechanisms of attachment of Rhizobium bacteria to plant roots. Mol. Microbiol. 6: 28972903.
166. Soupéne, E.,, M. Foussard,, P. Boistard,, G. Tru-chet, andj. Batut. 1995. Oxygen as a key developmental regulator of Rhizobium meliloti N2-fixation gene expression within the alfalfa root nodule. Proc. Natl. Acad. Sri. USA 92:37593763.
167. Soupéne, E.,, L. He,, D. Yan,, and S. Kustu. 1998. Ammonia acquisition in enteric bacteria: physiological role of the ammonium/methylammonium transport ? (AmtB) protein. Proc. Natl. Acad. Sci. USA 95:70307034.
168. Spaink, H. 1995. The molecular basis of infection and nodulation by Rhizobia: the ins and outs of sympathogenesis. Annu. Rev. Phytopathol. 33: 345368.
169. Spaink, H. P.,, C. A. Wijffelman,, W. Pees,, R. J. H. Okker,, and B. J. J. Lugtenberg. 1987. Rhizobium nodulation gene nodD as a determinant of host specificity. Nature 328:337340.
170. Sullivan, J. T.,, and C. W. Ronson. 1998. Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc. Natl. Acad. Sci USA 95:51455149.
171. Sulton, W. D. 1974. Some features of the DNA of Rhizobium bacteroids and bacteria. Biochim. Biophys. Acta 366:110.
172. Sutton, W. D. 1981. The Rhizobium bacteroid state. Int. Rev. Cytol. 13(Suppl.):149177.
173. Sutton, W. D.,, and A. D. Paterson. 1979. The detergent sensitivity of Rhizobium bacteroids and bacteria. Plant. Sci. Lett. 16:377385.
174. Sutton, W. D.,, N. M. Jepsen,, and B. D. Shaw. 1977. Changes in the number, viability, and amino-acid-incorporating activity of Rhizobium bacteroids during lupin nodule development. Plant Physiol. 59:741744.
175. Szczyglowski, K.,, P. Kapranov,, D. Hamburger,, and F. J. de Bruijn. 1998. The Lotus japonicus LjNOD70 nodulin gene encodes a protein with similarities to transporters. Plant Mol. Biol. 37: 651661.
176. Talibart, R.,, M. Jebbar,, G. Gouesbet,, S. Himdi-Kabbab,, H. Wroblewski,, C. Blanco,, and T. Bernard. 1994. Osmoadaptation in rhizobia: ectoine-induced salt tolerance. J. Bacteriol. 176: 52105217.
177. Tate, R.,, A. Riccio,, M. Merrick,, and E. J. Patriarca. 1998. The Rhizobium etli amtB gene coding for an NH4+ transporter is down-regulated early during bacteroid differentiation. Mol. Plant-Microbe Interact. 11:188198.
178. Timmers, A. C.,, M. C. Auriac,, F. de Billy,, and G. Truchet. 1998. Nod factor internalization and microtubular cytoskeleton changes occur concomitantly during nodule differentiation in alfalfa. Development 125:339349.
179. Truchet, G.,, P. Roche,, P. Lerouge,, J. Vasse,, S. Camut,, F. de Billy,, J.-C. Promé,, and J. Dénarié. 1991. Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351:670673.
180. Tsien, H. C.,, P. S. Cain,, and E. L. Schmidt. 1977. Viability of Rhizobium bacteroids. Appl. Environ. Microbiol. 34:854856.
181. Turgeon, B. G.,, and W. D. Bauer. 1985. Ultra-structure of infection-thread development during infection of soybean by Rhizobium japonicum. Planta 163:328349.
182. Tyerman, S. D.,, L. F. Whitehead,, and D. A. Day. 1995. A channel-like transporter for NH4+ on the symbiotic interface of N2 fixing plants. Nature 378: 629632.
183. Urban, J. E.,, and F. B. Dazzo. 1982. Succinate-induced morphology of Rhizobium trifolii 0403 resembles that of bacteroids in clover nodules. Appl. Environ. Microbiol. 44:219226.
184. van Brussel, A. A.,, J. W. Costerton,, and J. J. Child. 1979. Nitrogen fixation by Rhizobium sp. 32H1. A morphological and ultrastructural comparison of asymbiotic and symbiotic nitrogen-fixing forms. Can. J. Microbiol. 25:352361.
185. van Brussel, A. A. N.,, R. Bakhuizen,, P. van Spronsen,, H. P. Spaink,, T. Tak,, J. J. Lug-tenberg,, and J. Kijne. 1992. Induction of pre-infection thread structures in the host plant by lipo-oligosaccharides of Rhizobium. Science 257:7072.
186. Vance, C. P. 1983. Rhizobium infection and nodulation: a beneficial plant disease? Annu. Rev. Microbiol. 37:399424.
187. van Heeswijk, W. C.,, S. Hoving,, D. Molenaar,, C. Stegeman,, D. Kahn,, and H. V. Westerhoff. 1996. An alternative PII protein in the regulation of glutamine synthetase in Escherichia coli. Mol. Microbiol. 21:133146.
188. van Rhijn, P.,, R. B. Goldberg,, and A. M. Hirsch. 1998. Lotus comiculatus nodulation specificity is changed by the presence of a soybean lectin gene. Plant Cell 10:12331250.
189. van Spronsen, P. C.,, R. Bakhuizen,, A. A. van Brussel,, and J. W. Kijne. 1994. Cell wall degradation during infection thread formation by the root nodule bacterium Rhizobium leguminosarum is a two-step process. Eur. J. Cell Biol. 64:8894.
190. Vasse, J.,, F. de Billy,, S. Camut,, and G. Truchet. 1990. Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J. Bacteriol. 172:42954306.
191. Verde, F. 1998. On growth and form: control of cell morphogenesis in fission yeast. Curr. Opin. Microbiol. 1:712718.
192. Verma, D. P. 1998. Developmental and metabolic adaptations during symbiosis between legume hosts and rhizobia. Subcell. Biochem. 29:128.
193. Verma, D. P.,, and Z. Hong. 1996. Biogenesis of the peribacteroid membrane in root nodules. Trends Microbiol. 4:364368.
194. Verma, D. P. S. 1992. Signals in root nodule organogenesis and endocytosis of Rhizobium. Plant Cell 4: 373382.
195. Verma, D. P. S.,, and S. Long. 1983. The molecular biology of Rhizobium-legume symbiosis. Int. Rev. Cytol. 14(Suppl.):211245.
196. Vesper, S.J.,, and W. D. Bauer. 1986. Role of pili in Rhizobium japonicum attachment to soybean roots. Appl. Environ. Microbiol. 52:134141.
197. Viprey, V.,, A. Del Greco,, W. Golinowski,, W. J. Broughton,, and X. Perret. 1998. Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol. Microbiol. 28:13811389.
198. Wang, L.-X.,, Y. Wang,, B. Pellock,, and G. C. Walker. 1999. Structural characterization of the symbiotically important low-molecular-weight succinoglycan of Sinorhizobium meliloti. J. Bacteriol. 181, in press.
199. Waters, J. K.,, B. L. Hughes II,, L. C. Purcell,, K. O. Gerhardt,, T. P. Mawhinney,, and D. W. Emerich. 1998. Alanine, not ammonia, is excreted from N2-fixing soybean nodule bacteroids. Proc. Natl. Acad. Sci. USA 95:1203812042.
200. Werner, D.,, R. B. Mellor,, M. G. Hahn,, and H. Grisebach. 1985. Glyceollin I accumulation in an ineffective type of soybean nodule with an early loss of peribacteroid membrane. Z. Naturforsch. TeilC 40:179181.
201. Wheatcroft, R.,, D. G. McRae,, and R. W. Miller. 1990. Changes in the Rhizobium meliloti genome and the ability to detect supercoiled plasmids during bacteroid development. Mol. Plant-Microbe Interact. 3:917.
202. Wright, R.,, C. Stephens,, and L. Shapiro. 1997. The CcrM DNA methyltransferase is widespread in the alpha subdivision of proteobacteria, and its essential functions are conserved in Rhizobium meliloti and Caulobacter crescentus. J. Bacteriol. 179: 58695877.
203. Yang, W. C.,, C. de Blank,, I. Meskiene,, H. Hirt,, J. Bakker,, A. van Kammen,, H. Franssen,, and T. Bisseling. 1994. Rhizobium Nod factors reactivate the cell cycle during infection and nodule pri-mordium formation, but the cycle is only completed in primordium formation. Plant Cell 6: 14151426.
204. Yao, P. Y.,, and J. M. Vincent. 1969. Host specificity in the root hair "curling factor" of Rhizobium sp. Aust.J. Biol. Sci. 22:413422.
205. Yarosh, O. K.,, T. C. Charles,, and T. M. Finan. 1989. Analysis of C4-dicarboxylate transport genes in Rhizobium meliloti. Mol. Microbiol. 3:813823.
206. Yoon, H. S.,, and J. W. Golden. 1998. Heterocyst pattern formation controlled by a diffusible peptide. Science 282:935938.
207. Yost, C. K.,, P. Rochepeau,, and M. F. Hynes. 1998. Rhizobium leguminosarum contains a group of genes that appear to code for methyl-accepting chemotaxis proteins. Microbiology 144:19451956.
208. Zhan, H. J.,, C. C. Lee,, and J. A. Leigh. 1991. Induction of the second exopolysaccharide (EPSb) in Rhizobium meliloti SU47 by low phosphate concentrations. J. Bacteriol. 173:73917394.
209. Zhao, J. C.,, Y. T. Tchan,, and J. M. Vincent. 1985. Reproductive capacity of bacteroids in nodules of Trifolium repens L. and Glycine max (L.) Merr. Planta 163:473482.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error